Morphogenesis of the node and notochord: The cellular basis for the establishment and maintenance of left-right asymmetry in the mouse

Developmental Dynamics

Volumn 237, Issue 12, 2008, Pages 3464-3476

  Lee, Jeffrey D ^a   Anderson, Kathryn V ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Cilia; Embryo; Left right asymmetry; Mouse; Node; Notochord

Indexed keywords

CELL MOTILITY; CELL SPECIFICITY; CELL ULTRASTRUCTURE; CONFOCAL MICROSCOPY; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; ENDODERM; EUKARYOTIC FLAGELLUM; GENE CONTROL; GENE EXPRESSION; MORPHOGENESIS; NONHUMAN; NOTOCHORD; PHASE TRANSITION; PRIMITIVE STREAK; PRIMORDIUM; PRIORITY JOURNAL; REVIEW; SCANNING ELECTRON MICROSCOPY; XENOPUS; ZEBRA FISH;

ANIMALS; BODY PATTERNING; EMBRYO, MAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MORPHOGENESIS; NOTOCHORD;

EID: 57149115955     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21598     Document Type: Review

References (98)

1. Abdelkhalek HB, Beckers A, Schuster-Gossler K, Pavlova MN, Burkhardt H, Lickert H, Rossant J, Reinhardt R, Schalkwyk LC, Muller I, Herrmann BG, Ceolin M, Rivera-Pomar R, Gossler A. 2004. The mouse homeobox gene Not is required for caudal notochord development and affected by the truncate mutation. Genes Dev 18:1725-1736.
2. Amack JD, Yost HJ. 2004. The T box transcription factor no tail in ciliated cells controls zebrafish left-right asymmetry. Curr Biol 14:685-690.
3. Amack JD, Wang X, Yost HJ. 2007. Two T-box genes play independent and cooperative roles to regulate morphogenesis of ciliated Kupffer's vesicle in zebrafish. Dev Biol 310:196-210.
4. Ang SL, Rossant J. 1994. HNF-3 beta is essential for node and notochord formation in mouse development. Cell 78:561-574.
5. Ang SL, Jin O, Rhinn M, Daigle N, Stevenson L, Rossant J. 1996. A targeted mouse Otx2 mutation leads to severe defects in gastrulation and formation of axial mesoderm and to deletion of rostral brain. Development 122:243-252.
6. Beckers A, Alten L, Viebahn C, Andre P, Gossler A. 2007. The mouse homeobox gene Noto regulates node morphogenesis, notochordal ciliogenesis, and left right patterning. Proc Natl Acad Sci U S A 104:15765-15770.
7. Beddington RS. 1994. Induction of a second neural axis by the mouse node. Development 120:613-620.
8. Bellomo D, Lander A, Harragan I, Brown NA. 1996. Cell proliferation in mammalian gastrulation: the ventral node and notochord are relatively quiescent. Dev Dyn 205:471-485.
9. Bisgrove BW, Yost HJ. 2006. The roles of cilia in developmental disorders and disease. Development 133:4131-4143.
10. Blum M, Andre P, Muders K, Schweickert A, Fischer A, Bitzer E, Bogusch S, Beyer T, van Straaten HW, Viebahn C. 2007. Ciliation and gene expression distinguish between node and posterior notochord in the mammalian embryo. Differentiation 75:133-146.
11. Bonnafe E, Touka M, AitLounis A, Baas D, Barras E, Ucla C, Moreau A, Flamant F, Dubruille R, Couble P, Collignon J, Durand B, Reith W. 2004. The transcription factor RFX3 directs nodal cilium development and left-right asymmetry specification. Mol Cell Biol 24:4417-4427.
12. Brennan J, Norris DP, Robertson EJ. 2002. Nodal activity in the node governs left-right asymmetry. Genes Dev 16:2339-2344.
13. Brody SL, Yan XH, Wuerffel MK, Song SK, Shapiro SD. 2000. Ciliogenesis and left-right axis defects in forkhead factor HFH-4-null mice. Am J Respir Cell Mol Biol 23:45-51.
