Retinoblastoma-family protein


EVOLUTIONARY HOMOLOGS


Table of contents

Promoter structure and transcriptional regulation of retinoblastoma genes

Two oncogenic point mutations present in the RB gene promoter region are found at consensus Sp1 and ATF sites, respectively, and in two separate hereditary RB families. However, Sp1 protein does not bind to the Sp1 site; this indicates that the Sp1 consensus site mutation is blocking the action of an alternative transcription factor, which has been called RBF-1 (retinoblastoma binding factor-1). Subsequent purification of RBF-1 reveals it to be hGABP/E4TF1, a transactivator from the adenovirus early-region 4 promoter. The effects of hGABP/E4TF1 were examined on transactivation of the RB gene promoter through the RBF-1 site. As expected, hGABP/E4TF1 enhances the core RB promoter activity, whereas it does not stimulate a mutant RBF-1 site. It is concluded that the most essential transcription factor in the human RB gene is likely to be hGABP/E4TF1 (Sowa, 1997).

The complete intron-exon organization of human Rb2/p130 has been elucidated. The gene contains 22 exons spanning over 50 kb of genomic DNA. The length of individual exons ranges from 65 to 1517 bp. The largest intron spans over 9 kb; the smallest has only 82 bp. The 5' flanking region reveals a structural organization characteristic of promoters of "housekeeping" and growth control-related genes. A typical TATA or CAAT box is not present, but there are several GC boxes and potential binding sites for numerous transcription factors. This study provides a molecular basis for understanding the transcriptional control of the Rb2/p130 gene and for implementing a comprehensive Rb2/p130 mutation screen using genomic DNA as a template (Baldi, 1996).

Retinoblastoma proteins associate with and are targeted by cyclin/cdks: the role of phosphorylation in regulation of RB activity and cell cycle arrest

Mammalian retinoblastoma tumor suppressor protein, pRB, is inactivated by phosphorylation. While there exists strong evidence suggesting that such phosphorylation is mediated by one or more cyclin-dependent kinases (CDKs) active during G1/S, it remains unclear which of the various CDKs is responsible. Three candidate pRB-inactivating kinases [CDK4-cyclin D1, CDK2-cyclin E (See Drosophila Cyclin E), and CDK2-cyclin A (See Drosophila Cyclin A)] phosphorylate pRB differentially, each on a subset of authentic pRB phosphorylation sites. Notably, two neighboring pRB phosphate acceptors, threonine 821 and threonine 826, which have previously been implicated in the regulation of LXCXE protein binding, are phosphorylated by different CDKs. Phosphorylation by either CDK2-cyclin A, which phosphorylates T821, or CDK4-cyclin D1, which phosphorylates threonine 826, can disable pRB for subsequent binding of an LXCXE protein. However, only one of these two kinases, CDK2-cyclin A, can dissociate a pre-existing LXCXE protein-pRB complex. Prior binding of an LXCXE protein blocks access to certain residues specifically targeted by CDK4-cyclin D1, explaining the inability of this kinase to resolve such complexes. While these results are not direct proof of the relevance of differential pRB phosphorylation in cells, these findings support a model whereby full phosphorylation of pRB may require the action of more than one kinase and explains how such differential phosphorylation by different CDKs might translate into a differential regulation of downstream effector pathways (Zarkowska, 1997).

Stable association of certain proteins, such as E2F1 and p21, with cyclin-cdk2 complexes is dependent on a conserved cyclin-cdk2 binding motif that contains the core sequence ZRXL, where Z and X are usually basic. In vitro phosphorylation of the retinoblastoma tumor suppressor protein, pRB, by cyclin A-cdk2 and cyclin E-cdk2 is inhibited by a short peptide spanning the cyclin-cdk2 binding motif present in E2F1. Examination of the pRB C terminus reveals that it contains sequence elements related to ZRXL. Site-directed mutagenesis of one of these sequences, beginning at residue 870, impairs the phosphorylation of pRB in vitro. A synthetic peptide spanning this sequence also inhibits the phosphorylation of pRB in vitro. pRB C-terminal truncation mutants lacking this sequence are hypophosphorylated in vitro and in vivo, despite the presence of intact cyclin-cdk phosphoacceptor sites. Phosphorylation of such mutants is restored by fusion to the ZRXL-like motif derived from pRB or to the ZRXL motifs from E2F1 or p21. Phospho-site-specific antibodies reveal that certain phosphoacceptor sites strictly require a C-terminal ZRXL motif, whereas at least one site does not. Furthermore, this residual phosphorylation is sufficient to inactivate pRB in vivo, implying that there are additional mechanisms for directing cyclin-cdk complexes to pRB. Thus, the C terminus of pRB contains a cyclin-cdk interaction motif of the type found in E2F1 and p21 that enables it to be recognized and phosphorylated by cyclin-cdk complexes (Adams, 1999).

