Effectors of tridimensional cell morphogenesis and their evolution

Seminars in Cell and Developmental Biology

Volumn 23, Issue 3, 2012, Pages 341-349

  Chanut Delalande, Hélène ^a,b   Ferrer, Pierre ^a,b   Payre, François ^a,b   Plaza, Serge ^a,b  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b CNRS   (France)

Author keywords

Cell morphogenesis; Cochlea; Drosophila; Epidermis; Stereocilia

Indexed keywords

REGULATOR PROTEIN;

CELL DIFFERENTIATION; CELL MATURATION; CELL SHAPE; COCHLEA; EPIDERMIS CELL; GENE FUNCTION; GENE IDENTIFICATION; HUMAN; MOLECULAR EVOLUTION; MORPHOGENESIS; NONHUMAN; PROTEIN FUNCTION; REVIEW; STEREOCILIUM;

VERTEBRATA;

EID: 84860387927     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2012.03.002     Document Type: Review

References (78)

1. Pilot F., Lecuit T. Compartmentalized morphogenesis in epithelia: from cell to tissue shape. Dev Dyn 2005, 232:685-694.
2. Blanchard G.B., Murugesu S., Adams R.J., Martinez-Arias A., Gorfinkiel N. Cytoskeletal dynamics and supracellular organisation of cell shape fluctuations during dorsal closure. Development 2010, 137:2743-2752.
3. David D.J., Tishkina A., Harris T.J. The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila. Development 2010, 137:1645-1655.
4. Fernandez-Gonzalez R., Simoes Sde M., Roper J.C., Eaton S., Zallen J.A. Myosin II dynamics are regulated by tension in intercalating cells. Dev Cell 2009, 17:736-743.
5. Rauzi M., Lenne P.F., Lecuit T. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 2010, 468:1110-1114.
6. Levayer R., Pelissier-Monier A., Lecuit T. Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat Cell Biol 2011, 13:529-540.
7. Payre F. Genetic control of epidermis differentiation in Drosophila. Int J Dev Biol 2004, 48:207-215.
8. Richardson G.P., de Monvel J.B., Petit C. How the genetics of deafness illuminates auditory physiology. Annu Rev Physiol 2011, 73:311-334.
9. Price M.H., Roberts D.M., McCartney B.M., Jezuit E., Peifer M. Cytoskeletal dynamics and cell signaling during planar polarity establishment in the Drosophila embryonic denticle. J Cell Sci 2006, 119:403-415.
10. Simone R.P., DiNardo S. Actomyosin contractility and Discs large contribute to junctional conversion in guiding cell alignment within the Drosophila embryonic epithelium. Development 2010, 137:1385-1394.
11. Kaplan N.A., Colosimo P.F., Liu X., Tolwinski N.S. Complex interactions between GSK3 and aPKC in Drosophila embryonic epithelial morphogenesis. PLoS One 2011, 6:e18616.
12. Dickinson W.J., Thatcher J.W. Morphogenesis of denticles and hairs in Drosophila embryos: involvement of actin-associated proteins that also affect adult structures. Cell Motil Cytoskeleton 1997, 38:9-21.
13. Uv A., Moussian B. The apical plasma membrane of Drosophila embryonic epithelia. Eur J Cell Biol 2010, 89:208-211.
14. Hatini V., DiNardo S. Divide and conquer: pattern formation in Drosophila embryonic epidermis. Trends Genet 2001, 17:574-579.
15. Payre F., Vincent A., Carreno S. ovo/svb Integrates Wingless and DER pathways to control epidermis differentiation. Nature 1999, 400:271-275.
16. Delon I., Chanut-Delalande H., Payre F. The ovo/shavenbaby transcription factor specifies actin remodelling during epidermal differentiation in Drosophila. Mech Dev 2003, 120:747-758.
17. Delon I., Payre F. Evolution of larval morphology in flies: get in shape with shavenbaby. Trends Genet 2004, 20:305-313.
18. Sucena E., Delon I., Jones I., Payre F., Stern D.L. Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism. Nature 2003, 424:935-938.
19. Sucena E., Stern D.L. Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. Proc Natl Acad Sci USA 2000, 97:4530-4534.
