Signaling in stem cell niches: Lessons from the Drosophila germline

Journal of Cell Science

Volumn 118, Issue 4, 2005, Pages 665-672

  Yamashita, Yukiko M ^a   Fuller, Margaret T ^a   Jones, D Leanne ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

Cadherin; Drosophila; Germline; JAK STAT; Stem cells; TGF

Indexed keywords

CADHERIN; JANUS KINASE; STAT PROTEIN; TRANSFORMING GROWTH FACTOR;

ARTICLE; CELL ADHESION; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL DIVISION; CELL FATE; CELL FUNCTION; CELL INTERACTION; CELL POLARITY; DROSOPHILA; HEMATOPOIETIC STEM CELL; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; CELL ADHESION; CELL DIFFERENTIATION; CELL POLARITY; DROSOPHILA; EXTRACELLULAR MATRIX; FEMALE; MALE; NEURONS; OVARY; SIGNAL TRANSDUCTION; STEM CELLS; TESTIS;

JANUS;

EID: 14944386163     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01680     Document Type: Article

References (66)

1. Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C., Nussaume, L., Noh, Y. S., Amasino, R. and Scheres, B. (2004). The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109-120.
2. Baurle, I. and Laux, T. (2003). Apical meristems: the plant's fountain of youth. BioEssays 25, 961-970.
3. Bolivar, J., Huynh, J. R., Lopez-Schier, H., Gonzalez, C., St Johnston, D. and Gonzalez-Reyes, A. (2001). Centrosome migration into the Drosophila oocyte is independent of BicD and egl, and of the organisation of the microtubule cytoskeleton. Development 128, 1889-1897.
4. Brawley, C. and Matunis, E. (2004). Regeneration of male germline stem cells by spermatogonial dedifferentiation in vivo. Science 304, 1331-1334.
5. Calvi, L. M., Adams, G. B., Weibrecht, K. W., Weber, J. M., Olson, D. P., Knight, M. C., Martin, R. P., Schipani, E., Divieti, P., Bringhurst, F. R. et al. (2003). Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841-846.
6. Casanueva, M. O. and Ferguson, E. L. (2004). Germline stem cell number in the Drosophila ovary is regulated by redundant mechanisms that control Dpp signaling. Development 131, 1881-1890.
7. Chen, D. and McKearin, D. (2003a). Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr. Biol. 13, 1786-1791.
8. Chen, D. and McKearin, D. M. (2003b). A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development 130, 1159-1170.
9. de Cuevas, M., Lee, J. K. and Spradling, A. C. (1996). alpha-spectrin is required for germline cell division and differentiation in the Drosophila ovary. Development 122, 3959-3968.
10. Deng, W. and Lin, H. (1997). Spectrosomes and fusomes anchor mitotic spindles during asymmetric germ cell divisions and facilitate the formation of a polarized microtubule array for oocyte specification in Drosophila. Dev. Biol. 189, 79-94.
11. Doetsch, F., Caille, L, Lim, D. A., Garcia-Verdugo, J. M. and Alvarez-Buylla, A. (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716.
12. Fuchs, E., Tumbar, T. and Guasch, G. (2004). Socializing with the neighbors: stem cells and their niche. Cell 116, 769-778.
13. Gage, F. H. (2000). Mammalian neural stem cells. Science 287, 1433-1438.
14. Gilboa, L., Forbes, A., Tazuke, S. I., Fuller, M. T. and Lehmann, R. (2003). Germ line stem cell differentiation in Drosophila requires gap junctions and proceeds via an intermediate state. Development 130, 6625-6634.
15. Gonzalez-Reyes, A. (2003). Stem cells, niches and cadherins: a view from Drosophila. J. Cell Sci. 116, 949-954.
16. Harrison, D. A., McCoon, P. E., Binari, R., Gilman, M. and Perrimon, N. (1998). Drosophila unpaired encodes a secreted protein that activates the JAK signaling pathway. Genes Dev. 12 3252-3263.
17. Jones, D. L. and Fuller, M. T. (2004). Stem cell niches. In Handbook of Stem Cells, Vol. 1: Adult and Fetal Stem Cells (ed. R. Lanza), pp. 59-72. San Diego, CA: Academic Press.
18. Jones, L. (2001). Stem cells: so what's in a niche? Curr. Biol. 11, R484-486.
