Restriction on self-renewing asymmetric division is coupled to terminal asymmetric division in the Drosophila CNS

English version

Autoři: Ivana Gaziova ^aff001; Michael Gazi ^aff001; Jordan Mar ^aff003; Krishna Moorthi Bhat ^aff001
Působiště autorů: Department of Neuroscience and Cell Biology, University of Texas Medical Branch, Galveston, United States of America ^aff001; Texas Biomedical Research Institute, Department of Virology, 8715 W. Military Dr. San Antonio, United States of America ^aff002; Department of Molecular Medicine, Morsani College of Medicine, University of South Florida, Tampa, United States of America ^aff003
Vyšlo v časopise: Restriction on self-renewing asymmetric division is coupled to terminal asymmetric division in the Drosophila CNS. PLoS Genet 16(9): e32767. doi:10.1371/journal.pgen.1009011
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009011

Souhrn

Neuronal precursor cells undergo self-renewing and non-self-renewing asymmetric divisions to generate a large number of neurons of distinct identities. In Drosophila, primary precursor neuroblasts undergo a varying number of self-renewing asymmetric divisions, with one known exception, the MP2 lineage, which undergoes just one terminal asymmetric division similar to the secondary precursor cells. The mechanism and the genes that regulate the transition from self-renewing to non-self-renewing asymmetric division or the number of times a precursor divides is unknown. Here, we show that the T-box transcription factor, Midline (Mid), couples these events. We find that in mid loss of function mutants, MP2 undergoes additional self-renewing asymmetric divisions, the identity of progeny neurons generated dependent upon Numb localization in the parent MP2. MP2 expresses Mid transiently and an over-expression of mid in MP2 can block its division. The mechanism which directs the self-renewing asymmetric division of MP2 in mid involves an upregulation of Cyclin E. Our results indicate that Mid inhibits cyclin E gene expression by binding to a variant Mid-binding site in the cyclin E promoter and represses its expression without entirely abolishing it. Consistent with this, over-expression of cyclin E in MP2 causes its multiple self-renewing asymmetric division. These results reveal a Mid-regulated pathway that restricts the self-renewing asymmetric division potential of cells via inhibiting cyclin E and facilitating their exit from cell cycle.

Klíčová slova:

Cell cycle and cell division – Cyclins – Drosophila melanogaster – Gene expression – Neurons – Precursor cells – Statistical data – Cell division analysis

Zdroje

1. Doe CQ., Goodman CS. Early Events in Insect Neurogenesis.1. Development and Segmental Differences in the Pattern of Neuronal Precursor Cells. Dev Biol. 1985;111 : 193–205 doi: 10.1016/0012-1606(85)90445-2 4029506

2. Broadus J., Skeath JB, Spana EP, Bossing T, Technau G, Doe CQ. New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system. Mech. Dev. 1995; 53 : 393–402 doi: 10.1016/0925-4773(95)00454-8 8645605

3. Bossing T., Udolph G, Doe CQ, Technau GM. The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev Biol. 1996;17 : 41–64

4. Schmidt H., Rickert C, Bossing T, Vef O, Urban J, Technau GM. The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev Biol. 1997;189 : 186–204 doi: 10.1006/dbio.1997.8660 9299113

5. Schmid A., Chiba A, Doe CQ. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development. 1999;126 : 4653–4689 10518486

6. Gaziova I., Bhat KM. Generating asymmetry: with and without self-renewal. Prog Mol Subcell Biol. 2007;45 : 143–178 doi: 10.1007/978-3-540-69161-7_7 17585500

7. Spana EP., Doe CQ. Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron. 1996;17 : 21–26 doi: 10.1016/s0896-6273(00)80277-9 8755475

8. Rhyu MS., Jan LY, Jan YN. Asymmetric distribution of Numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell. 1994;76 : 477–491 doi: 10.1016/0092-8674(94)90112-0 8313469

9. Knoblich JA., Jan LY, Jan YN. Asymmetric segregation of Numb and Prospero during cell division. Nature. 1995;377 : 624–627 doi: 10.1038/377624a0 7566172

10. Spana EP., Doe CQ. The Prospero Transcription Factor Is Asymmetrically Localized to the Cell Cortex during Neuroblast Mitosis in Drosophila. Development. 1995;121 : 3187–3195 7588053

