A novel Drosophila larval MAP (microtubule associated protein), with a relative molecular mass of 85kDa is found associated with taxol-polymerized microtubules. Thisprotein binds to mammalian tubulin and coassembles with purified bovine brain tubulin. The protein binds specifically to beta II tubulin peptide that contains the sequence of the MAP bindingdomain on beta II-tubulin. Affinity-purified 85-kDa protein enhances microtubule assembly in aconcentration-dependent manner. This protein also exhibits a strong affinity forcalmodulin. Monoclonal and polyclonal anti-tau antibodies,including sequence-specific probes that recognize repeated microtubule-binding motifs on tau, MAP-2, andMAP-4 and specific N-terminal sequences of tau, cross-reacted with the 85-kDa protein from Drosophilalarvae. These results suggest that tau and Drosophila 85-kDa protein share common functional andstructural epitopes (Cambiazo, 1995).
The ninefold microtubule symmetry of the eukaryotic basal body and motile axoneme has been long established. The basal body and axoneme contains a 9 + 2 arrangement of microtubules, with nine doublets surrounding two singlets. In Drosophila, these organelles contain distinct but similar ß-tubulin isoforms: basal bodies contain only ß1-tubulin, and only ß2-tubulin is used for assembly of sperm axonemes. A single alpha-tubulin functions throughout spermatogenesis. Thus, differences in organelle assembly reside in ß-tubulin. The ability of ß1 to function in axonemes has been tested and it was found that ß1 alone could not generate axonemes. Small sequence differences between the two isoforms therefore mediate large differences in assembly capacity, even though these two related organelles have a common evolutionarily ancient architecture. In males with equal ß1 and ß2, ß1 was co-incorporated at an equimolar ratio into functional sperm axonemes. When ß1 exceeds ß2, however, axonemes with 10 doublets are produced, an alteration unprecedented in natural phylogeny. Addition of the tenth doublet occurs by a novel mechanism, bypassing the basal body. It has been assumed that the instructions for axoneme morphogenesis reside primarily in the basal body, which normally serves as the axonemal template. These data reveal that ß-tubulin requirements for basal bodies and axonemes are distinct, and that key information for axoneme architecture resides in the axonemal ß-tubulin (Raff, 2000).
ß1 was expressed in post-mitotic cells under control of ß2 gene regulatory sequences. The transgenic construct drives ß1 expression to the same level as the endogenous ß2 gene, allowing for the examination of ß1 function with cellular tubulin pools at normal physiological levels. When ß1 was co-expressed with ß2 at gene doses such that ß1 comprises up to half of the ß-tubulin in the post-mitotic cells, spermatogenesis proceeds normally and ß1 is incorporated into sperm tail axonemes. Males with equimolar ß1 and ß2 in post-mitotic cells are fully fertile and sperm axonemes have wild-type morphology. Moreover, an equal gene dose of ß1 fully rescues defective microtubule function attributable to below-optimal tubulin pools, which cause diminished fecundity in males hemizygous for ß2 (Raff, 2000).
When ß1 is the only post-mitotic ß-tubulin, axoneme morphogenesis is profoundly defective; this shows that ß1 can not replace ß2. In ß1-only males, 9+0 axonemes are initiated at the basal body. Central pair microtubules, which in wild type invariably begin immediately distal to the basal body, were present in only 1 of 168 axonemes followed in serial sections in ß1-only males. The integrity of 9+0 axonemes is maintained for only a fraction of the normal 1.9mm sperm tail length (average, 20µm). Distally, axonemes either lose coherent organization or terminate. Disorganized axonemes in ß1-only males are remarkably like those assembled from ß2DeltaC, a truncated form of ß2 lacking the isotype-specific carboxyl terminus. Unlike ß2DeltaC, however, ß1 supports completion of accessory microtubules, and attachment of dynein arms and the spokelinker complex. Thus, an acidic carboxyl terminus is necessary for these processes, but the ß2-specific carboxyl terminus is not required (Raff, 2000).
