Notch and Delta are required for survival of the germline stem cell lineage in testes of Drosophila melanogaster
Autoři:
Chun L. Ng aff001; Yue Qian aff002; Cordula Schulz aff003
Působiště autorů:
University of Texas Southwestern Medical Center, Dallas, Texas, United States of America
aff001; University of North Georgia, Department of Biology, Oakwood, Georgia, United States of America
aff002; University of Georgia, Department of Cellular Biology, Athens, Georgia, United States of America
aff003
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0222471
Souhrn
In all metazoan species, sperm is produced from germline stem cells. These self-renew and produce daughter cells that amplify and differentiate dependent on interactions with somatic support cells. In the male gonad of Drosophila melanogaster, the germline and somatic cyst cells co-differentiate as cysts, an arrangement in which the germline is completely enclosed by cytoplasmic extensions from the cyst cells. Notch is a developmentally relevant receptor in a pathway requiring immediate proximity with the signal sending cell. Here, we show that Notch is expressed in the cyst cells of wild-type testes. Notch becomes activated in the transition zone, an apical area of the testes in which the cyst cells express stage-specific transcription factors and the enclosed germline finalizes transit-amplifying divisions. Reducing the ligand Delta from the germline cells via RNA-Interference or reducing the receptor Notch from the cyst cells via CRISPR resulted in cell death concomitant with loss of germline cells from the transition zone. This shows that Notch signaling is essential for the survival of the germline stem cell lineage.
Klíčová slova:
Biology and life sciences – Cell biology – Genetics – Organisms – Eukaryota – Research and analysis methods – Animal studies – Experimental organism systems – Model organisms – Animals – Invertebrates – Arthropoda – Insects – Drosophila – Drosophila melanogaster – Animal models – Phenotypes – Developmental biology – Cell differentiation – Cellular types – Animal cells – Stem cells – Anatomy – Medicine and health sciences – Reproductive system – Genital anatomy – Signal transduction – Cell signaling – Germ cells – Testes – Notch signaling – Sperm – Spermatogonia – Spermatocytes
Zdroje
1. Guruharsha KG, Kankel MW, Artavanis-Tsakonas S. The Notch signalling system: recent insights into the complexity of a conserved pathway. Nat Rev Genet. 2012;13(9):654–66. doi: 10.1038/nrg3272 22868267
2. Jain R, Rentschler S, Epstein JA. Notch and cardiac outflow tract development. Ann N Y Acad Sci. 2010;1188:184–90. doi: 10.1111/j.1749-6632.2009.05099.x 20201902
3. MacGrogan D, Nus M, de la Pompa JL. Notch signaling in cardiac development and disease. Curr Top Dev Biol. 2010;92:333–65. doi: 10.1016/S0070-2153(10)92011-5 20816401
4. Dorsky RI, Chang WS, Rapaport DH, Harris WA. Regulation of neuronal diversity in the Xenopus retina by Delta signalling. Nature. 1997;385(6611):67–70. doi: 10.1038/385067a0 8985247
5. Wang S, Sdrulla AD, diSibio G, Bush G, Nofziger D, Hicks C, et al. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron. 1998;21(1):63–75. doi: 10.1016/s0896-6273(00)80515-2 9697852
6. Berset T, Hoier EF, Battu G, Canevascini S, Hajnal A. Notch inhibition of RAS signaling through MAP kinase phosphatase LIP-1 during C. elegans vulval development. Science. 2001;291(5506):1055–8. doi: 10.1126/science.1055642 11161219
7. Mason HA, Rakowiecki SM, Gridley T, Fishell G. Loss of notch activity in the developing central nervous system leads to increased cell death. Dev Neurosci. 2006;28(1–2):49–57. doi: 10.1159/000090752 16508303
8. Nefedova Y, Sullivan DM, Bolick SC, Dalton WS, Gabrilovich DI. Inhibition of Notch signaling induces apoptosis of myeloma cells and enhances sensitivity to chemotherapy. Blood. 2008;111(4):2220–9. doi: 10.1182/blood-2007-07-102632 18039953
