diminutive


EVOLUTIONARY HOMOLOGS


Table of contents

Binding of Myc to DNA

The biological activity of the c-Abl protein is linked to its tyrosine kinase and DNA-binding activities. The protein, which plays a major role in the cell cycle response to DNA damage, interacts preferentially with sequences containing an AAC motif and exhibits a higher affinity for bent or bendable DNA, as is the case with high mobility group (HMG) proteins. The DNA-binding characteristics of the DNA-binding domain of human c-Abl and the HMG-D protein from Drosophila melanogaster have been compared. c-Abl binds tightly to circular DNA molecules and potentiates the interaction of DNA with HMG-D. In addition, a series of DNA molecules containing modified bases were used to determine how the exocyclic groups of DNA influence the binding of the two proteins. Interfering with the 2-amino group of purines affects the binding of the two proteins similarly. Adding a 2-amino group to adenines restricts the access of the proteins to the minor groove, whereas deleting this bulky substituent from guanines facilitates the protein-DNA interaction. In contrast, c-Abl and HMG-D respond very differently to deletion or addition of the 5-methyl group of pyrimidine bases in the major groove. Adding a methyl group to cytosines favors the binding of c-Abl to DNA but inhibits the binding of HMG-D. Conversely, deleting the methyl group from thymines promotes the interaction of the DNA with HMG-D but diminishes its interaction with c-Abl. The enhanced binding of c-Abl to DNA containing 5-methylcytosine residues may result from an increased propensity of the double helix to denature locally, coupled with a protein-induced reduction in the base stacking interaction. The results show that c-Abl has unique DNA-binding properties, quite different from those of HMG-D, and suggest an additional role for the protein kinase (David-Cordonnier, 1999).

N-Myc is a transcription factor that forms heterodimers with the protein Max and binds gene promoters by recognizing a DNA sequence, CACGTG, called E-box. The identification of N-myc target genes is an important step for understanding N-Myc biological functions in both physiological and pathological contexts. In this study, the identification of N-Myc-responsive genes through chromatin immunoprecipitation and methylation-sensitive restriction analysis is described. Results show that N-Myc is a direct regulator of several identified genes, and that methylation of the CpG dinucleotide within the E-box prevents the access of N-Myc to gene promoters in vivo. Furthermore, methylation profile of the E-box within the promoters of EGFR and CASP8, two genes directly controlled by Myc, is cell type-specific, suggesting that differential E-box methylation may contribute to generating unique patterns of Myc-dependent transcription. This study illuminates a central role of DNA methylation in controlling N-Myc occupancy at gene promoters and modulating its transcriptional activity in cancer cells (Perini, 2005).

Regulation of transcription and translation of vertebrate myc

Increasing evidence supports an important biological role for Myc in the downregulation of specific gene transcription. Recent studies suggest that c-Myc may suppress promoter activity through proteins of the basal transcription machinery. Myc protein, in combination with additional cellular factors, suppresses transcription initiation from the c-myc promoter. There is a four-fold to five-fold suppression of a c-myc P2 minimal promoter fragment upon induction of wild-type Myc protein activity, while induction of a mutant Myc protein lacking amino acids 106 to 143 required for Myc autosuppression fails to elicit this response. This assay is physiologically significant, as it reflects Myc autosuppression of the endogenous c-myc gene with regard to kinetics, dose dependency, cell type specificity, and c-Myc functional domains. Analysis of mutations within the P2 minimal promoter indicates that the cis components of Myc autosuppression could not be ascribed to any known protein-binding motifs. Myc-Max heterodimerization is obligatory for Myc autosuppression (Facchini, 1997).

Organization of DNA into chromatin has been shown to contribute to a repressed state of gene transcription. Disruption of nucleosomal structure is observed in response to gene induction, suggesting a model in which RNA polymerase II (pol II) is recruited to the promoter upon reorganization of nucleosomes. Induction of c-myc transcription correlates with the disruption of two nucleosomes in the upstream promoter region. However, this nucleosomal disruption is not necessary for the binding of pol II to the promoter. Transcriptionally engaged pol II complexes can be detected when the upstream chromatin is in a more closed configuration. Thus, upstream chromatin opening is suggested to affect activation of promoter-bound pol II rather than entry of polymerases into the promoter. Interestingly, pol II complexes are detectable in both sense and antisense transcriptional directions, but only complexes in the sense direction respond to activation signals resulting in processive transcription (Albert, 1997).

The small constitutively expressed bHLHZip protein Max is known to form sequence-specific DNA binding heterodimers with members of both the Myc and Mad families of bHLHZip proteins. Myc:Max complexes activate transcription, promote proliferation, and block terminal differentiation. In contrast, Mad:Max heterodimers act as transcriptional repressors, have an antiproliferative effect, and are induced upon differentiation in a wide variety of cell types. A novel bHLHZip Max-binding protein, Mnt, has been identified that belongs to neither the Myc nor the Mad families and that is coexpressed with Myc in a number of proliferating cell types. Mnt:Max heterodimers act as transcriptional repressors and efficiently suppress Myc-dependent activation from a promoter containing proximal CACGTG sites. Transcription repression by Mnt maps to a 13-amino-acid amino-terminal region related to the Sin3 interaction domain (SID) of Mad proteins. This region of Mnt mediates interaction with mSin3 corepressor proteins; its deletion converts Mnt from a repressor to an activator. Furthermore, wild-type Mnt suppresses Myc+Ras cotransformation of primary cells, whereas Mnt containing a SID deletion cooperates with Ras in the absence of Myc to transform cells. This suggests that Mnt and Myc regulate an overlapping set of target genes in vivo. When mnt is expressed as a transgene under control of the beta-actin promoter in mice the transgenic embryos exhibit a delay in development and die during mid-gestation, just when c- and N-Myc functions are critical. It is proposed that Mnt:Max:Sin3 complexes normally function to restrict Myc:Max activities associated with cell proliferation (Hurlin, 1997).

Interferons (IFNs) inhibit cell growth in a Stat1-dependent fashion that involves regulation of c-myc expression. IFN-gamma suppresses c-myc in wild-type mouse embryo fibroblasts, but not in Stat1-null cells, where IFNs induce c-myc mRNA rapidly and transiently, thus revealing a novel signaling pathway. Both tyrosine and serine phosphorylation of Stat1 are required for suppression. Induced expression of c-myc is likely to contribute to the proliferation of Stat1-null cells in response to IFNs. IFNs also suppress platelet-derived growth factor (PDGF)-induced c-myc expression in wild-type but not in Stat1-null cells. A gamma-activated sequence element in the promoter is necessary but not sufficient to suppress c-myc expression in wild-type cells. In PKR-null cells, the phosphorylation of Stat1 on Ser727 and transactivation are both defective, and c-myc mRNA is induced, not suppressed, in response to IFN-gamma. A role for Raf-1 in the Stat1-independent pathway is revealed by studies with geldanamycin, an HSP90-specific inhibitor, and by expression of a mutant of p50cdc37 that is unable to recruit HSP90 to the Raf-1 complex. Both agents abrogate the IFN-gamma-dependent induction of c-myc expression in Stat1-null cells (Ramana, 2000).