Differences in properties of ß1 and ß2 are striking when ß1 exceeds ß2 in the post-mitotic germ cells. Although equimolar amounts of ß1 and ß2 allow wild-type fertility, males are invariably sterile when ß1 is present with ß2 at a 2:1 ratio. Meiosis and cytoplasmic microtubules are normal in 2:1 males, but spermatids have a mixture of normal axonemes, axonemes lacking the central pair, and axonemes with 10 doublets -- a previously undescribed architecture. Initiation of 10-doublet axonemes was examined in serial sections. In all cases known, axonemal doublet microtubules are continuous with the basal body triplets. It was therefore hypothesized that when ß1 persists in the germ cells after its normal time of expression, basal bodies with 10 triplet microtubules are constructed, which would then template 10-doublet axonemes: this proved to be incorrect. Basal bodies observed in 2:1 males, just as in ß1-only males, have normal ninefold symmetry. Moreover, without exception, normal 9+2 axonemes are initiated at the basal body in 2:1 males. This 9+2 morphology is maintained for at least 40µm; 10-doublet axonemes are present only in more distal regions of the sperm tail. The tenth doublet is laterally inserted into axonemes de novo and appears abruptly, without obvious precursor structures. Loss of the tenth doublet and transition back to nine doublets was rarely observed. Only a few mature 10-doublet axonemes retained the central pair. A closed 10-doublet configuration appears to be incompatible with correct positioning of the central pair. Occasional axonemes containing more than 10 doublets are always in an opened configuration. The mechanism for association of the doublet microtubules with the spoke-linker apparatus in the internal axoneme 'cartwheel' structure can thus accommodate 10 doublets but not more (Raff, 2000).
Assembly at the basal body occurs with great fidelity. In 2:1 males, axoneme starts are 9+2. Similarly, in ß1-only males, axoneme starts have the canonical nine doublets. These observations suggest that the mechanism for initiating doublet microtubules from the basal body triplets constrains assembly -- either because of a direct 'templating' effect whereby the association of new tubulin dimers with pre-formed microtubules forces correct patterning even of imperfectly bonded subunits, or because of a high concentration near the basal body of other components involved in axoneme initiation. Defects in the central pair in 2:1 males, however, together with their absence in ß1-only males, suggests that assembly of the central pair apparatus and its association with the doublet microtubules is a key property of ß2 and other axonemal ß-tubulins, not possessed by ß1 (Raff, 2000).
The small sequence differences between ß1 and ß2 distinguish between two kinds of shared-wall microtubule assembly. ß1 has the capacity for basal body assembly, but these properties are not sufficient for axoneme morphogenesis. ß2 has the properties required for axoneme assembly, but it is inferred that ß2 cannot generate shared-wall microtubules de novo. Some of the instructions for each organelle are therefore intrinsic to the ß-tubulin subunits, and axoneme morphology is not solely dependent on the basal body template. It has been shown that ß-tubulin can specify microtubule protofilament substructure. Thus, to a hitherto unappreciated extent, information for a given microtubule-based structure can be built into the tubulins from which it is assembled (Raff, 2000).
This study demonstrates sorting of ß-tubulins during dimerization in the Drosophila male germ line. Different ß-tubulin isoforms exhibit distinct affinities for alpha-tubulin during dimerization. The data suggest that differences in dimerization properties are important in determining isoform-specific microtubulefunctions. The differential use of ß-tubulin during dimerizationreveals structural parameters of the tubulin heterodimer notdiscernible in the resolved three-dimensional structure. The variable ß-tubulin carboxyl terminus, a surface feature in theheterodimer and in microtubules, and which is disordered in thecrystallographic structure, is of key importance in forming a stablealpha-ß heterodimer. If the availability of alpha-tubulin is limiting,alpha-ß dimers preferentially incorporate intact ß-tubulins ratherthan a ß-tubulin missing the carboxyl terminus (ß2DeltaC). Whenalpha-tubulin is not limiting, ß2DeltaC forms stable alpha-ßheterodimers. Once dimers are formed, no further sorting occurs duringmicrotubule assembly: alpha-ß2DeltaC dimers are incorporated into axonemes in proportion to their contribution to the total dimer pool.Co-incorporation of ß2DeltaC and wild-type ß2-tubulin results innonmotile axonemes because of a disruption of the periodicity ofnontubulin axonemal elements. These data show that the ß-tubulin carboxyl terminus has two distinct roles: (1) forming the alpha-ß heterodimer, important for all microtubules and (2) providing contacts for nontubulin components required for specific microtubule structures, such as axonemes (Hoyle, 2001).
