Smurf-mediated differential proteolysis generates dynamic BMP signaling in germline stem cells during Drosophila testis development

Developmental Biology

Volumn 383, Issue 1, 2013, Pages 106-120

  Chang, Yi Jie ^a   Pi, Haiwei ^a   Hsieh, Chang Che ^a   Fuller, Margaret T ^b  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

BMP; Drosophila; Germline stem cells; Proteolysis; Smurf; Spermatogenesis

Indexed keywords

EID: 84885485110     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.08.014     Document Type: Article

References (57)

1. Asanuma K., Yanagida-Asanuma E., Faul C., Tomino Y., Kim K., Mundel P. Synaptopodin orchestrates actin organization and cell motility via regulation of RhoA signalling. Nat. Cell Biol. 2006, 8:485-491.
2. Barolo S., Carver L.A., Posakony J.W. GFP and beta-galactosidase transformation vectors for promoter/enhancer analysis in Drosophila. BioTechniques 2000, 29:726-732.
3. Bodenstein D. The postembryonic development of Drosophila. Biol. Drosophila 1950, 275-367.
4. Bunt S.M., Hime G.R. Ectopic activation of Dpp signalling in the male Drosophila germline inhibits germ cell differentiation. Genesis 2004, 39:84-93.
5. Casanueva M.O., Ferguson E.L. Germline stem cell number in the Drosophila ovary is regulated by redundant mechanisms that control Dpp signaling. Development 2004, 131:1881-1890.
6. Chen D., McKearin D. Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr. Biol. 2003, 13:1786-1791.
7. Chen D., McKearin D.M. A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 2003, 130:1159-1170.
8. Cheng P.L., Lu H., Shelly M., Gao H., Poo M.M. Phosphorylation of E3 ligase Smurf1 switches its substrate preference in support of axon development. Neuron 2011, 69:231-243.
9. Crickmore M.A., Mann R.A. Hox control of organ size by regulation of morphogen production and mobility. Science 2006, 313:63-68.
10. Davies E.L., Fuller M.T. Regulation of self-renewal and differentiation in adult stem cell lineages: lessons from the Drosophila male germ line. Cold Spring Harbor Symp. Quant. Biol. 2008, 73:137-145.
11. Edgar B.A., O'Farrell P.H. Genetic control of cell division patterns in the Drosophila embryo. Cell 1989, 57:177-187.
12. Gallagher E., Gao M., Liu Y.C., Karin M. Activation of the E3 ubiquitin ligase Itch through a phosphorylation-induced conformational change. Proc. Natl. Acad. Sci. USA 2006, 103:1717-1722.
13. Gancz D., Lengil T., Gilboa L. Coordinated regulation of niche and stem cell precursors by hormonal signaling. PLoS Biol. 2011, 9:e1001202.
14. Gonczy P., Matunis E., DiNardo S. bag-of-marbles and benign gonial cell neoplasm act in the germline to restrict proliferation during Drosophila spermatogenesis. Development 1997, 124:4361-4371.
15. Hayashi Y., Kobayashi S., Nakato H. Drosophila glypicans regulate the germline stem cell niche. J. Cell Biol. 2009, 187:473-480.
16. Hu X., Cherbas L., Cherbas P. Transcription activation by the ecdysone receptor (EcR/USP): identification of activation functions. Mol. Endocrinol. 2003, 17:716-731.
17. Inaba M., Yuan H., Salzmann V., Fuller M.T., Yamashita Y.M. E-cadherin is required for centrosome and spindle orientation in Drosophila male germline stem cells. PloS One 2010, 5:e12473.
18. Inaba M., Yuan H., Yamashita Y.M. String (Cdc25) regulates stem cell maintenance, proliferation and aging in Drosophila testis. Development 2011, 138:5079-5086.
