The Class Homeodomain Factors and Cooperate in . Embryonic Progenitor Cells to Regulate Robust Development

English version České info

Animals develop as one initial cell, the fertilized egg, repeatedly divides and its progeny differentiate, ultimately producing diverse cell types. This occurs in large part by the expression of unique combinations of regulatory genes, such as transcription factors, in precursors of each cell type. These early factors are typically reused in precursors of different cell types. The nematode worm Caenorhabditis elegans is a powerful system in which to identify developmental regulators because it has a rapid and reproducible development, yet it shares most of its developmental regulators with more complex organisms such as humans. We used state-of-the-art microscopy and computer-aided cell tracking methods to identify the developmental role of worm homologs of the OTX and PITX genes, whose human homologs play a role in the development of the brain, eye, and pituitary among other tissues. We identified broad roles for OTX in regulating development for many distinct cell types including muscles, neurons and skin, and found a redundant role for both OTX and PITX in a subset of cells. Future studies of these genes should address whether these genes also act redundantly in mammals.

Vyšlo v časopise: The Class Homeodomain Factors and Cooperate in . Embryonic Progenitor Cells to Regulate Robust Development. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1005003
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005003

Souhrn

Zdroje

1. Murray JI, Boyle TJ, Preston E, Vafeados D, Mericle B, et al. (2012) Multidimensional regulation of gene expression in the C. elegans embryo. Genome research.

2. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364–2368. 11743205

3. Ow MC, Martinez NJ, Olsen PH, Silverman HS, Barrasa MI, et al. (2008) The FLYWCH transcription factors FLH-1, FLH-2, and FLH-3 repress embryonic expression of microRNA genes in C. elegans. Genes Dev 22: 2520–2534. doi: 10.1101/gad.1678808 18794349

4. Reece-Hoyes JS, Pons C, Diallo A, Mori A, Shrestha S, et al. (2013) Extensive rewiring and complex evolutionary dynamics in a C. elegans multiparameter transcription factor network. Mol Cell 51: 116–127. doi: 10.1016/j.molcel.2013.05.018 23791784

5. Ritter AD, Shen Y, Fuxman Bass J, Jeyaraj S, Deplancke B, et al. (2013) Complex expression dynamics and robustness in C. elegans insulin networks. Genome Res 23: 954–965. doi: 10.1101/gr.150466.112 23539137

6. Good K, Ciosk R, Nance J, Neves A, Hill RJ, et al. (2004) The T-box transcription factors TBX-37 and TBX-38 link GLP-1/Notch signaling to mesoderm induction in C. elegans embryos. Development 131: 1967–1978. 15056620

7. Lehner B, Crombie C, Tischler J, Fortunato A, Fraser AG (2006) Systematic mapping of genetic interactions in Caenorhabditis elegans identifies common modifiers of diverse signaling pathways. Nat Genet 38: 896–903. 16845399

8. Sulston JE, Horvitz HR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Developmental Biology 56: 110–156. 838129

9. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology 100: 64–119. 6684600

10. Kaletta T, Schnabel H, Schnabel R (1997) Binary specification of the embryonic lineage in Caenorhabditis elegans. Nature 390: 294–298. 9384382

11. Mello CC, Draper BW, Krause M, Weintraub H, Priess JR (1992) The pie-1 and mex-1 genes and maternal control of blastomere identity in early C. elegans embryos. Cell 70: 163–176. 1623520

12. Bowerman B, Draper BW, Mello CC, Priess JR (1993) The maternal gene skn-1 encodes a protein that is distributed unequally in early C. elegans embryos. Cell 74: 443–452. 8348611

13. Mello CC, Draper BW, Priess JR (1994) The maternal genes apx-1 and glp-1 and establishment of dorsal-ventral polarity in the early C. elegans embryo. Cell 77: 95–106. 8156602

14. Lin R, Thompson S, Priess JR (1995) pop-1 encodes an HMG box protein required for the specification of a mesoderm precursor in early C. elegans embryos. Cell 83: 599–609. 7585963

15. Zhu J, Hill RJ, Heid PJ, Fukuyama M, Sugimoto A, et al. (1997) end-1 encodes an apparent GATA factor that specifies the endoderm precursor in Caenorhabditis elegans embryos. Genes Dev 11: 2883–2896. 9353257

16. Tenenhaus C, Schubert C, Seydoux G (1998) Genetic requirements for PIE-1 localization and inhibition of gene expression in the embryonic germ lineage of Caenorhabditis elegans. Developmental Biology 200: 212–224. 9705228