The retinoblastoma protein (pRb) acts to constrain the G1-S transition in mammalian cells. Phosphorylation of pRb in G1 inactivates its growth-inhibitory function, allowing for cell cycle progression. Phosphorylation of S780 results in a lose of Rb's ability to bind to E2F. Phosphorylation of S807 and/or S811 is required to abolish Rb binding to c-Abl, while modification of threonine 821 and or T826 is required to abolish Rb binding to LXCXE-containing proteins such as simian virus 40 large T antigen. Although several cyclins and associated cyclin-dependent kinases (cdks) have been implicated in pRb phosphorylation, the precise mechanism by which pRb is phosphorylated in vivo remains unclear. By selectively inhibiting either cdk4/6 (Drosophila homolog: Cyclin-dependent kinase 4/6) or cdk2, it has been shown that endogenous D-type cyclins, acting with cdk4/6, are able to phosphorylate pRb only partially, a process that is likely to be completed by cyclin E-cdk2 complexes. Cyclin E-cdk2 is unable to phosphorylate pRb in the absence of prior phosphorylation by cyclin D-cdk4/6 complexes. Complete phosphorylation of pRb, inactivation of E2F binding, and activation of E2F transcription occur only after the sequential action of at least two distinct G1 cyclin kinase complexes (Lundberg, 1998).

In cycling cells, the retinoblastoma protein (pRb) is un- and/or hypo-phosphorylated in early G1 and becomes hyper-phosphorylated in late G1. The role of hypo-phosphorylation and identity of the relevant kinase(s) remains unknown. Hypo-phosphorylated pRb associates with E2F in vivo and is therefore active. Increasing the intracellular concentration of the Cdk4/6 specific inhibitor p15(INK4b) by transforming growth factor beta treatment of keratinocytes results in G1 arrest and loss of hypo-phosphorylated pRb with an increase in unphosphorylated pRb. Conversely, p15(INK4b)-independent transforming growth factor beta-mediated G1 arrest of hepatocellular carcinoma cells results in loss of Cdk2 kinase activity with continued Cdk6 kinase activity and pRb remains only hypo-phosphorylated. Introduction of the Cdk4/6 inhibitor p16(INK4a) protein into cells by fusion to a protein transduction domain also prevents pRb hypo-phosphorylation with an increase in unphosphorylated pRb. It is concluded that cyclin D:Cdk4/6 complexes hypo-phosphorylate pRb in early G1 allowing continued E2F binding (Ezhevsky, 1997).

The retinoblastoma tumor suppressor protein, RB, contains at least three distinct protein binding domains. The A/B pocket binds proteins with the LXCXE motif; the C pocket binds the nuclear c-Abl tyrosine kinase, and the large A/B pocket binds the transcription factor E2F (See Drosophila E2F). Dissociation of RB from its targets is observed as RB becomes phosphorylated during G1/S progression. There are 16 Cdk consensus phosphorylation sites in RB. It was previously unknown whether the many phosphorylation sites had redundant or distinct functions in the regulation of RB. Using RB mutant proteins lacking specific phosphorylation sites, it has been shown that each of the binding domains is inhibited by different sites. Thr-821/826 phosphorylation is required to inhibit the binding to LXCXE containing proteins. Mutation of these two sites does not interfere with the hyperphosphorylation of RB. However, this phosphorylated mutant retains the ability to bind T-Ag, E7, and Elf-1, all of which contain the LXCXE motif. In contrast, Ser-807/811 phosphorylation is required to disrupt c-Abl binding. Mutation of Ser-807/811 and Thr-821/826 does not abolish the regulation of E2F binding. Taken together, these results show that the protein binding domains of RB are each regulated by distinct Cdk phosphorylation sites (Knudsen, 1996).