19. Kai, T. and Spradling, A. (2003). An empty Drosophila stem cell niche reactivates the proliferation of ectopic cells. Proc. Natl. Acad. Sci. USA 100, 4633-4638.
20. Kai, T. and Spradling, A. (2004). Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 428, 564-569.
21. Kawase, E., Wong, M. D., Ding, B. C. and Xie, T. (2004). Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 131, 1365-1375.
22. 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.
23. 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.
24. Klambt, C. (2002). EGF receptor signalling: roles of star and rhomboid revealed. Curr. Biol. 12, R21-23.
25. Kuhn, H. G., Winkler, J., Kempermann, G., Thal, L. J. and Gage, F. H. (1997). Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 17, 5820-5829.
26. Lim, D. A. and Alvarez-Buylla, A. (1999). Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc. Natl. Acad. Sci. USA 96, 7526-7531.
27. Lin, H. (2002). The stem-cell niche theory: lessons from flies. Nat. Rev. Genet. 3, 931-940.
28. Lin, H., Yue, L. and Spradling, A. C. (1994). The Drosophila fusome, a germline-specific organelle, contains membrane skeletal proteins and functions in cyst formation. Development 120, 947-956.
29. Matunis, E., Tran, J., Gonczy, P., Caldwell, K. and DiNardo, S. (1997). punt and schnurri regulate a somatically derived signal that restricts proliferation of committed progenitors in the germline. Development 124, 4383-4391.
30. Morris, R. J., Liu, Y., Marles, L., Yang, Z., Trempus, C., Li, S., Lin, J. S., Sawicki, J. A. and Cotsarelis, G. (2004). Capturing and profiling adult hair follicle stem cells. Nat. Biotechnol. 22, 411-417.
31. Moustakas, A. (2002). Smad signalling network. J. Cell Sci. 115, 3355-3356.
32. Nelson, W. J. and Nusse, R. (2004). Convergence of Wnt, beta-catenin, and cadherin pathways. Science 303, 1483-1487.
33. Ohlstein, B. and McKearin, D. (1997). Ectopic expression of the Drosophila Bam protein eliminates oogenic germline stem cells. Development 124, 3651-3662.
34. Ohlstein, B., Kai, T., Decotto, E. and Spradling, A. (2004). The stem cell niche: theme and variations. Curr. Opin. Cell Biol. 16, 693-699.
35. Pevny, L. and Rao, M. S. (2003). The stem-cell menagerie. Trends Neurosci. 26, 351-359.
36. Rawlings, J. S., Rosler, K. M. and Harrison, D. A. (2004). The JAK/STAT signaling pathway. J. Cell Sci. 117, 1281-1283.
37. Reya, T., Duncan, A. W., Ailles, L., Domen, J., Scherer, D. C., Willert, K., Hintz, L., Nusse, R. and Weissman, I. L. (2003). A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423, 409-414.
38. Reynolds, B. A. and Weiss, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710.
39. Sabatini, S., Heidstra, R., Wildwater, M. and Scheres, B. (2003). SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev. 17, 354-358.
40. Sanai, N., Tramontin, A. D., Quinones-Hinojosa, A., Barbaro, N. M., Gupta, N., Kunwar, S., Lawton, M. T., McDermott, M. W., Parsa, A. T., Manuel-Garcia Verdugo, J. et al. (2004). Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427, 740-744.
41. Schulz, C., Wood, C. G., Jones, D. L., Tazuke, S. I. and Fuller, M. T. (2002). Signaling from germ cells mediated by the rhomboid homolog stet organizes encapsulation by somatic support cells. Development 129, 4523-4534.
42. Schulz, C., Kiger, A. A., Tazuke, S. L, Yamashita, Y. M., Pantalena-Filho, L. C., Jones, D. L., Wood, C. G. and Fuller, M. T. (2004). A misexpression screen reveals effects of bag-of-marbles and TGFbeta class signaling on the Drosophila male germ-line stem cell lineage. Genetics 167, 707-723.
43. Shen, Q., Goderie, S. K., Jin, L., Karanth, N., Sun, Y., Abramova, N., Vincent, P., Pumiglia, K. and Temple, S. (2004). Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304, 1338-1340.
44. Shivdasani, A. A. and Ingham, P. W. (2003). Regulation of stem cell maintenance and transit amplifying cell proliferation by TGF-beta signaling in Drosophila spermatogenesis. Curr. Biol. 13, 2065-2072.
