Are there conserved roles for the extracellular matrix, cilia, and junctional complexes in left-right patterning?

Genesis

Volumn 52, Issue 6, 2014, Pages 488-502

  Collins, Michelle M ^a   Ryan, Aimee K ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Asymmetry; Gastrocoel roof plate; Hensen's node; Kupffer's vesicle; Laterality; Node

Indexed keywords

ADAPTOR PROTEIN; CLAUDIN; JUNCTIONAL ADHESION MOLECULE; PROTEIN KINASE C; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TIGHT JUNCTION PROTEIN; TRANSCRIPTION FACTOR;

CELL ADHESION; CELL COMMUNICATION; CELL CONTACT; CELL DISRUPTION; CELL FUNCTION; CELL INTERACTION; CELL JUNCTION; CELL MATURATION; CELL MIGRATION; CELL MOTION; CELL POLARITY; CELL STRUCTURE; CILIATED EPITHELIUM; EMBRYO DEVELOPMENT; EUKARYOTIC FLAGELLUM; EXTRACELLULAR MATRIX; FLUID FLOW; GENE EXPRESSION; HUMAN; INTRACELLULAR SIGNALING; KINETOSOME; MECHANOTRANSDUCTION; MICROENVIRONMENT; MOLECULAR DOCKING; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; TIGHT JUNCTION; WNT SIGNALING PATHWAY; ANIMAL; EPITHELIUM; METABOLISM; PHYSIOLOGY;

ANIMALS; BODY PATTERNING; CELL ADHESION; CELL COMMUNICATION; CELL POLARITY; CILIA; EPITHELIUM; EXTRACELLULAR MATRIX; HUMANS; INTERCELLULAR JUNCTIONS; MORPHOGENESIS;

EID: 84902662470     PISSN: 1526954X     EISSN: 1526968X     Source Type: Journal    
DOI: 10.1002/dvg.22774     Document Type: Review

References (128)

1. Ablooglu AJ, Tkachenko E, Kang J, Shattil SJ. 2010. Integrin alphaV is necessary for gastrulation movements that regulate vertebrate body asymmetry. Development 137:3449-3458.
2. Aijaz S, D'Atri F, Citi S, Balda MS, Matter K. 2005. Binding of GEF-H1 to the tight junction-associated adaptor cingulin results in inhibition of Rho signaling and G1/S phase transition. Dev Cell 8:777-786.
3. Anderson JM, Van Itallie CM. 2009. Physiology and function of the tight junction. Cold Spring Harb Perspect Biol 1:a002584.
4. Antic D, Stubbs JL, Suyama K, Kintner C, Scott MP, Axelrod JD. 2010. Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PLoS One 5:e8999.
5. Arrington CB, Peterson AG, Yost HJ. 2013. Sdc2 and Tbx16 regulate Fgf2-dependent epithelial cell morphogenesis in the ciliated organ of asymmetry. Development 140:4102-4109.
6. Aw S, Koster JC, Pearson W, Nichols CG, Shi NQ, Carneiro K, Levin M. 2010. The ATP-sensitive K(+)-channel (K(ATP)) controls early left-right patterning in Xenopus and chick embryos. Dev Biol 346:39-53.
7. Balda MS, Matter K. 2003. Epithelial cell adhesion and the regulation of gene expression. Trends Cell Biol 13:310-318.
8. Baum B, Georgiou M. 2011. Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J Cell Biol 192:907-917.
9. Beales PL, Elcioglu N, Woolf AS, Parker D, Flinter FA. 1999. New criteria for improved diagnosis of Bardet-Biedl syndrome: Results of a population survey. J Med Genet 36:437-446.
10. Becker-Heck A, Zohn IE, Okabe N, Pollock A, Lenhart KB, Sullivan-Brown J, McSheene J, Loges NT, Olbrich H, Haeffner K, Fliegauf M, Horvath J, Reinhardt R, Nielsen KG, Marthin JK, Baktai G, Anderson KV, Geisler R, Niswander L, Omran H, Burdine RD. 2011. The coiled-coil domain containing protein CCDC40 is essential for motile cilia function and left-right axis formation. Nat Genet 43:79-84.
