Cranial placodes: Models for exploring the multi-facets of cell adhesion in epithelial rearrangement, collective migration and neuronal movements

Developmental Biology

Volumn 401, Issue 1, 2015, Pages 25-36

  Breau, Marie Anne ^a,b   Schneider Maunoury, Sylvie ^a,b  

^a Université René Descartes   (France)

^b Département de Biologie   (France)

Author keywords

Adhesion; Collective migration; Epithelial morphogenesis; Morphogenesis; Neuronal migration; Placode; Sprouting

Indexed keywords

ANOSMIN1; CD151 ANTIGEN; CELL ADHESION MOLECULE; CHEMOKINE RECEPTOR CXCR4; NERVE CELL ADHESION MOLECULE; ROBO2 PROTEIN; SLIT1 PROTEIN; STROMAL CELL DERIVED FACTOR 1; TIGHT JUNCTION PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

ARTICLE; CELL ADHESION; CELL CONTACT; CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CELL STRUCTURE; CELLULAR PARAMETERS; CONTACT INHIBITION; CRANIAL PLACODE MORPHOGENESIS; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIAL REARRANGEMENT; EPITHELIUM CELL; EXTRACELLULAR MATRIX; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NEURAL CREST CELL; NEUROECTODERM; NONHUMAN; POSTERIOR LATERAL LINE PRIMORDIUM; PRIMORDIUM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CELL MOTION; CYTOLOGY; ECTODERM; EMBRYOLOGY; EPITHELIUM; HUMAN; PHYSIOLOGY; SKULL;

VERTEBRATA;

ANIMALS; CELL ADHESION; CELL MOVEMENT; ECTODERM; EMBRYONIC DEVELOPMENT; EPITHELIUM; EXTRACELLULAR MATRIX; HUMANS; MODELS, BIOLOGICAL; MORPHOGENESIS; SKULL;

EID: 84927952319     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2014.12.012     Document Type: Review

References (111)

