#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Coordination of Cell Proliferation and Cell Fate Determination by CES-1 Snail


The coordination of cell proliferation and cell fate determination is critical during development but the mechanisms through which this is accomplished are unclear. We present evidence that the Snail-related transcription factor CES-1 of Caenorhabditis elegans coordinates these processes in a specific cell lineage. CES-1 can cause loss of cell polarity in the NSM neuroblast. By repressing the transcription of the BH3-only gene egl-1, CES-1 can also suppress apoptosis in the daughters of the NSM neuroblasts. We now demonstrate that CES-1 also affects cell cycle progression in this lineage. Specifically, we found that CES-1 can repress the transcription of the cdc-25.2 gene, which encodes a Cdc25-like phosphatase, thereby enhancing the block in NSM neuroblast division caused by the partial loss of cya-1, which encodes Cyclin A. Our results indicate that CDC-25.2 and CYA-1 control specific cell divisions and that the over-expression of the ces-1 gene leads to incorrect regulation of this functional ‘module’. Finally, we provide evidence that dnj-11 MIDA1 not only regulate CES-1 activity in the context of cell polarity and apoptosis but also in the context of cell cycle progression. In mammals, the over-expression of Snail-related genes has been implicated in tumorigenesis. Our findings support the notion that the oncogenic potential of Snail-related transcription factors lies in their capability to, simultaneously, affect cell cycle progression, cell polarity and apoptosis and, hence, the coordination of cell proliferation and cell fate determination.


Vyšlo v časopise: Coordination of Cell Proliferation and Cell Fate Determination by CES-1 Snail. PLoS Genet 9(10): e32767. doi:10.1371/journal.pgen.1003884
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003884

Souhrn

The coordination of cell proliferation and cell fate determination is critical during development but the mechanisms through which this is accomplished are unclear. We present evidence that the Snail-related transcription factor CES-1 of Caenorhabditis elegans coordinates these processes in a specific cell lineage. CES-1 can cause loss of cell polarity in the NSM neuroblast. By repressing the transcription of the BH3-only gene egl-1, CES-1 can also suppress apoptosis in the daughters of the NSM neuroblasts. We now demonstrate that CES-1 also affects cell cycle progression in this lineage. Specifically, we found that CES-1 can repress the transcription of the cdc-25.2 gene, which encodes a Cdc25-like phosphatase, thereby enhancing the block in NSM neuroblast division caused by the partial loss of cya-1, which encodes Cyclin A. Our results indicate that CDC-25.2 and CYA-1 control specific cell divisions and that the over-expression of the ces-1 gene leads to incorrect regulation of this functional ‘module’. Finally, we provide evidence that dnj-11 MIDA1 not only regulate CES-1 activity in the context of cell polarity and apoptosis but also in the context of cell cycle progression. In mammals, the over-expression of Snail-related genes has been implicated in tumorigenesis. Our findings support the notion that the oncogenic potential of Snail-related transcription factors lies in their capability to, simultaneously, affect cell cycle progression, cell polarity and apoptosis and, hence, the coordination of cell proliferation and cell fate determination.


Zdroje

1. NietoMA (2002) The Snail superfamily of zinc-finger transcription factors. Nature reviews Molecular cell biology 3: 155–166.

2. Barrallo-GimenoA, NietoMA (2005) The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132: 3151–3161.

3. CobaledaC, Perez-CaroM, Vicente-DuenasC, Sanchez-GarciaI (2007) Function of the zinc-finger transcription factor SNAI2 in cancer and development. Annual review of genetics 41: 41–61.

4. PeinadoH, OlmedaD, CanoA (2007) Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nature reviews Cancer 7: 415–428.

5. NietoMA (2011) The ins and outs of the epithelial to mesenchymal transition in health and disease. Annual review of cell and developmental biology 27: 347–376.

6. WhitemanEL, LiuCJ, FearonER, MargolisB (2008) The transcription factor snail represses Crumbs3 expression and disrupts apico-basal polarity complexes. Oncogene 27: 3875–3879.

7. CanoA, Perez-MorenoMA, RodrigoI, LocascioA, BlancoMJ, et al. (2000) The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nature cell biology 2: 76–83.

8. BatlleE, SanchoE, FranciC, DominguezD, MonfarM, et al. (2000) The transcription factor Snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nature cell biology 2: 84–89.

9. CaiY, ChiaW, YangX (2001) A family of Snail-related zinc finger proteins regulates two distinct and parallel mechanisms that mediate Drosophila neuroblast asymmetric divisions. The EMBO journal 20: 1704–1714.

10. AshrafSI, IpYT (2001) The Snail protein family regulates neuroblast expression of inscuteable and string, genes involved in asymmetry and cell division in Drosophila. Development 128: 4757–4767.

