Signaling from germ cells mediated by the rhomboid homolog stet organizes encapsulation by somatic support cells

Development

Volumn 129, Issue 19, 2002, Pages 4523-4534

  Schulz, Cordula ^a   Wood, Cricket G ^a   Jones, D Leanne ^a   Tazuke, Salli I ^a   Fuller, Margaret T ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Drosophila; Gametogenesis; Rhomboid homolog; Signaling; Somatic niche; Stem cells

Indexed keywords

CELL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; LIGAND; MUTANT PROTEIN; PROTEIN STET; RHO FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL ENCAPSULATION; CELL INTERACTION; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE FUNCTION; GENETIC CODE; GERM CELL; MALE; MICROENVIRONMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SOMATIC CELL; WILD TYPE;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE PROTEINS; FEMALE; MALE; MEMBRANE PROTEINS; OVUM; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, CELL SURFACE; RECEPTORS, INVERTEBRATE PEPTIDE; SIGNAL TRANSDUCTION; SPERMATOZOA;

ANIMALIA; ARACHNIDA; HEXAPODA;

EID: 0036796861     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Ashburner, M. (1989). Drosophila. A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
2. Berry, L. W., Westlund, B. and Schedl, T. (1997). Germ-line tumor formation caused by activation of glp-1, a Caenorhabditis elegans member of the Notch family of receptors. Development 124, 925-936.
3. Bier, E., Jan, L. Y. and Jan, Y. N. (1990). rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev. 3, 190-203.
4. Bitgood, M. J., Shen, L. and McMahon, A. P. (1996). Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr Biol. 6, 298-304.
5. Bopp, D., Horabin, J. I., Lersch, R. A., Cline, T. W. and Schedl, P. (1993). Expression of the Sex-lethal gene is controlled at multiple levels during Drosophila oogenesis. Development 118, 797-812.
6. Bünning, J. (1994). The Insect Ovary. London: Chapman and Hall.
7. Carpenter, A. T. (1975). Electron microscopy of meiosis in Drosophila melanogaster females. I. Structure, arrangement, and temporal change of the synaptonemal complex in wild-type. Chromosoma 51, 157-182.
8. Church, D. L., Gunn, K. L. and Lambie, E. J. (1995). Three genes of the Map kinase cascade, mek-2, mpk-1/sur-1 and let-60 ras, are required for meiotic cell cycle progression in Caenorhabditis elegans. Development 121, 2525-2535.
9. Desjardins, C. and Ewing, L. L. (1993). Cell and Molecular Biology of the Testis. New York: Oxford University Press.
10. Erickson, G. F. (1986). An analysis of follicle development and ovum maturation. Semin. Reprod. Endocrinol. 4, 233-254.
11. FlyBase (1999). The FlyBase database of the Drosophila genome projects and community literature. Nucleic Acids Res. 27, 85-88.
12. Freeman, M. (1998). Complexity of the EGF receptor signaling revealed in Drosophila. Curr. Opin. Genet. Dev. 8, 407-411.
13. Ghiglione, C., Bach, E. A., Paraiso, Y., Carraway, K L., III, Noselli, S. and Perrimon, N. (2002). Mechanism of activation of the Drosophila EGF receptor by the TGFα ligand Gurken during oogenesis. Development 129, 175-186.
14. Gönczy, P., Viswanathan, S. and DiNardo, S. (1992). Probing spermatogenesis in Drosophila with P-element enhancer detectors. Development 114, 89-98.
15. Gönczy, P. and DiNardo, S. (1996). The germ line regulates somatic cyst cell proliferation and fate during Drosophila spermatogenesis. Development 122, 2437-2447.
16. Gönczy, P., Matunis, E. and DiNardo, S. (1997). bag-of-marbles and benign gonial cell neoplasm act in the germline to restrict proliferation during Drosophila spermatogenesis. Development 124, 4361-4371.
17. Golembo, M., Raz, E. and Shilo, B.-Z. (1996). The Drosophila embryonic midline is the site of Spitz processing, and induces activation of the EGF receptor in the ventral ectoderm. Development 122, 3363-3370.
18. Gonzales-Reyes, A., Elliott, H. and St Johnston, D. (1995). Polarization of both major body axes in Drosophila by gurken-torpedo signaling. Nature 375, 654-658.