ROR alpha1 (Drosophila homolog Hormone receptor-like/Hr46) and RVR are orphan members of the superfamily of nuclear hormone receptors that constitutively activate and repress, respectively, gene transcription by binding to a common DNA sequence. A consensus binding site for ROR alpha1 and RVR is found in the first intron of the N-myc gene. This site is designated N-myc RORE (ROR response element). Unlike most of the intronic sequence, the region encompassing the N-myc RORE is highly conserved between human and mouse, underscoring its importance. ROR alpha1 and RVR specifically bind to the human and mouse N-myc ROREs and transactivate and transrepress, respectively, reporter constructs containing the ROREs. There is a direct modulation of an exogenously introduced N-myc gene by ROR alpha1 and RVR in COS-1 cells. This effect is mediated through the N-myc RORE, since mutation of this site abolishes the regulatory effects of both receptors. While transfection of ROR alpha1 in P19 embryonic carcinoma cells has no effect on the levels of endogenous N-myc mRNA, RVR down-regulates its expression. Mutation of the RORE increases the oncogenic potential of the N-myc gene. Concomitant expression of ROR alpha1 and wild-type N-myc results in a twofold increase in the number of transformed foci. These observations show that ablation of the RORE results in a more oncogenic form of N-myc and suggest that deregulation of the activity of the ROR alpha1 and RVR could contribute to the initiation and progression of certain neoplasias (Dussault, 1997).

The receptor-binding factor (RBF) for the avian oviduct progesterone (Pg) receptor (PR) has previously been shown to be a unique 10-kDa nuclear matrix protein that generates high affinity PR-binding sites on avian DNA. This paper describes the use of Southwestern blot and DNA gel shift analyses with RBF protein to identify a minimal 54-base pair RBF-binding element in the matrix-associated region (MAR) of the Pg-regulated c-myc gene promoter. This element contains a 5'-GC-rich domain and a 3'-AT-rich domain, the latter having a homopurine/homopyrimidine structure. The gel shift assays required the generation of an RBF-maltose fusion protein (RBF-MBP), which specifically binds this element and is supershifted when the anti-RBF polyclonal antibody is added. Computer analysis of the full-length amino acid sequence for RBF predicts a DNA-binding motif involving a beta-sheet structure at the N-terminal domain. Southern blot analyses using nuclear matrix DNA suggests that there are dual MAR sites in the c-myc promoter, which flank an intervening domain containing the RBF element. The co-transfection of this MAR sequence, containing the RBF element and cloned into a luciferase reporter vector, together with an RBF expression vector construct, into steroid treated human MCF-7 cells, results in a decrease of the c-myc promoter activity relative to control transfections containing only the parent vector of the RBF expression construct. These data suggest that a unique chromatin/nuclear matrix structure, composed of the RBF-DNA element complex, flanked by nuclear matrix attachment sites, serves to bind the PR and repress the c-myc promoter (Lauber, 1997).

The far-upstream element-binding protein (FBP) is one of several recently described factors which bind to a single strand of DNA in the 5' region of the c-myc gene. Although cotransfection of FBP increases expression from a far-upstream element-bearing c-myc promoter reporter, the mechanism of this stimulation has been heretofore unknown. Can a single-strand-binding protein function as a classical transactivator, or are these proteins restricted to stabilizing or altering the conformation of DNA in an architectural role? The carboxyl-terminal region (residues 448 to 644) of FBP is a potent transcriptional activation domain. This region contains three copies of a unique amino acid sequence motif containing tyrosine diads. Analysis of deletion mutants demonstrates that a single tyrosine motif alone (residues 609 to 644) is capable of activating transcription. The activation property of the C-terminal domain is repressed by the N-terminal 107 amino acids of FBP. These results show that FBP contains a transactivation domain that can function alone, suggesting that FBP contributes directly to c-myc transcription while bound to a single-strand site. Furthermore, activation is mediated by a new motif that can be negatively regulated by a repression domain of FBP (Duncan, 1996).

The proto-oncoprotein c-Myc and the multifunctional transcriptional regulator YY1 (Drosophila homolog: Pleiohomeotic) have been shown to interact directly in a manner that excludes Max from the complex. Since binding to Max is necessary for all known c-Myc activities, the influence of YY1 on c-Myc function has been analyzed. YY1 is shown to be a potent inhibitor of c-Myc transforming activity. The region in YY1 required for inhibition corresponds to a functional DNA-binding domain and is distinct from the domains necessary for direct binding to c-Myc. Furthermore the transactivation domain of YY1 was not necessary, suggesting that gene regulation by YY1, for example, through DNA bending or displacement of regulators from DNA, could be the cause for the negative regulation of c-Myc. This model of indirect regulation of c-Myc by YY1 is supported by the finding that although YY1 does not bind to the c-Myc transactivation domain (TAD) in vitro it is able to inhibit transactivation by Gal4-MycTAD fusion proteins in transient transfections. As for the inhibition of transformation, an intact DNA-binding domain of YY1 was necessary and sufficient for this effect. In addition, YY1 does not alter c-Myc/Max DNA binding, further supporting an indirect mode of action. These findings point to a role of YY1 as a negative regulator of cell growth with a possible involvement in tumor suppression (Austen, 1998).

Transcription activation and repression of eukaryotic genes are associated with conformational and topological changes of the DNA and chromatin, altering the spectrum of proteins associated with an active gene. Segments of the human c-myc gene possessing non-B structure in vivo were first located with probes that cleave single stranded DNA. Sites hypertensive to cleavage include the major promoters P1 and P2 of c-myc, as well as the far upstream sequence element (FUSE) and CT elements. These bind, respectively, the single-strand-specific factors FUSE-binding protein and heterogeneous nuclear ribonucleoprotein K in vitro. Active and inactive c-myc genes yield different patterns of S1 nuclease and permanganate sensitivity, indicating alternative chromatin configurations of active and silent genes. The melting of specific cis elements of active c-myc genes in vivo suggests that transcriptionally associated torsional strain might assist strand separation and facilitate factor binding. Therefore, the interaction of FUSE-binding protein and heterogeneous nuclear ribonucleoprotein K with supercoiled DNA was examined. Remarkably, both proteins recognize their respective elements torsionally strained but not as liner duplexes. Single-strand- or supercoil-dependent gene regulatory proteins may directly link alterations in DNA conformation and topology with changes in gene expression (Michelotti, 1996).