9. Ye QF, Zhang YC, Peng XQ, Long Z, Ming YZ, He LY. Silencing Notch-1 induces apoptosis and increases the chemosensitivity of prostate cancer cells to docetaxel through Bcl-2 and Bax. Oncol Lett. 2012;3(4):879–84. doi: 10.3892/ol.2012.572 22741011
10. Zweidler-McKay PA, He Y, Xu L, Rodriguez CG, Karnell FG, Carpenter AC, et al. Notch signaling is a potent inducer of growth arrest and apoptosis in a wide range of B-cell malignancies. Blood. 2005;106(12):3898–906. doi: 10.1182/blood-2005-01-0355 16118316
11. Bray SJ. Notch signalling in context. Nat Rev Mol Cell Biol. 2016;17(11):722–35. doi: 10.1038/nrm.2016.94 27507209
12. Hori K, Sen A, Artavanis-Tsakonas S. Notch signaling at a glance. J Cell Sci. 2013;126(Pt 10):2135–40. doi: 10.1242/jcs.127308 23729744
13. Kopan R, Ilagan MX. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell. 2009;137(2):216–33. doi: 10.1016/j.cell.2009.03.045 19379690
14. Hardy RW, Tokuyasu KT, Lindsley DL, Garavito M. The germinal proliferation center in the testis of Drosophila melanogaster. J Ultrastruct Res. 1979;69(2):180–90. doi: 10.1016/s0022-5320(79)90108-4 114676
15. Griswold MD. The central role of Sertoli cells in spermatogenesis. Semin Cell Dev Biol. 1998;9(4):411–6. doi: 10.1006/scdb.1998.0203 9813187
16. Yamashita YM, Jones DL, Fuller MT. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science. 2003;301(5639):1547–50. doi: 10.1126/science.1087795 12970569
17. Schulz C, Wood CG, Jones DL, Tazuke SI, Fuller MT. Signaling from germ cells mediated by the rhomboid homolog stet organizes encapsulation by somatic support cells. Development. 2002;129(19):4523–34. 12223409
18. Sarkar A, Parikh N, Hearn SA, Fuller MT, Tazuke SI, Schulz C. Antagonistic roles of Rac and Rho in organizing the germ cell microenvironment. Curr Biol. 2007;17(14):1253–8. doi: 10.1016/j.cub.2007.06.048 17629483
19. Fairchild MJ, Islam F, Tanentzapf G. Identification of genetic networks that act in the somatic cells of the testis to mediate the developmental program of spermatogenesis. PLoS Genet. 2017;13(9):e1007026. doi: 10.1371/journal.pgen.1007026 28957323
20. Kiger AA, White-Cooper H, Fuller MT. Somatic support cells restrict germline stem cell self-renewal and promote differentiation. Nature. 2000;407(6805):750–4. doi: 10.1038/35037606 11048722
21. Matunis E, Tran J, Gonczy P, Caldwell K, DiNardo S. punt and schnurri regulate a somatically derived signal that restricts proliferation of committed progenitors in the germline. Development. 1997;124(21):4383–91. 9334286
22. Fuller MT. Spermatogenesis in Drosophila. In: Bate M, Martinez Arias A., editor. The development of Drosophila melanogaster. Cold Spring Harbor, New York, USA: Cold Spring Harbor Laboratory Press; 1993. p. 71–148.
23. Zoller R, Schulz C. The Drosophila cyst stem cell lineage: Partners behind the scenes? Spermatogenesis. 2012;2(3):145–57. doi: 10.4161/spmg.21380 23087834
24. Leatherman JL, Dinardo S. Zfh-1 controls somatic stem cell self-renewal in the Drosophila testis and nonautonomously influences germline stem cell self-renewal. Cell Stem Cell. 2008;3(1):44–54. doi: 10.1016/j.stem.2008.05.001 18593558
25. Li MA, Alls JD, Avancini RM, Koo K, Godt D. The large Maf factor Traffic Jam controls gonad morphogenesis in Drosophila. Nat Cell Biol. 2003;5(11):994–1000. doi: 10.1038/ncb1058 14578908
26. Fabrizio JJ, Boyle M, DiNardo S. A somatic role for eyes absent (eya) and sine oculis (so) in Drosophila spermatocyte development. Dev Biol. 2003;258(1):117–28. doi: 10.1016/s0012-1606(03)00127-1 12781687
27. Parrott BB, Hudson A, Brady R, Schulz C. Control of germline stem cell division frequency-a novel, developmentally regulated role for epidermal growth factor signaling. PLoS One. 2012;7(5):e36460. doi: 10.1371/journal.pone.0036460 22586473