11. Betanzos A, Huerta M, Lopez-Bayghen E, Azuara E, Amerena J, Gonzalez-Mariscal L. 2004. The tight junction protein ZO-2 associates with Jun, Fos and C/EBP transcription factors in epithelial cells. Exp Cell Res 292:51-66.
12. Beyer T, Thumberger T, Schweickert A, Blum M. 2012. Connexin26-mediated transfer of laterality cues in Xenopus. Biol Open 1:473-481.
13. Boorman CJ, Shimeld SM. 2002. The evolution of left-right asymmetry in chordates. Bioessays 24:1004-1011.
14. Botilde Y, Yoshiba S, Shinohara K, Hasegawa T, Nishimura H, Shiratori H, Hamada H. 2013. Cluap1 localizes preferentially to the base and tip of cilia and is required for ciliogenesis in the mouse embryo. Dev Biol 381:203-212.
15. Brancati F, Barrano G, Silhavy JL, Marsh SE, Travaglini L, Bielas SL, Amorini M, Zablocka D, Kayserili H, Al-Gazali L, Bertini E, Boltshauser E, D'Hooghe M, Fazzi E, Fenerci EY, Hennekam RC, Kiss A, Lees MM, Marco E, Phadke SR, Rigoli L, Romano S, Salpietro CD, Sherr EH, Signorini S, Stromme P, Stuart B, Sztriha L, Viskochil DH, Yuksel A, Dallapiccola B, Valente EM, Gleeson JG. 2007. CEP290 mutations are frequently identified in the oculo-renal form of Joubert syndrome-related disorders. Am J Hum Genet 81:104-113.
16. Briscoe J, Therond PP. 2013. The mechanisms of Hedgehog signalling and its roles in development and disease. Nat Rev Mol Cell Biol 14:416-429.
17. Brizuela BJ, Wessely O, De Robertis EM. 2001. Overexpression of the Xenopus tight-junction protein claudin causes randomization of the left-right body axis. Dev Biol 230:217-229.
18. Burdine RD, Caspary T. 2013. Left-right asymmetry: Lessons from Cancun. Development 140:4465-4470.
19. Capaldo CT, Nusrat A. 2009. Cytokine regulation of tight junctions. Biochim Biophys Acta 1788:864-871.
20. Chen L, Klass C, Woods A. 2004. Syndecan-2 regulates transforming growth factor-beta signaling. J Biol Chem 279:15715-15718.
21. Chu D, Pan H, Wan P, Wu J, Luo J, Zhu H, Chen J. 2012. AIP1 acts with cofilin to control actin dynamics during epithelial morphogenesis. Development 139:3561-3571.
22. Collinet C, Lecuit T. 2013. Stability and dynamics of cell-cell junctions. Prog Mol Biol Transl Sci 116:25-47.
23. Collins MM, Baumholtz AI, Ryan AK. 2013. Claudin family members exhibit unique temporal and spatial expression boundaries in the chick embryo. Tissue Barriers 1:e24517.
24. Cui C, Little CD, Rongish BJ. 2009. Rotation of organizer tissue contributes to left-right asymmetry. Anat Rec (Hoboken) 292:557-561.
25. Davis NM, Kurpios NA, Sun X, Gros J, Martin JF, Tabin CJ. 2008. The chirality of gut rotation derives from left-right asymmetric changes in the architecture of the dorsal mesentery. Dev Cell 15:134-145.
26. Drummond IA. 2012. Cilia functions in development. Curr Opin Cell Biol 24:24-30.
27. Essner JJ, Amack JD, Nyholm MK, Harris EB, Yost HJ. 2005. Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 132:1247-1260.
28. Eyckmans J, Boudou T, Yu X, Chen CS. 2011. A hitchhiker's guide to mechanobiology. Dev Cell 21:35-47.
29. Feistel K, Blum M. 2008. Gap junctions relay FGF8-mediated right-sided repression of Nodal in rabbit. Dev Dyn 237:3516-3527.