p107 is a retinoblastoma protein-related phosphoprotein that, when overproduced, displays a growth inhibitory function. It interacts with and modulates the activity of the transcription factor E2F-4. p107 physically associates with cyclin E-CDK2 (See Drosophila Cyclin E) and cyclin A-CDK2 complexes in late G1 and at G1/S, respectively, an indication that cyclin-dependent kinase complexes may regulate, contribute to, and/or benefit from p107 function during the cell cycle. These results show that p107 phosphorylation begins in mid G1 and proceeds through late G1 and S and that cyclin D-associated kinase(s) contributes to this process. E2F-4 also binds selectively to hypophosphorylated p107; G1 cyclin-dependent p107 phosphorylation leads to the dissociation of p107-E2F-4 complexes as well as inactivation of p107 G1 blocking function (Xiao, 1996).

Overexpression of human cyclin E shortens G1, causing a premature entry into S. The retinoblastoma protein is a target for the cyclin E-cdk2 complex. Coexpression of Rb with cyclin E induces Rb hyperphosphorylation and overrides the ability of Rb to suppress G1 exit. Hypophosphorylated Rb can interact with the transcription factor E2F during G1; this complex can then bind to DNA and repress transcription of E2F target genes. Conversely, hyperphosphorylation of Rb prevents its interaction with E2F, releasing E2F from an inhibitory constraint and enabling it to promote gene expression (Sherr, 1993 and references).

The Retinoblastoma-related protein p107, like the p21 family of cdk inhibitors, can inhibit the phosphorylation of target substrates by cyclin A/cdk2 and cyclin E/cdk2 complexes. The associations of p107 and p21 with cyclin/cdk2 rely on a structurally and functionally related interaction domain. Interactions between p107 and p21 are mutually exclusive: p21 causes a dissociation of p107/cyclin/cdk2 complexes to yield p21/cyclin/cdk2 complexes. The activation of the p107-bound cyclin/cdk kinases leads to dissociation of p107 from the transcription factor E2F. It has been suggested that p107 functions similarly to Rb, causing growth arrest of sensitive cells in the G1 phase of the cell cycle. The p107 molecule can be dissected into two domains, either of which is able to independently block cell cycle progression. One domain corresponds to the sequences needed for interaction with transcription E2F, and the other corresponds to the interaction domain for cyclin A or cyclin E complexes (Zhu, 1995 a and b).

The retinoblastoma (pRB) family of proteins includes three proteins known to suppress growth of mammalian cells. Growth suppression by two of these proteins, p107 and p130, could result from the inhibition of associated cyclin-dependent kinases (cdks). One important unresolved issue, however, is the mechanism by which inhibition occurs. In vivo and in vitro evidence suggests that p107 is a bona fide inhibitor of both cyclin A-cdk2 and cyclin E-cdk2. p107 exhibits an inhibitory constant (Ki) comparable to that of the cdk inhibitor p21/WAF1. In contrast, pRB is unable to inhibit cdks. Further reminiscent of p21, a second cyclin-binding site was mapped to the amino-terminal portions of p107 and p130. This amino-terminal domain is capable of inhibiting cyclin-cdk2 complexes, although it is not a potent substrate for these kinases. In contrast, a carboxy-terminal fragment of p107 that contains the previously identified cyclin-binding domain serves as an excellent kinase substrate although it is unable to inhibit either kinase. Clustered point mutations suggest that the amino-terminal domain is functionally important for cyclin binding and growth suppression. Moreover, peptides spanning the cyclin-binding region are capable of interfering with p107 binding to cyclin-cdk2 complexes and kinase inhibition. The ability to distinguish between p107 and p130 as inhibitors rather than simple substrates suggests that these proteins may represent true inhibitors of cdks (Castano, 1998).

