Unpolymerized tubulin modulates the level of tubulin mRNAs

Cleveland, Don W.; Lopata, Margaret A.; Sherline, Peter; Kirschner, Marc W.

doi:10.1016/0092-8674(81)90072-6

Cited by 390 publications

(241 citation statements)

References 30 publications

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“…The P-tubulin mRNA half-life in etiolated oat leaves was shown to be about 1.5 hr (Byrne et al, 1993). In a numberof mammalian cell cultures, a-tubulin and P-tubulin mRNA half-lives are 1 to 2 hr, and these mRNAs are destabilized by high levels of tubulin heterodimers (Cleveland et al, 1981;Pachter et ai., 1987;Gay et al, 1989). It is unknown whether funga1 elicitor treatment of plant cells triggers P-tubulin mRNA decay by a similar mechanism.…”

Section: Discussionmentioning

confidence: 99%

Fungal Elicitor-Induced Bean Proline-Rich Protein mRNA Down-Regulation Is Due to Destabilization That Is Transcription and Translation Dependent.

et al. 1993

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In bean cells treated with fungal elicitor, the transcripts of PwPRPí, a gene encoding a proline-rich protein, decreased to -6% of the original level within 4 hr. The apparent mRNA half-life during the period of rapid degradation was -45 min. The rate of PwPRPí gene transcription remained constant over this period, as determined by nuclear run-off assays, indicating a decrease in mRNA stability. By using actinomycin D to block transcription, the half-life of PwPRPl mRNA in unelicited cells was estimated to be -60 hr. In cells treated with actinomycin D followed by the addition of elicitor, the PwPRPl mRNA half-life was -18 hr, whereas cells treated with these reagents in reciproca1 order exhibited a half-life of -6 hr. The protein synthesis inhibitors emetine and anisomycin also inhibited the rate of PwPRPl mRNA degradation in elicited cells. Based on these data, we concluded that the rapid decrease in the PwPRPí mRNA level in elicited cells is due to destabilization, which is dependent on new RNA and protein synthesis.

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Section: Discussionmentioning

confidence: 99%

Fungal Elicitor-Induced Bean Proline-Rich Protein mRNA Down-Regulation Is Due to Destabilization That Is Transcription and Translation Dependent.

et al. 1993

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“…Tubulin biosynthesis is noted for its autoregulatory system in which the elevated level of free tubulin reduces synthesis of tubulin [16,181. Then, to examine whether an increase in free tubulin concentration is also required for the initiation of DNA synthesis by microtubule-disrupting agents, quiescent 3Y1 cells were incubated with a high concentration of vinblastine plus colcemid which led to formation of tubulin paracrystals concomitant with microtubule depolymerization without increasing free tubulin level (Fig.…”

Section: Discussionmentioning

confidence: 99%

Initiation of DNA synthesis by microtubule disruption in quiescent rat 3Y1 cells

Shinohara

Nishida

Sakai

1989

European Journal of Biochemistry

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Disruption of cytoplasmic microtubules by colchicine, colcemid or vinblastine induced the initiation of DNA synthesis and cell division in quiescent cultures of rat embryo fibroblast cell line, 3Y1, in the absence of growth factors. The microtubule-disruption-induced DNA synthesis was so marked that we could initiate analysis of the mechanism. Incubation of quiescent 3Y 1 cells with high concentrations of vinblastine or those of vinblastine plus colcemid, which formed large tubulin paracrystals concomitant with the depolymerization of cytoplasmic microtubules, initiated DNA synthesis in the cells. Because these treatments did not increase the free tubulin level in the cells, but rather decreased it, an increase in the free tubulin level may not be required for initiation of DNA synthesis induced by microtubule-disrupting agents. Culture fluid of the 3Y1 cells incubated with colchicine did not stimulate the initiation of DNA synthesis when added to other quiescent 3Y1 cells after conversion of the colchicine in thc culture fluid to lumicolchicine by ultraviolet irradiation. This suggested that colchicine treatment did not induce secretion of any mitogenic factors from 3Y1 cells. These results suggest that disruption of normal microtubules may elicit intracellular signals leading to cell proliferation.Cytoplasmic microtubules function in a wide variety of ways as a structural component and motility machinery. Cytoplasmic microtubules have also been suggested to play a regulatory role in cell growth, based on the observation that microtubule-depolymerizing agents have inhibitory or stimulatory effects on cell cycle traverse of quiescent cultures. Vasiliev et al. reported that colcemid stimulated the initiation of DNA synthesis in primary cultures of density-arrested mouse embryo fibroblast-like cells in the presence of 10% bovine serum [I]. On the other hand, colchicine inhibited the initiation of DNA synthesis in some cell lines [2][3][4][5][6][7][8]. But, as for confluently cultured, well-arrested fibroblastic cells, colchicine always potentiated the effect of growth factors on initiation of DNA synthesis [9-131. Crossin and Carney demonstrated that colchicine treatment alone initiated DNA synthesis in somc primary cultures in serum-free meclium [14, IS], though the stimulation of thymidine incorporation by colchicine was no more than 2-_?-fold, probably because the cultures might not be completely rendered quiescent.We have found in this study that microtubule-disrupting agents in the absence of any growth factors induce effectively the initiation of DNA synthesis in quiescent cultures of the rat embryo fibroblast cell line, 3Y1. Using this system we could further investigate how microtubule depolymerization relates to the induction of DNA synthesis. Recent excellent experiments done by Cleveland and co-workers [16, 171 and others [I 81 have established that cytoplasmic free tubulin concentration could be a signal for regulating the level of tubulinCorrespondence to E. Nishida, Department of Biophysics and ...