30. Fukumoto T, Blakely R, Levin M. 2005. Serotonin transporter function is an early step in left-right patterning in chick and frog embryos. Dev Neurosci 27:349-363.
31. Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S. 2002. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: A lesson from claudin-1-deficient mice. J Cell Biol 156:1099-1111.
32. Garcia-Castro MI, Vielmetter E, Bronner-Fraser M. 2000. N-Cadherin, a cell adhesion molecule involved in establishment of embryonic left-right asymmetry. Science 288:1047-1051.
33. Glazer AM, Wilkinson AW, Backer CB, Lapan SW, Gutzman JH, Cheeseman IM, Reddien PW. 2010. The Zn finger protein Iguana impacts Hedgehog signaling by promoting ciliogenesis. Dev Biol 337:148-156.
34. Goetz SC, Anderson KV. 2010. The primary cilium: A signalling centre during vertebrate development. Nat Rev Genet 11:331-344.
35. Gonzalez-Mariscal L, Betanzos A, Nava P, Jaramillo BE. 2003. Tight junction proteins. Prog Biophys Mol Biol 81:1-44.
36. Gottardi CJ, Arpin M, Fanning AS, Louvard D. 1996. The junction-associated protein, zonula occludens-1, localizes to the nucleus before the maturation and during the remodeling of cell-cell contacts. Proc Natl Acad Sci USA 93:10779-10784.
37. Gros J, Feistel K, Viebahn C, Blum M, Tabin CJ. 2009. Cell movements at Hensen's node establish left/right asymmetric gene expression in the chick. Science 324:941-944.
38. Gupta IR, Ryan AK. 2010. Claudins: Unlocking the code to tight junction function during embryogenesis and in disease. Clin Genet 77:314-325.
39. Harris TJ, Tepass U. 2010. Adherens junctions: From molecules to morphogenesis. Nat Rev Mol Cell Biol 11:502-514.
40. Hashimoto M, Hamada H. 2010. Translation of anterior-posterior polarity into left-right polarity in the mouse embryo. Curr Opin Genet Dev 20:433-437.
41. Hatada Y, Stern CD. 1994. A fate map of the epiblast of the early chick embryo. Development 120:2879-2889.
42. Hirokawa N, Tanaka Y, Okada Y, Takeda S. 2006. Nodal flow and the generation of left-right asymmetry. Cell 125:33-45.
43. Hochgreb-Hagele T, Yin C, Koo DE, Bronner ME, Stainier DY. 2013. Laminin beta1a controls distinct steps during the establishment of digestive organ laterality. Development 140:2734-2745.
44. Hori A, Ikebe C, Tada M, Toda T. 2014. Msd1/SSX2IP-dependent microtubule anchorage ensures spindle orientation and primary cilia formation. EMBO Rep 15:175-184.
45. Ioannou A, Santama N, Skourides PA. 2013. Xenopus laevis nucleotide binding protein 1 (xNubp1) is important for convergent extension movements and controls ciliogenesis via regulation of the actin cytoskeleton. Dev Biol 380:243-258.
46. Islas S, Vega J, Ponce L, Gonzalez-Mariscal L. 2002. Nuclear localization of the tight junction protein ZO-2 in epithelial cells. Exp Cell Res 274:138-148.
47. Kennedy MP, Omran H, Leigh MW, Dell S, Morgan L, Molina PL, Robinson BV, Minnix SL, Olbrich H, Severin T, Ahrens P, Lange L, Morillas HN, Noone PG, Zariwala MA, Knowles MR. 2007. Congenital heart disease and other heterotaxic defects in a large cohort of patients with primary ciliary dyskinesia. Circulation 115:2814-2821.
48. Kinzel D, Boldt K, Davis EE, Burtscher I, Trumbach D, Diplas B, Attie-Bitach T, Wurst W, Katsanis N, Ueffing M, Lickert H. 2010. Pitchfork regulates primary cilia disassembly and left-right asymmetry. Dev Cell 19:66-77.
49. Kohler K, Zahraoui A. 2005. Tight junction: A co-ordinator of cell signalling and membrane trafficking. Biol Cell 97:659-665.