11. KnoblichJA (2010) Asymmetric cell division: recent developments and their implications for tumour biology. Nature reviews Molecular cell biology 11: 849–860.

12. BetschingerJ, KnoblichJA (2004) Dare to be different: asymmetric cell division in Drosophila, C. elegans and vertebrates. Current biology : CB 14: R674–685.

13. LehmanDA, PattersonB, JohnstonLA, BalzerT, BrittonJS, et al. (1999) Cis-regulatory elements of the mitotic regulator, string/Cdc25. Development 126: 1793–1803.

14. EdgarBA, LehmanDA, O'FarrellPH (1994) Transcriptional regulation of string (cdc25): a link between developmental programming and the cell cycle. Development 120: 3131–3143.

15. VegaS, MoralesAV, OcanaOH, ValdesF, FabregatI, et al. (2004) Snail blocks the cell cycle and confers resistance to cell death. Genes & development 18: 1131–1143.

16. WuWS, HeinrichsS, XuD, GarrisonSP, ZambettiGP, et al. (2005) Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma. Cell 123: 641–653.

17. HatzoldJ, ConradtB (2008) Control of apoptosis by asymmetric cell division. Plos Biology 6: e84.

18. SulstonJE, SchierenbergE, WhiteJG, ThomsonJN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental biology 100: 64–119.

19. EllisRE, HorvitzHR (1991) Two C. elegans genes control the programmed deaths of specific cells in the pharynx. Development 112: 591–603.

20. MetzsteinMM, HorvitzHR (1999) The C. elegans cell death specification gene ces-1 encodes a Snail family zinc finger protein. Molecular cell 4: 309–319.

21. ThellmannM, HatzoldJ, ConradtB (2003) The Snail-like CES-1 protein of C. elegans can block the expression of the BH3-only cell-death activator gene egl-1 by antagonizing the function of bHLH proteins. Development 130: 4057–4071.

22. MetzsteinMM, HengartnerMO, TsungN, EllisRE, HorvitzHR (1996) Transcriptional regulator of programmed cell death encoded by Caenorhabditis elegans gene ces-2. Nature 382: 545–547.

23. NehmeR, ConradtB (2008) egl-1: a key activator of apoptotic cell death in C. elegans. Oncogene 27 Suppl 1: S30–40.

24. SzeJY, ZhangS, LiJ, RuvkunG (2002) The C. elegans POU-domain transcription factor UNC-86 regulates the tph-1 tryptophan hydroxylase gene and neurite outgrowth in specific serotonergic neurons. Development 129: 3901–3911.

25. AudhyaA, HyndmanF, McLeodIX, MaddoxAS, YatesJR (2005) A complex containing the Sm protein CAR-1 and the RNA helicase CGH-1 is required for embryonic cytokinesis in Caenorhabditis elegans. The Journal of cell biology 171: 267–279.

26. EllisHM, HorvitzHR (1986) Genetic control of programmed cell death in the nematode C. elegans. Cell 44: 817–829.

27. YanowitzJ, FireA (2005) Cyclin D involvement demarcates a late transition in C. elegans embryogenesis. Developmental biology 279: 244–251.

28. FayDS, HanM (2000) Mutations in cye-1, a Caenorhabditis elegans cyclin E homolog, reveal coordination between cell-cycle control and vulval development. Development 127: 4049–4060.

29. SchnabelR, HutterH, MoermanD, SchnabelH (1997) Assessing normal embryogenesis in Caenorhabditis elegans using a 4D microscope: variability of development and regional specification. Developmental biology 184: 234–265.

30. ZipperlenP, FraserAG, KamathRS, Martinez-CamposM, AhringerJ (2001) Roles for 147 embryonic lethal genes on C.elegans chromosome I identified by RNA interference and video microscopy. The EMBO journal 20: 3984–3992.

31. BoxemM (2006) Cyclin-dependent kinases in C. elegans. Cell division 1: 6.

32. AshcroftNR, SraykoM, KosinskiME, MainsPE, GoldenA (1999) RNA-Mediated interference of a cdc25 homolog in Caenorhabditis elegans results in defects in the embryonic cortical membrane, meiosis, and mitosis. Developmental biology 206: 15–32.

33. ChenMS, HurovJ, WhiteLS, Woodford-ThomasT, Piwnica-WormsH (2001) Absence of apparent phenotype in mice lacking Cdc25C protein phosphatase. Molecular and cellular biology 21: 3853–3861.

34. FergusonAM, WhiteLS, DonovanPJ, Piwnica-WormsH (2005) Normal cell cycle and checkpoint responses in mice and cells lacking Cdc25B and Cdc25C protein phosphatases. Molecular and cellular biology 25: 2853–2860.

35. GersteinMB, LuZJ, Van NostrandEL, ChengC, ArshinoffBI, et al. (2010) Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science 330: 1775–1787.