The ß2-specific carboxyl terminus is essential forassembly of the sperm tail flagella, the only motile axoneme inDrosophila. The 15 carboxyl residues missing from ß2DeltaCinclude the axoneme motif present in all ß-tubulins incorporated intomotile axonemes, as well as sites of posttranslational modification known to be important for axoneme motility. The axoneme motif specifies thecentral pair microtubules. Even when full-length ß2 makes up the majority of the ß-tubulin present, incorporation of stable ß2DeltaC into axonememicrotubules disrupts the organization of the central pair complex andthe radial spokes. Studies of paralyzed flagella mutants ofChlamydomonas have shown these two axonemal structures to beinvolved in regulating axoneme motility. A nontubulin component found inthe central pair complex of a wide range of species is the central pairprojection. Transient contact between the radial spokes and the central pair projections is thought to play an important role in the regulation of dynein and the generation of the complex flagellar waveform (Hoyle, 2001).
The identity of the repeated element found in theDrosophila central pair complex is not known. However, itsdisruption by ß2DeltaC, as well as the disruption of the radial spokes,implies that both components are in contact with the carboxyl terminus of ß-tubulin in wild-type axonemes, either directly or indirectly through other protein-protein interactions. In these experiments, allnontubulin components present are wild type. When the radial spokes orcentral pair components are themselves mutant, as is the case withChlamydomonas paralyzed flagellar mutants, the mutations arerecessive. In contrast, when ß2 subunits lacking the carboxyl terminus are incorporated at random into axonemes, the consequence is adominant disruption of axoneme motility. It appears that for eachalpha84B-ß2DeltaC dimer incorporated into an axoneme microtubule, thereis a stoichiometric loss of interaction with nontubulin components ofthe axoneme. When 30% of the ß-tubulin lacks the carboxyl terminus,the loss of organization becomes too great to permit axoneme function,and sperm become nonmotile. The higher the percentage of truncatedß-tubulin incorporated into the axoneme, the more severe are thedefects. Axonemes from males in which ß2DeltaC is 50% of totalß-tubulin exhibit the same kind of defects that occurred in sterilemales with 30% ß2DeltaC but to a much more marked degree, readilyapparent in axoneme cross-sections (Hoyle, 2001).
The ß2-tubulin carboxyl terminus plays two distinct roles. In its first role, the acidic carboxyl terminus is important for producing a stable alpha-ß heterodimer. The generalized nature of this requirement is reflected by the fact that any acidic carboxyl terminus seems to work; ß1- and ß3-tubulin both form stable alpha-ß dimers in the male germ line. Thus, although theß-tubulin carboxyl terminus is the hypervariable, isotype-definingregion of the molecule, the wrongcarboxyl terminus seems to be better than no carboxyl terminus. In adistinct second role, the carboxyl terminus is involved in interactionsbetween intact microtubules and nontubulin components required togenerate the architecture of specific microtubule-based structures.ß2DeltaC by itself fails to support any axonemal organization.However, not just any carboxyl terminus can support this function:other full-length Drosophila ß-tubulin isoforms cannotreplace ß2 for axoneme function. In contrast, thecarboxyl terminus is not required for generic microtubule functions:ß2DeltaC can support assembly of functional meiotic spindles as well asthe cytoplasmic microtubules associated with elongation of themitochondrial derivative. It should be noted that these generic functions can also be fully or partially supplied by other Drosophila isoforms (Hoyle, 2001).
These data demonstrate that competition between ß2DeltaC and intactß-tubulins takes place during dimerization and not during subsequent microtubule assembly. However, competition between full-length ß-tubulin and ß2DeltaC could occur at several steps in the dimerization process. This work does not distinguish between competition for binding with cytosolic chaperonin, competition for cofactors of the dimer-making machine, or direct competition between ß2 and ß2DeltaC for alpha84B. However, the resolved three-dimensional structure of the alpha-ß dimer allows for the possibility that the unresolved ß-tubulin carboxyl residues are in contact with the alpha-tubulin moiety of the same alpha-ß dimer. Direct competition between ß-tubulins for binding to alpha is consistent with the finding that different ß-tubulin isoforms exhibit differential abilities to form alpha-ß dimers. This model suggests the possibility that alpha-tubulin residues contacted by the ß-tubulin carboxyl terminus play a direct role in stabilizing the alpha-ß dimer. The resolved structure predicts these alpha-tubulin residues to be non-carboxyl-terminal residues. As is the case with ß-tubulin, thealpha-tubulin carboxyl terminus is also unresolved in both the structuresof the heterodimer and the microtubule. The 11 unresolved alpha residues are in position to contact ß-tubulin in another heterodimer, either in the same protofilament or perhaps in an adjacent protofilament. This leads to the prediction that the alpha-tubulin carboxyl terminus will be of relatively little importance in forming or stabilizing intrasubunit associations in the dimer but may be involved in interdimer associations in the protofilament substructure of microtubules (Hoyle, 2001).