1. Aman A., Piotrowski T. Wnt/b-catenin and Fgf signaling control collective cell migration by restricting chemokine receptor expression. Dev. Cell 2008, 15:749-761.
2. Aman A., Piotrowski T. Multiple signaling interactions coordinate collective cell migration of the posterior lateral line primordium. Cell Adhes. Migr. 2009, 3:365-368.
3. Babb-Clendenon S., Shen Y.C., Liu Q., Turner K.E., Mills M.S., Cook G.W., Miller C.A., Gattone V.H., Barald K.F., Marrs J.A. Cadherin-2 participates in the morphogenesis of the zebrafish inner ear. J. Cell Sci. 2006, 119:5169-5177.
4. Belvindrah R., Hankel S., Walker J., Patton B.L., Muller U. Beta1 integrins control the formation of cell chains in the adult rostral migratory stream. J. Neurosci. 2007, 27:2704-2717.
5. Bhat N., Riley B.B. Integrin-α5 coordinates assembly of posterior cranial placodes in zebrafish and enhances Fgf-dependent regulation of otic/epibranchial cells. PLoS One 2011, 6:e27778.
6. Blentic A., Chambers D., Skinner A., Begbie J., Graham A. The formation of the cranial ganglia by placodally-derived sensory neuronal precursors. Mol. Cell. Neurosci. 2011, 46:452-459.
7. Bogdanović O., Delfino-Machín M., Nicolás-Pérez M., Gavilán M.P., Gago-Rodrigues I., Fernandez-Minan A., Lillo C., Ríos R.M., Wittbrodt J., Martínez-Morales J.R. Numb/Numbl-Opo antagonism controls retinal epithelium morphogenesis by regulating integrin endocytosis. Dev. Cell 2012, 23:782-795.
8. Bok J., Chang W., Wu D.K. Patterning and morphogenesis of the vertebrate inner ear. Int. J. Dev. Biol. 2007, 51:521-533.
9. Breau M.A., Schneider-Maunoury S. Mechanisms of cranial placode assembly. Int. J. Dev. Biol. 2014, 58:9-19.
10. Breau M.A., Wilson D., Wilkinson D.G., Xu Q. Chemokine and Fgf signalling act as opposing guidance cues in formation of the lateral line primordium. Development 2012, 139:2246-2253.
11. Breau M.A., Wilkinson D.G., Xu Q. A Hox gene controls lateral line cell migration by regulating chemokine receptor expression downstream of Wnt signaling. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:16892-16897.
12. Busch-Nentwich E. The deafness gene dfna5 is crucial for ugdh expression and HA production in the developing ear in zebrafish. Development 2004, 131:943-951.
13. Cai D., Chen S.-C., Prasad M., He L., Wang X., Choesmel-Cadamuro V., Sawyer J.K., Danuser G., Montell D.J. Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration. Cell 2014, 157:1146-1159.
14. Caplan M.J., Kamsteeg E.J., Duffield A. Tetraspan proteins: regulators of renal structure and function. Curr. Opin. Nephrol. Hypertens. 2007, 16:353-358.
15. Carmona-Fontaine C., Matthews H.K., Kuriyama S., Moreno M., Dunn G.A., Parsons M., Stern C.D., Mayor R. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 2008, 456:957-961.
16. Chauhan B.K., Disanza A., Choi S.Y., Faber S.C., Lou M., Beggs H.E., Scita G., Zheng Y., Lang R.A. Cdc42- and IRSp53-dependent contractile filopodia tether presumptive lens and retina to coordinate epithelial invagination. Development 2009, 136:3657-3667.
17. Christophorou N.A.D., Mende M., Lleras-Forero L., Grocott T., Streit A. Pax2 coordinates epithelial morphogenesis and cell fate in the inner ear. Dev. Biol. 2010, 345:180-190.
18. Cooper J.A. Cell biology in neuroscience: mechanisms of cell migration in the nervous system. J. Cell Biol. 2013, 202:725-734.
19. Dalle Nogare D., Somers K., Rao S., Matsuda M., Reichman-Fried M., Raz E., Chitnis A.B. Leading and trailing cells cooperate in collective migration of the zebrafish posterior lateral line primordium. Development 2014, 141:3188-3196.
20. D'Amico-Martel A., Noden D.M. Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. Am. J. Anat. 1983, 166:445-468.
21. David N.B., Sapède D., Saint-Etienne L., Thisse C., Thisse B., Dambly-Chaudière C., Rosa F.M., Ghysen A. Molecular basis of cell migration in the fish lateral line: role of the chemokine receptor CXCR4 and of its ligand, SDF1. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:16297-16302.
