Convergence and Extrusion Are Required for Normal Fusion of the Mammalian Secondary Palate

PLoS Biology

Volumn 13, Issue 4, 2015, Pages

  Kim, Seungil ^a   Lewis, Ace E ^a   Singh, Vivek ^a   Ma, Xuefei ^b   Adelstein, Robert ^b   Bush, Jeffrey O ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN IIA; MYOSIN LIGHT CHAIN KINASE; RHO KINASE; MYOSIN;

ACTIN MYOSIN INTERACTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL EXTRUSION; CELL INTERCALATION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; DEVELOPMENT; EMBRYO; EPITHELIUM; EPITHELIUM CELL; MAMMAL; NONHUMAN; SECONDARY PALATE; TISSUE FUSION; ANIMAL; EMBRYOLOGY; MORPHOGENESIS; MOUSE; PALATE; PHYSIOLOGY;

MAMMALIA; MUS;

ANIMALS; MICE; MORPHOGENESIS; MYOSINS; PALATE;

EID: 84929493084     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002122     Document Type: Article

References (73)

1. Ray HJ, Niswander L, Mechanisms of tissue fusion during development. Development. 2012;139: 1701–1711. doi: 10.1242/dev.068338 22510983
2. Bush JO, Jiang R, Palatogenesis: morphogenetic and molecular mechanisms of secondary palate development. Development. 2012;139: 231–243. doi: 10.1242/dev.067082 22186724
3. Jiang R, Bush JO, Lidral AC, Development of the upper lip: morphogenetic and molecular mechanisms. Dev Dyn. 2006;235: 1152–1166. 16292776
4. Ferguson MW, Palate development. Development. 1988;103 Suppl: 41–60. 3074914
5. Fitchett JE, Hay ED, Medial edge epithelium transforms to mesenchyme after embryonic palatal shelves fuse. Dev Biol. 1989;131: 455–474. 2463946
6. Shapiro BL, Sweney L, Electron microscopic and histochemical examination of oral epithelial-mesenchymal interaction (programmed cell death). J Dent Res. 1969;48: 652–660. 5259404
7. Dudas M, Li W-Y, Kim J, Yang A, Kaartinen V, Palatal fusion—where do the midline cells go? A review on cleft palate, a major human birth defect. Acta Histochem. 2007;109: 1–14. 16962647
8. Taya Y, O’Kane S, Ferguson MW, Pathogenesis of cleft palate in TGF-beta3 knockout mice. Development. 1999;126: 3869–79. 10433915
9. Waterman RE, Ross LM, Meller SM, Alterations in the epithelial surface of A/Jax mouse palatal shelves prior to and during palatal fusion: A scanning electron microscopic study. Anat Rec. 1973;176: 361–375. 4716420
10. Carette MJ, Ferguson MW, The fate of medial edge epithelial cells during palatal fusion in vitro: an analysis by DiI labelling and confocal microscopy. Development. 1992;114: 379–388. 1591998
11. Cuervo R, Covarrubias L, Death is the major fate of medial edge epithelial cells and the cause of basal lamina degradation during palatogenesis. Development. 2004;131: 15–24. 14645125
12. Tudela C, Formoso M-A, Martínez T, Pérez R, Aparicio M, Maestro C, et al. TGF-beta3 is required for the adhesion and intercalation of medial edge epithelial cells during palate fusion. Int J Dev Biol. 2002;46: 333–336. 12068957
13. Nawshad A, Palatal seam disintegration: to die or not to die? that is no longer the question. Dev Dyn. 2008;237: 2643–2656. doi: 10.1002/dvdy.21599 18629865
14. Griffith CM, Hay ED, Epithelial-mesenchymal transformation during palatal fusion: carboxyfluorescein traces cells at light and electron microscopic levels. Development. 1992;116: 1087–1099. 1295731
15. Martı́nez-Álvarez C, Tudela C, Pérez-Miguelsanz J, O’Kane S, Puerta J, Ferguson MWJ, Medial Edge Epithelial Cell Fate during Palatal Fusion. Dev Biol. 2000;220: 343–357. 10753521
16. Shuler CF, Guo Y, Majumder A, Luo RY, Molecular and morphologic changes during the epithelial-mesenchymal transformation of palatal shelf medial edge epithelium in vitro. Int J Dev Biol. 1991;35: 463–472. 1801871