The CT element of the c-myc gene is required for promoter P1 usage and can drive expression of a heterologous promoter. Both double strand (Sp1) and single strand (hnRNP K) CT-binding proteins have been implicated as mediators of CT action. Although significant levels of CT activity persist following Sp1 immunodepletion, EGTA totally abolishes transactivation, thus implicating another metal requiring factor in CT element activity. Since hnRNP K binds to one strand of the CT element, but has no metal requirement, the opposite (purine-rich strand) was examined as a target for a metal-dependent protein. A zinc-requiring purine strand binding activity was identified as cellular nucleic acid binding protein (CNBP), a protein previously implicated in the regulation of sterol responsive genes. Two forms of CNBP differ in their relative binding to the CT- or sterol-response elements. CNBP is a bona fide regulator of the CT element by cotransfection of a CNBP expression vector that stimulates expression of a CT-driven (but not an AP1-dependent) reporter. These data suggest that hnRNP K and CNBP bind to opposite strands and co-regulate the CT element (Michelotti, 1995).

The far upstream element (FUSE) is required for proper expression of the human c-myc gene. FUSE-binding protein (FBP) binds the single-stranded far upstream element of active c-myc genes; it possesses potent transcription activation and repression domains, and is necessary for c-myc expression. The FUSE-binding protein (FBP) specifically recognizes this site and stimulates expression in a FUSE-dependent manner. The up and downregulation of c-myc and FBP are highly correlated, suggesting that FBP and c-myc transcription are linked in vivo. Moreover, interfering directly with the levels or activity of FBP extinguishes c-myc expression and arrests cell growth. FBP, first discerned from its primary structure, is a 644-amino acid protein possessing three domains. The central domain of the protein employs a set of four KH motifs to destabilize the double helix of FUSE and to bind sequence specifically with the noncoding strand. The carboxyl terminus of FBP (FBPC, amino acids 488-644) contains three copies of an unusual tyrosine-rich motif, which strongly activates transcription when fused with the GAL4 DNA-binding domain. In contrast, the amino terminus of FBP (FBPN) represses expression driven by FBPC as well as some, but not all, heterologous activators. A novel 60 kDa protein, the FBP interacting repressor (FIR), blocks activator-dependent, but not basal, transcription through TFIIH. Recruited through FBP's nucleic acid-binding domain, FIR forms a ternary complex with FBP and FUSE. FIR represses a c-myc reporter via the FUSE. The amino terminus of FIR contains an activator-selective repression domain capable of acting in cis or even in trans in vivo and in vitro. The repression domain of FIR targets only TFIIH's p89/XPB helicase, required at several stages in transcription, but not factors required for promoter selection. Thus, FIR locks TFIIH in an activation-resistant configuration that still supports basal transcription (Liu, 2000).

Can sequence specific single strand binding proteins find their cognate elements and modify transcription? Heterogeneous nuclear ribonucleoprotein K (hnRNP K) binds the single stranded sequence (CCCTCCCCA; CT-element) of the human c-myc gene in vitro. To monitor its DNA binding in vivo, the ability of hnRNP K to activate a reporter gene was amplified by fusion with the VP16 transactivation domain. This chimeric protein transactivates circular (but not linear) CT-element driven reporters, suggesting that hnRNP K recognizes a single strand region generated by negative supercoiling in circular plasmid. When CT-elements are engineered to overlap with lexA operators, addition of lexA protein, either in vivo or in vitro, abrogates hnRNP K binding most likely by preventing single strand formation. These results not only reveal hnRNP K to be a single strand DNA binding protein in vivo, but demonstrate how a segment of DNA may modify the transcriptional activity of an adjacent gene through the interconversion of duplex and single strands (Tomonaga, 1996).

beta-Catenin and gamma-catenin (plakoglobin), vertebrate homologs of Drosophila armadillo, function in cell adhesion and the Wnt signaling pathway. In colon and other cancers, mutations in the APC tumor suppressor protein or beta-catenin's amino terminus stabilize beta-catenin, enhancing its ability to activate transcription of Tcf/Lef target genes. Though beta- and gamma-catenin have analogous structures and functions and like binding to APC, evidence that gamma-catenin has an important role in cancer has been lacking. APC is shown in this study to regulate both beta- and gamma-catenin and gamma-catenin functions as an oncogene. In contrast to beta-catenin, for which only amino-terminal mutated forms transform RK3E epithelial cells, wild-type and several amino-terminal mutated forms of gamma-catenin have similar transforming activity. gamma-Catenin's transforming activity, like beta-catenin's, is dependent on Tcf/Lef function. However, in contrast to beta-catenin, gamma-catenin strongly activates c-Myc expression and c-Myc function is crucial for gamma-catenin transformation. These findings suggest APC mutations alter regulation of both beta- and gamma-catenin, perhaps explaining why the frequency of APC mutations in colon cancer far exceeds that of beta-catenin mutations. Elevated c-Myc expression in cancers with APC defects may be due to altered regulation of both beta- and gamma-catenin. Furthermore, the data imply beta- and gamma-catenin may have distinct roles in Wnt signaling and cancer via differential effects on downstream target genes (Kolligs, 2000).

The data presented here are the first to suggest that beta- and gamma-catenin may have differential effects on Tcf/Lef target genes. Specifically, it was found wild-type beta-catenin has a roughly twofold greater effect and S33Y mutated beta-catenin a roughly 15-fold greater effect than wild-type gamma-catenin in activating gene expression from a model promoter construct containing three Tcf-binding sites upstream of a minimal c-Fos promoter. In contrast, the ability of wild-type gamma-catenin to activate c-MYC reporter gene constructs is similar to that of S33Y beta-catenin. S33Y is a cancer-derived missense substitution in beta-catenin's presumptive GSK3beta phosphorylation sequences. gamma-Catenin activates endogenous c-Myc gene expression in RK3E cells more strongly than does the S33Y mutant beta-catenin protein. The underlying mechanisms for their differential effects on the reporter gene constructs and on endogenous c-Myc are not yet clear, though differences in the interactions of the distantly related amino- and carboxy-terminal domains of gamma- and beta-catenin with specific transcription factors, coactivators, and/or other chromatin-associated proteins are among the possible explanations. For instance, gamma-catenin may enhance or facilitate the binding of certain transcription factors to promoters, whereas beta-catenin may cooperate with other factors. The presence or absence of specific DNA-binding sites for certain transcription factors in regulatory elements of a particular Tcf/Lef-regulated target gene might account for its differential activation by beta- or gamma-catenin. Alternatively, beta- and gamma-catenin may differ in their ability to interact with certain chromatin remodeling proteins, some of which likely have differential effects on specific genes in vivo. Regardless of the particular mechanisms underlying their differential effects on c-Myc and potentially other target genes, the data presented here support the view that beta- and gamma-catenin are likely to have distinct but complementary roles in Wnt signaling and cancer development (Kolligs, 2000).