22. Davies D. Cell-extracellular matrix versus cell-cell interactions during the development of the cochlear-vestibular ganglion. J. Neurosci. Res. 2011, 89:1375-1387.
23. Donà E., Barry J.D., Valentin G., Quirin C., Khmelinskii A., Kunze A., Durdu S., Newton L.R., Fernandez-Minan A., Huber W., Knop M., Gilmour D. Directional tissue migration through a self-generated chemokine gradient. Nature 2013, 503:285-289.
24. Duband J.L. Diversity in the molecular and cellular strategies of epithelium-to-mesenchyme transitions: insights from the neural crest. Cell Adhes. Migr. 2010, 4:458-482.
25. Dumortier J.G., Martin S., Meyer D., Rosa F.M., David N.B. Collective mesendoderm migration relies on an intrinsic directionality signal transmitted through cell contacts. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:16945-16950.
26. Durdu S., Iskar M., Revenu C., Schieber N., Kunze A., Bork P., Schwab Y., Gilmour D. Luminal signalling links cell communication to tissue architecture during organogenesis. Nature 2014, 515:120-124.
27. Ernst S., Liu K., Agarwala S., Moratscheck N., Avci M.E., Nogare D.D., Chitnis A.B., Ronneberger O., Lecaudey V. Shroom3 is required downstream of FGF signalling to mediate proneuromast assembly in zebrafish. Development 2012, 139:4571-4581.
28. Famulski J.K., Solecki D.J. New spin on an old transition: epithelial parallels in neuronal adhesion control. Trends Neurosci. 2013, 36:163-173.
29. Fata J.E., Werb Z., Bissell M.J. Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast Cancer Res 2004, 6:1-11.
30. Friedl P., Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 2009, 10:445-457.
31. Friedl P., Locker J., Sahai E., Segall J.E. Classifying collective cancer cell invasion. Nat. Cell Biol. 2012, 14:777-783.
32. Gato A., Martin C., Alonso M.I., Martinez-Alvarez C., Moro J.A. Chondroitin sulphate proteoglycan is involved in lens vesicle morphogenesis in chick embryos. Exp. Eye Res. 2001, 73:469-478.
33. Geng F.S., Abbas L., Baxendale S., Holdsworth C.J., Swanson A.G., Slanchev K., Hammerschmidt M., Topczewski J., Whitfield T.T. Semicircular canal morphogenesis in the zebrafish inner ear requires the function of gpr126 (lauscher), an adhesion class G protein-coupled receptor gene. Development 2013, 140:4362-4374.
34. Gerchman E., Hilfer S.R., Brown J.W. Involvement of extracellular matrix in the formation of the inner ear. Dev. Dyn. 1995, 202:421-432.
35. Gerety S.S., Wilkinson D.G. Morpholino artifacts provide pitfalls and reveal a novel role for pro-apoptotic genes in hindbrain boundary development. Dev. Biol. 2011, 350:279-289.
36. Ghysen A., Dambly-Chaudière C. Development of the zebrafish lateral line. Curr. Opin. Neurobiol. 2004, 14:67-73.
37. Govek E.E., Hatten M.E., Van Aelst L. The role of Rho GTPase proteins in CNS neuronal migration. Dev. Neurobiol. 2011, 71:528-553.
38. Graham A., Blentic A., Duque S., Begbie J. Delamination of cells from neurogenic placodes does not involve an epithelial-to-mesenchymal transition. Development 2007, 134:4141-4145.
39. Greiling T.M., Clark J.I. Early lens development in the zebrafish: a three-dimensional time-lapse analysis. Dev. Dyn. 2009, 238:2254-2265.
40. Guillot C., Lecuit T. Mechanics of epithelial tissue homeostasis and morphogenesis. Science 2013, 340:1185-1189.
41. Gutzman J.H., Graeden E.G., Lowery L.A., Holley H.S., Sive H. Formation of the zebrafish midbrain-hindbrain boundary constriction requires laminin-dependent basal constriction. Mech. Dev. 2008, 125:974-983.
42. Haas P., Gilmour D. Chemokine signaling mediates self-organizing tissue migration in the zebrafish lateral line. Dev. Cell 2006, 10:673-680.
43. Haddon C.M., Lewis J.H. Hyaluronan as a propellant for epithelial movement: the development of semicircular canals in the inner ear of Xenopus. Development 1991, 112:541-550.
44. Harding M.J., McGraw H.F., Nechiporuk A. The roles and regulation of multicellular rosette structures during morphogenesis. Development 2014, 141:2549-2558.
