Receptor guanylyl cyclase Gyc76C is required for invagination, collective migration and lumen shape in the Drosophila embryonic salivary gland

Biology Open

Volumn 2, Issue 7, 2013, Pages 711-717

  Patel, Unisha ^a   Myat, Monn Monn ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Drosophila; Guanylyl cyclase; Integrin; Migration; Morphogenesis; Salivary gland

Indexed keywords

EID: 84971003166     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.20134887     Document Type: Article

References (43)

1. Ayoob, J. C., Yu, H. H., Terman, J. R. and Kolodkin, A. L. (2004). The Drosophila receptor guanylyl cyclase Gyc76C is required for semaphorin-1a-plexin A-mediated axonal repulsion. J. Neurosci. 24, 6639-6649.
2. Bradley, P. L., Myat, M. M., Comeaux, C. A. and Andrew, D. J. (2003). Posterior migration of the salivary gland requires an intact visceral mesoderm and integrin function. Dev. Biol. 257, 249-262.
3. Brown, N. H., Gregory, S. L., Rickoll, W. L., Fessler, L. I., Prout, M., White, R. A. and Fristrom, J. W. (2002). Talin is essential for integrin function in Drosophila. Dev. Cell 3, 569-579.
4. Campbell, D. S., Regan, A. G., Lopez, J. S., Tannahill, D., Harris, W. A. and Holt, C. E. (2001). Semaphorin 3A elicits stage-dependent collapse, turning, and branching in Xenopus retinal growth cones. J. Neurosci. 21, 8538-8547.
5. Davies, S. A. (2006). Signalling via cGMP: lessons from Drosophila. Cell. Signal. 18, 409-421.
6. Deng, W. M., Schneider, M., Frock, R., Castillejo-Lopez, C., Gaman, E. A., Baumgartner, S. and Ruohola-Baker, H. (2003). Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila. Development 130, 173-184.
7. Giancotti, F. G. and Ruoslahti, E. (1999). Integrin signaling. Science 285, 1028-1033.
8. Ismat, A., Cheshire, A. M. and Andrew, D. J. (2013). The secreted AdamTS-A metalloprotease is required for collective cell migration. Development 140, 1981-1993.
9. Jattani, R., Patel, U., Kerman, B. and Myat, M. M. (2009). Deficiency screen identifies a novel role for beta 2 tubulin in salivary gland and myoblast migration in the Drosophila embryo. Dev. Dyn. 238, 853-863.
10. Lucas, K. A., Pitari, G. M., Kazerounian, S., Ruiz-Stewart, I., Park, J., Schulz, S., Chepenik, K. P. and Waldman, S. A. (2000). Guanylyl cyclases and signaling by cyclic GMP. Pharmacol. Rev. 52, 375-414.
11. MacPherson, M. R., Lohmann, S. M. and Davies, S. A. (2004). Analysis of Drosophila cGMP-dependent protein kinases and assessment of their in vivo roles by targeted expression in a renal transporting epithelium. J. Biol. Chem. 279, 40026-40034.
12. Martin, D., Zusman, S., Li, X., Williams, E. L., Khare, N., DaRocha, S., Chiquet- Ehrismann, R. and Baumgartner, S. (1999). wing blister, a new Drosophila laminin a chain required for cell adhesion and migration during embryonic and imaginal development. J. Cell Biol. 145, 191-201.
13. Maruyama, R. and Andrew, D. J. (2012). Drosophila as a model for epithelial tube formation. Dev. Dyn. 241, 119-135.
14. Montell, D. J. and Goodman, C. S. (1989). Drosophila laminin: sequence of B2 subunit and expression of all three subunits during embryogenesis. J. Cell Biol. 109, 2441-2453.
15. Morton, D. B. (2004). Invertebrates yield a plethora of atypical guanylyl cyclases. Mol. Neurobiol. 29, 97-115.
16. Myat, M. M. and Andrew, D. J. (2002). Epithelial tube morphology is determined by the polarized growth and delivery of apical membrane. Cell 111, 879-891.
17. Myat, M. M., Lightfoot, H., Wang, P. and Andrew, D. J. (2005). A molecular link between FGF and Dpp signaling in branch-specific migration of the Drosophila trachea. Dev. Biol. 281, 38-52.
18. Narasimha, M. and Brown, N. H. (2004). Novel functions for integrins in epithelial morphogenesis. Curr. Biol. 14, 381-385.
19. Overend, G., Cabrero, P., Guo, A. X., Sebastian, S., Cundall, M., Armstrong, H., Mertens, I., Schoofs, L., Dow, J. A. and Davies, S. A. (2012). The receptor guanylate cyclase Gyc76C and a peptide ligand, NPLP1-VQQ, modulate the innate immune IMD pathway in response to salt stress. Peptides 34, 209-218.
20. Pasterkamp, R. J. and Kolodkin, A. L. (2003). Semaphorin junction: making tracks toward neural connectivity. Curr. Opin. Neurobiol. 13, 79-89.