19. Insco, M.L., Leon, A., Tam, C.H., McKearin, D.M., Fuller, M.T., 2009. Accumulation of a differentiation regulator specifies transit amplifying division number in an adult stem cell lineage. Proc. Natl. Acad. Sci. USA 106, 22311-22316.
20. Itman C., Wong C., Whiley P.A., Fernando D., Loveland K.L. TGFbeta superfamily signaling regulators are differentially expressed in the developing and adult mouse testis. Spermatogenesis 2011, 1:63-72.
21. 2 receptor for degradation. Mol. cell 2000, 6:1365-1375.
22. Kawase E., Wong M.D., Ding B.C., Xie T. Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 2004, 131:1365-1375.
23. 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.
24. 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.
25. Liang Y.Y., Lin X., Liang M., Brunicardi F.C., ten Dijke P., Chen Z., Choi K.W., Feng X.H. dSmurf selectively degrades decapentaplegic-activated MAD, and its overexpression disrupts imaginal disc development. J. Biol. Chem. 2003, 278:26307-26310.
26. Lin X., Liang M., Feng X.H. Smurf2 is a ubiquitin E3 ligase mediating proteasome-dependent degradation of Smad2 in transforming growth factor-beta signaling. J. Biol. Chem. 2000, 275:36818-36822.
27. Lu K., Yin X., Weng T., Xi S., Li L., Xing G., Cheng X., Yang X., Zhang L., He F. Targeting WW domains linker of HECT-type ubiquitin ligase Smurf1 for activation by CKIP-1. Nat. Cell Biol. 2008, 10:994-1002.
28. Lu W., Casanueva M.O., Mahowald A.P., Kato M., Lauterbach D., Ferguson E.L. Niche-associated activation of rac promotes the asymmetric division of Drosophila female germline stem cells. PLoS Biol. 2012, 10:e1001357.
29. McKearin D., Spradling A.C. Bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev. 1990, 4:2242-2251.
30. McKearin D., Ohlstein B. A role for the Drosophila bag-of-marbles protein in the differentiation of cystoblasts from germline stem cells. Development 1995, 121:2937-2947.
31. Michel M., Raabe I., Kupinski A.P., Perez-Palencia R., Bokel C. Local BMP receptor activation at adherens junctions in the Drosophila germline stem cell niche. Nat. Commun. 2011, 2:415.
32. Narbonne-Reveau K., Besse F., Lamour-Isnard C., Busson D., Pret A.M. fused regulates germline cyst mitosis and differentiation during Drosophila oogenesis. Mech. Dev. 2006, 123:197-209.
33. Narimatsu M., Bose R., Pye M., Zhang L., Miller B., Ching P., Sakuma R., Luga V., Roncari L., Attisano L., Wrana J.L. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 2009, 137:295-307.
34. Ohlstein B., McKearin D. Ectopic expression of the Drosophila Bam protein eliminates oogenic germline stem cells. Development 1997, 124:3651-3662.
35. Orvedahl A., Sumpter R., Xiao G., Ng A., Zou Z., Tang Y., Narimatsu M., Gilpin C., Sun Q., Roth M., Forst C.V., Wrana J.L., Zhang Y.E., Luby-Phelps K., Xavier R.J., Xie Y., Levine B. Image-based genome-wide siRNA screen identifies selective autophagy factors. Nature 2011, 480:113-117.
36. Podos S.D., Hanson K.K., Wang Y.-C., Ferguson E.L. The DSmurf ubiquitin-protein ligase restricts BMP signaling spatially and temporally during drosophila embryogenesis. Dev. cell 2001, 1:567-578.
37. Preat T., Therond P., Limbourg-Bouchon B., Pham A., Tricoire H., Busson D., Lamour-Isnard C. Segmental polarity in Drosophila melanogaster: genetic dissection of fused in a Suppressor of fused background reveals interaction with costal-2. Genetics 1993, 135:1047-1062.