A prominent feature of cell differentiation is the initiation and maintenance of an irreversible cell cycle arrest with the complex involvement of the retinoblastoma (RB) family (RB, p130, p107). The HBP1 transcriptional repressor has been isolated as a potential target of the RB family in differentiated cells. By homology, HBP1 is a sequence-specific HMG transcription factor, of which LEF-1 (Drosophila homolog: Pangolin) is the best-characterized family member. Several features of HBP1 suggest an intriguing role as a transcriptional and cell cycle regulator in differentiated cells:

  1. Inspection of the HBP1 protein sequence revealed two consensus RB interaction motifs (LXCXE and IXCXE).
  2. HBP1 interaction is selective for RB and p130, but not p107. HBP1, RB, and p130 levels are all up-regulated with differentiation; in contrast, p107 levels decline.
  3. HBP1 can function as a transcriptional repressor of the promoter for N-MYC, which is a critical cell cycle and developmental gene.
  4. Because the activation of the N-MYC promoter in cycling cells required the E2F (See Drosophila E2F) transcription factor, E2F-1 and HBP1 represent opposite transcriptional signals that can be integrated within the N-MYC promoter.
  5. The expression of HBP1 leads to efficient cell cycle arrest. The arrest phenotype is manifested in the presence of optimal proliferation signals, suggesting that HBP1 exerts a dominant regulatory role.

Taken together, the results suggest that HBP1 may represent a unique transcriptional repressor with a role in initiation and establishment of cell cycle arrest during differentiation (Tevosian. 1997).

The adenomatous polyposis coli gene (APC) is a tumor suppressor gene that is inactivated in most colorectal cancers. Mutations of APC cause aberrant accumulation of beta-catenin, which then binds T cell factor-4 (Tcf-4), causing increased transcriptional activation of unknown genes. The c-MYC oncogene has been identified as a target gene in this signaling pathway. Expression of c-MYC is repressed by wild-type APC and activated by beta-catenin; these effects are mediated through Tcf-4 binding sites in the c-MYC promoter. These results provide a molecular framework for understanding the previously enigmatic overexpression of c-MYC in colorectal cancers (He, 1998).

The v-abl oncogene of Abelson murine leukemia virus encodes a deregulated form of the cellular nonreceptor tyrosine kinase. v-Abl activates c-myc transcription, and c-Myc is an essential downstream component in the v-Abl transformation program. To explore the mechanism by which v-Abl activates c-myc transcription, a cotransfection assay was developed. Transactivation of a c-myc promoter by v-Abl requires the SH1 (tyrosine kinase) and SH2 domains of v-Abl; the C-terminal domains are not required for transactivation. The assay also identifies the E2F site in the c-myc promoter as a v-Abl-responsive element. In addition, multimerized E2F sites were shown to be sufficient to confer v-Abl-dependent activation on a minimal promoter. This is the first identification of a v-Abl response element for transcriptional activation. v-Abl tyrosine kinase-dependent changes in proteins binding the c-myc E2F site have also been demonstrated, including induction of a complex containing DP1, p107, cyclin A, and cdk2. Identification of v-Abl-dependent changes in E2F-binding proteins provides an important link between v-Abl, transcription, cell cycle regulation, and control of cellular growth (Wong, 1995).

A novel human Polycomb homolog, hPc2, is more closely related to a Xenopus Pc homolog, XPc, than to a previously described human Pc homolog, CBX2 (hPc1). However, the hPc2 and CBX2/hPc1 proteins colocalize in interphase nuclei of human U-2 OS osteosarcoma cells, suggesting that the proteins are part of a common protein complex. To study the functions of the novel human Pc homolog, a mutant protein, delta hPc2, was generated, lacking an evolutionarily conserved C-terminal domain. This C-terminal domain is important for hPc2 function, since the delta hPc2 mutant protein that lacks the C-terminal domain is unable to repress gene activity. Expression of the delta hPc2 protein, but not of the wild-type hPc2 protein, results in cellular transformation of mammalian cell lines as judged by phenotypic changes, altered marker gene expression, and anchorage-independent growth. Specifically in delta hPc2-transformed cells, the expression of the c-myc proto-oncogene is strongly enhanced; serum deprivation results in apoptosis. In contrast, overexpression of the wild-type hPc2 protein results in decreased c-myc expression. These data suggest that hPc2 is a repressor of proto-oncogene activity and that interference with hPc2 function can lead to derepression of proto-oncogene transcription and subsequently to cellular transformation (Satijn, 1997).

Turnover of labile mRNAs is thought to be mediated in part by the interactions of trans-acting factors with elements withing the 3' untranslated region. Neuronal and non-neuronal cells established from neuroblastoma tumors differ in N-myc mRNA levels. There are two distinct regions within the 3'-UTR of N-myc mRNA that bind a 40kDA protein complex present in non-neuronal cells but absent from neuronal cells. The N-myc binding protein is identified as a member of the ELAV-like family of RNA-binding proteins (See Drosophila ELAV). It is likely that the ELAV-like mRNA-binding protein acts to stabilize the mRNA, and potentially regulates N-myc mRNA turnover (Chagnovich, 1996)

Mutation of the p53 tumor suppressor gene is the most common genetic alteration in human cancer, and tumors that express mutant p53 may be more aggressive and have a worse prognosis than p53-null cancers. Mutant p53 enhances tumorigenicity in the absence of a transdominant negative mechanism, and this tumor-promoting activity correlates with its ability to transactivate reporter genes in transient transfection assays. However, the mechanism by which mutant p53 functions in transactivation and its endogenous cellular targets that promote tumorigenicity are unknown. Mutant p53 is shown to be able to regulate the expression of the endogenous c-myc gene and is a potent activator of the c-myc promoter. Wild-type p53 normally represses p53. The region of mutant p53 responsiveness in the c-myc gene has been mapped to the 3' end of exon 1. The mutant p53 response region is position and orientation dependent and therefore does not function as an enhancer. Transactivation by mutant p53 requires the C terminus, which is not essential for wild-type p53 transactivation. These data suggest that it may be possible to selectively inhibit mutant p53 gain of function and consequently reduce the tumorigenic potential of cancer cells (Frazier, 1998).