11. Spana EP., Kopczynski C, Goodman CS, Doe CQ. Asymmetric localization of Numb autonomously deter -⁠ mines sibling neuron identity in the Drosophila CNS. Development. 1995;121 : 3489–3494 8582263

12. Hirata J., Nakagoshi H, Nabeshima Y, Matsuzaki F. Asymmetric segregation of the homeodomain protein prospero during Drosophila development. Nature. 1995;377(6550): 627–630 doi: 10.1038/377627a0 7566173

13. Guo M., Jan LY, Jan YN. Control of daughter cell fates during asymmetric division: Interaction of Numb and Notch. Neuron. 1996;17 : 27–41 doi: 10.1016/s0896-6273(00)80278-0 8755476

14. Kraut R., Chia W, Jan LY, Jan YN, Knoblich JA. Role of inscuteable in orienting asymmetric cell divisions in Drosophila. Nature. 1996;383 : 50–55 doi: 10.1038/383050a0 8779714

15. Wai P., Truong B, Bhat KM. Cell division genes promote asymmetric interaction between Numb and Notch in the Drosophila CNS. Development. 1999;126 : 2759–2770 10331986

16. Bhat KM., Gaziova I, Katipalla S. Neuralized mediates asymmetric division of neural precursors by two distinct and sequential events: Promoting asymmetric localization of Numb and enhancing activation of Notch-signaling. Dev Biol. 2011;351 : 186–198 doi: 10.1016/j.ydbio.2010.12.008 21147089

17. Bhat KM. Notch signaling acts before cell division to promote asymmetric cleavage and cell fate of neural precursor cells. Sci Signal. 2014;7 : 348

18. Nusslein-Volhard C., Wieschaus, Kluding H. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Roux Arch. Dev. Biol. 1984;193 : 267–282

19. Kolodziej PA., Jan LY, Jan YN. Mutations that affect the length, fasciculation, or ventral orientation of specific sensory axons in the Drosophila embryo. Neuron. 1995;15 : 273–286 doi: 10.1016/0896-6273(95)90033-0 7646885

20. Gaziova I., Bhat KM. 2009 Ancestry-independent fate specification and plasticity in the developmental timing of a typical Drosophila neuronal lineage. Development. 2009;136 : 263–274 doi: 10.1242/dev.027854 19088087

21. Manavalan MA., Gaziova I, Bhat KM. The Midline Protein Regulates Axon Guidance by Blocking the Reiteration of Neuroblast Rows within the Drosophila Ventral Nerve Cord. PLoS Genetics. 2013; 9

22. Kispert A., Hermann BG. The Brachyury gene encodes a novel DNA binding protein. EMBO J. 1993;12 : 4898–4899 8223498

23. Porsch M., Sauer M, Schulze S, Bahlo A, Roth M, et al. The relative role of the T-domain and flanking sequences for developmental control and transcriptional regulation in protein chimeras of Drosophila OMB and ORG -⁠ 1. Mech Dev. 2005; 122 : 81–96 doi: 10.1016/j.mod.2004.08.007 15582779

24. Bamshad M., Lin RC, Law DJ, Watkins WC, Krakowiak PA, Moore ME, et al. Mutations in human TBX3 alter limb, apocrine and genital development in ulnar-mammary syndrome. Nat Genet. 1997;16 : 311–315 doi: 10.1038/ng0797-311 9207801

25. Merscher S., Funke B, Epstein JA, Heyer J, Puech A, Lu MM, et al. TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell. 2001;104 : 619–629 doi: 10.1016/s0092-8674(01)00247-1 11239417

26. Li QY., Newbury-Ecob RA, Terrett JA, Wilson DI, Curtis AR, Yi CH, et al. Holt-Oram syndrome is caused by mutations in TBX5, a member of the Brachyury (T) gene family. Nat Genet. 1997;15 : 21–29 doi: 10.1038/ng0197-21 8988164

27. Basson CT., Huang T, Lin RC, Bachinsky DR, Weremowicz S, Vaglio A, et al. Different TBX5 interactions in heart and limb defined by Holt-Oram syndrome mutations. Proc Natl Acad Sci U S A. 1999;96 : 2919–2924 doi: 10.1073/pnas.96.6.2919 10077612

