The actin-binding protein profilin is required for germline stem cell maintenance and germ cell enclosure by somatic cyst cells

Development (Cambridge)

Volumn 141, Issue 1, 2014, Pages 73-82

  Shields, Alicia R ^a   Spence, Allyson C ^a   Yamashita, Yukiko M ^a,b   Davies, Erin L ^a,c   Fuller, Margaret T ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

APC2; Profilin; Stem cells

Indexed keywords

ADENOMATOUS POLYPOSIS COLI 2 PROTEIN; F ACTIN; PROFILIN; STAT PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL JUNCTION; CELL LINEAGE; CELL LOSS; CELL PROLIFERATION; COLON POLYPOSIS; CONTROLLED STUDY; CYST; DROSOPHILA; GENE OVEREXPRESSION; GERM CELL; GERMLINE STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN LOCALIZATION; SOMATIC CELL;

APC2; PROFILIN; STEM CELLS;

ACTINS; ADHERENS JUNCTIONS; ANIMALS; CADHERINS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; PROFILINS; PROTEIN BINDING; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SPERMATOGONIA; SPERMATOZOA; STEM CELL NICHE; STEM CELLS; TUMOR SUPPRESSOR PROTEINS;

EID: 84890497979     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.101931     Document Type: Article

References (40)