17. Vaziri Sani F, Hallberg K, Harfe BD, McMahon AP, Linde A, Gritli-Linde A, Fate-mapping of the epithelial seam during palatal fusion rules out epithelial–mesenchymal transformation. Dev Biol. 2005;285: 490–495. 16109396
18. Xu X, Han J, Ito Y, Bringas P, Jr.Urata MM, Chai Y, Cell autonomous requirement for Tgfbr2 in the disappearance of medial edge epithelium during palatal fusion. Dev Biol. 2006;297: 238–248. 16780827
19. Cecconi F, Alvarez-Bolado G, Meyer BI, Roth KA, Gruss P, Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell. 1998;94: 727–737. 9753320
20. Cuervo R, Valencia C, Chandraratna RAS, Covarrubias L, Programmed cell death is required for palate shelf fusion and is regulated by retinoic acid. Dev Biol. 2002;245: 145–156. 11969262
21. Honarpour N, Du C, Richardson JA, Hammer RE, Wang X, Herz J, Adult Apaf-1-deficient mice exhibit male infertility. Dev Biol. 2000;218: 248–258. 10656767
22. Honarpour N, Gilbert SL, Lahn BT, Wang X, Herz J, Apaf-1 deficiency and neural tube closure defects are found in fog mice. Proc Natl Acad Sci U S A. 2001;98: 9683–9687. 11504943
23. Jin J-Z, Ding J, Analysis of cell migration, transdifferentiation and apoptosis during mouse secondary palate fusion. Development. 2006;133: 3341–3347. 16887819
24. Takahara S, Takigawa T, Shiota K, Programmed cell death is not a necessary prerequisite for fusion of the fetal mouse palate. Int J Dev Biol. 2004;48: 39–46. 15005573
25. Martin AC, Pulsation and stabilization: contractile forces that underlie morphogenesis. Dev Biol. 2010;341: 114–125. doi: 10.1016/j.ydbio.2009.10.031 19874815
26. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR, Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol. 2009;10: 778–790. doi: 10.1038/nrm2786 19851336
27. Conti MA, Adelstein RS, Nonmuscle myosin II moves in new directions. J Cell Sci. 2008;121: 11–18. 28. 18096687
28. Behrndt M, Salbreux G, Campinho P, Hauschild R, Oswald F, Roensch J, et al. Forces Driving Epithelial Spreading in Zebrafish Gastrulation. Science. 2012;338: 257–260. doi: 10.1126/science.1224143 23066079
29. Franke JD, Montague RA, Kiehart DP, Nonmuscle Myosin II Generates Forces that Transmit Tension and Drive Contraction in Multiple Tissues during Dorsal Closure. Curr Biol. 2005;15: 2208–2221. 16360683
30. Kiehart DP, Galbraith CG, Edwards KA, Rickoll WL, Montague RA, Multiple Forces Contribute to Cell Sheet Morphogenesis for Dorsal Closure in Drosophila. J Cell Biol. 2000;149: 471–490. 10769037
31. Martin P, Parkhurst SM, Parallels between tissue repair and embryo morphogenesis. Development. 2004;131: 3021–3034. 15197160
32. Solon J, Kaya-Copur A, Colombelli J, Brunner D, Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell. 2009;137: 1331–1342. doi: 10.1016/j.cell.2009.03.050 19563762
33. Young PE, Richman AM, Ketchum AS, Kiehart DP, Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 1993;7: 29–41. 8422986
34. 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 CB. 2000;10: 1420–1426. 11102803
35. Bertet C, Sulak L, Lecuit T, Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature. 2004;429: 667–671. 15190355
36. Skoglund P, Rolo A, Chen X, Gumbiner BM, Keller R, Convergence and extension at gastrulation require a myosin IIB-dependent cortical actin network. Development. 2008;135: 2435–2444. doi: 10.1242/dev.014704 18550716
37. Dassule HR, Lewis P, Bei M, Maas R, McMahon AP, Sonic hedgehog regulates growth and morphogenesis of the tooth. Development. 2000;127: 4775–4785. 11044393
38. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L, A global double-fluorescent Cre reporter mouse. genesis. 2007;45: 593–605. 17868096
39. Munjal A, Lecuit T, Actomyosin networks and tissue morphogenesis. Development. 2014;141: 1789–1793. doi: 10.1242/dev.091645 24757001
40. Golomb E, Ma X, Jana SS, Preston YA, Kawamoto S, Shoham NG, et al. Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family. J Biol Chem. 2004;279: 2800–8. 14594953
41. Ma X, Kawamoto S, Hara Y, Adelstein RS, A point mutation in the motor domain of nonmuscle myosin II-B impairs migration of distinct groups of neurons. Mol Biol Cell. 2004;15: 2568–79. 15034141
42. Martinelli M, Di Stazio M, Scapoli L, Marchesini J, Di Bari F, Pezzetti F, et al. Cleft lip with or without cleft palate: implication of the heavy chain of non-muscle myosin IIA. J Med Genet. 2007;44: 387–392. 17337617
43. Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ, Sellers JR, et al. Dissecting Temporal and Spatial Control of Cytokinesis with a Myosin II Inhibitor. Science. 2003;299: 1743–1747. 12637748
44. Conti MA, Even-Ram S, Liu C, Yamada KM, Adelstein RS, Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice. J Biol Chem. 2004;279: 41263–6. 15292239
45. Yang L-T, Li W-Y, Kaartinen V, Tissue-specific expression of Cre recombinase from the Tgfb3 locus. Genesis. 2008;46: 112–118. doi: 10.1002/dvg.20372 18257072
46. Richardson RJ, Dixon J, Jiang R, Dixon MJ, Integration of IRF6 and Jagged2 signalling is essential for controlling palatal adhesion and fusion competence. Hum Mol Genet. 2009;18: 2632–2642. doi: 10.1093/hmg/ddp201 19439425
47. Shindo A, Wallingford JB, PCP and septins compartmentalize cortical actomyosin to direct collective cell movement. Science. 2014;343: 649–652. doi: 10.1126/science.1243126 24503851
48. Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, et al. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem. 1996;271: 20246–20249. 8702756
49. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, et al. Lifeact: a versatile marker to visualize F-actin. Nat Methods. 2008;5: 605–7. doi: 10.1038/nmeth.1220 18536722
50. Riedl J, Flynn KC, Raducanu A, Gartner F, Beck G, Bosl M, et al. Lifeact mice for studying F-actin dynamics. Nat Methods. 2010;7: 168–9. doi: 10.1038/nmeth0310-168 20195247
51. Eisenhoffer GT, Loftus PD, Yoshigi M, Otsuna H, Chien C-B, Morcos PA, et al. Crowding induces live cell extrusion to maintain homeostatic cell numbers in epithelia. Nature. 2012;484: 546–549. doi: 10.1038/nature10999 22504183
52. Lubkov V, Bar-Sagi D, E-cadherin-mediated cell coupling is required for apoptotic cell extrusion. Curr Biol. 2014;24: 868–874. doi: 10.1016/j.cub.2014.02.057 24704076
53. Rosenblatt J, Raff MC, Cramer LP, An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol. 2001;11: 1847–1857. 11728307
54. Toyama Y, Peralta XG, Wells AR, Kiehart DP, Edwards GS, Apoptotic force and tissue dynamics during Drosophila embryogenesis. Science. 2008;321: 1683–1686. doi: 10.1126/science.1157052 18802000
55. Yang XC, Sachs F, Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science. 1989;243: 1068–1071. 2466333
56. Bhattacharya MRC, Bautista DM, Wu K, Haeberle H, Lumpkin EA, Julius D, Radial stretch reveals distinct populations of mechanosensitive mammalian somatosensory neurons. Proc Natl Acad Sci U S A. 2008;105: 20015–20020. doi: 10.1073/pnas.0810801105 19060212
57. Pyrgaki C, Trainor P, Hadjantonakis A-K, Niswander L, Dynamic imaging of mammalian neural tube closure. Dev Biol. 2010;344: 941–947. doi: 10.1016/j.ydbio.2010.06.010 20558153