p107 and p130 immune complexes exhibit kinase activity. These immune complexes were tested with four substrates commonly utilized to assay Cdk activity, including all three known members of the retinoblastoma family. Kinase activity can be abolished by removal of either cyclin A or Cdk2 but is unaffected by removal of Cdk4 or any D-type cyclin. The appearance of p107 associated activity follows the accumulation of p107 protein. In contrast, the kinase activity associated with p130 immune complexes becomes apparent after mid-G1, coincident with p130 hyperphosphorylation. GST-Rb, GST-p107, and GST-p130 (where GST indicates glutathione S-transferase) are equally suitable substrates in p107 and p130 immune complex kinase assays, yielding activity equal to 25% of the cyclin A activity present. The p107 and p130 associated activity is unable to phosphorylate histone H1, suggesting the p107 and p130 associated cyclin A/Cdk2 may represent a distinct pool with a distinct substrate specificity. The p107 and p130 associated activity is released from the immune complexes upon incubation with ATP and Mg2+ and exhibits the same substrate preference observed with the untreated immune complex. These data suggest that p107 and p130 recognize, or form by association, a distinct pool of cyclin A/Cdk2 that preferentially phosphorylates retinoblastoma family members (Hauser, 1997).

Complexes of the cyclin-dependent kinase, cdk4, and each of three different D-type cyclins phosphorylate the Retinoblastoma protein. Cyclins D2 and D3 but not D1 bind Rb in intact cells. Introduction of cdk4, together with Rb and D-type cyclins, induces Rb hyperphosphorylation and dissociation of cyclins D2 and D3. The transcription factor E2F-1 also binds Rb, and coexpression of the cyclin D-cdk4 complex triggers Rb phosphorylation and prevents its interaction with E2F-1. Thus D-type cyclins play a dual role as cdk4 regulatory subunits and as adaptor proteins that physically target active enzyme complexes to particular substrates (Kato, 1993).

The pRB-related proteins p107 and p130 are thought to suppress growth, partially through their associations with transcription factor E2F and two important cell cycle kinases: cyclin A-cdk2 and cyclin E-cdk2. Although each protein plays a critical role in cell proliferation, the functional consequences of the association among growth suppressor, cyclin-dependent kinase, and transcription factor have remained elusive. In an attempt to understand the biochemical properties of such complexes, each of the p130-cyclin-cdk2 and p107-cyclin-cdk2 complexes found in vivo were reconstituted with purified, recombinant proteins. Strikingly, stoichiometric association of p107 or p130 with either cyclin E-cdk2 or cyclin A-cdk2 negates the activities of these kinases. The results of these experiments suggest that inhibition does not result from substrate competition or loss of cdk2 activation. Kinase inhibitory activity is dependent upon an amino-terminal region of p107 that is highly conserved with p130. A role for this amino-terminal region in growth suppression is uncovered by using p107 mutants unable to bind E2F. To determine whether cellular complexes might display similar regulatory properties, p130-cyclin A-cdk2 complexes were purified from human cells. Such complexes are found to exist in two forms: one that contains E2F-4-DP-1, and one that lacks the heterodimer. These endogenous complexes behave like in vitro-reconstituted complexes, exhibiting low levels of associated kinase activity that could be significantly augmented by dissociation of p130. These results suggest a mechanism whereby p130 and p107 suppress growth by inhibiting important cell cycle kinases (Woo, 1997).

Cyclin E is necessary and rate limiting for the passage of mammalian cells through the G1 phase of the cell cycle. Control of cell cycle progression by cyclin E involves cdk2 kinase, which requires cyclin E for catalytic activity. Expression of cyclin E/cdk2 leads to an activation of cyclin A gene expression, as monitored by reporter gene constructs derived from the human cyclin A promoter. Promoter activation by cyclin E/cdk2 requires an E2F binding site in the cyclin A promoter. Cyclin E/cdk2 kinase can directly bind to E2F/p107 complexes formed on the cyclin A promoter-derived E2F binding site; this association is controlled by p27KIP1, most likely through direct protein-protein interaction. These observations suggest that cyclin E/cdk2 associates with E2F/p107 complexes in late G1 phase, once p27KIP1 has decreased below a critical threshold level. Since a kinase-negative mutant of cdk2 prevents promoter activation, it appears that transcriptional activation of the cyclin A gene requires an active cdk2 kinase tethered to its promoter region (Zerfass-Thome, 1997).