50. Kramer KL, Barnette JE, Yost HJ. 2002. PKCgamma regulates syndecan-2 inside-out signaling during xenopus left-right development. Cell 111:981-990.
51. Kramer KL, Yost HJ. 2002. Ectodermal syndecan-2 mediates left-right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev Cell 2:115-124.
52. Kramer-Zucker AG, Olale F, Haycraft CJ, Yoder BK, Schier AF, Drummond IA. 2005. Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132:1907-1921.
53. Kurpios NA, Ibanes M, Davis NM, Lui W, Katz T, Martin JF, Izpisua Belmonte JC, Tabin CJ. 2008. The direction of gut looping is established by changes in the extracellular matrix and in cell: Cell adhesion. Proc Natl Acad Sci USA 105:8499-8506.
54. Ladoux B, Anon E, Lambert M, Rabodzey A, Hersen P, Buguin A, Silberzan P, Mege RM. 2010. Strength dependence of cadherin-mediated adhesions. Biophys J 98:534-542.
55. le Duc Q, Shi Q, Blonk I, Sonnenberg A, Wang N, Leckband D, de Rooij J. 2010. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J Cell Biol 189:1107-1115.
56. Legate KR, Wickstrom SA, Fassler R. 2009. Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 23:397-418.
57. Leigh MW, Pittman JE, Carson JL, Ferkol TW, Dell SD, Davis SD, Knowles MR, Zariwala MA. 2009. Clinical and genetic aspects of primary ciliary dyskinesia/Kartagener syndrome. Genet Med 11:473-487.
58. Levin M, Johnson RL, Stern CD, Kuehn M, Tabin C. 1995. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82:803-814.
59. Levin M, Mercola M. 1998. Gap junctions are involved in the early generation of left-right asymmetry. Dev Biol 203:90-105.
60. Levin M, Mercola M. 1999. Gap junction-mediated transfer of left-right patterning signals in the early chick blastoderm is upstream of Shh asymmetry in the node. Development 126:4703-4714.
61. Levin M, Pagan S, Roberts DJ, Cooke J, Kuehn MR, Tabin CJ. 1997. Left/right patterning signals and the independent regulation of different aspects of situs in the chick embryo. Dev Biol 189:57-67.
62. Levin M. 2005. Left-right asymmetry in embryonic development: a comprehensive review. Mech Dev 122:3-25.
63. Levy V, Khaner O. 1998. Limited left-right cell migration across the midline of the gastrulating avian embryo. Dev Genet 23:175-184.
64. Liu Z, Tan JL, Cohen DM, Yang MT, Sniadecki NJ, Ruiz SA, Nelson CM, Chen CS. 2010. Mechanical tugging force regulates the size of cell-cell junctions. Proc Natl Acad Sci USA 107:9944-9949.
65. Lorda-Sanchez I, Ayuso C, Sanz R, Ibanez A. 2001. Does Bardet-Biedl syndrome have a characteristic face? J Med Genet 38:E14.
66. Mahaffey JP, Grego-Bessa J, Liem KF Jr, Anderson KV. 2013. Cofilin and Vangl2 cooperate in the initiation of planar cell polarity in the mouse embryo. Development 140:1262-1271.
67. Mammoto A, Mammoto T, Ingber DE. 2012. Mechanosensitive mechanisms in transcriptional regulation. J Cell Sci 125:3061-3073.
68. Mancuso VP, Parry JM, Storer L, Poggioli C, Nguyen KC, Hall DH, Sundaram MV. 2012. Extracellular leucine-rich repeat proteins are required to organize the apical extracellular matrix and maintain epithelial junction integrity in C. Elegans. Development 139:979-990.
69. Manner J. 2001. Does an equivalent of the "ventral node" exist in chick embryos? A scanning electron microscopic study. Anat Embryol (Berl) 203:481-490.
70. Marjoram L, Wright C. 2011. Rapid differential transport of Nodal and Lefty on sulfated proteoglycan-rich extracellular matrix regulates left-right asymmetry in Xenopus. Development 138:475-485.
71. Maruthamuthu V, Sabass B, Schwarz US, Gardel ML. 2011. Cell-ECM traction force modulates endogenous tension at cell-cell contacts. Proc Natl Acad Sci USA 108:4708-4713.