28. Qian L., Liu J, Bodmer R. Neuromancer Tbx20-related genes (H15/midline) promote cell fate specification and morphogenesis of the Drosophila heart. Dev Biol. 2005;279 : 509–524 doi: 10.1016/j.ydbio.2005.01.013 15733676

29. Edgar BA., O’Farrell PH. Genetic-Control of Cell-Division Patterns in the Drosophila Embryo. Cell. 1989;57 : 177–187 doi: 10.1016/0092-8674(89)90183-9 2702688

30. Knoblich JA., Sauer K, Jones L, Richardson H, Saint R, Lehner CF. Cyclin-E Controls S-Phase Progression and Its down-Regulation during Drosophila Embryogenesis Is Required for the Arrest of Cell-Proliferation. Cell. 1994;77 : 107–120 doi: 10.1016/0092-8674(94)90239-9 8156587

31. Duronio RJ., O’Farrell PH. Developmental control of the G1 to S transition in Drosophila: cyclin E is a limiting downstream target of E2F. Genes and Dev. 1995;9 : 1456–1468 doi: 10.1101/gad.9.12.1456 7601350

32. Duronio RJ., Brook A, Dyson N, O'Farrell PH. E2F-induced S phase requires cyclin E. Genes Dev. 1996;10 : 2505–2513 doi: 10.1101/gad.10.19.2505 8843201

33. Duronio RJ., Bonnette PC, O'Farrell PH. Mutations of the Drosophila dDP, dE2F, and cyclin E genes reveal distinct roles for the E2F-DP transcription factor and cyclin E during the G1-S transition. Mol Cell Biol. 1998;18 : 141–151 doi: 10.1128/mcb.18.1.141 9418862

34. Menne TV., Klambt C. The formation of commissures in the Drosophila CNS depends on the midline cells and on the Notch gene. Development. 1994;120 : 123–133 8119121

35. Doe CQ., Chu-LaGraff Q, Wright DM, Scott MP. The prospero gene specifies cell fates in the Drosophila central nervous system. Cell. 1991; 65 : 451–464 doi: 10.1016/0092-8674(91)90463-9 1673362

36. Vaessin H., Grell E, Wolff E, Bier E, Jan LY, Jan YN. Prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell. 1991; 67 : 941–953 doi: 10.1016/0092-8674(91)90367-8 1720353

37. Choksi SP., Southall TD, Bossing T, Edoff K, de Wit E, Fischer BE, et al. Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells. Dev Cell. 2006; 11 : 775–789 doi: 10.1016/j.devcel.2006.09.015 17141154

38. Costello I., Pimeis I-M, Drager S, Bikoff EK, Robertson EJ, Arnold SA. The T-box transcription factor Eomesodermin acts upstream of Mesp1 to specify cardiac mesoderm during mouse gastrulation. Nature Cell Biol. 2011;3 : 1084–91

39. Bhat KM., Apsel N. Upregulation of Mitimere and Nubbin acts through Cyclin E to confer self-renewing asymmetric division potential to neural precursor cells. Development. 2004; 131(5): 1123–1134 doi: 10.1242/dev.01014 14973280

40. Isshiki T., Pearson B, Holbrook S, Doe CQ. Drosophila neuroblasts sequentially express transcription factors, which specify the temporal identity of their neuronal progeny. Cell. 2001;106 : 511–521 doi: 10.1016/s0092-8674(01)00465-2 11525736

41. Li X., Erclik T, Bertet C, Chen Z, Voutev R, Venkatesh S, et al. Temporal patterning of Drosophila medulla neuroblasts controls neural fates. Nature. 2013;498 : 456–462 doi: 10.1038/nature12319 23783517

42. Berger C., Pallavi SK, Prasad M, Shashidhara LS, Technau GM. A critical role for Cyclin E in cell fate determination in the central nervous system of Drosophila melanogaster. Nat. Cell Biol. 2005;7 : 56–62 doi: 10.1038/ncb1203 15580266

43. Hayflick L., Moorhead PS. The serial cultivation of human diploid cell strains. Exp Cell Res. 1961;25 : 585–621 doi: 10.1016/0014-4827(61)90192-6 13905658

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