45. Song, H., Stevens, C. F. and Gage, F. H. (2002a). Astroglia induce neurogenesis from adult neural stem cells. Nature 417, 39-44.
46. Song, H. J., Stevens, C. F. and Gage, F. H. (2002b). Neural stem cells from adult hippocampus develop essential properties of functional CNS neurons. Nat. Neurosci. 5, 438-445.
47. Song, X., Zhu, C. H., Doan, C. and Xie, T. (2002). Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science 296, 1855-1857.
48. Song, X., Wong, M. D., Kawase, E., Xi, R., Ding, B. C., McCarthy, J. J. and Xie, T. (2004). Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131, 1353-1364.
49. Taupin, P., Ray, J., Fischer, W. H., Suhr, S. T., Hakansson, K., Grubb, A. and Gage, F. H. (2000). FGF-2-responsive neural stem cell proliferation requires CCg, a novel autocrine/paracrine cofactor. Neuron 28, 385-397.
50. Tazuke, S. I, Schulz, C., Gilboa, L., Fogarty, M., Mahowald, A. P., Guichet, A., Ephrussi, A., Wood, C. G., Lehmann, R. and Fuller, M. T. (2002). A germline-specific gap junction protein required for survival of differentiating early germ cells. Development 129, 2529-2539.
51. Tran, J., Brenner, T. J. and DiNardo, S. (2000). Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature 407, 754-757.
52. Tulina, N. and Matunis, E. (2001). Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294, 2546-2549.
53. Tumbar, T., Guasch, G., Greco, V., Blanpain, C., Lowry, W. E., Rendl, M. and Fuchs, E. (2004). Defining the epithelial stem cell niche in skin. Science 303, 359-363.
54. Uchida, N., Buck, D. W., He, D., Reitsma, M. J., Masek, M., Phan, T. V., Tsukamoto, A. S., Gage, R H. and Weissman, I. L. (2000). Direct isolation of human central nervous system stem cells. Proc. Natl. Acad. Sci. USA 97, 14720-14725.
55. Urban, S., Lee, J. R. and Freeman, M. (2001). Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107, 173-182.
56. van den Berg, C., Willemsen, V., Hage, W., Weisbeek, P. and Scheres, B. (1995). Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378, 62-65.
57. Wagers, A. J., Allsopp, R. C. and Weissman, I. L. (2002). Changes in integrin expression are associated with altered homing properties of Lin(-/lo)Thy1.1(lo)Sca-1(+)c-kit(+) hematopoietic stem cells following mobilization by cyclophosphamide/granulocyte colony- stimulating factor. Exp. Hematol. 30, 176-185.
58. Wagner, J. P., Black, I. B. and DiCicco-Bloom, E. (1999). Stimulation of neonatal and adult brain neurogenesis by subcutaneous injection of basic fibroblast growth factor. J. Neurosci. 19, 6006-6016.
59. Watt, F. M. and Hogan, B. L. (2000). Out of Eden: stem cells and their niches. Science 287, 1427-1430.
60. Willert, K., Brown, J. D., Danenberg, E., Duncan, A. W., Weissman, I. L., Reya, T., Yates, J. R., III and Nusse, R. (2003). Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448-452.
61. Wright, D. E., Wagers, A. J., Gulati, A. P., Johnson, F. L. and Weissman, I. L. (2001). Physiological migration of hematopoietic stem and progenitor cells. Science 294, 1933-1936.
62. Wurmser, A. E., Nakashima, K., Summers, R. G., Toni, N., D'Amour, K. A., Lie, D. C. and Gage, F. H. (2004). Cell fusion-independent differentiation of neural stem cells to the endothelial lineage. Nature 430, 350-356.
63. Xie, T. and Spradling, A. C. (1998). decapentaplegic is essential for the maintenance and division of germline stem cells in the Drosophila ovary. Cell 94, 251-260.
64. Xie, T. and Spradling, A. C. (2000). A niche maintaining germ line stem cells in the Drosophila ovary. Science 290, 328-330.
65. Yamashita, Y., 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.
66. Zhang, J., Niu, C., Ye, L., Huang, H., He, X., Tong, W. G., Ross, J., Haug, J., Johnson, T., Feng, J. Q. et al. (2003). Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425, 836-841.