14. Brueckner M. 2001. Cilia propel the embryo in the right direction. Am J Med Genet 101:339-344.
15. Cartwright JH, Piro O, Tuval I. 2004. Fluid-dynamical basis of the embryonic development of left-right asymmetry in vertebrates. Proc Natl Acad Sci U S A 101:7234-7239.
16. Caspary T, Larkins CE, Anderson KV. 2007. The graded response to Sonic Hedgehog depends on cilia architecture. Dev Cell 12:767-778.
17. Chen J, Knowles HJ, Hebert JL, Hackett BP. 1998. Mutation of the mouse hepatocyte nuclear factor/forkhead homologue 4 gene results in an absence of cilia and random left-right asymmetry. J Clin Invest 102:1077-1082.
18. Cooper MS, D'Amico LA. 1996. A cluster of noninvoluting endocytic cells at the margin of the zebrafish blastoderm marks the site of embryonic shield formation. Dev Biol 180:184-198.
19. Curtin JA, Quint E, Tsipouri V, Arkell RM, Cattanach B, Copp AJ, Henderson DJ, Spurr N, Stanier P, Fisher EM, Nolan PM, Steel KP, Brown SD, Gray IC, Murdoch JN. 2003. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr Biol 13:1129-1133.
20. Danos MC, Yost HJ. 1996. Role of notochord in specification of cardiac left-right orientation in zebrafish and Xenopus. Dev Biol 177:96-103.
21. Davenport JR, Yoder BK. 2005. An incredible decade for the primary cilium: a look at a once-forgotten organelle. Am J Physiol Renal Physiol 289:F1159-F1169.
22. Downs KM, Davies T. 1993. Staging of gastrulating mouse embryos by morphological landmarks in the dissecting microscope. Development 118:1255-1266.
23. Emery P, Durand B, Mach B, Reith W. 1996. RFX proteins, a novel family of DNA binding proteins conserved in the eukaryotic kingdom. Nucleic Acids Res 24:803-807.
24. Essner JJ, Vogan KJ, Wagner MK, Tabin CJ, Yost HJ, Brueckner M. 2002. Conserved function for embryonic nodal cilia. Nature 418:37-38.
25. 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.
26. Feistel K, Blum M. 2006. Three types of cilia including a novel 9+4 axoneme on the notochordal plate of the rabbit embryo. Dev Dyn 235:3348-3358.
27. Frolenkov GI, Belyantseva IA, Friedman TB, Griffith AJ. 2004. Genetic insights into the morphogenesis of inner ear hair cells. Nat Rev Genet 5:489-498.
28. Furuta Y, Ilic D, Kanazawa S, Takeda N, Yamamoto T, Aizawa S. 1995. Mesodermal defect in late phase of gastrulation by a targeted mutation of focal adhesion kinase, FAK. Oncogene 11:1989-1995.
29. George EL, Georges-Labouesse EN, Patel-King RS, Rayburn H, Hynes RO. 1993. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119:1079-1091.
30. Greene ND, Gerrelli D, Van Straaten HW, Copp AJ. 1998. Abnormalities of floor plate, notochord and somite differentiation in the loop-tail (Lp) mouse: a model of severe neural tube defects. Mech Dev 73:59-72.
31. Hagel M, George EL, Kim A, Tamimi R, Opitz SL, Turner CE, Imamoto A, Thomas SM. 2002. The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol Cell Biol 22:901-915.
32. Hagiwara H, Ohwada N, Takata K. 2004. Cell biology of normal and abnormal ciliogenesis in the ciliated epithelium. Int Rev Cytol 234:101-141.
33. Hamblet NS, Lijam N, Ruiz-Lozano P, Wang J, Yang Y, Luo Z, Mei L, Chien KR, Sussman DJ, Wynshaw-Boris A. 2002. Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development 129:5827-5838.
34. Hirokawa N, Tanaka Y, Okada Y, Takeda S. 2006. Nodal flow and the generation of left-right asymmetry. Cell 125:33-45.
