Cdc42 is required in a genetically distinct subset of cardiac cells during Drosophila dorsal vessel closure

Developmental Biology

Volumn 392, Issue 2, 2014, Pages 221-232

  Swope, David ^a   Kramer, Joseph ^a   King, Tiffany R ^a   Cheng, Yi Shan ^a   Kramer, Sunita G ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Cdc42; Dorsal vessel; Drosophila; Rho GTPase

Indexed keywords

PROTEIN CDC42; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ARTICLE; CELL MIGRATION; CELL MOTILITY; CELL SPECIFICITY; CELL TYPE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME INHIBITION; EPIDERMIS; HEART MUSCLE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

CDC42; DORSAL VESSEL; DROSOPHILA; RHO GTPASE;

ANIMALS; CELL MOVEMENT; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GTP-BINDING PROTEINS; HEART; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MYOCARDIUM; SIGNAL TRANSDUCTION;

EID: 84904385067     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.05.024     Document Type: Article

References (55)

1. Abreu-Blanco M.T., Verboon J.M., Liu R., Watts J.J., Parkhurst S.M. Drosophila embryos close epithelial wounds using a combination of cellular protrusions and an actomyosin purse string. J. Cell Sci. 2012, 125:5984-5997.
2. Abu-Issa R., Kirby M.L. Heart field: from mesoderm to heart tube. Annu. Rev. Cell Dev. Biol. 2007, 23:45-68.
3. Arias-Romero L.E., Chernoff J. A tale of two Paks. Biol. Cell 2008, 100:97-108.
4. Bahri S., Wang S., Conder R., Choy J., Vlachos S., Dong K., Merino C., Sigrist S., Molnar C., Yang X., Manser E., Harden N. The leading edge during dorsal closure as a model for epithelial plasticity: Pak is required for recruitment of the Scribble complex and septate junction formation. Development 2010, 137:2023-2032.
5. Barolo, S., Castro, B., and Posakony, JW. 2004. New Drosophila Transgenic Reporters: Insulated P-element Vectors Expressing Fast-maturing RFP. Biotechniques. 36(3), 436-40, 442.
6. Bokoch G.M. Biology of the p21-activated kinases. Annu. Rev. Biochem. 2003, 72:743-781.
7. Campos I., Geiger J.A., Santos A.C., Carlos V., Jacinto A. Genetic screen in Drosophila melanogaster uncovers a novel set of genes required for embryonic epithelial repair. Genetics 2010, 184:129-140.
8. Chartier A., Zaffran S., Astier M., Semeriva M., Gratecos D. Pericardin, a Drosophila type IV collagen-like protein is involved in the morphogenesis and maintenance of the heart epithelium during dorsal ectoderm closure. Development 2002, 129:3241-3253.
9. Chihara T., Kato K., Taniguchi M., Ng J., Hayashi S. Rac promotes epithelial cell rearrangement during tracheal tubulogenesis in Drosophila. Development 2003, 130:1419-1428.
10. Conder R., Yu H., Ricos M., Hing H., Chia W., Lim L., Harden N. dPak is required for integrity of the leading edge cytoskeleton during Drosophila dorsal closure but does not signal through the JNK cascade. Dev. Biol. 2004, 276:378-390.
11. Cripps R.M., Olson E.N. Control of cardiac development by an evolutionarily conserved transcriptional network. Dev. Biol. 2002, 246:14-28.
12. Crossley A.C. The ultrastructure and function of pericardial cells and other nephrocytes in an insect: Calliphora erythrocephala. Tissue Cell 1972, 4:529-560.
13. Denholm B., Brown S., Ray R.P., Ruiz-Gomez M., Skaer H., Hombria J.C. Crossveinless-c is a RhoGAP required for actin reorganisation during morphogenesis. Development 2005, 132:2389-2400.
14. Eaton S., Auvinen P., Luo L., Jan Y.N., Simons K. CDC42 and Rac1 control different actin-dependent processes in the Drosophila wing disc epithelium. J. Cell Biol. 1995, 131:151-164.