During Drosophila spermatogenesis transcriptional activity is restricted mainly to premeiotic stages. However, translation during sperm morphogenesis proceeds for several days, requiring a highstability for mRNAs translated postmeiotically. From the primary spermatocyte stageonward the ß2tubulin gene is expressed solely in the male germ line. In adult testes, mRNA amounts are elevated about threefold due to the presenceof beta 2DE1, an 18-bp AT-rich element. This element ispresent at about the same position in the 5' untranslated regions of the ß2 tubulin mRNA in both of thedistantly related species Drosophila melanogaster and D. hydei. Changing the position of theelement on the mRNA reduces the stabilizing effect, while inversion of the beta 2DE1 abolishes itsfunction. The element also acts in an artificial combination with the ß1 tubulin transcription start site, andthe beta 2UE1, which is required to achieve tissue-specific expression. Acomparison of premeiotic with postmeiotic stages strongly implies that this element is involved inregulating mRNA stability. This mRNA stabilizing element acts in a position-independent manner andalso on a heterologous mRNA, demonstrating its autonomous functional activity (Michiels, 1993).
ß tubulins are encoded by members of multigene families and are generally highly conserved atthe sequence level. The carboxyl terminal 15 amino acids are markedly more diverged than the restof the sequence and constitute an "isotype defining region," one that is conserved in the correspondingß tubulin isoforms of different vertebrate species. It is thought that the carboxy terminus ofß tubulin may not be required for assembly of microtubules per se, but it may be necessary forconferring properties on beta-tubulins required for isotype-specific functions. A ß tubulin isoform lacking its carboxy terminus was prepared by mutation. ß tubulin variants with largetruncations (171 or 50 amino acids) do not accumulate to detectable levels and provide nobeta-tubulin function. However, a small truncation missing only the terminal 15 amino acids iscapable of being assembled into ultrastructurally normal looking microtubules in vivo, even thoughthe truncated protein is less stable than wildtype ß2. The functional failings of this truncatedß-tubulin are manifest in defective microtubule-based spermatogenic suprastructures, ratherthan at the assembly level of individual microtubules. The most remarkable defect conferred by thetruncated ß2 is the failure of axonemes to assemble with proper organization, even thoughmicrotubules with presumptive axoneme identity are clearly present. Thereforethe carboxy terminus of ß2 tubulin is required for organization of microtubulesuprastructures in spermatogenesis. This observation supports the hypothesis that the variablecarboxy terminus mediates isotype-specific microtubule-dependent functions (Fackenthal, 1993).
Mutations responsible fordifferent classes of functional phenotypes are distributed throughout the ß2 tubulin molecule.There is a telling correlation between the degree of phylogenetic conservation of the altered residuesand the number of different microtubule categories disrupted by the lesions. The majority of lesionsoccur at positions that are evolutionarily highly conserved in all ß tubulins; these lesions disruptgeneral mitotic and structural functions common to multiple classes of microtubules. However, a single allele B2t6 containsan amino acid substitution within an internal cluster of variable amino acids that has been identified asan isotype-defining domain in vertebrate ß tubulins. Correspondingly, B2t6 disrupts only a subsetof microtubule functions, resulting in mis-specification of the morphology of the doublet microtubulesof the sperm tail axoneme. ß3 tubulin confers the same restricted morphological phenotype in a dominantway when it is coexpressed in the testis with wild-type ß2 tubulin. ß3 tubulin and the B2t6 product disrupt a common aspect of microtubuleassembly. It is therefore concluded that the amino acid sequence of the ß2 tubulin internal variableregion is required for the generation of correct axoneme morphology but not for general microtubulefunctions. Theß2 variant lacking the carboxy terminus and the B2t6 variant complement each other formild-to-moderate meiotic defects but do not complement for proper axonemal morphology. It is believed that the two isotype-defining domains interact in a three-dimensional structure in wild-type ß tubulins.The integrity of this structure in the Drosophila testis ß2 tubulin isoform isrequired for proper axoneme assembly but not necessarily for general microtubule functions (Fackenthal, 1995).