28. Zacharioudaki E, Bray SJ. Tools and methods for studying Notch signaling in Drosophila melanogaster. Methods. 2014;68(1):173–82. doi: 10.1016/j.ymeth.2014.03.029 24704358
29. Kitadate Y, Kobayashi S. Notch and Egfr signaling act antagonistically to regulate germ-line stem cell niche formation in Drosophila male embryonic gonads. Proc Natl Acad Sci U S A. 2010;107(32):14241–6. doi: 10.1073/pnas.1003462107 20660750
30. Hudson AG, Parrott BB, Qian Y, Schulz C. A temporal signature of epidermal growth factor signaling regulates the differentiation of germline cells in testes of Drosophila melanogaster. PLoS One. 2013;8(8):e70678. doi: 10.1371/journal.pone.0070678 23940622
31. Qian Y, Dominado N, Zoller R, Ng C, Kudyba K, Siddall NA, et al. Ecdysone signaling opposes epidermal growth factor signaling in regulating cyst differentiation in the male gonad of Drosophila melanogaster. Dev Biol. 2014;394(2):217–27. doi: 10.1016/j.ydbio.2014.08.019 25169192
32. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993;118(2):401–15. 8223268
33. Duffy JB. GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis. 2002;34(1–2):1–15. doi: 10.1002/gene.10150 12324939
34. Baker R, Schubiger G. Autonomous and nonautonomous Notch functions for embryonic muscle and epidermis development in Drosophila. Development. 1996;122(2):617–26. 8625813
35. Hayashi S, Ito K, Sado Y, Taniguchi M, Akimoto A, Takeuchi H, et al. GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis. 2002;34(1–2):58–61. doi: 10.1002/gene.10137 12324948
36. Xu T, Rubin GM. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development. 1993;117(4):1223–37. 8404527
37. Van Doren M, Williamson AL, Lehmann R. Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr Biol. 1998;8(4):243–6. doi: 10.1016/s0960-9822(98)70091-0 9501989
38. Gratz SJ, Rubinstein CD, Harrison MM, Wildonger J, O'Connor-Giles KM. CRISPR-Cas9 Genome Editing in Drosophila. Curr Protoc Mol Biol. 2015;111:31 2 1–20.
39. Gao Y, Liu T, Huang Y. MicroRNA-134 suppresses endometrial cancer stem cells by targeting POGLUT1 and Notch pathway proteins. FEBS Lett. 2015;589(2):207–14. doi: 10.1016/j.febslet.2014.12.002 25528443
40. Murata A, Hayashi S. Notch-Mediated Cell Adhesion. Biology (Basel). 2016;5(1).
41. Le Gall M, De Mattei C, Giniger E. Molecular separation of two signaling pathways for the receptor, Notch. Dev Biol. 2008;313(2):556–67. doi: 10.1016/j.ydbio.2007.10.030 18062953
42. Bradley WD, Koleske AJ. Regulation of cell migration and morphogenesis by Abl-family kinases: emerging mechanisms and physiological contexts. J Cell Sci. 2009;122(Pt 19):3441–54. doi: 10.1242/jcs.039859 19759284
43. Zandy NL, Pendergast AM. Abl tyrosine kinases modulate cadherin-dependent adhesion upstream and downstream of Rho family GTPases. Cell Cycle. 2008;7(4):444–8. doi: 10.4161/cc.7.4.5452 18235247
44. Zandy NL, Playford M, Pendergast AM. Abl tyrosine kinases regulate cell-cell adhesion through Rho GTPases. Proc Natl Acad Sci U S A. 2007;104(45):17686–91. doi: 10.1073/pnas.0703077104 17965237
45. Ohlstein B, Spradling A. The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature. 2006;439(7075):470–4. doi: 10.1038/nature04333 16340960
46. Ohlstein B, Spradling A. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science. 2007;315(5814):988–92. doi: 10.1126/science.1136606 17303754
47. Micchelli CA, Perrimon N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature. 2006;439(7075):475–9. doi: 10.1038/nature04371 16340959
48. Perdigoto CN, Schweisguth F, Bardin AJ. Distinct levels of Notch activity for commitment and terminal differentiation of stem cells in the adult fly intestine. Development. 2011;138(21):4585–95. doi: 10.1242/dev.065292 21965616
49. Song X, Call GB, Kirilly D, Xie T. Notch signaling controls germline stem cell niche formation in the Drosophila ovary. Development. 2007;134(6):1071–80. doi: 10.1242/dev.003392 17287246
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