Smad3 is a direct mediator of transcriptional activation by the TGFß receptor. Its target genes in epithelial cells include cyclin-dependent kinase inhibitors that generate a cytostatic reponse. This study defines how, in the same context, Smad3 can also mediate transcriptional repression of the growth-promoting gene c-myc. A complex containing Smad3, the transcription factors E2F4/5 and DP1, and the corepressor p107 preexists in the cytoplasm. In response to TGFbeta, this complex moves into the nucleus and associates with Smad4, recognizing a composite Smad-E2F site on c-myc for repression. Previously known as the ultimate recipients of cdk regulatory signals, E2F4/5 and p107 act here as transducers of TGFbeta receptor signals upstream of cdk. Smad proteins therefore mediate transcriptional activation or repression depending on their associated partners (Chen, 2002).

The liver is capable of completely regenerating itself in response to injury and after partial hepatectomy. In liver of old animals, the proliferative response is dramatically reduced, the mechanism for which is unknown. The liver specific protein, C/EBPalpha (see Drosophila Slbo), normally arrests proliferation of hepatocytes through inhibiting cyclin dependent kinases (cdks). Evidence that aging switches the liver-specific pathway of C/EBPalpha growth arrest to repression of E2F transcription. An age-specific C/EBPalpha-Rb-E2F4 complex has been identified that binds to E2F-dependent promoters and represses these genes. The C/EBPalpha-Rb-E2F4 complex occupies the c-myc promoter and blocks induction of c-myc in livers of old animals after partial hepatectomy. These results show that the age-dependent switch from cdk inhibition to repression of E2F transcription causes a loss of proliferative response in the liver because of an inability to induce E2F target genes after partial hepatectomy, providing a possible mechanism for the age-dependent loss of liver regenerative capacity (Iakova, 2003).

Rel/NF-kappaB transcription factors regulate the division and survival of B lymphocytes. B cells lacking NF-kappaB1 and c-Rel fail to increase in size upon mitogenic stimulation due to a reduction in induced c-myc expression. Mitogen-induced B cell growth, although not markedly impaired by FRAP/mTOR or MEK inhibitors, requires phosphatidylinositol 3-kinase (PI3K) activity. Inhibition of PI3K-dependent growth coincides with a block in the nuclear import of NF-kappaB1/c-Rel dimers and a failure to upregulate c-myc. In addition, PI3K has been shown to be necessary for a transcription-independent increase in c-Myc protein levels that accompanies mitogenic activation. Collectively, these findings establish a role for Rel/NF-kappaB signaling in the mitogen-induced growth of mammalian cells; such growth in B lymphocytes requires a PI3K/c-myc-dependent pathway (Grumont, 2003).

Neuronal precursor cells in the developing cerebellum require activity of the sonic hedgehog (Shh) and phosphoinositide-3-kinase (PI3K) pathways for growth and survival. Synergy between the Shh and PI3K signaling pathways are implicated in the cerebellar tumor medulloblastoma. A mechanism through which these disparate signaling pathways cooperate to promote proliferation of cerebellar granule neuron precursors is described. Shh signaling drives expression of mRNA encoding the Nmyc1 oncoprotein (previously N-myc), which is essential for expansion of cerebellar granule neuron precursors. The PI3K pathway stabilizes Nmyc1 protein via inhibition of GSK3-dependent Nmyc1 phosphorylation and degradation. The effects of PI3K activity on Nmyc1 stabilization are mimicked by insulin-like growth factor, a PI3K agonist with roles in central nervous system precursor growth and tumorigenesis. These findings indicate that Shh and PI3K signaling pathways converge on N-Myc to regulate neuronal precursor cell cycle progression. Furthermore, they provide a rationale for therapeutic targeting of PI3K signaling in medulloblastoma (Kenney, 2004).

Myc synergizes with Ras and PI3-kinase in cell transformation, yet the molecular basis for this behavior is poorly understood. Myc is shown to recruit TFIIH, P-TEFb and Mediator to the cyclin D2 and other target promoters, while the PI3-kinase pathway controls formation of the preinitiation complex and loading of RNA polymerase II. The PI3-kinase pathway involves Akt-mediated phosphorylation of FoxO transcription factors. In a nonphosphorylated state, FoxO factors inhibit induction of multiple Myc target genes, Myc-induced cell proliferation and transformation by Myc and Ras. Abrogation of FoxO function enables Myc to activate target genes in the absence of PI3-kinase activity and to induce foci formation in primary cells in the absence of oncogenic Ras. It is suggested that the cooperativity between Myc and Ras is at least in part due to the fact that Myc and FoxO proteins control distinct steps in the activation of an overlapping set of critical target genes (Bouchard, 2004).

Renal dysplasia, the major cause of childhood renal failure in humans, arises from perturbed renal morphogenesis and molecular signaling during embryogenesis. Induction of molecular crosstalk between Smad1 and ß-catenin occurs in the TgAlk3QD mouse model of renal medullary cystic dysplasia. The finding that Myc, a Smad and ß-catenin transcriptional target and effector of renal epithelial dedifferentiation, is misexpressed in dedifferentiated epithelial tubules provides a basis for investigating coordinate transcriptional control by Smad1 and ß-catenin in disease. Enhanced interactions occur between a molecular complex consisting of Smad1, ß-catenin and Tcf4 and adjacent Tcf- and Smad-binding regions located within the Myc promoter in TgAlk3QD dysplastic renal tissue, and Bmp-dependent cooperative control of Myc transcription by Smad1, ß-catenin and Tcf4. Analysis of nuclear extracts derived from TgAlk3QD and wild-type renal tissue revealed increased levels of Smad1/ß-catenin molecular complexes, and de novo formation of chromatin-associated Tcf4/Smad1 molecular complexes in TgAlk3QD tissues. Analysis of a 476 nucleotide segment of the 1490 nucleotide Myc genomic region upstream of the transcription start site demonstrated interactions between Tcf4 and the Smad consensus binding region and associations of Smad1, ß-catenin and Tcf4 with oligo-duplexes that encode the adjacent Tcf- and Smad-binding elements only in TgAlk3QD tissues. In collecting duct cells that express luciferase under the control of the 1490 nucleotide Myc genomic region, Bmp2-dependent stimulation of Myc transcription is dependent on contributions by each of Tcf4, ß-catenin and Smad1. These results provide novel insights into mechanisms by which interacting signaling pathways control transcription during the genesis of renal dysplasia (Hu, 2005)

Murine ES cells can be maintained as a pluripotent, self-renewing population by IL6 family members such as cytokine leukemia inhibitory factor (LIF) ---> STAT3-dependent signaling. The downstream effectors of this pathway have not been defined. A key target of the LIF self-renewal pathway was identified by showing that STAT3 directly regulates the expression of the Myc transcription factor. Murine ES cells express elevated levels of Myc and following LIF withdrawal, Myc mRNA levels collapse and Myc protein becomes phosphorylated on threonine 58 (T58), triggering its GSK3ß dependent degradation. Maintained expression of stable Myc (T58A) renders self-renewal and maintenance of pluripotency independent of LIF. By contrast, expression of a dominant negative form of Myc antagonizes self-renewal and promotes differentiation. Transcriptional control by STAT3 and suppression of T58 phosphorylation are crucial for regulation of Myc activity in ES cells and therefore in promoting self-renewal. Together, these results establish a mechanism for how LIF and STAT3 regulate ES cell self-renewal and pluripotency (Cartwright, 2005).

