The Jak-STAT target chinmo prevents sex transformation of adult stem cells in the drosophila testis niche

Developmental Cell

Volumn 31, Issue 4, 2014, Pages 474-486

  Ma, Qing ^a   Wawersik, Matthew ^b   Matunis, Erika L ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Dept of Economics and Thomas Jefferson Program in Public Policy at the College of William and Mary   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

JANUS KINASE; STAT PROTEIN; CHINMO PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; NERVE PROTEIN; TRANSCRIPTION FACTOR;

ADULT STEM CELL; ARTICLE; CELL PROLIFERATION; CELL TRANSDIFFERENTIATION; CHRONOLOGICALLY INAPPROPRIATE MORPHOGENESIS; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENDER IDENTITY; GERM CELL; MALE; MORPHOGENESIS; NONHUMAN; OVARY FOLLICLE CELL; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN TARGETING; SEX DETERMINATION; SEX TRANSFORMATION; SOMATIC CELL; STEM CELL NICHE; TESTIS; AGING; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; SEX DETERMINATION PROCESS; SIGNAL TRANSDUCTION; STEM CELL;

MAMMALIA;

AGING; ANIMALS; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; JANUS KINASES; MALE; NERVE TISSUE PROTEINS; SEX DETERMINATION PROCESSES; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; STEM CELL NICHE; STEM CELLS; TESTIS; TRANSCRIPTION FACTORS;

EID: 84921280508     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.10.004     Document Type: Article

References (44)