20. Khila A., El Haidani A., Vincent A., Payre F., Souda S.I. The dual function of ovo/shavenbaby in germline and epidermis differentiation is conserved between Drosophila melanogaster and the olive fruit fly Bactrocera oleae. Insect Biochem Mol Biol 2003, 33:691-699.
21. Frankel N., Davis G.K., Vargas D., Wang S., Payre F., Stern D.L. Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 2010, 466:490-493.
22. McGregor A.P., Orgogozo V., Delon I., Zanet J., Srinivasan D.G., Payre F., et al. Morphological evolution through multiple cis-regulatory mutations at a single gene. Nature 2007, 448:587-590.
23. Galindo M.I., Pueyo J.I., Fouix S., Bishop S.A., Couso J.P. Peptides encoded by short ORFs control development and define a new eukaryotic gene family. PLoS Biol 2007, 5:e106.
24. Kondo T., Hashimoto Y., Kato K., Inagaki S., Hayashi S., Kageyama Y. Small peptide regulators of actin-based cell morphogenesis encoded by a polycistronic mRNA. Nat Cell Biol 2007, 9:660-665.
25. Savard J., Marques-Souza H., Aranda M., Tautz D. A segmentation gene in tribolium produces a polycistronic mRNA that codes for multiple conserved peptides. Cell 2006, 126:559-569.
26. Kondo T., Plaza S., Zanet J., Benrabah E., Valenti P., Hashimoto Y., et al. Small peptides switch the transcriptional activity of Shavenbaby during Drosophila embryogenesis. Science 2010, 329:336-339.
27. Chanut-Delalande H., Fernandes I., Roch F., Payre F., Plaza S. Shavenbaby couples patterning to epidermal cell shape control. PLoS Biol 2006, 4:e290.
28. Strutt D., Warrington S.J. Planar polarity genes in the Drosophila wing regulate the localisation of the FH3-domain protein Multiple Wing Hairs to control the site of hair production. Development 2008, 135:3103-3111.
29. Yan J., Huen D., Morely T., Johnson G., Gubb D., Roote J., et al. The multiple-wing-hairs gene encodes a novel GBD-FH3 domain-containing protein that functions both prior to and after wing hair initiation. Genetics 2008, 180:219-228.
30. Ren N., He B., Stone D., Kirakodu S., Adler P.N. The shavenoid gene of Drosophila encodes a novel actin cytoskeleton interacting protein that promotes wing hair morphogenesis. Genetics 2006, 172:1643-1653.
31. Fernandes I., Chanut-Delalande H., Ferrer P., Latapie Y., Waltzer L., Affolter M., et al. Zona pellucida domain proteins remodel the apical compartment for localized cell shape changes. Dev Cell 2010, 18:64-76.
32. Jovine L., Darie C.C., Litscher E.S., Wassarman P.M. Zona pellucida domain proteins. Annu Rev Biochem 2005, 74:83-114.
33. Wassarman P.M. Zona pellucida glycoproteins. J Biol Chem 2008, 283:24285-24289.
34. Plaza S., Chanut-Delalande H., Fernandes I., Wassarman P.M., Payre F. From A to Z: apical structures and zona pellucida-domain proteins. Trends Cell Biol 2010, 20:524-532.
35. Andrew D.J., Baker B.S. Expression of the Drosophila secreted cuticle protein 73 (dsc73) requires shavenbaby. Dev Dyn 2008, 237:1198-1206.
36. Adler P.N. Planar signaling and morphogenesis in Drosophila. Dev Cell 2002, 2:525-535.
37. Donoughe S., Dinardo S. Dachsous and frizzled contribute separately to planar polarity in the Drosophila ventral epidermis. Development 2011, 138:2751-2759.
38. Repiso A., Saavedra P., Casal J., Lawrence P.A. Planar cell polarity: the orientation of larval denticles in Drosophila appears to depend on gradients of Dachsous and Fat. Development 2010, 137:3411-3415.
39. Baum B., Georgiou M. Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J Cell Biol 2011, 192:907-917.
40. Walters J.W., Dilks S.A., DiNardo S. Planar polarization of the denticle field in the Drosophila embryo: roles for Myosin II (zipper) and fringe. Dev Biol 2006, 297:323-339.