36. CelnikerSE, DillonLA, GersteinMB, GunsalusKC, HenikoffS, et al. (2009) Unlocking the secrets of the genome. Nature 459: 927–930.

37. SarovM, MurrayJI, SchanzeK, PozniakovskiA, NiuW, et al. (2012) A genome-scale resource for in vivo tag-based protein function exploration in C. elegans. Cell 150: 855–866.

38. SarovM, SchneiderS, PozniakovskiA, RoguevA, ErnstS, et al. (2006) A recombineering pipeline for functional genomics applied to Caenorhabditis elegans. Nature methods 3: 839–844.

39. NicolJW, HeltGA, BlanchardSGJr, RajaA, LoraineAE (2009) The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics 25: 2730–2731.

40. KimJ, KawasakiI, ShimYH (2010) cdc-25.2, a C. elegans ortholog of cdc25, is required to promote oocyte maturation. Journal of cell science 123: 993–1000.

41. BudirahardjaY, GonczyP (2009) Coupling the cell cycle to development. Development 136: 2861–2872.

42. van den HeuvelS (2005) Cell-cycle regulation. WormBook : the online review of C. elegans biology 1–16.

43. SegrefA, CabelloJ, ClucasC, SchnabelR, JohnstoneIL (2010) Fate specification and tissue-specific cell cycle control of the Caenorhabditis elegans intestine. Molecular biology of the cell 21: 725–738.

44. KirienkoNV, ManiK, FayDS (2010) Cancer models in Caenorhabditis elegans. Developmental dynamics : an official publication of the American Association of Anatomists 239: 1413–1448.

45. KosticI, RoyR (2002) Organ-specific cell division abnormalities caused by mutation in a general cell cycle regulator in C. elegans. Development 129: 2155–2165.

46. AshcroftN, GoldenA (2002) CDC-25.1 regulates germline proliferation in Caenorhabditis elegans. Genesis 33: 1–7.

47. JamoraC, LeeP, KocieniewskiP, AzharM, HosokawaR, et al. (2005) A signaling pathway involving TGF-beta2 and Snail in hair follicle morphogenesis. Plos Biology 3: e11.

48. LaiSL, MillerMR, RobinsonKJ, DoeCQ (2012) The Snail family member Worniu is continuously required in neuroblasts to prevent Elav-induced premature differentiation. Developmental cell 23: 849–857.

49. KentWJ, SugnetCW, FureyTS, RoskinKM, PringleTH, et al. (2002) The human genome browser at UCSC. Genome research 12: 996–1006.

50. Moreno-BuenoG, PortilloF, CanoA (2008) Transcriptional regulation of cell polarity in EMT and cancer. Oncogene 27: 6958–6969.

51. EvdokimovaV, TognonC, NgT, SorensenPH (2009) Reduced proliferation and enhanced migration: two sides of the same coin? Molecular mechanisms of metastatic progression by YB-1. Cell cycle 8: 2901–2906.

52. EvdokimovaV, TognonC, NgT, RuzanovP, MelnykN, et al. (2009) Translational activation of snail1 and other developmentally regulated transcription factors by YB-1 promotes an epithelial-mesenchymal transition. Cancer cell 15: 402–415.

53. GuoW, KeckesovaZ, DonaherJL, ShibueT, TischlerV, et al. (2012) Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 148: 1015–1028.

54. JordanNV, JohnsonGL, AbellAN (2011) Tracking the intermediate stages of epithelial-mesenchymal transition in epithelial stem cells and cancer. Cell cycle 10: 2865–2873.

55. ManiSA, GuoW, LiaoMJ, EatonEN, AyyananA, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704–715.

56. BrennerS (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94.

57. Riddle DL, Blumenthal T, Meyer B, Priess JR, editors(1997) C. elegans II: Cold Spring Harbor: Cold Spring Harobr Laboratory Press.

58. SimmerF, TijstermanM, ParrishS, KoushikaSP, NonetML, et al. (2002) Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Current biology 12: 1317–1319.

59. TimmonsL, FireA (1998) Specific interference by ingested dsRNA. Nature 395: 854.

60. FireA, XuS, MontgomeryMK, KostasSA, DriverSE, et al. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806–811.

61. MelloC, FireA (1995) DNA transformation. Methods in cell biology 48: 451–482.

62. StromeS, WoodWB (1982) Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 79: 1558–1562.

63. KimJ, LeeAR, KawasakiI, StromeS, ShimYH (2009) A mutation of cdc-25.1 causes defects in germ cells but not in somatic tissues in C. elegans. Molecules and Cells 28: 43–48.

64. ZhongM, NiuW, LuZJ, SarovM, MurrayJI, et al. (2010) Genome-wide identification of binding sites defines distinct functions for Caenorhabditis elegans PHA-4/FOXA in development and environmental response. PLoS genetics 6: e1000848.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#