35. Huangfu D, Liu A, Rakeman AS, Murcia NS, Niswander L, Anderson KV. 2003. Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426:83-87.
36. Hummel KP, Chapman DB. 1959. Visceral inversion and associated anomalies in the mouse. J Hered 50:9-13.
37. Jones C, Roper VC, Foucher I, Qian D, Banizs B, Petit C, Yoder BK, Chen P. 2008. Ciliary proteins link basal body polarization to planar cell polarity regulation. Nat Genet 40:69-77.
38. Jurand A. 1974. Some aspects of the development of the notochord in mouse embryos. J Embryol Exp Morphol 32:1-33.
39. Kelly M, Chen P. 2007. Shaping the mammalian auditory sensory organ by the planar cell polarity pathway. Int J Dev Biol 51:535-547.
40. Kelly KA, Wei Y, Mikawa T. 2002. Cell death along the embryo midline regulates left-right sidedness. Dev Dyn 224:238-244.
41. Kinder SJ, Tsang TE, Wakamiya M, Sasaki H, Behringer RR, Nagy A, Tam PP. 2001. The organizer of the mouse gastrula is composed of a dynamic population of progenitor cells for the axial mesoderm. Development 128:3623-3634.
42. 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.
43. Krebs LT, Iwai N, Nonaka S, Welsh IC, Lan Y, Jiang R, Saijoh Y, O'Brien TP, Hamada H, Gridley T. 2003. Notch signaling regulates left-right asymmetry determination by inducing Nodal expression. Genes Dev 17:1207-1212.
44. Kreiling JA, Williams G, Creton R. 2007. Analysis of Kupffer's vesicle in zebrafish embryos using a cave automated virtual environment. Dev Dyn 236:1963-1969.
45. Layton WM Jr. 1976. Random determination of a developmental process: reversal of normal visceral asymmetry in the mouse. J Hered 67:336-338.
46. Lee JD, Silva-Gagliardi NF, Tepass U, McGlade CJ, Anderson KV. 2007. The FERM protein Epb4.1l5 is required for organization of the neural plate and for the epithelial-mesenchymal transition at the primitive streak of the mouse embryo. Development 134:2007-2016.
47. Levin M. 2005. Left-right asymmetry in embryonic development: a comprehensive review. Mech Dev 122:3-25.
48. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, Bradley A. 1999. Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22:361-365.
49. Lohr JL, Danos MC, Yost HJ. 1997. Left-right asymmetry of a nodal-related gene is regulated by dorsoanterior midline structures during Xenopus development. Development 124:1465-1472.
50. McGrath J, Somlo S, Makova S, Tian X, Brueckner M. 2003. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 114:61-73.
51. Melby AE, Warga RM, Kimmel CB. 1996. Specification of cell fates at the dorsal margin of the zebrafish gastrula. Development 122:2225-2237.
52. Meno C, Saijoh Y, Fujii H, Ikeda M, Yokoyama T, Yokoyama M, Toyoda Y, Hamada H. 1996. Left-right asymmetric expression of the TGF beta-family member lefty in mouse embryos. Nature 381:151-155.
53. Meno C, Shimono A, Saijoh Y, Yashiro K, Mochida K, Ohishi S, Noji S, Kondoh H, Hamada H. 1998. lefty-1 is required for left-right determination as a regulator of lefty-2 and nodal. Cell 94:287-297.
54. Meyers EN, Martin GR. 1999. Differences in left-right axis pathways in mouse and chick: functions of FGF8 and SHH. Science 285:403-406.
55. 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.
56. Murcia NS, Richards WG, Yoder BK, Mucenski ML, Dunlap JR, Woychik RP. 2000. The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination. Development 127:2347-2355.
