Soma-to-Germline Interactions During Drosophila Oogenesis Are Influenced by Dose-Sensitive Interactions Between cut and the Genes cappuccino, ovarian tumor and agnostic

Corresponding author: Stephen M. Jackson, Department of Genetics, Box 357360, University of Washington, Seattle, WA 98195-7360., sjackson{at}u.washington.edu (E-mail)

Communicating editor: T. SCHÜPBACH

The cut gene of Drosophila melanogaster encodes a homeodomain protein that regulates a soma-to-germline signaling pathway required for proper morphology of germline cells during oogenesis. cut is required solely in somatic follicle cells, and when cut function is disrupted, membranes separating adjacent nurse cells break down and the structural integrity of the actin cytoskeleton is compromised. To understand the mechanism by which cut expression influences germline cell morphology, we determined whether binucleate cells form by defective cytokinesis or by fusion of adjacent cells. Egg chambers produced by cut, cappuccino, and chickadee mutants contained binucleate cells in which ring canal remnants stained with antibodies against Hu-li tai shao and Kelch, two proteins that are added to ring canals after cytokinesis is complete. In addition, defects in egg chamber morphology were observed only in middle to late stages of oogenesis, suggesting that germline cell cytokineses were normal in these mutants. cut exhibited dose-sensitive genetic interactions with cappuccino but not with chickadee or other genes that regulate cytoskeletal function, including armadillo, spaghetti squash, quail, spire, Src64B, and Tec29A. Genomic regions containing genes that cooperate with cut were identified by performing a second-site noncomplementing screen using a collection of chromosomal deficiencies. Sixteen regions that interact with cut during oogenesis and eight regions that interact during the development of other tissues were identified. Genetic interactions between cut and the ovarian tumor gene were identified as a result of the screen. In addition, the gene agnostic was found to be required during oogenesis, and genetic interactions between cut and agnostic were revealed. These results demonstrate that a signaling pathway regulating the morphology of germline cells is sensitive to genetic doses of cut and the genes cappuccino, ovarian tumor, and agnostic. Since these genes regulate cytoskeletal function and cAMP metabolism, the cut-mediated pathway functionally links these elements to preserve the cytoarchitecture of the germline cells.

This article has been cited by other articles:

				J. J. Krupp, L. E. Yaich, R. J. Wessells, and R. Bodmer Identification of Genetic Loci That Interact With cut During Drosophila Wing-Margin Development Genetics, August 1, 2005; 170(4): 1775 - 1795. [Abstract] [Full Text] [PDF]

				J. A. McDonald, E. M. Pinheiro, and D. J. Montell PVF1, a PDGF/VEGF homolog, is sufficient to guide border cells and interacts genetically with Taiman Development, August 1, 2003; 130(15): 3469 - 3478. [Abstract] [Full Text] [PDF]

				T. F. Satterfield, S. M. Jackson, and L. J. Pallanck A Drosophila Homolog of the Polyglutamine Disease Gene SCA2 Is a Dosage-Sensitive Regulator of Actin Filament Formation Genetics, December 1, 2002; 162(4): 1687 - 1702. [Abstract] [Full Text] [PDF]

				S. M. Jackson and C. A. Berg An A-kinase anchoring protein is required for Protein kinase A regulatory subunit localization and morphology of actin structures during oogenesis in Drosophila Development, January 10, 2002; 129(19): 4423 - 4433. [Abstract] [Full Text] [PDF]

				K. E. James, J. B. Dorman, and C. A. Berg Mosaic analyses reveal the function of Drosophila Ras in embryonic dorsoventral patterning and dorsal follicle cell morphogenesis Development, January 5, 2002; 129(9): 2209 - 2222. [Abstract] [Full Text] [PDF]

				K. J. Yook, S. R. Proulx, and E. M. Jorgensen Rules of Nonallelic Noncomplementation at the Synapse in Caenorhabditis elegans Genetics, May 1, 2001; 158(1): 209 - 220. [Abstract] [Full Text]

				A. Swan, S. Hijal, A. Hilfiker, and B. Suter Identification of New X-Chromosomal Genes Required for Drosophila Oogenesis and Novel Roles for fs(1)Yb, brainiac and dunce Genome Res., January 1, 2001; 11(1): 67 - 77. [Abstract] [Full Text]