1. Amoyel M., Sanny J., Burel M., Bach E.A. Hedgehog is required for CySC self-renewal but does not contribute to the GSC niche in the Drosophila testis. Development 2013, 140:56-65.
2. Brawley C., Matunis E. Regeneration of male germline stem cells by spermatogonial dedifferentiation invivo. Science 2004, 304:1331-1334.
3. Brennan M.D., Weiner A.J., Goralski T.J., Mahowald A.P. The follicle cells are a major site of vitellogenin synthesis in Drosophila melanogaster. Dev. Biol. 1982, 89:225-236.
4. Burtis K.C., Coschigano K.T., Baker B.S., Wensink P.C. The doublesex proteins of Drosophila melanogaster bind directly to a sex-specific yolk protein gene enhancer. EMBO J. 1991, 10:2577-2582.
5. Cai D., Chen S.C., Prasad M., He L., Wang X., Choesmel-Cadamuro V., Sawyer J.K., Danuser G., Montell D.J. Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration. Cell 2014, 157:1146-1159.
6. Chang Y.C., Jang A.C., Lin C.H., Montell D.J. Castor is required for Hedgehog-dependent cell-fate specification and follicle stem cell maintenance in Drosophila oogenesis. Proc. Natl. Acad. Sci. USA 2013, 110:E1734-E1742.
7. Coschigano K.T., Wensink P.C. Sex-specific transcriptional regulation by the male and female doublesex proteins of Drosophila. Genes Dev. 1993, 7:42-54.
8. de Cuevas M., Lilly M.A., Spradling A.C. Germline cyst formation in Drosophila. Annu. Rev. Genet. 1997, 31:405-428.
9. Flaherty M.S., Salis P., Evans C.J., Ekas L.A., Marouf A., Zavadil J., Banerjee U., Bach E.A. chinmo is a functional effector of the JAK/STAT pathway that regulates eye development, tumor formation, and stem cell self-renewal in Drosophila. Dev. Cell 2010, 18:556-568.
10. Fuller M.T., Spradling A.C. Male and female Drosophila germline stem cells: two versions of immortality. Science 2007, 316:402-404.
11. Gönczy P., DiNardo S. The germ line regulates somatic cyst cell proliferation and fate during Drosophila spermatogenesis. Development 1996, 122:2437-2447.
12. Hanson J.A., Ambaye A.B. Adult testicular granulosa cell tumor: a review of the literature for clinicopathologic predictors of malignancy. Arch. Pathol. Lab. Med. 2011, 135:143-146.
13. Hempel L.U., Oliver B. Sex-specific DoublesexM expression in subsets of Drosophila somatic gonad cells. BMC Dev. Biol. 2007, 7:113.
14. Hime G.R., Brill J.A., Fuller M.T. Assembly of ring canals in the male germ line from structural components of the contractile ring. J.Cell Sci. 1996, 109:2779-2788.
15. Issigonis M., Matunis E. The Drosophila BCL6 homolog Ken and Barbie promotes somatic stem cell self-renewal in the testis niche. Dev. Biol. 2012, 368:181-192.
16. Jackson S.M., Blochlinger K. cut interacts with Notch and protein kinase A to regulate egg chamber formation and to maintain germline cyst integrity during Drosophila oogenesis. Development 1997, 124:3663-3672.
17. Jinks T.M., Polydorides A.D., Calhoun G., Schedl P. The JAK/STAT signaling pathway is required for the initial choice of sexual identity in Drosophila melanogaster. Mol. Cell 2000, 5:581-587.
18. Kai T., Spradling A. An empty Drosophila stem cell niche reactivates the proliferation of ectopic cells. Proc. Natl. Acad. Sci. USA 2003, 100:4633-4638.
19. Kopp A. Dmrt genes in the development and evolution of sexual dimorphism. Trends Genet. 2012, 28:175-184.
20. Leatherman J.L., 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, 3:44-54.
21. Leatherman J.L., DiNardo S. Germline self-renewal requires cyst stem cells and stat regulates niche adhesion in Drosophila testes. Nat. Cell Biol. 2010, 12:806-811.
22. Lee G., Hall J.C., Park J.H. Doublesex gene expression in the central nervous system of Drosophila melanogaster. J.Neurogenet. 2002, 16:229-248.
23. Lin H., Yue L., Spradling A.C. The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 1994, 120:947-956.
24. Logan S.K., Garabedian M.J., Wensink P.C. DNA regions that regulate the ovarian transcriptional specificity of Drosophila yolk protein genes. Genes Dev. 1989, 3:1453-1461.
25. Mahowald A.P., Kambysellis M.P. Oogenesis. The Genetics and Biology of Drosophila 1980, 141-224. Academic Press, New York. M. Ashburner, T.R.F. Wright (Eds.).
26. Margolis J., Spradling A. Identification and behavior of epithelial stem cells in the Drosophila ovary. Development 1995, 121:3797-3807.
27. Masuyama H., Yamada M., Kamei Y., Fujiwara-Ishikawa T., Todo T., Nagahama Y., Matsuda M. Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka. Chromosome Res. 2012, 20:163-176.
28. Matson C.K., Zarkower D. Sex and the singular DM domain: insights into sexual regulation, evolution and plasticity. Nat. Rev. Genet. 2012, 13:163-174.
29. Matson C.K., Murphy M.W., Sarver A.L., Griswold M.D., Bardwell V.J., Zarkower D. DMRT1 prevents female reprogramming in the postnatal mammalian testis. Nature 2011, 476:101-104.
30. Matunis E., Tran J., Gönczy P., Caldwell K., DiNardo S. punt and schnurri regulate a somatically derived signal that restricts proliferation of committed progenitors in the germline. Development 1997, 124:4383-4391.
31. Matunis E.L., Stine R.R., de Cuevas M. Recent advances in Drosophila male germline stem cell biology. Spermatogenesis 2012, 2:137-144.
32. McKearin D.M., Spradling A.C. bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev. 1990, 4(12B):2242-2251.
33. Michel M., Kupinski A.P., Raabe I., Bökel C. Hh signalling is essential for somatic stem cell maintenance in the Drosophila testis niche. Development 2012, 139:2663-2669.
34. Nakada D., Oguro H., Levi B.P., Ryan N., Kitano A., Saitoh Y., Takeichi M., Wendt G.R., Morrison S.J. Oestrogen increases haematopoietic stem-cell self-renewal in females and during pregnancy. Nature 2014, 505:555-558.
35. Robinett C.C., Vaughan A.G., Knapp J.M., Baker B.S. Sex and the single cell. II. There is a time and place for sex. PLoS Biol. 2010, 8:e1000365.
36. Shibata K., Takase M., Nakamura M. The Dmrt1 expression in sex-reversed gonads of amphibians. Gen. Comp. Endocrinol. 2002, 127:232-241.
37. Stine R.R., Matunis E.L. Stem cell competition: finding balance in the niche. Trends Cell Biol. 2013, 23:357-364.
38. Tran J., Brenner T.J., DiNardo S. Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature 2000, 407:754-757.
39. Uhlenhaut N.H., Jakob S., Anlag K., Eisenberger T., Sekido R., Kress J., Treier A.C., Klugmann C., Klasen C., Holter N.I., et al. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 2009, 139:1130-1142.
40. Van Doren M., Williamson A.L., Lehmann R. Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr. Biol. 1998, 8:243-246.
41. Wawersik M., Milutinovich A., Casper A.L., Matunis E., Williams B., Van Doren M. Somatic control of germline sexual development is mediated by the JAK/STAT pathway. Nature 2005, 436:563-567.
42. Whitworth C., Jimenez E., Van Doren M. Development of sexual dimorphism in the Drosophila testis. Spermatogenesis 2012, 2:129-136.
43. Zhao D., McBride D., Nandi S., McQueen H.A., McGrew M.J., Hocking P.M., Lewis P.D., Sang H.M., Clinton M. Somatic sex identity is cell autonomous in the chicken. Nature 2010, 464:237-242.
44. Zhu S., Lin S., Kao C.F., Awasaki T., Chiang A.S., Lee T. Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 2006, 127:409-422.