41. Cant K., Knowles B.A., Mooseker M.S., Cooley L. Drosophila singed, a fascin homolog, is required for actin bundle formation during oogenesis and bristle extension. J Cell Biol 1994, 125:369-380.
42. Tilney L.G., Tilney M.S., Guild G.M. F actin bundles in Drosophila bristles. I. Two filament cross-links are involved in bundling. J Cell Biol 1995, 130:629-638.
43. Bogdan S., Stephan R., Lobke C., Mertens A., Klambt C. Abi activates WASP to promote sensory organ development. Nat Cell Biol 2005, 7:977-984.
44. Lu Q., Yan J., Adler P.N. The Drosophila planar polarity proteins inturned and multiple wing hairs interact physically and function together. Genetics 2010, 185:549-558.
45. Lee K., Gallop J.L., Rambani K., Kirschner M.W. Self-assembly of filopodia-like structures on supported lipid bilayers. Science 2010, 329:1341-1345.
46. Fricke R., Gohl C., Dharmalingam E., Grevelhorster A., Zahedi B., Harden N., et al. Drosophila Cip4/Toca-1 integrates membrane trafficking and actin dynamics through WASP and SCAR/WAVE. Curr Biol 2009, 19:1429-1437.
47. Roch F., Alonso C.R., Akam M. Drosophila miniature and dusky encode ZP proteins required for cytoskeletal reorganisation during wing morphogenesis. J Cell Sci 2003, 116:1199-1207.
48. Bokel C., Prokop A., Brown N.H. Papillote and Piopio Drosophila ZP-domain proteins required for cell adhesion to the apical extracellular matrix and microtubule organization. J Cell Sci 2005, 118:633-642.
49. Nagaraj R., Adler P.N. Dusky-like functions as a Rab11 effector for the deposition of cuticle during Drosophila bristle development. Development 2012, 139:906-916.
50. DiBartolomeis S.M., Akten B., Genova G., Roberts M.A., Jackson F.R. Molecular analysis of the Drosophila miniature-dusky (m-dy) gene complex: m-dy mRNAs encode transmembrane proteins with similarity to C. elegans cuticulin. Mol Genet Genomics 2002, 267:564-576.
51. Tilney L.G., Tilney M.S., DeRosier D.J. Actin filaments, stereocilia, and hair cells: how cells count and measure. Annu Rev Cell Biol 1992, 8:257-274.
52. Kelly M.C., Chen P. Development of form and function in the mammalian cochlea. Curr Opin Neurobiol 2009, 19:395-401.
53. DeRosier D.J., Tilney L.G. F-actin bundles are derivatives of microvilli: what does this tell us about how bundles might form. J Cell Biol 2000, 148:1-6.
54. Lynch E.D., Lee M.K., Morrow J.E., Welcsh P.L., Leon P.E., King M.C. Nonsyndromic deafness DFNA1 associated with mutation of a human homolog of the Drosophila gene diaphanous. Science 1997, 278:1315-1318.
55. Sekerkova G., Richter C.P., Bartles J.R. Roles of the espin actin-bundling proteins in the morphogenesis and stabilization of hair cell stereocilia revealed in CBA/CaJ congenic jerker mice. PLoS Genet 2011, 7:e1002032.
56. Sekerkova G., Zheng L., Mugnaini E., Bartles J.R. Differential expression of espin isoforms during epithelial morphogenesis, stereociliogenesis and postnatal maturation in the developing inner ear. Dev Biol 2006, 291:83-95.
57. Grieshaber S.S., Lankenau D.H., Talbot T., Holland S., Petersen N.S. Expression of the 53kD forked protein rescues F-actin bundle formation and mutant bristle phenotypes in Drosophila. Cell Motil Cytoskeleton 2001, 50:198-206.
58. Shin J.B., Longo-Guess C.M., Gagnon L.H., Saylor K.W., Dumont R.A., Spinelli K.J., et al. The R109H variant of fascin-2, a developmentally regulated actin crosslinker in hair-cell stereocilia, underlies early-onset hearing loss of DBA/2J mice. J Neurosci 2010, 30:9683-9694.
59. Chou S.W., Hwang P., Gomez G., Fernando C.A., West M.C., Pollock L.M., et al. Fascin 2b is a component of stereocilia that lengthens actin-based protrusions. PLoS One 2011, 6:e14807.