45. Harding M.J., Nechiporuk A.V. Fgfr-Ras-MAPK signaling is required for apical constriction via apical positioning of Rho-associated kinase during mechanosensory organ formation. Development 2012, 139. (3467-3467).
46. Harrington M.J., Hong E., Fasanmi O., Brewster R. Cadherin-mediated adhesion regulates posterior body formation. BMC. Dev. Biol. 2007, 7:130.
47. Hava D., Forster U., Matsuda M., Cui S., Link B.A., Eichhorst J., Wiesner B., Chitnis A., Abdelilah-Seyfried S. Apical membrane maturation and cellular rosette formation during morphogenesis of the zebrafish lateral line. J. Cell Sci. 2009, 122:687-695.
48. He L., Wang X., Tang H.L., Montell D.J. Tissue elongation requires oscillating contractions of a basal actomyosin network. Nat. Cell Biol. 2010, 12:1133-1142.
49. Huang J., Rajagopal R., Liu Y., Dattilo L.K., Shaham O., Ashery-Padan R., Beebe D.C. The mechanism of lens placode formation: a case of matrix-mediated morphogenesis. Dev. Biol. 2011, 355:32-42.
50. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110:673-687.
51. Kasza K.E., Farrell D.L., Zallen J.A. Spatiotemporal control of epithelial remodeling by regulated myosin phosphorylation. Proc. Natl. Acad. Sci. 2014, 111:11732-11737.
52. Kerstetter A.E., Azodi E., Marrs J.A., Liu Q. Cadherin-2 function in the cranial ganglia and lateral line system of developing zebrafish. Dev. Dyn. 2004, 230:137-143.
53. Kollmar R., Nakamura S.K., Kappler J.A., Hudspeth A.J. Expression and phylogeny of claudins in vertebrate primordia. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:10196-10201.
54. Knaut H., Blader P., Strähle U., Schier A.F. Assembly of trigeminal sensory ganglia by chemokine signaling. Neuron 2005, 47:653-666.
55. Kreslova J., Machon O., Ruzickova J., Lachova J., Wawrousek E.F., Kemler R., Krauss S., Piatigorsky J., Kozmik Z. Abnormal lens morphogenesis and ectopic lens formation in the absence of β-catenin function. Genesis 2007, 45:157-168.
56. LaMora A., Voigt M.M. Cranial sensory ganglia neurons require intrinsic N-cadherin function for guidance of afferent fibers to their final targets. Neuroscience 2009, 159:1175-1184.
57. Lang R.A., Herman K., Reynolds A.B., Hildebrand J.D., Plageman T.F. p120-catenin-dependent junctional recruitment of Shroom3 is required for apical constriction during lens pit morphogenesis. Development 2014, 141:3177-3187.
58. Lassiter R.N.T., Reynolds S.B., Marin K.D., Mayo T.F., Stark M.R. FGF signaling is essential for ophthalmic trigeminal placode cell delamination and differentiation. Dev. Dyn. 2009, 238:1073-1082.
59. Lassiter R.N.T., Stark M.R., Zhao T., Zhou C.J. Signaling mechanisms controlling cranial placode neurogenesis and delamination. Dev. Biol. 2014, 389:39-49.
60. Lecaudey V., Cakan-Akdogan G., Norton W.H.J., Gilmour D. Dynamic Fgf signaling couples morphogenesis and migration in the zebrafish lateral line primordium. Development 2008, 135:2695-2705.
61. 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.
62. Legouis R., Hardelin J.P., Levilliers J., Claverie J.M., Compain S., Wunderle V., Millasseau P., Le Paslier D., Cohen D., Caterina D., Bougueleret L., Delemarre-Van de Waal, H., Lutfalla G., Weissenbach J., Petit C. The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molecules. Cell 1991, 67:423-435.
63. Levi G., Gumbiner B., Thiery J.P. The distribution of E cadherin during Xenopus laevis development. Development 1991, 111:159-169.
64. Liu Q., Dalman M.R., Sarmah S., Chen S., Chen Y., Hurlbut A.K., Spencer M.A., Pancoe L., Marrs J.A. Cell adhesion molecule cadherin-6 function in zebrafish cranial and lateral line ganglia development. Dev. Dyn. 2011, 240:1716-1726.
65. Liu Q., Ensign R.D., Azodi E. Cadherin-1, -2 and -4 expression in the cranial ganglia and lateral line system of developing zebrafish. Gene Expression Patterns 2003, 3:653-658.
66. Liu Q., Marrs J.A., Azodi E., Kerstetter A.E., Babb S.G., Hashmi L. Differential expression of cadherins in the developing and adult zebrafish olfactory system. J. Comp. Neurol. 2004, 478:269-281.