Although LIF/STAT3 signaling is crucial for murine ES cell maintenance, this pathway does not appear to have a role in human ES cell self-renewal, indicating the existence of alternate self-renewal mechanisms. A role has been defined for Wnt-dependent signaling in self-renewal of human and murine ES cells that functions independently of LIF and STAT3. Moreover, suppression of GSK3beta, an antagonist of Wnt signaling, is sufficient to maintain self-renewal and pluripotency of human and murine ES cells in the absence of LIF and Wnt. These observations signify a common mechanism of self-renewal that may be further applicable to adult stem cell populations that require Wnt-dependent signaling (Cartwright, 2005 and references therein).

Although LIF and Wnt promote self-renewal by activation of separate signaling pathways, it was reasoned that they would converge on a common target(s). It was hypothesized that Myc could be a common effector on which these signals converge because the Myc gene is a transcriptional target of STAT3 in a number of biological contexts, and signals transduced by Wnt can activate the Myc transcription through a ß-catenin/TCF-dependent mechanism. Myc belongs to a family of helix-loop-helix/leucine zipper transcription factors and together with its obligatory binding partner, Max, performs roles in control of cell proliferation, transformation, growth, differentiation and apoptosis. A potential role for Myc in ES cell maintenance is suggested by two reports. (1) Expression of an RLF/L-myc minigene that frequently arises from a chromosomal translocation event in human small lung carcinomas, delays ES cell differentiation and interferes with early embryonic development. (2) Elevated Myc activity is able to block the differentiation of multiple cell lineages. These lines of evidence prompted an investigation of whether Myc plays a role in ES cell self-renewal downstream of LIF and/or Wnt. This report shows that elevated Myc activity is required for ES cell maintenance and that Myc is a key effector of the LIF/STAT3 self-renewal pathway. The data indicate that signals transduced by LIF and possibly Wnt, converge on Myc to maintain ES cell identity (Cartwright, 2005).

Shh signaling induces proliferation of many cell types during development and disease, but how Gli transcription factors regulate these mitogenic responses remains unclear. By genetically altering levels of Gli activator and repressor functions in mice, it has been demonstrated that both Gli functions are involved in the transcriptional control of N-myc and Cyclin D2 during embryonic hair follicle development. The results also indicate that additional Gli-activator-dependent functions are required for robust mitogenic responses in regions of high Shh signaling. Through posttranscriptional mechanisms, including inhibition of GSK3-β activity, Shh signaling leads to spatially restricted accumulation of N-myc and coordinated cell cycle progression. Furthermore, a temporal shift in the regulation of GSK3-β activity occurs during embryonic hair follicle development, resulting in a synergy with β-catenin signaling to promote coordinated proliferation. These findings demonstrate that Shh signaling controls the rapid and patterned expansion of epithelial progenitors through convergent Gli-mediated regulation (Mill, 2005).

The APC tumor suppressor controls the stability and nuclear export of β-catenin (β-cat), a transcriptional coactivator of LEF-1/TCF HMG proteins in the Wnt/Wg signaling pathway. β-cat and APC have opposing actions at Wnt target genes in vivo. The β-cat C-terminal activation domain associates with TRRAP/TIP60 and mixed-lineage-leukemia (MLL1/MLL2) SET1-type chromatin-modifying complexes in vitro, and β-cat promotes H3K4 trimethylation at the c-Myc gene in vivo. H3K4 trimethylation in vivo requires prior ubiquitination of H2B, and ubiquitin is found necessary for transcription initiation on chromatin but not nonchromatin templates in vitro. Chromatin immunoprecipitation experiments reveal that β-cat recruits Pygopus, Bcl-9/Legless, and MLL/SET1-type complexes to the c-Myc enhancer together with the negative Wnt regulators, APC, and βTrCP. Interestingly, APC-mediated repression of c-Myc transcription in HT29-APC colorectal cancer cells is initiated by the transient binding of APC, βTrCP, and the CtBP corepressor to the c-Myc enhancer, followed by stable binding of the TLE-1 and HDAC1 corepressors. Moreover, nuclear CtBP physically associates with full-length APC, but not with mutant SW480 or HT29 APC proteins. It is concluded that, in addition to regulating the stability of β-cat, APC facilitates CtBP-mediated repression of Wnt target genes in normal, but not in colorectal cancer cells (Sierra, 2006).

The data presented here support a model in which the APC tumor suppressor functions directly to counteract β-cat-mediated transcription at Wnt target genes in vivo. This possibility was first suggested by the finding that full-length APC cycles on and off the c-Myc enhancer in conjunction with β-cat and associated coactivators in LiCl-treated C2C12 cells. In contrast, the enhancer complex appears to be stable and does not cycle in HT29 CRC cells, which contain a Class II APC mutant protein that is unable to degrade β-cat. Most strikingly, the binding of the full-length APC protein to the c-Myc gene in HT29-APC cells correlates with the rapid disassembly of the Wnt enhancer complex in vivo and the subsequent decline in steady-state c-Myc mRNA levels, both of which significantly precede the drop in β-cat protein levels that occurs as a result of proteolytic degradation in the cytoplasm. Thus, the effect of APC on c-Myc transcription appears to be immediate and direct, and may serve to coordinate the switch between the β-cat coactivator and TLE1 corepressor complexes (Sierra, 2006).

The β-cat enhancer complex includes the Wnt coactivators Pygopus and Bcl-9/Lgs, which control the retention of β-cat in the nucleus and may also function directly in transcription. The observation that APC can also regulate nuclear transport of β-cat raises the possibility that these factors may reside within a larger regulatory complex that chaperones β-cat in and out of the nucleus and mediates its release from the DNA. Indeed, sequential ChIP (re-ChIP) data indicate that the mutant APC in HT29 colorectal cancer cells exists in a stable complex with β-cat and LEF-1 at the active c-Myc gene. This finding is unexpected because β-cat cannot bind simultaneously to APC and LEF-1, and thus, if the full-length APC is part of a larger β-cat:LEF enhancer complex, it may interact with other subunits. Alternatively, the full-length APC and β-cat may exist in different complexes that rapidly exchange at the enhancer. The current data indicate that targeting is mediated by the N-terminal half of the APC protein, and that CtBP and βTrCP appear only in conjunction with the full-length APC protein. How APC is recruited to Wnt enhancers remains an open and important question (Sierra, 2006).