60. Adams J.C. Roles of fascin in cell adhesion and motility. Curr Opin Cell Biol 2004, 16:590-596.
61. Zanet J., Stramer B., Millard T., Martin P., Payre F., Plaza S. Fascin is required for blood cell migration during Drosophila embryogenesis. Development 2009, 136:2557-2565.
62. Russell I.J., Legan P.K., Lukashkina V.A., Lukashkin A.N., Goodyear R.J., Richardson G.P. Sharpened cochlear tuning in a mouse with a genetically modified tectorial membrane. Nat Neurosci 2007, 10:215-223.
63. Hughes D.C., Legan P.K., Steel K.P., Richardson G.P. Mapping of the alpha-tectorin gene (TECTA) to mouse chromosome 9 and human chromosome 11: a candidate for human autosomal dominant nonsyndromic deafness. Genomics 1998, 48:46-51.
64. Verhoeven K., Van Laer L., Kirschhofer K., Legan P.K., Hughes D.C., Schatteman I., et al. Mutations in the human alpha-tectorin gene cause autosomal dominant non-syndromic hearing impairment. Nat Genet 1998, 19:60-62.
65. Legan P.K., Lukashkina V.A., Goodyear R.J., Lukashkin A.N., Verhoeven K., Van Camp G., et al. A deafness mutation isolates a second role for the tectorial membrane in hearing. Nat Neurosci 2005, 8:1035-1042.
66. Monne M., Han L., Schwend T., Burendahl S., Jovine L. Crystal structure of the ZP-N domain of ZP3 reveals the core fold of animal egg coats. Nature 2008, 456:653-657.
67. Montcouquiol M., Rachel R.A., Lanford P.J., Copeland N.G., Jenkins N.A., Kelley M.W. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 2003, 423:173-177.
68. Montcouquiol M., Sans N., Huss D., Kach J., Dickman J.D., Forge A., et al. Asymmetric localization of Vangl2 and Fz3 indicate novel mechanisms for planar cell polarity in mammals. J Neurosci 2006, 26:5265-5275.
69. Wang J., Mark S., Zhang X., Qian D., Yoo S.J., Radde-Gallwitz K., et al. Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nat Genet 2005, 37:980-985.
70. Belyantseva I.A., Boger E.T., Naz S., Frolenkov G.I., Sellers J.R., Ahmed Z.M., et al. Myosin-XVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nat Cell Biol 2005, 7:148-156.
71. Mburu P., Mustapha M., Varela A., Weil D., El-Amraoui A., Holme R.H., et al. Defects in whirlin, a PDZ domain molecule involved in stereocilia elongation, cause deafness in the whirler mouse and families with DFNB31. Nat Genet 2003, 34:421-428.
72. Hertzano R., Shalit E., Rzadzinska A.K., Dror A.A., Song L., Ron U., et al. A Myo6 mutation destroys coordination between the myosin heads, revealing new functions of myosin VI in the stereocilia of mammalian inner ear hair cells. PLoS Genet 2008, 4:e1000207.
73. Polesello C., Payre F. Small is beautiful: what flies tell us about ERM protein function in development. Trends Cell Biol 2004, 14:294-302.
74. Pataky F., Pironkova R., Hudspeth A.J. Radixin is a constituent of stereocilia in hair cells. Proc Natl Acad Sci USA 2004, 101:2601-2606.
75. Kitajiri S., Fukumoto K., Hata M., Sasaki H., Katsuno T., Nakagawa T., et al. Radixin deficiency causes deafness associated with progressive degeneration of cochlear stereocilia. J Cell Biol 2004, 166:559-570.
76. Lecuit T., Lenne P.F. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat Rev Mol Cell Biol 2007, 8:633-644.
77. Tilney L.G., Connelly P.S., Ruggiero L., Vranich K.A., Guild G.M., Derosier D. The role actin filaments play in providing the characteristic curved form of Drosophila bristles. Mol Biol Cell 2004, 15:5481-5491.
78. Manor U., Disanza A., Grati M., Andrade L., Lin H., Di Fiore P.P., et al. Regulation of stereocilia length by myosin XVa and whirlin depends on the actin-regulatory protein Eps8. Curr Biol 2011, 21:167-172.