67. Malicki J., Jo H., Pujic Z. Zebrafish N-cadherin, encoded by the glass onion locus, plays an essential role in retinal patterning. Dev. Biol. 2003, 259:95-108.
68. Martin A.C., Goldstein B. Apical constriction: themes and variations on a cellular mechanism driving morphogenesis. Development 2014, 141:1987-1998.
69. Martinez-Morales J.R., Rembold M., Greger K., Simpson J.C., Brown K.E., Quiring R., Pepperkok R., Martin-Bermudo M.D., Himmelbauer H., Wittbrodt J. Ojoplano-mediated basal constriction is essential for optic cup morphogenesis. Development 2009, 136:2165-2175.
70. Matsuda M., Chitnis A.B. Atoh1a expression must be restricted by Notch signaling for effective morphogenesis of the posterior lateral line primordium in zebrafish. Development 2010, 137:3477-3487.
71. McCabe K.L., Bronner M. Tetraspanin, CD151, is required for maintenance of trigeminal placode identity. J. Neurochem. 2011, 117:221-230.
72. McCabe K.L., Sechrist J.W., Bronner-Fraser M. Birth of ophthalmic trigeminal neurons initiates early in the placodal ectoderm. J. Comp. Neurol. 2009, 514:161-173.
73. McKeown S.J., Wallace A.S., Anderson R.B. Expression and function of cell adhesion molecules during neural crest migration. Dev. Biol. 2013, 373:244-257.
74. Moore K.A., Polte T., Huang S., Shi B., Alsberg E., Sunday M.E., Ingber D.E. Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension. Dev. Dyn. 2005, 232:268-281.
75. Moro-Balbás J.A., Gato A., Alonso M.I., Martín P., de la Mano A. Basal lamina heparan sulphate proteoglycan is involved in otic placode invagination in chick embryos. Anat. Embryol. 2000, 202:333-343.
76. Nechiporuk A., Raible D.W. FGF-dependent mechanosensory organ patterning in zebrafish. Science 2008, 320:1774-1777.
77. Nishimura T., Takeichi M. Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 2008, 135:1493-1502.
78. Ochoa-Espinosa A., Affolter M. Branching morphogenesis: from cells to organs and back. Cold Spring Harbor Perspect. Biol. 2012, 4. (pii: a008243).
79. Pai Y.-J., Abdullah N.L., Mohd Zin S.W., Mohammed R.S., Rolo A., Greene N.D.E., Abdul-Aziz N.M., Copp A.J. Epithelial fusion during neural tube morphogenesis. Birth Defects Res. Part A: Clin. Mol. Teratol. 2012, 94:817-823.
80. Plageman T.F., Chauhan B.K., Yang C., Jaudon F., Shang X., Zheng Y., Lou M., Debant A., Hildebrand J.D., Lang R.A. A Trio-RhoA-Shroom3 pathway is required for apical constriction and epithelial invagination. Development 2011, 138:5177-5188.
81. Plageman T.F., Chung M.I., Lou M., Smith A.N., Hildebrand J.D., Wallingford J.B., Lang R.A. Pax6-dependent Shroom3 expression regulates apical constriction during lens placode invagination. Development 2010, 137:405-415.
82. Pontoriero G.F., Smith A.N., Miller L.-A.D., Radice G.L., West-Mays J.A., Lang R.A. Co-operative roles for E-cadherin and N-cadherin during lens vesicle separation and lens epithelial cell survival. Dev. Biol. 2009, 326:403-417.
83. Revenu C., Gilmour D. EMT 2.0: shaping epithelia through collective migration. Curr. Opin. Genet. Dev. 2009, 19:338-342.
84. Revenu C., Streichan S., Dona E., Lecaudey V., Hufnagel L., Gilmour D. Quantitative cell polarity imaging defines leader-to-follower transitions during collective migration and the key role of microtubule-dependent adherens junction formation. Development 2014, 141:1282-1291.
85. Roh-Johnson M., Shemer G., Higgins C.D., McClellan J.H., Werts A.D., Tulu U.S., Gao L., Betzig E., Kiehart D.P., Goldstein B. Triggering a cell shape change by exploiting preexisting actomyosin contractions. Science 2012, 335:1232-1235.
86. Rørth P. Fellow travellers: emergent properties of collective cell migration. EMBO Rep. 2012, 13:984-991.
87. Sadej R., Grudowska A., Turczyk L., Kordek R., Romanska H.M. CD151 in cancer progression and metastasis: a complex scenario. Lab. Invest. 2014, 94:41-51.
88. Sai X., Ladher R.K. FGF signaling regulates cytoskeletal remodeling during epithelial morphogenesis. Curr. Biol. 2008, 18:976-981.