58. Economou AD, Brock LJ, Cobourne MT, Green JBA, Whole population cell analysis of a landmark-rich mammalian epithelium reveals multiple elongation mechanisms. Development. 2013;140: 4740–4750. doi: 10.1242/dev.096545 24173805
59. Birnbaum S, Reutter H, Mende M, de Assis NA, Diaz-Lacava A, Herms S, et al. Further evidence for the involvement of MYH9 in the etiology of non-syndromic cleft lip with or without cleft palate. Eur J Oral Sci. 2009;117: 200–203. doi: 10.1111/j.1600-0722.2008.00604.x 19320731
60. Chiquet BT, Hashmi SS, Henry R, Burt A, Mulliken JB, Stal S, et al. Genomic screening identifies novel linkages and provides further evidence for a role of MYH9 in nonsyndromic cleft lip and palate. Eur J Hum Genet. 2009;17: 195–204. doi: 10.1038/ejhg.2008.149 18716610
61. Jia Z-L, Li Y, Chen C-H, Li S, Wang Y, Zheng Q, et al. Association among polymorphisms at MYH9, environmental factors, and nonsyndromic orofacial clefts in western China. DNA Cell Biol. 2010;29: 25–32. doi: 10.1089/dna.2009.0935 19891592
62. Paranaíba L-M-R, de Aquino S-N, Bufalino A, Martelli-Júnior H, Graner E, Brito L-A, et al. Contribution of polymorphisms in genes associated with craniofacial development to the risk of nonsyndromic cleft lip and/or palate in the Brazilian population. Med Oral Patol Oral Cir Bucal. 2013;18: e414–420. 23524414
63. Eisenhoffer GT, Rosenblatt J, Bringing balance by force: live cell extrusion controls epithelial cell numbers. Trends Cell Biol. 2013;23: 185–192. doi: 10.1016/j.tcb.2012.11.006 23273931
64. Schüpbach PM, Schroeder HE, Cell release from the palatal shelves and the fusion line. J Biol Buccale. 1983;11: 227–241. 6581161
65. Schüpbach PM, Chamberlain JG, Schroeder HE, Development of the secondary palate in the rat: a scanning electron microscopic study. J Craniofac Genet Dev Biol. 1983;3: 159–177. 6619276
66. Charoenchaikorn K, Yokomizo T, Rice DP, Honjo T, Matsuzaki K, Shintaku Y, et al. Runx1 is involved in the fusion of the primary and the secondary palatal shelves. Dev Biol. 2009;326: 392–402. doi: 10.1016/j.ydbio.2008.10.018 19000669
67. Takigawa T, Shiota K, Terminal differentiation of palatal medial edge epithelial cells in vitro is not necessarily dependent on palatal shelf contact and midline epithelial seam formation. Int J Dev Biol. 2004;48: 307–317. 15300511
68. Jacobelli J, Friedman RS, Conti MA, Lennon-Dumenil A-M, Piel M, Sorensen CM, et al. Confinement-optimized three-dimensional T cell amoeboid motility is modulated via myosin IIA-regulated adhesions. Nat Immunol. 2010;11: 953–961. doi: 10.1038/ni.1936 20835229
69. Ma X, Takeda K, Singh A, Yu Z-X, Zerfas P, Blount A, et al. Conditional Ablation of Nonmuscle Myosin II-B Delineates Heart Defects in Adult Mice. Circ Res. 2009;105: 1102–1109. doi: 10.1161/CIRCRESAHA.109.200303 19815823
70. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L, A global double-fluorescent Cre reporter mouse. genesis. 2007;45: 593–605. 17868096
71. Veenman CJ, Reinders MJT, Backer E, Resolving motion correspondence for densely moving points. IEEE Trans Pattern Anal Mach Intell. 2001;23: 54–72.
72. Meijering E, Dzyubachyk O, Smal I, Michael conn P., Chapter nine—Methods for Cell and Particle Tracking. In: Methods in Enzymology. Academic Press; 2012. pp. 183–200. http://www.sciencedirect.com/science/article/pii/B9780123918574000094 doi: 10.1016/B978-0-12-381272-8.00012-X 22975054
73. Kang P, Svoboda KKH, PI-3 kinase activity is required for epithelial-mesenchymal transformation during palate fusion. Dev Dyn. 2002;225: 316–321. 12412014