Multiplexin Promotes Heart but Not Aorta Morphogenesis by Polarized Enhancement of Slit/Robo Activity at the Heart Lumen

PLoS Genetics

Volumn 9, Issue 6, 2013, Pages

  Harpaz, Nofar ^a   Ordan, Elly ^a   Ocorr, Karen ^b   Bodmer, Rolf ^b   Volk, Talila ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; F ACTIN; MULTIPLEXIN; ROUNDABOUT RECEPTOR; SLIT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENDOSOME; FEMALE; GENE; GENE INTERACTION; GENE OVEREXPRESSION; HEART DEVELOPMENT; HEART MUSCLE CELL; INTRACELLULAR SIGNALING; MP GENE; MYOTUBE; NONHUMAN; POLARIZATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; ROBO GENE; SLIT GENE;

ACTINS; ANIMALS; AORTA; CHONDROITIN SULFATE PROTEOGLYCANS; COLLAGEN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HEART; MORPHOGENESIS; NERVE TISSUE PROTEINS; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION;

MAMMALIA; VERTEBRATA;

EID: 84879619967     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003597     Document Type: Article

References (40)

1. Zaffran S, Frasch M, (2002) Early signals in cardiac development. Circ Res 91: 457-469.
2. Olson EN, (2006) Gene regulatory networks in the evolution and development of the heart. Science 313: 1922-1927.
3. Bier E, Bodmer R, (2004) Drosophila, an emerging model for cardiac disease. Gene 342: 1-11.
4. Tao Y, Schulz RA, (2007) Heart development in Drosophila. Semin Cell Dev Biol 18: 3-15.
5. Haag TA, Haag NP, Lekven AC, Hartenstein V, (1999) 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 208: 56-69.
6. Yarnitzky T, Volk T, (1995) Laminin is required for heart, somatic muscles, and gut development in the Drosophila embryo. Dev Biol 169: 609-618.
7. Vanderploeg J, Vazquez Paz LL, MacMullin A, Jacobs JR, (2012) Integrins are required for cardioblast polarisation in Drosophila. BMC Dev Biol 12: 8.
8. MacMullin A, Jacobs JR, (2006) Slit coordinates cardiac morphogenesis in Drosophila. Dev Biol 293: 154-164.
9. Medioni C, Astier M, Zmojdzian M, Jagla K, Semeriva M, (2008) Genetic control of cell morphogenesis during Drosophila melanogaster cardiac tube formation. J Cell Biol 182: 249-261.
10. Santiago-Martinez E, Soplop NH, Patel R, Kramer SG, (2008) Repulsion by Slit and Roundabout prevents Shotgun/E-cadherin-mediated cell adhesion during Drosophila heart tube lumen formation. J Cell Biol 182: 241-248.
11. Qian L, Liu J, Bodmer R, (2005) Slit and Robo control cardiac cell polarity and morphogenesis. Curr Biol 15: 2271-2278.
12. Albrecht S, Altenhein B, Paululat A, (2011) The transmembrane receptor Uncoordinated5 (Unc5) is essential for heart lumen formation in Drosophila melanogaster. Dev Biol 350: 89-100.
13. Meyer F, Moussian B, (2009) Drosophila multiplexin (Dmp) modulates motor axon pathfinding accuracy. Dev Growth Differ 51: 483-498.
14. Momota R, Naito I, Ninomiya Y, Ohtsuka A, (2011) Drosophila type XV/XVIII collagen, Mp, is involved in Wingless distribution. Matrix Biol 30: 258-266.
15. Muona A, Eklund L, Vaisanen T, Pihlajaniemi T, (2002) Developmentally regulated expression of type XV collagen correlates with abnormalities in Col15a1(-/-) mice. Matrix Biol 21: 89-102.
16. Rasi K, Piuhola J, Czabanka M, Sormunen R, Ilves M, et al. (2010) Collagen XV is necessary for modeling of the extracellular matrix and its deficiency predisposes to cardiomyopathy. Circ Res 107: 1241-1252.
17. Eklund L, Piuhola J, Komulainen J, Sormunen R, Ongvarrasopone C, et al. (2001) Lack of type XV collagen causes a skeletal myopathy and cardiovascular defects in mice. Proc Natl Acad Sci U S A 98: 1194-1199.
18. Medioni C, Bertrand N, Mesbah K, Hudry B, Dupays L, et al. (2010) Expression of Slit and Robo genes in the developing mouse heart. Dev Dyn 239: 3303-3311.
19. Mommersteeg MT, Andrews WD, Ypsilanti AR, Zelina P, Yeh ML, et al. (2013) Slit-roundabout signaling regulates the development of the cardiac systemic venous return and pericardium. Circ Res 112: 465-475.