21. Patel, U., Davies, S. A. and Myat, M. M. (2012). Receptor-type guanylyl cyclase Gyc76C is required for development of the Drosophila embryonic somatic muscle. Biol. Open 1, 507-515.
22. Pfeifer, A., Aszódi, A., Seidler, U., Ruth, P., Hofmann, F. and Fässler, R. (1996). Intestinal secretory defects and dwarfism in mice lacking cGMP-dependent protein kinase II. Science 274, 2082-2086.
23. Pines, M., Das, R., Ellis, S. J., Morin, A., Czerniecki, S., Yuan, L., Klose, M., Coombs, D. and Tanentzapf, G. (2012). Mechanical force regulates integrin turnover in Drosophila in vivo. Nat. Cell Biol. 14, 935-943.
24. Pirraglia, C. and Myat, M. M. (2010). Genetic regulation of salivary gland development in Drosophila melanogaster. In Salivary Glands: Development, Adaptations And Disease, Vol. 14 (ed. A. S. Tucker and I. Miletich), pp. 32-47. Basel; New York, NY: Karger.
25. Pirraglia, C., Jattani, R. and Myat, M. M. (2006). Rac function in epithelial tube morphogenesis. Dev. Biol. 290, 435-446.
26. Pirraglia, C., Walters, J. and Myat,M.M. (2010). Pak1 control of E-cadherin endocytosis regulates salivary gland lumen size and shape. Development 137, 4177-4189.
27. Pirraglia, C., Walters, J., Ahn, N. and Myat, M. M. (2013). Rac1 GTPase acts downstream of aPS1bPS integrin to control collective migration and lumen size in the Drosophila salivary gland. Dev. Biol. 377, 21-32.
28. Qin, J., Vinogradova, O. and Plow, E. F. (2004). Integrin bidirectional signaling: a molecular view. PLoS Biol. 2, e169.
29. Shcherbata, H. R., Yatsenko, A. S., Patterson, L., Sood, V. D., Nudel, U., Yaffe, D., Baker, D. and Ruohola-Baker, H. (2007). Dissecting muscle and neuronal disorders in a Drosophila model of muscular dystrophy. EMBO J. 26, 481-493.
30. Song, H. J. and Poo, M. M. (1999). Signal transduction underlying growth cone guidance by diffusible factors. Curr. Opin. Neurobiol. 9, 355-363.
31. Song, H., Ming, G., He, Z., Lehmann, M., McKerracher, L., Tessier-Lavigne, M. and Poo, M. (1998). Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281, 1515-1518.
32. Tamagnone, L. and Comoglio, P. M. (2004). To move or not to move? Semaphorin signalling in cell migration. EMBO Rep. 5, 356-361.
33. Tanentzapf, G., Devenport, D., Godt, D. and Brown, N. H. (2007). Integrin-dependent anchoring of a stem-cell niche. Nat. Cell Biol. 9, 1413-1418.
34. Tran, T. S., Kolodkin, A. L. and Bharadwaj, R. (2007). Semaphorin regulation of cellular morphology. Annu. Rev. Cell Dev. Biol. 23, 263-292.
35. Urbano, J. M., Torgler, C. N., Molnar, C., Tepass, U., López-Varea, A., Brown, N. H., de Celis, J. F. and Martín-Bermudo, M. D. (2009). Drosophila laminins act as key regulators of basement membrane assembly and morphogenesis. Development 136, 4165-4176.
36. Urbano, J. M., Domínguez-Giménez, P., Estrada, B. and Martín-Bermudo, M. D. (2011). PS integrins and laminins: key regulators of cell migration during Drosophila embryogenesis. PLoS ONE 6, e23893.
37. Vermehren-Schmaedick, A., Ainsley, J. A., Johnson, W. A., Davies, S. A. and Morton, D. B. (2010). Behavioral responses to hypoxia in Drosophila larvae are mediated by atypical soluble guanylyl cyclases. Genetics 186, 183-196.
38. Vining, M. S., Bradley, P. L., Comeaux, C. A. and Andrew, D. J. (2005). Organ positioning in Drosophila requires complex tissue-tissue interactions. Dev. Biol. 287, 19-34.
39. Wolfstetter, G. and Holz, A. (2012). The role of LamininB2 (LanB2) during mesoderm differentiation in Drosophila. Cell. Mol. Life Sci. 69, 267-282.
40. Xu, N., Keung, B. and Myat, M. M. (2008). Rho GTPase controls invagination and cohesive migration of the Drosophila salivary gland through Crumbs and Rho-kinase. Dev. Biol. 321, 88-100.
41. Xu, N., Bagumian, G., Galiano, M. and Myat, M. M. (2011). Rho GTPase controls Drosophila salivary gland lumen size through regulation of the actin cytoskeleton and Moesin. Development 138, 5415-5427.
42. Yurchenco, P. D. (2011). Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb. Perspect. Biol. 3, a004911.
43. Zhou, Y., Gunput, R. A. and Pasterkamp, R. J. (2008). Semaphorin signaling: progress made and promises ahead. Trends Biochem. Sci. 33, 161-170.