57. Murdoch JN, Henderson DJ, Doudney K, Gaston-Massuet C, Phillips HM, Paternotte C, Arkell R, Stanier P, Copp AJ. 2003. Disruption of scribble (Scrb1) causes severe neural tube defects in the circletail mouse. Hum Mol Genet 12:87-98.
58. 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.
59. 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.
60. Nonaka S, Yoshiba S, Watanabe D, Ikeuchi S, Goto T, Marshall WF, Hamada H. 2005. De novo formation of left-right asymmetry by posterior tilt of nodal cilia. PLoS Biol 3:e268.
61. 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.
62. Okada Y, Takeda S, Tanaka Y, Belmonte JC, Hirokawa N. 2005. Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 121:633-644.
63. 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.
64. Pennekamp P, Karcher C, Fischer A, Schweickert A, Skryabin B, Horst J, Blum M, Dworniczak B. 2002. The ion channel polycystin-2 is required for left-right axis determination in mice. Curr Biol 12:938-943.
65. Placzek M, Tessier-Lavigne M, Yamada T, Jessell T, Dodd J. 1990. Mesodermal control of neural cell identity: floor plate induction by the notochord. Science 250:985-988.
66. Poelmann RE. 1981. The head-process and the formation of the definitive endoderm in the mouse embryo. Anat Embryol (Berl) 162:41-49.
67. Przemeck GK, Heinzmann U, Beckers J, Hrabe de Angelis M. 2003. Node and midline defects are associated with left-right development in Delta1 mutant embryos. Development 130:3-13.
68. Psychoyos D, Stern CD. 1996. Fates and migratory routes of primitive streak cells in the chick embryo. Development 122:1523-1534.
69. Rashbass P, Wilson V, Rosen B, Beddington RS. 1994. Alterations in gene expression during mesoderm formation and axial patterning in Brachyury (T) embryos. Int J Dev Biol 38:35-44.
70. Raya A, Belmonte JC. 2006. Left-right asymmetry in the vertebrate embryo: from early information to higher-level integration. Nat Rev Genet 7:283-293.
71. Raya A, Kawakami Y, Rodriguez-Esteban C, Buscher D, Koth CM, Itoh T, Morita M, Raya RM, Dubova I, Bessa JG, de la Pompa JL, Belmonte JC. 2003. Notch activity induces Nodal expression and mediates the establishment of left-right asymmetry in vertebrate embryos. Genes Dev 17:1213-1218.
72. Roelink H, Augsburger A, Heemskerk J, Korzh V, Norlin S, Ruiz i Altaba A, Tanabe Y, Placzek M, Edlund T, Jessell TM, et al. 1994. Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76:761-775.
73. Satir P, Christensen ST. 2007. Overview of structure and function of mammalian cilia. Annu Rev Physiol 69:377-400.
74. Schlueter J, Brand T. 2007. Left-right axis development: examples of similar and divergent strategies to generate asymmetric morphogenesis in chick and mouse embryos. Cytogenet Genome Res 117:256-267.
75. 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.
76. Selleck MA, Stern CD. 1991. Fate mapping and cell lineage analysis of Hensen's node in the chick embryo. Development 112:615-626.
77. Shawlot W, Behringer RR. 1995. Requirement for Lim1 in head-organizer function. Nature 374:425-430.
78. Shiratori H, Hamada H. 2006. The left-right axis in the mouse: from origin to morphology. Development 133:2095-2104.
79. Shook DR, Majer C, Keller R. 2004. Pattern and morphogenesis of presumptive superficial mesoderm in two closely related species, Xenopus laevis and Xenopus tropicalis. Dev Biol 270:163-185.