19. Goode, S., Wright, D. and Mahowald, A. P. (1992). The neurogenic locus brainiac cooperates with the Drosophila EGF receptor to establish the ovarian follicle and to determine its dorsal-ventral polarity. Development 116, 177-192.
20. Goode, S., Morgan, M., Liang, Y.-P. and Mahowald, A. P. (1996a). brainiac encodes a novel, putative secreted protein that cooperates with grk TGFα in the genesis of the follicular epithelium. Dev. Biol. 178, 35-50.
21. Goode, S., Melnick, M., Chou, T.-B. and Perrimon, N. (1996b). The neurogenic genes egghead and brainiac define a novel signaling pathway essential for epithelial morphogenesis during Drosophila oogenesis. Development 122, 3863-3879.
22. Guichard, A., Biehs, B., Sturtevant, M. A., Wickline, L., Chacko, J., Howard, K. and Bier, E. (1999). rhomboid and Star interact synergistically to promote EGFR/MAPK signaling during Drosophila wing vein development. Development 126, 2663-2676.
23. Guichard, A., Roark, M., Ronshaugen, M. and Bier, E. (2000). brother of rhomboid, a rhomboid-related gene expressed during early Drosophila oogenesis, promotes EGF-R/MAPK signaling. Dev. Biol. 226, 255-266.
24. Hall, D. H., Winfrey, V. P., Blaeuer, G., Hoffman, L. H., Furuta, T., Rose, K. L., Hobert, O. and Greenstein, D. (1999). Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: relations between germ line and soma. Dev. Biol. 212, 101-123.
25. Hardy, R. W., Tokuyasu, K. T., Lindsley, D. L. and Garavito, M. (1979). The germinal proliferation center in the testis of Drosophila melanogaster. J. Ultrastruct. Res. 69, 180-190.
26. Hime, G. R., Brill, J. A. and Fuller, M. T. (1996). Assembly of ring canals in the male germ line from structural components of the contractile ring. J. Cell Sci. 109, 2779-2788.
27. Hsuesh, A. J. and Schomberg, D. W. (1993). Ovarian Cell Interactions. Berlin: Springer Verlag.
28. Kammermeyer, K. L. and Wadsworth, S. C. (1987). Expression of Drosophila epidermal growth factor homologue in mitotic cell populations. Development 100, 201-210.
29. 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.
30. Kiger, A. A. and Fuller, M. T. (2001). Male germ-line stem cells. In Stem Cell Biology (ed. D. R. Marshak, R. L. Gardner and D. Gottlieb), pp. 149-187. New York: Cold Spring Harbor Laboratory Press.
31. Kimble, J. and White, J. (1981). On the control of germ cell development in Caenorhabditis elegans. Dev. Biol. 81, 208-219.
32. King, R. C. (1970). Ovarian Development in Drosophila melanogaster. New York, London: Academic Press.
33. King, F. J. and Lin, H. (1999). Somatic signaling mediated by the fs(1)Yb is essential for germline stem cell maintenance during Drosophila oogenesis. Development 126, 1833-1844.
34. Klingler, M. and Gergen, J. P. (1993). Regulation of runt transcription by Drosophila segmentation genes. Mech. Dev. 43, 3-19.
35. Kolodkin, A. L., Pickup, A. T., Lin, D. M., Goodman, C. S. and Banerjee, U. (1994). Characterization of Star and its interactions with sevenless and EGF receptor during photoreceptor cell development in Drosophila. Development 120, 1731-1745.
36. Lee, J. R., Urban, S., Garvey, C. F. and Freeman, M. (2001). Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila. Cell 107, 161-171.
37. Lev, Z., Shilo, B.-Z. and Kimchie, Z. (1985). Developmental changes in the expression of the Drosophila melanogaster epidermal growth factor receptor gene. Dev. Biol. 110, 499-502.
38. Lindsley, D. L. and Zimm, G. G. (1992). The Genome of Drosophila melanogaster. San Diego: Academic Press.
39. Matunis, E., Tran, J., Gönczy, P. 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.
40. Margolis, J. and Spradling, A. C. (1995). Identification and behavior of epithelial stem cells in the Drosophila ovary. Development 121, 3797-3807.
41. d Sertoli cells is defective and is rescued by expression of the transmembrane form of the c-kit ligand. Dev. Biol. 157, 182-190.
42. Matzug, M. M. (2000). Revelations of ovarian follicle biology from gene knockout mice. Mol. Cell. Endocrinol. 163, 61-66.
43. McCarter, J., Bartlett, B., Dang, T. and Schedl, T. (1997). Soma-germ cell interactions in Caenorhabditis elegans: Multiple events of hermaphrodite germline development require the somatic sheath and spermathecal lineage. Dev. Biol. 181, 121-143.