The ChIP experiments also suggest that APC-mediated inhibition of c-Myc transcription in HT29 cells occurs in two steps, initiated by transient binding of APC, βTrCP, CtBP, and YY1 to the enhancer, and followed by stable binding of the TLE-1 and HDAC1 corepressors. The transient recruitment of APC and CtBP, at the time when β-cat, Bcl-9, Pygo, and other Wnt enhancer factors leave the DNA, strongly suggests a role for these factors in the exchange of Wnt coactivator and corepressor complexes. In this respect it is interesting that CtBP was shown recently to associate with APC, both in vivo and in vitro. The results confirm a high-affinity interaction between CtBP and the full-length APC protein induced in HT29-APC cells, as well as with the native (full-length) APC protein in 293 cells. Consequently, APC may function to recruit CtBP to Wnt enhancers. Although both CtBP and TLE-1 are well-established corepressors of Wnt target genes, the different functions of the two types of corepressors remain unclear, and the ChIP data suggest that they act at distinct steps. Together, these data suggest that APC counteracts β-cat function in the nucleus, as well as in the cytoplasm, and may facilitate turnover of the enhancer complex at responsive genes by recruiting βTrCP and CtBP (Sierra, 2006).

Human acute T-cell lymphoblastic leukemias and lymphomas (T-ALL) are commonly associated with gain-of-function mutations in Notch1 that contribute to T-ALL induction and maintenance. Starting from an expression-profiling screen, c-myc was identified as a direct target of Notch1 in Notch-dependent T-ALL cell lines, in which Notch accounts for the majority of c-myc expression. In functional assays, inhibitors of c-myc interfere with the progrowth effects of activated Notch1, and enforced expression of c-myc rescues multiple Notch1-dependent T-ALL cell lines from Notch withdrawal. The existence of a Notch-c-myc signaling axis was bolstered further by experiments using c-myc-dependent murine T-ALL cells, which are rescued from withdrawal of c-myc by retroviral transduction of activated Notch1. This Notch1-mediated rescue is associated with the up-regulation of endogenous murine c-myc and its downstream transcriptional targets, and the acquisition of sensitivity to Notch pathway inhibitors. Additionally, this study shows that primary murine thymocytes at the DN3 stage of development depend on ligand-induced Notch signaling to maintain c-myc expression. Together, these data implicate c-myc as a developmentally regulated direct downstream target of Notch1 that contributes to the growth of T-ALL cells (Weng, 2006; full text of article).

Replication origin associated with myc: The BAH domain facilitates the ability of human Orc1 protein to activate replication origins in vivo

Selection of initiation sites for DNA replication in eukaryotes is determined by the interaction between the origin recognition complex (ORC) and genomic DNA. In mammalian cells, this interaction appears to be regulated by Orc1, the only ORC subunit that contains a bromo-adjacent homology (BAH) domain. Since BAH domains mediate protein-protein interactions, the human Orc1 BAH domain was mutated, and the mutant proteins expressed in human cells to determine their affects on ORC function. The BAH domain was not required for nuclear localization of Orc1, association of Orc1 with other ORC subunits, or selective degradation of Orc1 during S-phase. It does, however, facilitate reassociation of Orc1 with chromosomes during the M to G1-phase transition, and it is required for binding Orc1 to the Epstein-Barr virus oriP and stimulating oriP-dependent plasmid DNA replication. Moreover, the BAH domain affects Orc1's ability to promote binding of Orc2 to chromatin as cells exit mitosis. Thus, the BAH domain in human Orc1 facilitates its ability to activate replication origins in vivo by promoting association of ORC with chromatin (Noguchi, 2006).

Eukaryotic DNA replication initiates at a large number of chromosomal origins, controlled by the ordered assembly of multiprotein replication complexes and the cell cycle-dependent activity of kinases that phosphorylate them. In cases where origins have been transposed to other chromosomal locations, they have been found to colocalize with genetically defined replicators, i.e., sequences capable of promoting DNA replication at ectopic genomic sites. In metazoan systems, replication origins or replicators are bound by homologues of proteins first characterized for the yeast Saccharomyces cerevisiae, suggesting that the basic mechanisms controlling replication initiation are conserved among eukaryotes. In S. cerevisiae, replicators typically comprise a binding site for the hexameric origin recognition complex ORC and a DNA unwinding element (DUE). ORC enables the Cdc6-, Cdt1-dependent recruitment of the MCM helicase complex to replication origins, forming a prereplication complex (pre-RC) early during the G1 phase of the cell cycle. Cyclin-dependent kinase and DDK activities promote the binding of Mcm10, Cdc45, and RPA to form preinitiation complexes and unwind the DNA template in advance of replication. The effect of kinase activity on the pre-RC is partially to disassemble ORC and release MCMs and Cdc6 from chromatin (Noguchi, 2006 and references therein).

The 2.4-kb 5' region of the human c-myc gene contains multiple transcription factor binding sites and a DUE that is unwound in vivo. The DUE is situated in a 100-bp zone containing three 10/11 matches to the S. cerevisiae ARS consensus sequence. It was initially reported that replication initiates in this region, and quantitative PCR (qPCR) has been used to define the replication initiation zone. Subsequent work has confirmed that replication initiates in the 5' flanking DNA of the c-myc gene in multiple species. The 2.4-kb c-myc core origin endows plasmids with ARS activity in vitro and shows replicator activity when moved to an ectopic chromosomal location. This region displays an ordered chromatin structure stable to chromosomal translocation, and mutational analyses have identified regions of the replicator essential for replication initiation, including the DUE (Noguchi, 2006 and references therein).

Chromatin immunoprecipitation (ChIP) was used in this work to show that the human analogs of the yeast ORC, MCM, and Cdc6 proteins bind preferentially and selectively to the c-myc replicator. The distributions of Mcm3 and Mcm7 are similar in asynchronous cells, with the greatest ChIP signal at, and upstream of, the DNA unwinding element. These distributions change in parallel in cells synchronized in G1 or M phases. By contrast, Orc1, Orc2, and Cdc6 appear to be least abundant at the DUE and each displays a different temporal pattern of replicator binding. The DNA unwinding element binding protein DUE-B, identified using the c-myc DUE as bait in a yeast one-hybrid assay, preferentially binds near the c-myc DUE in a pattern comparable to that of the MCMs in asynchronous and G1-phase cells. Furthermore, at an ectopic locus, c-myc replicator deletions that removed the DUE or altered chromatin structure suppressed DUE-B or Mcm3 binding, respectively, and eliminated origin activity. The relationship between chromatin structure, MCM binding, and origin activity is supported by the demonstration that inhibition of histone deacetylase activity by trichostatin A (TSA) causes a redistribution of Mcm3 binding similar to the broadening of the c-myc replication initiation zone. These results suggest that pre-RC proteins bind nonrandomly to the c-myc replicator and that c-myc origin activity is a function of ORC, MCM, Cdc6, and DUE-B binding to c-myc chromatin (Noguchi, 2006).