80. Sobkowicz HM, Slapnick SM, August BK. 1995. The kinocilium of auditory hair cells and evidence for its morphogenetic role during the regeneration of stereocilia and cuticular plates. J Neurocytol 24:633-653.
81. Sulik K, Dehart DB, Iangaki T, Carson JL, Vrablic T, Gesteland K, Schoenwolf GC. 1994. Morphogenesis of the murine node and notochordal plate. Dev Dyn 201:260-278.
82. Supp DM, Brueckner M, Kuehn MR, Witte DP, Lowe LA, McGrath J, Corrales J, Potter SS. 1999. Targeted deletion of the ATP binding domain of left-right dynein confirms its role in specifying development of left-right asymmetries. Development 126:5495-5504.
83. Swoboda P, Adler HT, Thomas JH. 2000. The RFX-type transcription factor DAF-19 regulates sensory neuron cilium formation in C. elegans. Mol Cell 5:411-421.
84. Tabin CJ, Vogan KJ. 2003. A two-cilia model for vertebrate left-right axis specification. Genes Dev 17:1-6.
85. Takeda S, Yonekawa Y, Tanaka Y, Okada Y, Nonaka S, Hirokawa N. 1999. Left-right asymmetry and kinesin superfamily protein KIF3A: new insights in determination of laterality and mesoderm induction by kif3A-/- mice analysis. J Cell Biol 145:825-836.
86. Takeuchi JK, Lickert H, Bisgrove BW, Sun X, Yamamoto M, Chawengsaksophak K, Hamada H, Yost HJ, Rossant J, Bruneau BG. 2007. Baf60c is a nuclear Notch signaling component required for the establishment of left-right asymmetry. Proc Natl Acad Sci U S A 104:846-851.
87. 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.
88. Torban E, Kor C, Gros P. 2004. Van Gogh-like2 (Strabismus) and its role in planar cell polarity and convergent extension in vertebrates. Trends Genet 20:570-577.
89. 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 U S A 96: 11376-11381.
90. Wang Y, Nathans J. 2007. Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134:647-658.
91. Wang Y, Guo N, Nathans J. 2006. The role of Frizzled3 and Frizzled6 in neural tube closure and in the planar polarity of inner-ear sensory hair cells. J Neurosci 26:2147-2156.
92. Weinstein DC, Ruiz i Altaba A, Chen WS, Hoodless P, Prezioso VR, Jessell TM, Darnell JE Jr. 1994. The winged-helix transcription factor HNF-3 beta is required for notochord development in the mouse embryo. Cell 78:575-588.
93. Yamamoto M, Meno C, Sakai Y, Shiratori H, Mochida K, Ikawa Y, Saijoh Y, Hamada H. 2001. The transcription factor FoxH1 (FAST) mediates Nodal signaling during anterior-posterior patterning and node formation in the mouse. Genes Dev 15:1242-1256.
94. Yamamoto M, Mine N, Mochida K, Sakai Y, Saijoh Y, Meno C, Hamada H. 2003. Nodal signaling induces the midline barrier by activating Nodal expression in the lateral plate. Development 130:1795-1804.
95. Yamanaka Y, Tamplin OJ, Beckers A, Gossler A, Rossant J. 2007. Live imaging and genetic analysis of mouse notochord formation reveals regional morphogenetic mechanisms. Dev Cell 13:884-896.
96. Ybot-Gonzalez P, Savery D, Gerrelli D, Signore M, Mitchell CE, Faux CH, Greene ND, Copp AJ. 2007. Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure. Development 134:789-799.
97. Yokoyama T, Copeland NG, Jenkins NA, Montgomery CA, Elder FF, Overbeek PA. 1993. Reversal of left-right asymmetry: a situs inversus mutation. Science 260:679-682.
98. Zhang M, Bolfing MF, Knowles HJ, Karnes H, Hackett BP. 2004. Foxj1 regulates asymmetric gene expression during left-right axis patterning in mice. Biochem Biophys Res Commun 324:1413-1420.