72. Matsui T, Thitamadee S, Murata T, Kakinuma H, Nabetani T, Hirabayashi Y, Hirate Y, Okamoto H, Bessho Y. 2011. Canopy1, a positive feedback regulator of FGF signaling, controls progenitor cell clustering during Kupffer's vesicle organogenesis. Proc Natl Acad Sci USA 108:9881-9886.
73. Matter K, Balda MS. 2003. Signalling to and from tight junctions. Nat Rev Mol Cell Biol 4:225-236.
74. May-Simera HL, Kai M, Hernandez V, Osborn DP, Tada M, Beales PL. 2010. Bbs8, together with the planar cell polarity protein Vangl2, is required to establish left-right asymmetry in zebrafish. Dev Biol 345:215-225.
75. McGrath J, Brueckner M. 2003. Cilia are at the heart of vertebrate left-right asymmetry. Curr Opin Genet Dev 13:385-392.
76. Meyers EN, Martin GR. 1999. Differences in left-right axis pathways in mouse and chick: Functions of FGF8 and SHH. Science 285:403-406.
77. Montcouquiol M, Rachel RA, Lanford PJ, Copeland NG, Jenkins NA, Kelley MW. 2003. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423:173-177.
78. Nakamura T, Hamada H. 2012. Left-right patterning: conserved and divergent mechanisms. Development 139:3257-3262.
79. Nishimura N, Sasaki T. 2009. Rab family small G proteins in regulation of epithelial apical junctions. Front Biosci (Landmark Ed) 14:2115-2129.
80. Nonaka S, Shiratori H, Saijoh Y, Hamada H. 2002. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418:96-99.
81. Nonaka S, Tanaka Y, Okada Y, Takeda S, Harada A, Kanai Y, Kido M, Hirokawa N. 1998. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95:829-837.
82. Norris DP. 2012. Cilia, calcium and the basis of left-right asymmetry. BMC Biol 10:102.
83. Okabe N, Xu B, Burdine RD. 2008. Fluid dynamics in zebrafish Kupffer's vesicle. Dev Dyn 237:3602-3612.
84. Okada Y, Nonaka S, Tanaka Y, Saijoh Y, Hamada H, Hirokawa N. 1999. Abnormal nodal flow precedes situs inversus in iv and inv mice. Mol Cell 4:459-468.
85. Okada Y, Takeda S, Tanaka Y, Izpisua Belmonte JC, Hirokawa N. 2005. Mechanism of nodal flow: A conserved symmetry breaking event in left-right axis determination. Cell 121:633-644.
86. Oki S, Hashimoto R, Okui Y, Shen MM, Mekada E, Otani H, Saijoh Y, Hamada H. 2007. Sulfated glycosaminoglycans are necessary for Nodal signal transmission from the node to the left lateral plate in the mouse embryo. Development 134:3893-3904.
87. Otani T, Ichii T, Aono S, Takeichi M. 2006. Cdc42 GEF Tuba regulates the junctional configuration of simple epithelial cells. J Cell Biol 175:135-146.
88. Oteiza P, Koppen M, Concha ML, Heisenberg CP. 2008. Origin and shaping of the laterality organ in zebrafish. Development 135:2807-2813.
89. Pagan-Westphal SM, Tabin CJ. 1998. The transfer of left-right positional information during chick embryogenesis. Cell 93:25-35.
90. Park TJ, Haigo SL, Wallingford JB. 2006. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat Genet 38:303-311.
91. Park TJ, Mitchell BJ, Abitua PB, Kintner C, Wallingford JB. 2008. Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat Genet 40:871-879.
92. Pulina MV, Hou SY, Mittal A, Julich D, Whittaker CA, Holley SA, Hynes RO, Astrof S. 2011. Essential roles of fibronectin in the development of the left-right embryonic body plan. Dev Biol 354:208-220.
93. Qiu D, Cheng SM, Wozniak L, McSweeney M, Perrone E, Levin M. 2005. Localization and loss-of-function implicates ciliary proteins in early, cytoplasmic roles in left-right asymmetry. Dev Dyn 234:176-189.