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“…The higher peak concentration in the animalized embryo (5 x 10 s, compared with 3 x l0 s molecules per embryo) indicates that any concentration-dependent feedback control mechanism responsible for such a regulation would be pitched at a different level of sensitivity from that in the control embryo. Such a mechanism, which can be expected to depend directly on the levels of protein generated by the ~-tubulin mRNA, has indeed been posited to depend on the pool size of unpolymerized tubulin in mammalian cells (Ben Ze'ev et al 1979;Cleveland et al 1981;Caron et al 1985a}, and to involve tubulin mRNA stability in response to microtubule depolymerization in enucleated fibroblasts (Caron et al 1985b) and during flagellum regeneration in Chlamydomonas (Baker et al 1984). Posttranscriptional regulation is also apparent during cilium regeneration in the animalized embryo, since f~-tubulin mRNA levels increase without a change in transcription rate.…”

Section: Altered Regulation Of Fl-tubulin Mrna Expression In the Zincmentioning

confidence: 99%

Coordinate and selective beta-tubulin gene expression associated with cilium formation in sea urchin embryos.

Harlow¹,

Nemer²

1987

Genes Dev.

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13-Tubulin mRNAs associated with cilium formation in Strongylocentrotus purpurpatus sea urchin embryos are expressed selectively from a multiple gene family. The accumulations of three 13-tubulin mRNAs (131, 132, and 133) are temporally coordinated with ciliogenesis during blastula development and with the regeneration of cilia after their amputation. In contrast, another 13-tubulin mRNA, 134, is not induced in either case. The zincanimalized embryo with its exaggerated blastula phenotype forms longer cilia through a protracted period of ciliogenesis, in which the 13-tubulin mRNAs, principally 131, accumulate to higher than normal levels. The rate of 13-tubulin transcription per nucleus in the animalized embryo is greater than that of the normal embryo and is not changed through deciliation, although the tubulin mRNAs accumulate to higher levels. However, deciliation raises the 13-tubulin transcription rate in the normal embryo to that in the animalized embryo. Thus, the induction of 13-tubulin mRNA by cilium amputation is regulated transcriptionally in the normal embryo, but post-transcriptionally in the zinc-animalized embryos. Moreover, the 13-tubulin genes that are expressed in association with cilium formation appear to be induced selectively within the framework of ectodermal celltype specificity.

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Unpolymerized tubulin modulates the level of tubulin mRNAs

Cited by 390 publications

References 30 publications

Fungal Elicitor-Induced Bean Proline-Rich Protein mRNA Down-Regulation Is Due to Destabilization That Is Transcription and Translation Dependent.

Fungal Elicitor-Induced Bean Proline-Rich Protein mRNA Down-Regulation Is Due to Destabilization That Is Transcription and Translation Dependent.

Initiation of DNA synthesis by microtubule disruption in quiescent rat 3Y1 cells

Coordinate and selective beta-tubulin gene expression associated with cilium formation in sea urchin embryos.

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