89. Sawyer J.M., Harrell J.R., Shemer G., Sullivan-Brown J., Roh-Johnson M., Goldstein B. Apical constriction: a cell shape change that can drive morphogenesis. Dev. Biol. 2010, 341:5-19.
90. Schlosser G. Making senses: development of vertebrate cranial placodes. Int. Rev. Cell Mol. Biol. 2010, 283:129-234.
91. Schwartz M.A., DeSimone D.W. Cell adhesion receptors in mechanotransduction. Curr. Opin. Cell Biol. 2008, 20:551-556.
92. Shiau C.E., Bronner-Fraser M. N-cadherin acts in concert with Slit1-Robo2 signaling in regulating aggregation of placode-derived cranial sensory neurons. Development 2009, 136:4155-4164.
93. Shiau C.E., Das R.M., Storey K.G. An effective assay for high cellular resolution time-lapse imaging of sensory placode formation. BMC Neurosci. 2011, 12:37.
94. Shiau C.E., Lwigale P.Y., Das R.M., Wilson S.A., Bronner-Fraser M. Robo2-Slit1 dependent cell-cell interactions mediate assembly of the trigeminal ganglion. Nat. Neurosci. 2008, 11:269-276.
95. Smith A.N., Miller L.A., Radice G., Ashery-Padan R., Lang R.A. Stage-dependent modes of Pax6-Sox2 epistasis regulate lens development and eye morphogenesis. Development 2009, 136. (3377-3377).
96. Solecki D.J. Sticky situations: recent advances in control of cell adhesion during neuronal migration. Curr. Opin. Neurobiol. 2012, 22:791-798.
97. Soussi-Yanicostas N., Faivre-Sarrailh C., Hardelin J.P., Levilliers J., Rougon G., Petit C. Anosmin-1 underlying the X chromosome-linked Kallmann syndrome is an adhesion molecule that can modulate neurite growth in a cell-type specific manner. J. Cell Sci. 1998, 111:2953-2965.
98. Stepniak E., Radice G.L., Vasioukhin V. Adhesive and signaling functions of cadherins and catenins in vertebrate development. Cold Spring Harbor Perspect. Biol. 2009, 1:a002949.
99. Steventon B., Mayor R., Streit A. Neural crest and placode interaction during the development of the cranial sensory system. Dev. Biol. 2014, 389:28-38.
100. Streit A. The Cranial Sensory Nervous System: Specification of Sensory Progenitors and Placodes. StemBook [Internet] 2008, Harvard Stem Cell Institute, Cambridge (MA).
101. Strobl-Mazzulla P.H., Bronner M.E. Epithelial to mesenchymal transition: new and old insights from the classical neural crest model. Sem. Cancer Biol. 2012, 22:411-416.
102. Suzuki M., Morita H., Ueno N. Molecular mechanisms of cell shape changes that contribute to vertebrate neural tube closure. Dev. Growth Differ. 2012, 54:266-276.
103. Theveneau E., Marchant L., Kuriyama S., Gull M., Moepps B., Parsons M., Mayor R. Collective chemotaxis requires contact-dependent cell polarity. Dev. Cell 2010, 19:39-53.
104. Theveneau E., Mayor R. Neural crest delamination and migration: from epithelium-to-mesenchyme transition to collective cell migration. Dev. Biol. 2012, 366:34-54.
105. Theveneau E., Steventon B., Scarpa E., Garcia S., Trepat X., Streit A., Mayor R. Chase-and-run between adjacent cell populations promotes directional collective migration. Nature 2013, 15:1-12.
106. Thiery J.P., Acloque H., Huang R.Y.J., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
107. Venkiteswaran G., Lewellis S.W., Wang J., Reynolds E., Nicholson C., Knaut H. Generation and dynamics of an endogenous, self-generated signaling gradient across a migrating tissue. Cell 2013, 155:674-687.
108. Visconti R.P., Hilfer S.R. Perturbation of extracellular matrix prevents association of the otic primordium with the posterior rhombencephalon and inhibits subsequent invagination. Dev. Dyn. 2002, 223:48-58.
109. Wheelock M.J., Shintani Y., Maeda M., Fukumoto Y., Johnson K.R. Cadherin switching. J. Cell Sci. 2008, 121:727-735.
110. Yanicostas C., Ernest S., Dayraud C., Petit C., Soussi-Yanicostas N. Essential requirement for zebrafish anosmin-1a in the migration of the posterior lateral line primordium. Dev. Biol. 2008, 320:469-479.
111. Yona S., Lin H.-H., Siu W.O., Gordon S., Stacey M. Adhesion-GPCRs: emerging roles for novel receptors. Trends Biochem. Sci. 2008, 33:491-500.