38. Sangadala S., Boden S.D., Viggeswarapu M., Liu Y., Titus L. LIM mineralization protein-1 potentiates bone morphogenetic protein responsiveness via a novel interaction with Smurf1 resulting in decreased ubiquitination of Smads. J. Biol. Chem. 2006, 281:17212-17219.
39. Schulz C., Kiger A.A., Tazuke S.I., Yamashita Y.M., Pantalena-Filho L.C., Jones D.L., Wood C.G., Fuller M.T. A misexpression screen reveals effects of bag-of-marbles and TGF beta class signaling on the Drosophila male germ-line stem cell lineage. Genetics 2004, 167:707-723.
40. Schwamborn J.C., Khazaei M.R., Puschel A.W. The interaction of mPar3 with the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. J. Biol. Chem. 2007, 282:35259-35268.
41. Schwamborn J.C., Muller M., Becker A.H., Puschel A.W. Ubiquitination of the GTPase Rap1B by the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. EMBO J. 2007, 26:1410-1422.
42. Sekelsky J.J., Newfeld S.J., Raftery L.A., Chartoff E.H., Gelbart W.M. Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in drosophila melanogaster. Genetics 1995, 139:1347-1358.
43. Sheng X.R., Posenau T., Gumulak-Smith J.J., Matunis E., Van Doren M., Wawersik M. Jak-STAT regulation of male germline stem cell establishment during Drosophila embryogenesis. Dev. Biol. 2009, 334:335-344.
44. 2 signaling in Drosophila spermatogenesis. Curr. Biol.: CB 2003, 13:2065-2072.
45. Tsuneizumi K., Nakayama T., Kamoshida Y., Kornberg T.B., Christian J.L., Tabata T. Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature 1997, 389:627-631.
46. Van Doren M., Williamson A.L., Lehmann R. Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr. Biol.: CB 1998, 8:243-246.
47. Wang H.R., Zhang Y., Ozdamar B., Ogunjimi A.A., Alexandrova E., Thomsen G.H., Wrana J.L. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 2003, 302:1775-1779.
48. Wang X., Harris R.E., Bayston L.J., Ashe H.L. Type IV collagens regulate BMP signalling in Drosophila. Nature 2008, 455:72-77.
49. Wiersdorff V., Lecuit T., Cohen S.M., Mlodzik M. Mad acts downstream of Dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. Development 1996, 122:2153-2162.
50. Wiesner S., Ogunjimi A.A., Wang H.R., Rotin D., Sicheri F., Wrana J.L., Forman-Kay J.D. Autoinhibition of the HECT-type ubiquitin ligase Smurf2 through its C2 domain. Cell 2007, 130:651-662.
51. Xia L., Jia S., Huang S., Wang H., Zhu Y., Mu Y., Kan L., Zheng W., Wu D., Li X., Sun Q., Meng A., Chen D. The fused/Smurf complex controls the fate of Drosophila germline stem cells by generating a gradient BMP response. Cell 2010, 143:978-990.
52. Yamashita M., Ying S.X., Zhang G.M., Li C., Cheng S.Y., Deng C.X., Zhang Y.E. Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell 2005, 121:101-113.
53. Yamashita Y.M., Yuan H., Cheng J., Hunt A.J. Polarity in stem cell division: asymmetric stem cell division in tissue homeostasis. Cold Spring Harbor Perspect. Biol. 2010, 2:a001313.
54. Zhang J., Li L. BMP signaling and stem cell regulation. Dev. Biol. 2005, 284:1-11.
55. Zhang Y., Chang C., Gehling D.J., Hemmati-Brivanlou A., Derynck R. Regulation of Smad degradation and activity by Smurf2, an E3 ubiquitin ligase. Proc. Natl. Acad. Sci. USA 2001, 98:974-979.
56. Zhu C.H., Xie T. Clonal expansion of ovarian germline stem cells during niche formation in Drosophila. Development 2003, 130:2579-2588.
57. Zhu H., Kavsak P., Abdollah S., Wrana J.L., Thomsen G.H. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 1999, 400:687-693.