15. Edwards K.A., Demsky M., Montague R.A., Weymouth N., Kiehart D.P. GFP-moesin illuminates actin cytoskeleton dynamics in living tissue and demonstrates cell shape changes during morphogenesis in Drosophila. Dev. Biol. 1997, 191:103-117.
16. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
17. Fox D.T., Homem C.C., Myster S.H., Wang F., Bain E.E., Peifer M. Rho1 regulates Drosophila adherens junctions independently of p120ctn. Development 2005, 132:4819-4831.
18. Gajewski K., Choi C.Y., Kim Y., Schulz R.A. Genetically distinct cardial cells within the Drosophila heart. Genesis 2000, 28:36-43.
19. Gates J., Mahaffey J.P., Rogers S.L., Emerson M., Rogers E.M., Sottile S.L., Van Vactor D., Gertler F.B., Peifer M. Enabled plays key roles in embryonic epithelial morphogenesis in Drosophila. Development 2007, 134:2027-2039.
20. Haag T.A., Haag N.P., Lekven A.C., Hartenstein V. The role of cell adhesion molecules in Drosophila heart morphogenesis: faint sausage, shotgun/DE-cadherin, and laminin A are required for discrete stages in heart development. Dev. Biol. 1999, 208:56-69.
21. Hall A. Rho family GTPases. Biochem. Soc. Trans. 2012, 40:1378-1382.
22. Han Z., Yi P., Li X., Olson E.N. Hand, an evolutionarily conserved bHLH transcription factor required for Drosophila cardiogenesis and hematopoiesis. Development 2006, 133:1175-1182.
23. Harden N., Lee J., Loh H.Y., Ong Y.M., Tan I., Leung T., Manser E., Lim L. A Drosophila homolog of the Rac- and Cdc42-activated serine/threonine kinase PAK is a potential focal adhesion and focal complex protein that colocalizes with dynamic actin structures. Mol. Cell. Biol. 1996, 16:1896-1908.
24. Harden N., Loh H.Y., Chia W., Lim L. A dominant inhibitory version of the small GTP-binding protein Rac disrupts cytoskeletal structures and inhibits developmental cell shape changes in Drosophila. Development 1995, 121:903-914.
25. Harden N., Ricos M., Ong Y.M., Chia W., Lim L. Participation of small GTPases in dorsal closure of the Drosophila embryo: distinct roles for Rho subfamily proteins in epithelial morphogenesis. J. Cell Sci. 1999, 112(Pt. 3):273-284.
26. Hing H., Xiao J., Harden N., Lim L., Zipursky S.L. Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila. Cell 1999, 97:853-863.
27. Jacinto A., Wood W., Balayo T., Turmaine M., Martinez-Arias A., Martin P. Dynamic actin-based epithelial adhesion and cell matching during Drosophila dorsal closure. Curr. Biol. 2000, 10:1420-1426.
28. Johndrow J.E., Magie C.R., Parkhurst S.M. Rho GTPase function in flies: insights from a developmental and organismal perspective. Biochem. Cell Biol. 2004, 82:643-657.
29. Kamiyama D., Chiba A. Endogenous activation patterns of Cdc42 GTPase within Drosophila embryos. Science 2009, 324:1338-1340.
30. Kawahara A., Nishi T., Hisano Y., Fukui H., Yamaguchi A., Mochizuki N. The sphingolipid transporter spns2 functions in migration of zebrafish myocardial precursors. Science 2009, 323:524-527.
31. Lo P.C., Skeath J.B., Gajewski K., Schulz R.A., Frasch M. Homeotic genes autonomously specify the anteroposterior subdivision of the Drosophila dorsal vessel into aorta and heart. Dev. Biol. 2002, 251:307-319.
32. Lu Y., Settleman J. The Drosophila Pkn protein kinase is a Rho/Rac effector target required for dorsal closure during embryogenesis. Genes Dev. 1999, 13:1168-1180.
33. Macabenta F.D., Jensen A.G., Cheng Y.S., Kramer J.J., Kramer S.G. Frazzled/DCC facilitates cardiac cell outgrowth and attachment during Drosophila dorsal vessel formation. Dev. Biol. 2013, 380:233-242.
34. Magie C.R., Meyer M.R., Gorsuch M.S., Parkhurst S.M. Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development. Development 1999, 126:5353-5364.