17. Azzaria M, Goszczynski B, Chung MA, Kalb JM, McGhee JD (1996) A fork head/HNF-3 homolog expressed in the pharynx and intestine of the Caenorhabditis elegans embryo. Dev Biol 178: 289–303. 8812130

18. Fukushige T, Hawkins MG, McGhee JD (1998) The GATA-factor elt-2 is essential for formation of the Caenorhabditis elegans intestine. Dev Biol 198: 286–302. 9659934

19. Fukushige T, Krause M (2005) The myogenic potency of HLH-1 reveals wide-spread developmental plasticity in early C. elegans embryos. Development 132: 1795–1805. 15772130

20. Bao Z, Murray JI, Boyle T, Ooi SL, Sandel MJ, et al. (2006) Automated cell lineage tracing in Caenorhabditis elegans. Proc Natl Acad Sci U S A.

21. Murray JI, Bao Z, Boyle TJ, Boeck ME, Mericle BL, et al. (2008) Automated analysis of embryonic gene expression with cellular resolution in C. elegans. Nat Methods 5: 703–709. doi: 10.1038/nmeth.1228 18587405

22. Sarov M, Murray JI, Schanze K, Pozniakovski A, Niu W, et al. (2012) A genome-scale resource for in vivo tag-based protein function exploration in C. elegans. Cell 150: 855–866. doi: 10.1016/j.cell.2012.08.001 22901814

23. Mace DL, Weisdepp P, Gevirtzman L, Boyle T, Waterston RH (2013) A High-Fidelity Cell Lineage Tracing Method for Obtaining Systematic Spatiotemporal Gene Expression Patterns in Caenorhabditis elegans. G3 3: 851–863. doi: 10.1534/g3.113.005918 23550142

24. Hutter H, Schnabel R (1994) glp-1 and inductions establishing embryonic axes in C. elegans. Development 120: 2051–2064. 7925009

25. Du Z, Santella A, He F, Tiongson M, Bao Z (2014) De novo inference of systems-level mechanistic models of development from live-imaging-based phenotype analysis. Cell 156: 359–372. doi: 10.1016/j.cell.2013.11.046 24439388

26. Giurumescu CA, Kang S, Planchon TA, Betzig E, Bloomekatz J, et al. (2012) Quantitative semi-automated analysis of morphogenesis with single-cell resolution in complex embryos. Development.

27. Richards JL, Zacharias AL, Walton T, Burdick JT, Murray JI (2013) A quantitative model of normal Caenorhabditis elegans embryogenesis and its disruption after stress. Developmental biology 374: 12–23. doi: 10.1016/j.ydbio.2012.11.034 23220655

28. Simeone A, Acampora D, Mallamaci A, Stornaiuolo A, D’Apice MR, et al. (1993) A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J 12: 2735–2747. 8101484

29. Chen S, Wang QL, Nie Z, Sun H, Lennon G, et al. (1997) Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19: 1017–1030. 9390516

30. Matsuo I, Kuratani S, Kimura C, Takeda N, Aizawa S (1995) Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev 9: 2646–2658. 7590242

31. Acampora D, Mazan S, Avantaggiato V, Barone P, Tuorto F, et al. (1996) Epilepsy and brain abnormalities in mice lacking the Otx1 gene. Nat Genet 14: 218–222. 8841200

32. Kablar B, Vignali R, Menotti L, Pannese M, Andreazzoli M, et al. (1996) Xotx genes in the developing brain of Xenopus laevis. Mech Dev 55: 145–158. 8861095

33. Andreazzoli M, Pannese M, Boncinelli E (1997) Activating and repressing signals in head development: the role of Xotx1 and Xotx2. Development 124: 1733–1743. 9165121

34. Furukawa T, Morrow EM, Cepko CL (1997) Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91: 531–541. 9390562

35. Zhang Y, Miki T, Iwanaga T, Koseki Y, Okuno M, et al. (2002) Identification, tissue expression, and functional characterization of Otx3, a novel member of the Otx family. J Biol Chem 277: 28065–28069. 12055180

36. Viczian AS, Vignali R, Zuber ME, Barsacchi G, Harris WA (2003) XOtx5b and XOtx2 regulate photoreceptor and bipolar fates in the Xenopus retina. Development 130: 1281–1294. 12588845

37. Ohtoshi A, Behringer RR (2004) Neonatal lethality, dwarfism, and abnormal brain development in Dmbx1 mutant mice. Mol Cell Biol 24: 7548–7558. 15314164

38. Chang S, Johnston RJ Jr., Hobert O (2003) A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans. Genes & Development 17: 2123–2137.