44. Morgan, M. M. and Mahowald, A. P. (1996). Multiple signaling pathways establish both the individuation and the polarity of the oocyte follicle in Drosophila. Arch. Insect Biochem. Physiol. 33, 211-230.
45. Ojeda, S. R., Romero, C., Tapia, V. and Dissen, G. A. (2000). Neurotrophic and cell-cell dependent control of early follicular development. Mol. Cell. Endocrinol. 163, 67-71.
46. Pesce, M., di Carlo, A. and de Felici, M. (1997). The c-kit receptor is involved in the adhesion of mouse primordial germ cells to somatic cells in culture. Mech. Dev. 68, 37-44.
47. Phelps, C. B., Brand, A. H. (1998). Ectopic gene expression in Drosophila using GAL4 system. Methods 14, 367-379.
48. Pickup, A. T. and Banerjee, U. (1999). The role of Star in the production of an activated ligand for the EGF receptor signaling pathway. Dev. Biol. 205, 254-259.
49. Ruohola-Baker, H., Grell, E., Chou, T. B., Baker, D., Jan, L. Y., Jan, Y. N. (1993). Spatially localized rhomboid is required for establishment of the dorsal-ventral axis in Drosophila oogenesis. Cell 73, 953-965.
50. Ray, R. P. and Schüpbach, T. (1996). Intercellular signaling and the polarization of body axes during Drosophila oogenesis. Genes Dev. 10, 1711-1723.
51. Rutledge, B. J., Zhang, K., Bier, E., Jan, Y. N. and Perrimon, N. (1992). The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis. Genes Dev. 6, 1503-1517.
52. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning. A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
53. Sapir, A., Schweitzer, R. and Shilo, B.-Z. (1998). Sequential activation of the EGF receptor pathway during Drosophila oogenesis establishes the dorsoventral axis. Development 125, 191-200.
54. Schulz, C., Perezgasga, L. and Fuller, M. T. (2002) Molecular-genetic analysis of dPsa, the Drosophila orthologue of puromycin-sensitive aminopeptidase, suggests redundancy of aminopeptidases. Dev. Genes Evol. 211, 591-598.
55. Schüpbach, T. (1987). Germ line and soma cooperate during oogenesis to establish the dorsoventral pattern of egg shell and embryo in Drosophila melanogaster. Cell 49, 669-707.
56. Schweitzer, R., Shaharabany, M., Seger, R. and Shilo, B-Z. (1995) Secreted spitz triggers the DER signaling pathway and is a limiting component in embryonic ventral ectoderm determination. Genes Dev. 9, 1518-1529.
57. Schweitzer, R. and Shilo, B.-Z. (1997). A thousand and one roles for the Drosophila EGF receptor. Trends Genet. 13, 191-196.
58. Spradling, A. C (1986). P-element mediated transformation. In Drosophila: A Practical Approach (ed. D.B. Roberts), pp. 175-197. Oxford: IRL Press.
59. Sturtevant, M. A., Roark, M. and Bier, E. (1993). The Drosophila rhomboid gene mediates the localized formation of wing veins and interacts genetically with components of the EGF-R signaling pathway. Genes Dev. 7, 961-973.
60. Tautz, D. and Pfeifle, C. (1989). A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 9B, 81-85.
61. Tran, J., Brenner, T. J. and DiNardo, S. (2000). Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature 407, 754-757.
62. Urban, S., Lee, J. R. and Freeman, M. (2001). Drosophila Rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107, 173-182.
63. Wasserman, J. D. and Freeman, M. (1998). An autoregulatory cascade of EGF receptor signaling patterns the Drosophila egg. Cell 95, 355-364.
64. Wasserman, J. D., Urban, S. and Freeman, M. (2000). A family of rhomboid-like genes: Drosophila rhomboid-1 and roughoid/rhomboid-3 cooperate to activate EGF receptor signaling. Genes Dev. 14, 1651-1663.
65. 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.
66. Xie, T. and Spradling, A. C. (2000). A niche maintaining germ line stem cells in the Drosophila ovary. Science 290, 328-330.
67. Xie, T. and Spradling, A. C. (2001). The Drosophila ovary: An in vivo stem cell system. In Stem Cell Biology (ed. D. R. Marshak, R. L. Gardner and D. Gottlieb), pp. 129-148. New York: Cold Spring Harbor Laboratory Press.
68. Xu, T. and Rubin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.