94. Rauzi M, Lenne PF, Lecuit T. 2010. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468:1110-1114.
95. Ross AJ, May-Simera H, Eichers ER, Kai M, Hill J, Jagger DJ, Leitch CC, Chapple JP, Munro PM, Fisher S, Tan PL, Phillips HM, Leroux MR, Henderson DJ, Murdoch JN, Copp AJ, Eliot MM, Lupski JR, Kemp DT, Dollfus H, Tada M, Katsanis N, Forge A, Beales PL. 2005. Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat Genet 37:1135-1140.
96. Samarin S, Nusrat A. 2009. Regulation of epithelial apical junctional complex by Rho family GTPases. Front Biosci (Landmark Ed) 14:1129-1142.
97. Saund RS, Kanai-Azuma M, Kanai Y, Kim I, Lucero MT, Saijoh Y. 2012. Gut endoderm is involved in the transfer of left-right asymmetry from the node to the lateral plate mesoderm in the mouse embryo. Development 139:2426-2435.
98. Schnatwinkel C, Niswander L. 2012. Nubp1 is required for lung branching morphogenesis and distal progenitor cell survival in mice. PLoS One 7:e44871.
99. Schweickert A, Weber T, Beyer T, Vick P, Bogusch S, Feistel K, Blum M. 2007. Cilia-driven leftward flow determines laterality in Xenopus. Curr Biol 17:60-66.
100. Serluca FC, Xu B, Okabe N, Baker K, Lin SY, Sullivan-Brown J, Konieczkowski DJ, Jaffe KM, Bradner JM, Fishman MC, Burdine RD. 2009. Mutations in zebrafish leucine-rich repeat-containing six-like affect cilia motility and result in pronephric cysts, but have variable effects on left-right patterning. Development 136:1621-1631.
101. Sharma N, Berbari NF, Yoder BK. 2008. Ciliary dysfunction in developmental abnormalities and diseases. Curr Top Dev Biol 85:371-427.
102. Shen MM. 2007. Nodal signaling: developmental roles and regulation. Development 134:1023-1034.
103. Shinohara K, Kawasumi A, Takamatsu A, Yoshiba S, Botilde Y, Motoyama N, Reith W, Durand B, Shiratori H, Hamada H. 2012. Two rotating cilia in the node cavity are sufficient to break left-right symmetry in the mouse embryo. Nat Commun 3:622.
104. Simard A, Di Pietro E, Ryan AK. 2005. Gene expression pattern of Claudin-1 during chick embryogenesis. Gene Expr Patterns 5:553-560.
105. Simard A, Di Pietro E, Young CR, Plaza S, Ryan AK. 2006. Alterations in heart looping induced by overexpression of the tight junction protein Claudin-1 are dependent on its C-terminal cytoplasmic tail. Mech Dev 123:210-227.
106. Sourisseau T, Georgiadis A, Tsapara A, Ali RR, Pestell R, Matter K, Balda MS. 2006. Regulation of PCNA and cyclin D1 expression and epithelial morphogenesis by the ZO-1-regulated transcription factor ZONAB/DbpA. Mol Cell Biol 26:2387-2398.
107. Spadaro D, Tapia R, Pulimeno P, Citi S. 2012. The control of gene expression and cell proliferation by the epithelial apical junctional complex. Essays Biochem 53:83-93.
108. Stephen LA, Davis GM, McTeir KE, James J, McTeir L, Kierans M, Bain A, Davey MG. 2013. Failure of centrosome migration causes a loss of motile cilia in talpid(3) mutants. Dev Dyn 242:923-931.
109. Tabin CJ, Vogan KJ. 2003. A two-cilia model for vertebrate left-right axis specification. Genes Dev 17:1-6.
110. Tanaka Y, Okada Y, Hirokawa N. 2005. FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination. Nature 435:172-177.
111. Tay HG, Schulze SK, Compagnon J, Foley FC, Heisenberg CP, Yost HJ, Abdelilah-Seyfried S, Amack JD. 2013. Lethal giant larvae 2 regulates development of the ciliated organ Kupffer's vesicle. Development 140:1550-1559.