39. Lanjuin A, VanHoven MK, Bargmann CI, Thompson JK, Sengupta P (2003) Otx/otd homeobox genes specify distinct sensory neuron identities in C. elegans. Dev Cell 5: 621–633. 14536063

40. Nakano S, Ellis RE, Horvitz HR (2010) Otx-dependent expression of proneural bHLH genes establishes a neuronal bilateral asymmetry in C. elegans. Development 137: 4017–4027. doi: 10.1242/dev.058834 21041366

41. Sarin S, O’Meara MM, Flowers EB, Antonio C, Poole RJ, et al. (2007) Genetic screens for Caenorhabditis elegans mutants defective in left/right asymmetric neuronal fate specification. Genetics 176: 2109–2130. 17717195

42. Kim K, Kim R, Sengupta P (2010) The HMX/NKX homeodomain protein MLS-2 specifies the identity of the AWC sensory neuron type via regulation of the ceh-36 Otx gene in C. elegans. Development 137: 963–974. doi: 10.1242/dev.044719 20150279

43. Raj A, van den Bogaard P, Rifkin SA, van Oudenaarden A, Tyagi S (2008) Imaging individual mRNA molecules using multiple singly labeled probes. Nat Methods 5: 877–879. doi: 10.1038/nmeth.1253 18806792

44. Bao Z, Zhao Z, Boyle TJ, Murray JI, Waterston RH (2008) Control of cell cycle timing during C. elegans embryogenesis. Dev Biol 318: 65–72. doi: 10.1016/j.ydbio.2008.02.054 18430415

45. Smit RB, Schnabel R, Gaudet J (2008) The HLH-6 transcription factor regulates C. elegans pharyngeal gland development and function. PLoS Genet 4: e1000222. doi: 10.1371/journal.pgen.1000222 18927627

46. Hunt-Newbury R, Viveiros R, Johnsen R, Mah A, Anastas D, et al. (2007) High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS Biol 5: e237. 17850180

47. Berger MF, Badis G, Gehrke AR, Talukder S, Philippakis AA, et al. (2008) Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133: 1266–1276. doi: 10.1016/j.cell.2008.05.024 18585359

48. Jolma A, Yan J, Whitington T, Toivonen J, Nitta KR, et al. (2013) DNA-binding specificities of human transcription factors. Cell 152: 327–339. doi: 10.1016/j.cell.2012.12.009 23332764

49. Jin Y, Hoskins R, Horvitz HR (1994) Control of type-D GABAergic neuron differentiation by C. elegans UNC-30 homeodomain protein. Nature 372: 780–783. 7997265

50. Williams-Masson EM, Malik AN, Hardin J (1997) An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis. Development 124: 2889–2901. 9247332

51. Chin-Sang ID, George SE, Ding M, Moseley SL, Lynch AS, et al. (1999) The ephrin VAB-2/EFN-1 functions in neuronal signaling to regulate epidermal morphogenesis in C. elegans. Cell 99: 781–790. 10619431

52. Van Auken K, Weaver DC, Edgar LG, Wood WB (2000) Caenorhabditis elegans embryonic axial patterning requires two recently discovered posterior-group Hox genes. Proceedings of the National Academy of Sciences of the United States of America 97: 4499–4503. 10781051

53. Stone CE, Hall DH, Sundaram MV (2009) Lipocalin signaling controls unicellular tube development in the Caenorhabditis elegans excretory system. Developmental biology 329: 201–211. doi: 10.1016/j.ydbio.2009.02.030 19269285

54. Abdus-Saboor I, Mancuso VP, Murray JI, Palozola K, Norris C, et al. (2011) Notch and Ras promote sequential steps of excretory tube development in C. elegans. Development 138: 3545–3555. doi: 10.1242/dev.068148 21771815

55. Abdus-Saboor I, Stone CE, Murray JI, Sundaram MV (2012) The Nkx5/HMX homeodomain protein MLS-2 is required for proper tube cell shape in the C. elegans excretory system. Developmental biology.