Skp2 regulates Myc protein degradation and acts as a transcriptional coactivator of Myc

Myc is an oncoprotein transcription factor that plays a prominent role in cancer. Like many transcription factors, Myc is an unstable protein that is destroyed by ubiquitin (Ub)-mediated proteolysis. The oncoprotein and Ub ligase Skp2 regulate Myc ubiquitylation and stability. Because of the growing number of Ub ligases that function as transcriptional coactivators, it has been speculated that Skp2 might also regulate Myc's transcriptional activity. Consistent with this model, Skp2 has been shown to be a transcriptional coactivator for Myc, recognizing an essential element within the Myc activation domain and activating Myc target genes. These data suggest that Skp2 functions to connect Myc activity and destruction, and reveal an unexpected oncoprotein connection that may play an important role in controlling cell growth in normal and cancer cells (Kim, 2003).

The ability of Skp2 to stimulate the transcriptional activity of Myc reveals a previously unanticipated function for Skp2 -- regulation of gene expression. This activity places Skp2 in an emerging group of Ub ligases that are transcriptional coactivators and suggests that one way in which Skp2 regulates cell growth is via transcriptional control of Myc and perhaps other transcription factors. In this regard, it is interesting that Skp2 also targets the transcription factor E2F-1 for destruction. It has been proposed that Skp2-mediated destruction of E2F-1 allows cells to exit from S phase, but, on the basis of these findings, it is tempting to speculate that Skp2 may also stimulate E2F's transcriptional activity. Interestingly, the Skp2-E2F-1 interaction may also be phosphorylation independent, although there is no obvious homology between the Skp2-interacting sites on E2F-1 and Myc (Kim, 2003 and references therein).

It has been argued that Skp2 controls cell proliferation through its ability to target destruction of the CDK inhibitor p27. This, however, cannot be the only essential function of Skp2 in mammalian cell growth control, because although Skp2 collaborates with Ras to induce cellular transformation, Ras alone will not transform p27-deficient fibroblasts. The observation that Skp2 stimulates Myc transcriptional activity reveals a second pathway through which Skp2 controls cell growth. It is suggested that, as cells approach S phase, increasing levels of Skp2 not only target destruction of p27 but also serve to transiently activate the Myc protein. The transient activation of Myc synergizes with p27 downregulation to enforce the commitment of cells to enter S phase. As the cell cycle proceeds and Skp2 levels drop, the self-limiting action of activator licensing results in Myc destruction and attenuation of the signal to proliferate (Kim, 2003).

It is suggested that the ability of Skp2 to both activate Myc and destroy p27 is likely to have a significant role in the development of cancer. It is intriguing to note that loss of p27 has been shown to cooperate with Myc overexpression to drive lymphomagenesis in mice, suggesting that p27 can antagonize Myc function. Perhaps, therefore, one reason why Skp2 is overexpressed in cancer is that it confers a unique growth advantage, not only stimulating Myc's transcriptional activity but at the same time destroying a potential inhibitor of Myc function (Kim, 2003).

The transcription regulatory oncoprotein c-Myc controls genes involved in cell growth, apoptosis, and oncogenesis. c-Myc is turned over very quickly through the ubiquitin/proteasome pathway. Skp2 is shown to interact with c-Myc and participates in c-Myc ubiquitylation and degradation. The interaction between Skp2 and c-Myc occurs during the G1 to S phase transition of the cell cycle in normal lymphocytes. Surprisingly, Skp2 enhances c-Myc-induced S phase transition and activates c-Myc target genes in a Myc-dependent manner. Further, Myc-induced transcription is Skp2 dependent, suggesting interdependence between c-Myc and Skp2 in activation of transcription. Moreover, Myc-dependent association of Skp2, ubiquitylated proteins, and subunits of the proteasome to a c-Myc target promoter has been demonstrated in vivo. The results suggest that Skp2 is a transcriptional cofactor for c-Myc and indicate a close relationship between transcription activation and transcription factor ubiquitination (von der Lehr, 2003).

In what way could E3 ligase activity stimulate c-Myc-induced transcription? One possibility is that SCFSkp2 ubiquitylates and degrades negative regulators of transcription at the promoter. This could also be part of an autoregulatory loop, where the Myc activator protein needs to be eliminated at some step in order to complete the transcription cycle. Another possibility is that ubiquitin modifications of c-Myc or other substrates at the promoter play a nonproteolytic function in, for instance, protein-protein interactions of importance for transcription. It remains to be determined whether degradation of c-Myc is a necessary step for activation of transcription. This general model has been proposed in the 'licensing' hypothesis, linking transcription factor activity to their destruction in order to maintain stringent control of transcription activation in cells (von der Lehr, 2003).

Cerebellar granule cells are the most abundant neurons in the brain, and granule cell precursors (GCPs) are a common target of transformation in the pediatric brain tumor medulloblastoma. Proliferation of GCPs is regulated by the secreted signaling molecule Sonic hedgehog (Shh), but the mechanisms by which Shh controls proliferation of GCPs remain inadequately understood. DNA microarrays have been used to identify targets of Shh in these cells; Shh was found to activate a program of transcription that promotes cell cycle entry and DNA replication. Among the genes most robustly induced by Shh are cyclin D1 and N-myc. N-myc transcription is induced in the presence of the protein synthesis inhibitor cycloheximide, so it appears to be a direct target of Shh. Retroviral transduction of N-myc into GCPs induces expression of cyclin D1, E2F1, and E2F2, and promotes proliferation. Moreover, dominant-negative N-myc substantially reduces Shh-induced proliferation, indicating that N-myc is required for the Shh response. Finally, cyclin D1 and N-myc are overexpressed in murine medulloblastoma. These findings suggest that cyclin D1 and N-myc are important mediators of Shh-induced proliferation and tumorigenesis (Oliver, 2003).


Table of contents


diminutive: Biological Overview | Regulation | Developmental Biology | Effects of Mutation | References

Home page: The Interactive Fly © 1995, 1996 Thomas B. Brody, Ph.D.

The Interactive Fly resides on the
Society for Developmental Biology's Web server.