The retinoblastoma tumour-suppressor protein, a regulator of G1 exit, functionally links Ras to passage through the G1 phase. Inactivation of Ras in cycling cells causes a decline in cyclin D1 protein levels, accumulation of the hypophosphorylated, growth-suppressive form of Rb and G1 arrest. When Rb is disrupted either genetically or biochemically, cells fail to arrest in G1 following Ras inactivation. In contrast, inactivation of Ras in quiescent cells prevents growth-factor induction of both immediate-early gene transcription and exit from G0 in an Rb-independent manner. It is suggested that the Ras pathway regulates the expression of cyclin D1 protein, which in turn targets Rb, resulting in Rb phosphorylation and consequently in Rb inactivation, thereby provoking exit from G1 (Peeper, 1997).

Transforming growth factor-beta1 (TGF-beta1) is a potent inhibitor of hematopoietic cell growth. TGF-beta1 signals inhibition of IL-3-dependent 32D-123 murine myeloid cell growth by modulating the activities of cyclin E and cyclin-dependent kinase 2 (cdk2) proteins and their complex formation in the G1 phase of the cell cycle. Whereas the cyclin E protein is hyperphosphorylated in TGF-beta1 treated cells, TGF-beta1 decreases both the phosphorylation of cdk2 and the kinase activity of the cyclin E-cdk2 complex. Decreased cyclin E-cdk2 kinase activity correlates with decreased phosphorylation of the retinoblastoma-related protein p107. In support of these observations, transient overexpression of p107 inhibits the proliferation of the myeloid cells, and expression of antisense oligodeoxynucleotides to p107 mRNA blocks TGF-beta1 inhibition of myeloid cell growth. In 32D-123 TGF-beta1 treated cells, c-Myc protein expression is decreased. TGF-beta1 increases the binding of p107 to the transcription factor E2F, leading to decreased c-Myc protein levels. p107 inhibits E2F transactivation activity and is also found to bind the c-Myc protein, suggesting p107 negative regulation of c-Myc protein function. These studies demonstrate the modulation of p107 function by TGF-beta1 and suggest a novel mechanism by which TGF-beta1 blocks cell cycle progression in myeloid cells (Bang, 1996).

Does the inability of p53 to induce G1 arrest after the restriction point relate to an inability to modulate pRb phosphorylation? Transient p53 overexpression in normal human diploid fibroblasts and p53-deficient cancer cells leads to increased levels of the cyclin-dependent kinase inhibitor p21 cip1/Waf1/Sdi1 and an accumulation of hypophosphorylated pRb in cells growing asynchronously and in cells synchronized in late G1 or M. Similarly, gamma-irradiation of asynchronous, late-G1, or S phase fibroblasts leads to an increase in hypophosphorylated pRb. Experiments with fibroblasts expressing the HPV16 E6 protein indicate that accumulation of hypophosphorylated pRb requires functional p53. Progression into and through S phase is not altered by the presence of hypophosphorylated pRb in late G1, consistent with the failure of p53 to mediate G1 arrest in cells that are past the restriction point. These data indicate that accumulation of hypophosphorylated pRb has significantly different effects on cell cycle progression in early G1 versus late G1 or S phase (Linke, 1997).

In mammalian cells, the retinoblastoma protein (Rb) is thought to negatively regulate progression through the G1 phase of the cell cycle by its association with the transcription factor E2F. Rb-E2F complexes suppress transcription of genes required for DNA synthesis; the prevailing view is that phosphorylation of Rb by complexes of cyclin-dependent kinases (Cdks) and their regulatory cyclin subunits, and the subsequent release of active E2F, is required for S-phase entry. This view is based, in part, on the fact that ectopic expression of cyclin-Cdks leads to Rb phosphorylation and that this modification correlates with S-phase entry. In Drosophila, however, cyclin E expression can bypass a requirement for E2F, suggesting that cyclins may activate replication independent of the Rb/E2F pathway. Is Rb phosphorylation a prerequisite for S-phase entry in Rb-deficient SAOS-2 osteosarcoma cells? This was examined, employing a commonly used cotransfection assay. A G1 arrest in SAOS-2 cells mediated by an Rb mutant lacking all 14 consensus Cdk phosphorylation sites is bypassed by coexpressing G1-specific E-type or D-type cyclin-Cdk complexes; injection of purified cyclin-Cdks during G1 accelerates S-phase entry. These results indicate that Rb phosphorylation is not essential for S-phase entry when G1 cyclin-Cdks are overexpressed, and that other substrates of these kinases can be rate-limiting for the G1 to S-phase transition. These data also reveal that the SAOS-2 cotransfection assay is complicated by Rb-independent effects of the coexpressed Cdks (Leng, 1997).