56. Mancuso VP, Parry JM, Storer L, Poggioli C, Nguyen KC, et al. (2012) Extracellular leucine-rich repeat proteins are required to organize the apical extracellular matrix and maintain epithelial junction integrity in C. elegans. Development 139: 979–990. doi: 10.1242/dev.075135 22278925

57. Yoshimura S, Murray JI, Lu Y, Waterston RH, Shaham S (2008) mls-2 and vab-3 Control glia development, hlh-17/Olig expression and glia-dependent neurite extension in C. elegans. Development 135: 2263–2275. doi: 10.1242/dev.019547 18508862

58. Cochella L, Hobert O (2012) Embryonic priming of a miRNA locus predetermines postmitotic neuronal left/right asymmetry in C. elegans. Cell 151: 1229–1242. doi: 10.1016/j.cell.2012.10.049 23201143

59. Raj A, Rifkin SA, Andersen E, van Oudenaarden A (2010) Variability in gene expression underlies incomplete penetrance. Nature 463: 913–918. doi: 10.1038/nature08781 20164922

60. Maduro MF, Hill RJ, Heid PJ, Newman-Smith ED, Zhu J, et al. (2005) Genetic redundancy in endoderm specification within the genus Caenorhabditis. Dev Biol 284: 509–522. 15979606

61. Andachi Y (2004) Caenorhabditis elegans T-box genes tbx-9 and tbx-8 are required for formation of hypodermis and body-wall muscle in embryogenesis. Genes to cells: devoted to molecular & cellular mechanisms 9: 331–344.

62. Neves A, Priess JR (2005) The REF-1 family of bHLH transcription factors pattern C. elegans embryos through Notch-dependent and Notch-independent pathways. Dev Cell 8: 867–879. 15935776

63. Boeck ME, Boyle T, Bao Z, Murray J, Mericle B, et al. (2011) Specific roles for the GATA transcription factors end-1 and end-3 during C. elegans E-lineage development. Developmental Biology 358: 245–255.

64. Nakano S, Stillman B, Horvitz HR (2011) Replication-coupled chromatin assembly generates a neuronal bilateral asymmetry in C. elegans. Cell 147: 1525–1536. doi: 10.1016/j.cell.2011.11.053 22177093

65. Wightman B, Ebert B, Carmean N, Weber K, Clever S (2005) The C. elegans nuclear receptor gene fax-1 and homeobox gene unc-42 coordinate interneuron identity by regulating the expression of glutamate receptor subunits and other neuron-specific genes. Dev Biol 287: 74–85. 16183052

66. Grove CA, De Masi F, Barrasa MI, Newburger DE, Alkema MJ, et al. (2009) A multiparameter network reveals extensive divergence between C. elegans bHLH transcription factors. Cell 138: 314–327. doi: 10.1016/j.cell.2009.04.058 19632181

67. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94. 4366476

68. Praitis V, Casey E, Collar D, Austin J (2001) Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 157: 1217–1226. 11238406

69. McNally K, Audhya A, Oegema K, McNally FJ (2006) Katanin controls mitotic and meiotic spindle length. J Cell Biol 175: 881–891. 17178907

70. Shaham S (2006) WormBook: Methods in Cell Biology. In: Community TCeR, editor. Wormbook.

71. Bao Z, Murray JI (2011) Mounting Caenorhabditis elegans embryos for live imaging of embryogenesis. Cold Spring Harbor protocols 2011. doi: 10.1101/pdb.prot065599 21880814

72. Boyle TJ, Bao Z, Murray JI, Araya CL, Waterston RH (2006) AceTree: a tool for visual analysis of Caenorhabditis elegans embryogenesis. BMC Bioinformatics 7: 275. 16740163

73. Murray JI, Bao Z, Boyle T, Waterston RH (2006) The lineaging of fluorescently-labeled Caenorhabditis elegans embryos with StarryNite and AceTree. Nature Protocols 1: 1468–1476. 17406437

74. Santella A, Du Z, Nowotschin S, Hadjantonakis AK, Bao Z (2010) A hybrid blob-slice model for accurate and efficient detection of fluorescence labeled nuclei in 3D. BMC Bioinformatics 11: 580. doi: 10.1186/1471-2105-11-580 21114815

75. Murray JI, Bao Z (2012) Automated Lineage and Expression Profiling in Live Caenorhabditis elegans Embryos. Cold Spring Harbor protocols 2012. doi: 10.1101/pdb.prot070615 22854571

76. Raj A, Tyagi S (2010) Detection of individual endogenous RNA transcripts in situ using multiple singly labeled probes. Methods Enzymol 472: 365–386. doi: 10.1016/S0076-6879(10)72004-8 20580972