35. Martin P., Wood W. Epithelial fusions in the embryo. Curr. Opin. Cell Biol. 2002, 14:569-574.
36. Medioni C., Astier M., Zmojdzian M., Jagla K., Semeriva M. Genetic control of cell morphogenesis during Drosophila melanogaster cardiac tube formation. J. Cell Biol. 2008, 182:249-261.
37. Medioni C., Senatore S., Salmand P.A., Lalevee N., Perrin L., Semeriva M. The fabulous destiny of the Drosophila heart. Curr. Opin. Genet. Dev. 2009, 19:518-525.
38. Millard T.H., Martin P. Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure. Development 2008, 135:621-626.
39. Molina M.R., Cripps R.M. Ostia, the inflow tracts of the Drosophila heart, develop from a genetically distinct subset of cardial cells. Mech. Dev. 2001, 109:51-59.
40. Moreno-Rodriguez R.A., Krug E.L., Reyes L., Villavicencio L., Mjaatvedt C.H., Markwald R.R. Bidirectional fusion of the heart-forming fields in the developing chick embryo. Dev. Dyn. 2006, 235:191-202.
41. Nobes C.D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995, 81:53-62.
42. Panfilio K.A., Oberhofer G., Roth S. High plasticity in epithelial morphogenesis during insect dorsal closure. Biol. Open 2013, 2:1108-1118.
43. Pirraglia C., Jattani R., Myat M.M. Rac function in epithelial tube morphogenesis. Dev. Biol. 2006, 290:435-446.
44. Qian L., Wythe J.D., Liu J., Cartry J., Vogler G., Mohapatra B., Otway R.T., Huang Y., King I.N., Maillet M., Zheng Y., Crawley T., Taghli-Lamallem O., Semsarian C., Dunwoodie S., Winlaw D., Harvey R.P., Fatkin D., Towbin J.A., Molkentin J.D., Srivastava D., Ocorr K., Bruneau B.G., Bodmer R. Tinman/Nkx2-5 acts via miR-1 and upstream of Cdc42 to regulate heart function across species. J. Cell Biol. 2011, 193:1181-1196.
45. Ruggendorff A., Younossi-Hartenstein A., Hartenstein V. Embryonic origin and differentiation of the Drosophila heart. Roux's Arch. Dev. Biol. 1994, 203:266-280.
46. Santiago-Martinez E., Soplop N.H., Patel R., Kramer S.G. Repulsion by Slit and Roundabout prevents Shotgun/E-cadherin-mediated cell adhesion during Drosophila heart tube lumen formation. J. Cell Biol. 2008, 182:241-248.
47. Sellin J., Albrecht S., Kolsch V., Paululat A. Dynamics of heart differentiation, visualized utilizing heart enhancer elements of the Drosophila melanogaster bHLH transcription factor Hand. Gene Expr. Patterns 2006, 6:360-375.
48. Tao Y., Schulz R.A. Heart development in Drosophila. Semin. Cell Dev. Biol. 2007, 18:3-15.
49. Togel M., Pass G., Paululat A. The Drosophila wing hearts originate from pericardial cells and are essential for wing maturation. Dev. Biol. 2008, 318:29-37.
50. Totong R., Schell T., Lescroart F., Ryckebusch L., Lin Y.F., Zygmunt T., Herwig L., Krudewig A., Gershoony D., Belting H.G., Affolter M., Torres-Vazquez J., Yelon D. The novel transmembrane protein Tmem2 is essential for coordination of myocardial and endocardial morphogenesis. Development 2011, 138:4199-4205.
51. Trinh L.A., Stainier D.Y. Fibronectin regulates epithelial organization during myocardial migration in zebrafish. Dev. Cell 2004, 6:371-382.
52. Van Aelst L., Symons M. Role of Rho family GTPases in epithelial morphogenesis. Genes Dev. 2002, 16:1032-1054.
53. Warner S.J., Longmore G.D. Distinct functions for Rho1 in maintaining adherens junctions and apical tension in remodeling epithelia. J. Cell Biol. 2009, 185:1111-1125.
54. Wood W., Jacinto A., Grose R., Woolner S., Gale J., Wilson C., Martin P. Wound healing recapitulates morphogenesis in Drosophila embryos. Nat. Cell Biol. 2002, 4:907-912.
55. Woolner S., Jacinto A., Martin P. The small GTPase Rac plays multiple roles in epithelial sheet fusion - dynamic studies of Drosophila dorsal closure. Dev. Biol. 2005, 282:163-173.