The functional capacity of different beta tubulin isoforms has been tested in vivo by expressing ß3-tubulineither in place of or in addition to ß2-tubulin in the male germ line of the fly. Thetestes-specific isoform, ß2, is conserved relative to major metazoan beta tubulins, while the developmentallyregulated isoform, ß3, is considerably divergent in sequence. ß3-tubulin is normally expressed in discretesubsets of cells at specific times during development, but is not expressed in the male germ line. ß2-Tubulinis normally expressed only in the postmitotic germ cells of the testis, and is required for all microtubule-basedfunctions in these cells. The normal functions of ß2-tubulin include assembly of meiotic spindles, axonemes,and at least two classes of cytoplasmic microtubules, including those associated with the differentiatingmitochondrial derivatives. A hybrid gene was constructed in which 5' sequences from the ß2 gene werejoined to protein coding and 3' sequences of the ß3 gene. Drosophila transformed with the hybrid geneexpress ß3-tubulin in the postmitotic male germ cells. When expressed in the absence of the normal testisisoform, ß3-tubulin supports assembly of one class of functional cytoplasmic microtubules. In such males themicrotubules associated with the membranes of the mitochondrial derivatives are assembled and normalmitochondrial derivative elongation occurs, but axoneme assembly and other microtubule-mediated processes,including meiosis and nuclear shaping, do not occur. These data show that ß3 tubulin can support only asubset of the multiple functions normally performed by ß2, and also suggest that the microtubules associatedwith the mitochondrial derivatives mediate their elongation. When ß3 is coexpressed in the male germ linewith ß2, at any level, spindles and all classes of cytoplasmic microtubules are assembled and functionnormally. However, when ß3-tubulin exceeds 20% of the total testis beta tubulin pool, it acts in a dominantway to disrupt normal axoneme assembly. In the axonemes assembled in such males, the doublet tubules acquiresome of the morphological characteristics of the singlet microtubules of the central pair and accessory tubules.These data therefore unambiguously demonstrate that the Drosophila beta tubulin isoforms ß2 and ß3 arenot equivalent in intrinsic functional capacity, and furthermore show that assembly of the doublet tubules of theaxoneme imposes different constraints on beta tubulin function than does assembly of singlet microtubules (Hoyle, 1990).
Since ß2 delta C cannot support organizationof axonemal microtubules into the supramolecular architecture of the axoneme, a test was made to see whetherbeta 2 carboxyl sequences can rescue the functional failure of the ß3 isoform in spermatogenesis. A chimeric protein was constructed at the gene level, ß3 beta 2C, in which beta 3 sequences in thecarboxyl region were replaced with those of beta 2. Unlike either beta 3 or beta 2 delta C, beta 3 beta2C can provide partial function for both assembly of axonemal microtubules and their organizationinto the supramolecular architecture of the axoneme. In particular, the beta 2 carboxyl sequencesmediate morphogenesis of the axoneme doublet tubule complex, including accessory microtubuleassembly and attachment of spokes and linkers. However, there are aspects of beta2-specific function that require structural features other than the primary sequence of theisotype-defining variable regions, the C terminus and the internal variable region. Tests of fecundity inmales that coexpress beta 2 and the chimeric beta 3 beta 2C protein show that in Drosophilathere are differential requirements for sperm motility in the male and in the female reproductive tract.Since some aspects of microtubule function in spermatogenesis are sensitive to the tubulin pool size, the mechanisms for control of tubulin protein levels in the male germ cells were examined. Both beta 2-tubulin mRNA accumulation and protein synthesis are dependent on gene dose, and the level of expression is regulated by 3' noncoding sequences in the beta 2 gene. These datashow that the regulatory mechanisms that control tubulin pool levels in the Drosophila male germ linediffer from those observed in cultured animal somatic cells. Finally, expression of transgenicconstructs is consistent with early cessation of X chromosome expression in Drosophilaspermatogenesis (Hoyle, 1995).
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