Evidence is presented that phosphorylation of the C-terminal region of Rb by Cdk4/6 initiates successive intramolecular interactions between the C-terminal region and the central pocket. The initial interaction displaces histone deacetylase from the pocket, blocking active transcriptional repression by Rb. This facilitates a second interaction that leads to phosphorylation of the pocket by Cdk2 and disruption of pocket structure. These intramolecular interactions provide a molecular basis for sequential phosphorylation of Rb by Cdk4/6 and Cdk2. Cdk4/6 is activated early in G1, blocking active repression by Rb. However, it is not until near the end of G1, when cyclin E is expressed and Cdk2 is activated, that Rb is prevented from binding and inactivating E2F (Harbour, 1999).

G0 is a physiological state occupied by resting or terminally differentiated cells that have exited the cell cycle. In contrast to the well-characterized cyclin/cdk-mediated inactivation of pRb that controls the G1/S transition, little is known about regulation of the G0/G1 transition. However, pRb is likely to participate in this process because its acute somatic inactivation is sufficient for G0-arrested cells to reenter the cell cycle. One physiological regulator of this event may be cyclin C because its highest mRNA levels occur during G0 exit. A non-cdk8-associated cellular pool of cyclin C combines with cdk3 to stimulate pRb phosphorylation at S807/811 during the G0/G1 transition, and this phosphorylation is required for cells to exit G0 efficiently. Thus, G1 entry is regulated in an analogous fashion to S phase entry, but involves a distinct cyclin/cdk combination (Ren, 2004).

One possible regulator of G0 events is cyclin C because its highest mRNA expression levels occur during G0 exit. Cyclin C was identified in genetic screens for mammalian or Drosophila genes that could rescue a triple CLN-deficient strain of S. cerevisiae (Leopold, 1991; Lew, 1991). These same screens discovered cyclins D1 and E, and although they have found places as regulators of cdks that have a direct effect on cell cycle progression, cyclin C has not. Instead, it has been shown to regulate the activity of cdk8, which phosphorylates the C-terminal domain (CTD) of RNA polymerase II. This function is consistent with the close structural similarities between cyclin C/cdk8 and the SRB11/SRB10 complex which is a component of the S. cerevisiae RNA polymerase II holoenzyme and is required for optimal CTD phosphorylation. Cyclin C/cdk8 also phosphorylates cyclin H, which negatively regulates TFIIH (Ren, 2004 and references therein).

Although cyclin C's contribution to transcriptional regulation is well established, this activity does not readily explain its capacity to rescue G1 cyclin deficiency in yeast. While cyclin C's ability to stimulate CDC28 in S. cerevisiae may simply be a consequence of the same structurally conserved cyclin domains that activate cdk8 in its native mammalian or insect contexts, cyclin C may also have an unappreciated G0/G1 cyclin activity. In this study, cyclin C's ability to regulate events in G0 and early G1 was tested. During exit from G0, cyclin C directs pRb phosphorylation in a temporal pattern that precedes pRb phosphorylation by cyclin D/cdk4, cyclin D/cdk6, and cyclin E/cdk2. Furthermore, this activity does not involve cdk8 but rather is mediated by cdk3, and targets specific pRb substrate sites that must be phosphorylated in order for cells to exit G0. Together, these results indicate that cyclin C/cdk3 plays an important role in regulating the G0 to G1 transition and does so, in part, through specific phosphorylation of pRb (Ren, 2004).