112. Traweger A, Fuchs R, Krizbai IA, Weiger TM, Bauer HC, Bauer H. 2003. The tight junction protein ZO-2 localizes to the nucleus and interacts with the heterogeneous nuclear ribonucleoprotein scaffold attachment factor-B. J Biol Chem 278:2692-2700.
113. Tsuda T, Majumder K, Linask KK. 1998. Differential expression of flectin in the extracellular matrix and left-right asymmetry in mouse embryonic heart during looping stages. Dev Genet 23:203-214.
114. Tsukui T, Capdevila J, Tamura K, Ruiz-Lozano P, Rodriguez-Esteban C, Yonei-Tamura S, Magallon J, Chandraratna RA, Chien K, Blumberg B, Evans RM, Belmonte JC. 1999. Multiple left-right asymmetry defects in Shh(-/-) mutant mice unveil a convergence of the shh and retinoic acid pathways in the control of Lefty-1. Proc Natl Acad Sci USA 96:11376-11381.
115. Van Itallie CM, Colegio OR, Anderson JM. 2004. The cytoplasmic tails of claudins can influence tight junction barrier properties through effects on protein stability. J Membr Biol 199:29-38.
116. Vick P, Schweickert A, Weber T, Eberhardt M, Mencl S, Shcherbakov D, Beyer T, Blum M. 2009. Flow on the right side of the gastrocoel roof plate is dispensable for symmetry breakage in the frog Xenopus laevis. Dev Biol 331:281-291.
117. Viotti M, Niu L, Shi SH, Hadjantonakis AK. 2012. Role of the gut endoderm in relaying left-right patterning in mice. PLoS Biol 10:e1001276.
118. Wang C, Low WC, Liu A, Wang B. 2013. Centrosomal protein DZIP1 regulates Hedgehog signaling by promoting cytoplasmic retention of transcription factor GLI3 and affecting ciliogenesis. J Biol Chem 288:29518-29529.
119. Watanabe D, Saijoh Y, Nonaka S, Sasaki G, Ikawa Y, Yokoyama T, Hamada H. 2003. The left-right determinant Inversin is a component of node monocilia and other 9+0 cilia. Development 130:1725-1734.
120. Waters AM, Beales PL. 2011. Ciliopathies: An expanding disease spectrum. Pediatr Nephrol 26:1039-1056.
121. Welsh IC, Thomsen M, Gludish DW, Alfonso-Parra C, Bai Y, Martin JF, Kurpios NA. 2013. Integration of left-right Pitx2 transcription and Wnt signaling drives asymmetric gut morphogenesis via Daam2. Dev Cell 26:629-644.
122. Yoshiba S, Hamada H. 2014. Roles of cilia, fluid flow, and Ca2+ signaling in breaking of left-right symmetry. Trends Genet 30:10-17.
123. Yoshiba S, Shiratori H, Kuo IY, Kawasumi A, Shinohara K, Nonaka S, Asai Y, Sasaki G, Belo JA, Sasaki H, Nakai J, Dworniczak B, Ehrlich BE, Pennekamp P, Hamada H. 2012. Cilia at the node of mouse embryos sense fluid flow for left-right determination via Pkd2. Science 338:226-231.
124. Yost HJ. 1990. Inhibition of proteoglycan synthesis eliminates left-right asymmetry in Xenopus laevis cardiac looping. Development 110:865-874.
125. Yost HJ. 1992. Regulation of vertebrate left-right asymmetries by extracellular matrix. Nature 357:158-161.
126. Zamir EA, Rongish BJ, Little CD. 2008. The ECM moves during primitive streak formation-computation of ECM versus cellular motion. PLoS Biol 6:e247.
127. Zeng H, Hoover AN, Liu A. 2010. PCP effector gene Inturned is an important regulator of cilia formation and embryonic development in mammals. Dev Biol 339:418-428.
128. Zhang Y, Levin M. 2009. Left-right asymmetry in the chick embryo requires core planar cell polarity protein Vangl2. Genesis 47:719-728.