20. Rothberg JM, Hartley DA, Walther Z, Artavanis-Tsakonas S, (1988) slit: an EGF-homologous locus of D. melanogaster involved in the development of the embryonic central nervous system. Cell 55: 1047-1059.
21. Spitzweck B, Brankatschk M, Dickson BJ, (2010) Distinct protein domains and expression patterns confer divergent axon guidance functions for Drosophila Robo receptors. Cell 140: 409-420.
22. Evans TA, Bashaw GJ, (2010) Functional diversity of Robo receptor immunoglobulin domains promotes distinct axon guidance decisions. Curr Biol 20: 567-572.
23. Reuveny A, Elhanany H, Volk T, (2009) Enhanced sensitivity of midline glial cells to apoptosis is achieved by HOW(L)-dependent repression of Diap1. Mech Dev 126: 30-41.
24. Yang L, Bashaw GJ, (2006) Son of sevenless directly links the Robo receptor to rac activation to control axon repulsion at the midline. Neuron 52: 595-607.
25. Hsouna A, Kim YS, VanBerkum MF, (2003) Abelson tyrosine kinase is required to transduce midline repulsive cues. J Neurobiol 57: 15-30.
26. Hsouna A, VanBerkum MF, (2008) Abelson tyrosine kinase and Calmodulin interact synergistically to transduce midline guidance cues in the Drosophila embryonic CNS. Int J Dev Neurosci 26: 345-354.
27. Ocorr K, Reeves NL, Wessells RJ, Fink M, Chen HS, et al. (2007) KCNQ potassium channel mutations cause cardiac arrhythmias in Drosophila that mimic the effects of aging. Proc Natl Acad Sci U S A 104: 3943-3948.
28. Chanana B, Steigemann P, Jackle H, Vorbruggen G, (2009) Reception of Slit requires only the chondroitin-sulphate-modified extracellular domain of Syndecan at the target cell surface. Proc Natl Acad Sci U S A 106: 11984-11988.
29. Knox J, Moyer K, Yacoub N, Soldaat C, Komosa M, et al. (2011) Syndecan contributes to heart cell specification and lumen formation during Drosophila cardiogenesis. Dev Biol 356 (2):: 279-90.
30. Rodriguez-Fraticelli AE, Auzan M, Alonso MA, Bornens M, Martin-Belmonte F, (2012) Cell confinement controls centrosome positioning and lumen initiation during epithelial morphogenesis. J Cell Biol 198: 1011-1023.
31. Rhee J, Buchan T, Zukerberg L, Lilien J, Balsamo J, (2007) Cables links Robo-bound Abl kinase to N-cadherin-bound beta-catenin to mediate Slit-induced modulation of adhesion and transcription. Nat Cell Biol 9: 883-892.
32. Hanai J, Gloy J, Karumanchi SA, Kale S, Tang J, et al. (2002) Endostatin is a potential inhibitor of Wnt signaling. J Cell Biol 158: 529-539.
33. Passos-Bueno MR, Suzuki OT, Armelin-Correa LM, Sertie AL, Errera FI, et al. (2006) Mutations in collagen 18A1 and their relevance to the human phenotype. An Acad Bras Cienc 78: 123-131.
34. Fukai N, Eklund L, Marneros AG, Oh SP, Keene DR, et al. (2002) Lack of collagen XVIII/endostatin results in eye abnormalities. Embo J 21: 1535-1544.
35. Wang X, Harris RE, Bayston LJ, Ashe HL, (2008) Type IV collagens regulate BMP signalling in Drosophila. Nature 455: 72-77.
36. Bunt S, Hooley C, Hu N, Scahill C, Weavers H, et al. (2010) Hemocyte-secreted type IV collagen enhances BMP signaling to guide renal tubule morphogenesis in Drosophila. Dev Cell 19: 296-306.
37. Deng WM, Schneider M, Frock R, Castillejo-Lopez C, Gaman EA, et al. (2003) Dystroglycan is required for polarizing the epithelial cells and the oocyte in Drosophila. Development 130: 173-184.
38. Harpaz N, Volk T, (2011) A novel method for obtaining semi-thin cross sections of the Drosophila heart and their labeling with multiple antibodies. Methods 56: 63-68.
39. Gilsohn E, Volk T, (2010) Slowdown promotes muscle integrity by modulating integrin-mediated adhesion at the myotendinous junction. Development 137: 785-794.
40. Ocorr K, Fink M, Cammarato A, Bernstein S, Bodmer R, (2009) Semi-automated Optical Heartbeat Analysis of small hearts. J Vis Exp.