Rb is a target of the MAPK cascade

The E2F transcription factor plays a major role in cell cycle regulation, differentiation and apoptosis, but it is not clear how it is regulated by non-mitogenic signaling cascades. Two kinases involved in signal transduction have opposite effects on E2F function: the stress-induced kinase JNK1 inhibits E2F1 activity whereas the related p38 kinase reverses Rb-mediated repression of E2F1. JNK1 phosphorylates E2F1 in vitro, and co-transfection of JNK1 reduces the DNA binding activity of E2F1; treatment of cells with TNFalpha has a similar effect. Fas stimulation of Jurkat cells is known to induce p38 kinase and a pronounced increase in Rb phosphorylation is found within 30 min of Fas stimulation. Phosphorylation of Rb correlates with a dissociation of E2F and increased transcriptional activity. The inactivation of Rb by Fas is blocked by SB203580, a p38-specific inhibitor, as well as a dominant-negative p38 construct; cyclin-dependent kinase (cdk) inhibitors as well as dominant-negative cdks have no effect. These results suggest that Fas-mediated inactivation of Rb is mediated via the p38 kinase, independent of cdks. The Rb/E2F-mediated cell cycle regulatory pathway appears to be a normal target for non-mitogenic signaling cascades and could be involved in mediating the cellular effects of such signals (Wang, 1999).

Signaling upstream of Rb

The humpty dumpty (humdy) mouse mutant exhibits failure to close the neural tube and optic fissure, causing exencephaly and retinal coloboma, common birth defects. The humdy mutation disrupts Phactr4, an uncharacterized protein phosphatase 1 (PP1) and actin regulator family member, and the missense mutation specifically disrupts binding to PP1. Phactr4 is initially expressed in the ventral cranial neural tube, a region of regulated proliferation, and after neural closure throughout the dorsoventral axis. humdy embryos display elevated proliferation and abnormally phosphorylated, inactive PP1, resulting in Rb hyperphosphorylation, derepression of E2F targets, and abnormal cell-cycle progression. Exencephaly, coloboma, and abnormal proliferation in humdy embryos are rescued by loss of E2f1, demonstrating the cell cycle is the key target controlled by Phactr4. Thus, Phactr4 is critical for the spatially and temporally regulated transition in proliferation through differential regulation of PP1 and the cell cycle during neurulation and eye development (Kim, 2007).

p130, a RB family member, can substitute for cyclin-dependent kinase inhibitors

The ability of cyclin-dependent kinases (CDKs) to promote cell proliferation is opposed by cyclin-dependent kinase inhibitors (CKIs), proteins that bind tightly to cyclin-CDK complexes and block the phosphorylation of exogenous substrates. Mice with targeted CKI gene deletions have only subtle proliferative abnormalities, however, and cells prepared from these mice seem remarkably normal when grown in vitro. One explanation may be the operation of compensatory pathways that control CDK activity and cell proliferation when normal pathways are inactivated. Mice lacking the CKIs p21(Cip1) and p27(Kip1) were used to investigate this issue, specifically with respect to CDK regulation by mitogens. p27 is the major inhibitor of Cdk2 activity in mitogen-starved wild-type murine embryonic fibroblasts (MEFs). Nevertheless, inactivation of the cyclin E-Cdk2 complex in response to mitogen starvation occurs normally in MEFs that have a homozygous deletion of the p27 gene. Moreover, CDK regulation by mitogens is also not affected by the absence of both p27 and p21. A titratable Cdk2 inhibitor compensates for the absence of both CKIs, and this inhibitor is identified as p130, a protein related to the retinoblastoma gene product Rb. Thus, cyclin E-Cdk2 kinase activity cannot be inhibited by mitogen starvation of MEFs that lack both p27 and p130. In addition, cell types that naturally express low amounts of p130, such as T lymphocytes, are completely dependent on p27 for regulation of the cyclin E-Cdk2 complex by mitogens. It is concluded that inhibition of Cdk2 activity in mitogen-starved fibroblasts is usually performed by the CKI p27, and to a minor extent by p21. Remarkably p130, a protein in the Rb family that is not related to either p21 or p27, will directly substitute for the CKIs and restore normal CDK regulation by mitogens in cells lacking both p27 and p21. p130 has the 'RxL' (Arg-X-Lys) motif, which is present in other cyclin-binding proteins and is required for CDK inhibition by members of the p21/p27 family. It is not clear, however, whether or not this motif is required for p130 to inhibit cyclin E-Ck2 in vitro, because the motif is absent from the amino-terminal inhibitory fragment of p130. Hence, the mode of inhibition of p130 may not mimic the one employed by the p21/p27 proteins. This compensatory use of p130 may be important in settings in which CKIs are not expressed at standard levels, as is the case in many human tumors (Coats, 1999).


Table of contents


Retinoblastoma-family protein: Biological Overview | Regulation | Developmental Biology | Effects of Mutation | References

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