1. Baum, B. and Perrimon, N. (2001). Spatial control of the actin cytoskeleton in Drosophila epithelial cells. Nat. Cell Biol. 3, 883-890.
2. Carramusa, L., Ballestrem, C., Zilberman, Y. and Bershadsky, A. D. (2007). Mammalian diaphanous-related formin Dia1 controls the organization of E-cadherinmediated cell-cell junctions. J. Cell Sci. 120, 3870-3882.
3. Castrillon, D. H., Gönczy, P., Alexander, S., Rawson, R., Eberhart, C. G., Viswanathan, S., DiNardo, S. and Wasserman, S. A. (1993). Toward a molecular genetic analysis of spermatogenesis in Drosophila melanogaster: characterization of male-sterile mutants generated by single P element mutagenesis. Genetics 135, 489-505.
4. Chen, P., Xie, H., Sekar, M. C., Gupta, K. and Wells, A. (1994). Epidermal growth factor receptor-mediated cell motility: phospholipase C activity is required, but mitogen-activated protein kinase activity is not sufficient for induced cell movement. J. Cell Biol. 127, 847-857.
5. Chen, P., Murphy-Ullrich, J. E. and Wells, A. (1996). A role for gelsolin in actuating epidermal growth factor receptor-mediated cell motility. J. Cell Biol. 134, 689-698.
6. Chen, X., Hiller, M., Sancak, Y. and Fuller, M. T. (2005). Tissue-specific TAFs counteract Polycomb to turn on terminal differentiation. Science 310, 869-872.
7. Chou, J., Stolz, D. B., Burke, N. A., Watkins, S. C. and Wells, A. (2002). Distribution of gelsolin and phosphoinositol 4,5-bisphosphate in lamellipodia during EGF-induced motility. Int. J. Biochem. Cell Biol. 34, 776-790.
8. Chu, Y. S., Thomas, W. A., Eder, O., Pincet, F., Perez, E., Thiery, J. P. and Dufour, S. (2004). Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. J. Cell Biol. 167, 1183-1194.
9. Collinet, C. and Lecuit, T. (2013). Stability and dynamics of cell-cell junctions. Prog. Mol. Biol. Transl. Sci. 116, 25-47.
10. Cooley, L., Verheyen, E. and Ayers, K. (1992). chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell 69, 173-184.
11. Desai, R., Sarpal, R., Ishiyama, N., Pellikka, M., Ikura, M. and Tepass, U. (2013). Monomeric α-catenin links cadherin to the actin cytoskeleton. Nat. Cell Biol. 15, 261-273.
12. Goldschmidt-Clermont, P. J., Kim, J. W., Machesky, L. M., Rhee, S. G. and Pollard, T. D. (1991). Regulation of phospholipase C-γ 1 by profilin and tyrosine phosphorylation. Science 251, 1231-1233.
13. Gonçalves-Pimentel, C., Gombos, R., Mihály, J., Sánchez-Soriano, N. and Prokop, A. (2011). Dissecting regulatory networks of filopodia formation in a Drosophila growth cone model. PLoS ONE 6, e18340.
14. Gönczy, P. and DiNardo, S. (1996). The germ line regulates somatic cyst cell proliferation and fate during Drosophila spermatogenesis. Development 122, 2437-2447.
15. Hong, S., Troyanovsky, R. B. and Troyanovsky, S. M. (2013). Binding to F-actin guides cadherin cluster assembly, stability, and movement. J. Cell Biol. 201, 131-143.
16. Imamura, Y., Itoh, M., Maeno, Y., Tsukita, S. and Nagafuchi, A. (1999). Functional domains of alpha-catenin required for the strong state of cadherin-based cell adhesion. J. Cell Biol. 144, 1311-1322.
17. Inaba, M., Yuan, H., Salzmann, V., Fuller, M. T. and Yamashita, Y. M. (2010). Ecadherin is required for centrosome and spindle orientation in Drosophila male germline stem cells. PLoS ONE 5, e12473.
18. Jamora, C. and Fuchs, E. (2002). Intercellular adhesion, signalling and the cytoskeleton. Nat. Cell Biol. 4, E101-E108.
19. Kiger, A. A., White-Cooper, H. and Fuller, M. T. (2000). Somatic support cells restrict germline stem cell self-renewal and promote differentiation. Nature 407, 750-754.
20. Kiger, A. A., Jones, D. L., Schulz, C., Rogers, M. B. and Fuller, M. T. (2001). Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 294, 2542-2545.
21. Lambert, M., Thoumine, O., Brevier, J., Choquet, D., Riveline, D. and Mège, R. M. (2007). Nucleation and growth of cadherin adhesions. Exp. Cell Res. 313, 4025-4040.
22. Leatherman, J. L. and Dinardo, S. (2008). Zfh-1 controls somatic stem cell selfrenewal in the Drosophila testis and nonautonomously influences germline stem cell self-renewal. Cell Stem Cell 3, 44-54.
23. Leatherman, J. L. and Dinardo, S. (2010). Germline self-renewal requires cyst stem cells and stat regulates niche adhesion in Drosophila testes. Nat. Cell Biol. 12, 806-811.
24. Lim, J. G. and Fuller, M. T. (2012). Somatic cell lineage is required for differentiation and not maintenance of germline stem cells in Drosophila testes. Proc. Natl. Acad. Sci. USA 109, 18477-18481.
25. Mège, R. M., Gavard, J. and Lambert, M. (2006). Regulation of cell-cell junctions by the cytoskeleton. Curr. Opin. Cell Biol. 18, 541-548.
26. Nola, S., Daigaku, R., Smolarczyk, K., Carstens, M., Martin-Martin, B., Longmore, G., Bailly, M. and Braga, V. M. (2011). Ajuba is required for Rac activation and maintenance of E-cadherin adhesion. J. Cell Biol. 195, 855-871.
27. Oda, H. and Tsukita, S. (1999). Nonchordate classic cadherins have a structurally and functionally unique domain that is absent from chordate classic cadherins. Dev. Biol. 216, 406-422.
28. Sarkar, A., Parikh, N., Hearn, S. A., Fuller, M. T., Tazuke, S. I. and Schulz, C. (2007). Antagonistic roles of Rac and Rho in organizing the germ cell microenvironment. Curr. Biol. 17, 1253-1258.
29. Srinivasan, S., Mahowald, A. P. and Fuller, M. T. (2012). The receptor tyrosine phosphatase Lar regulates adhesion between Drosophila male germline stem cells and the niche. Development 139, 1381-1390.
30. Theriot, J. A. and Mitchison, T. J. (1993). The three faces of profilin. Cell 75, 835-838.
31. Townsley, F. M. and Bienz, M. (2000). Actin-dependent membrane association of a Drosophila epithelial APC protein and its effect on junctional Armadillo. Curr. Biol. 10, 1339-1348.
32. Tran, J., Brenner, T. J. and DiNardo, S. (2000). Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature 407, 754-757.
33. Tran, V., Lim, C., Xie, J. and Chen, X. (2012). Asymmetric division of Drosophila male germline stem cell shows asymmetric histone distribution. Science 338, 679-682.
34. Tulina, N. and Matunis, E. (2001). Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294, 2546-2549.
35. Van Doren, M., Williamson, A. L. and Lehmann, R. (1998). Regulation of zygotic gene expression in Drosophila primordial germ cells. Curr. Biol. 8, 243-246.
36. Verheyen, E. M. and Cooley, L. (1994). Profilin mutations disrupt multiple actindependent processes during Drosophila development. Development 120, 717-728.
37. Voog, J., D'Alterio, C. and Jones, D. L. (2008). Multipotent somatic stem cells contribute to the stem cell niche in the Drosophila testis. Nature 454, 1132-1136.
38. Yadlapalli, S., Cheng, J. and Yamashita, Y. M. (2011). Drosophila male germline stem cells do not asymmetrically segregate chromosome strands. J. Cell Sci. 124, 933-939.
39. Yamashita, Y. M., Jones, D. L. and Fuller, M. T. (2003). Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science 301, 1547-1550.
40. Yu, X., Waltzer, L. and Bienz, M. (1999). A new Drosophila APC homologue associated with adhesive zones of epithelial cells. Nat. Cell Biol. 1, 144-151.