Linking early determinants and cilia-driven leftward flow in left-right axis specification of Xenopus laevis: A theoretical approach

Differentiation

Volumn 83, Issue 2, 2012, Pages

  Schweickert, Axel ^a   Walentek, Peter ^a   Thumberger, Thomas ^a   Danilchik, Mike ^b  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Cilia; Early determinants; Ion flux; Left right asymmetry; Leftward flow; Xenopus laevis

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA; PROTEIN COCO; PROTEIN FOXJ1; PROTEIN XNR1; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CILIARY MOTILITY; EMBRYO AXIS; EMBRYO DEVELOPMENT; EMBRYO POLARITY; EUKARYOTIC FLAGELLUM; GASTROINTESTINAL TRACT; GENE EXPRESSION; GENETIC REGULATION; HEART; ION TRANSPORT; LATERAL PLATE MESODERM; LEFT RIGHT AXIS; LEFTWARD FLOW; LUNG; MESODERM; MOLECULAR INTERACTION; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THEORETICAL STUDY; XENOPUS; XENOPUS LAEVIS;

ANIMALS; BODY PATTERNING; CILIA; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MESODERM; ORGANIZERS, EMBRYONIC; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

AMPHIBIA; ANURA; AVES; MAMMALIA; VERTEBRATA; XENOPUS LAEVIS;

EID: 84856321241     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2011.11.005     Document Type: Article

References (103)

1. Adams D.S., Robinson K.R., Fukumoto T., Yuan S., Albertson R.C., Yelick P., Kuo L., McSweeney M., Levin M. Early, H+-V-ATPase-dependent proton flux is necessary for consistent left-right patterning of non-mammalian vertebrates. Development 2006, 133:1657-1671.
2. Afzelius B.A. A human syndrome caused by immotile cilia. Science 1976, 193:317-319.
3. Antic D., Stubbs J.L., Suyama K., Kintner C., Scott M.P., Axelrod J.D. Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PLoS One 2010, 5:e8999.
4. Aw S., Adams D.S., Qiu D., Levin M. H,K-ATPase protein localization and Kir4.1 function reveal concordance of three axes during early determination of left-right asymmetry. Mechanisms of Development 2008, 125:353-372.
5. Bangs F., Antonio N., Thongnuek P., Welten M., Davey M.G., Briscoe J., Tickle C. Generation of mice with functional inactivation of talpid3, a gene first identified in chicken. Development 2011, 138:3261-3272.
6. Basu B., Brueckner M. Cilia multifunctional organelles at the center of vertebrate left-right asymmetry. Current Topics in Develpomental Biology 2008, 85:151-174.
7. Bell E., Munoz-Sanjuan I., Altmann C.R., Vonica A., Brivanlou A.H. Cell fate specification and competence by Coco, a maternal BMP, TGFbeta and Wnt inhibitor. Development 2003, 130:1381-1389.
8. Ben J., Elworthy S., Ng A.S., van Eeden F., Ingham P.W. Targeted mutation of the talpid3 gene in zebrafish reveals its conserved requirement for ciliogenesis and Hedgehog signalling across the vertebrates. Development 2011, 138:4969-4978.
9. Black S.D., Vincent J.P. The first cleavage plane and the embryonic axis are determined by separate mechanisms in Xenopus laevis. II. Experimental dissociation by lateral compression of the egg. Developmental Biology 1988, 128:65-71.
10. Blum M., Andre P., Muders K., Schweickert A., Fischer A., Bitzer E., Bogusch S., Beyer T., van Straaten H.W., Viebahn C. Ciliation and gene expression distinguish between node and posterior notochord in the mammalian embryo. Differentiation 2007, 75:133-146.
11. Blum M., Beyer T., Weber T., Vick P., Andre P., Bitzer E., Schweickert A. Xenopus, an ideal model system to study vertebrate left-right asymmetry. Develpmental Dynamics 2009, 238:1215-1225.
12. Blum M., Weber T., Beyer T., Vick P. Evolution of leftward flow. Seminars in Cell and Developmental Biology 2009, 20:464-471.
13. Brennan J., Norris D.P., Robertson E.J. Nodal activity in the node governs left-right asymmetry. Genes and Development 2002, 16:2339-2344.
14. Campione M., Steinbeisser H., Schweickert A., Deissler K., van Bebber F., Lowe L.A., Nowotschin S., Viebahn C., Haffter P., Kuehn M.R., et al. The homeobox gene Pitx2: mediator of asymmetric left-right signaling in vertebrate heart and gut looping. Development 1999, 126:1225-1234.
15. Carneiro K., Donnet C., Rejtar T., Karger B.L., Barisone G.A., Diaz E., Kortagere S., Lemire J.M., Levin M. Histone deacetylase activity is necessary for left-right patterning during vertebrate development. BMC Develpomental Biology 2011, 11:29.
16. Cheng A.M., Thisse B., Thisse C., Wright C.V. The lefty-related factor Xatv acts as a feedback inhibitor of nodal signaling in mesoderm induction and L-R axis development in xenopus. Development 2000, 127:1049-1061.
17. Coombs G.S., Yu J., Canning C.A., Veltri C.A., Covey T.M., Cheong J.K., Utomo V., Banerjee N., Zhang Z.H., Jadulco R.C., et al. WLS-dependent secretion of WNT3A requires Ser209 acylation and vacuolar acidification. Journal of Cell Science 2010, 123:3357-3367.
18. Cruciat C.M., Ohkawara B., Acebron S.P., Karaulanov E., Reinhard C., Ingelfinger D., Boutros M., Niehrs C. Requirement of prorenin receptor and vacuolar H+-ATPase-mediated acidification for Wnt signaling. Science 2010, 327:459-463.
19. Danilchik M.V., Black S.D. The first cleavage plane and the embryonic axis are determined by separate mechanisms in Xenopus laevis. I. Independence in undisturbed embryos. Developmental Biology 1988, 128:58-64.
20. Danos M.C., Yost H.J. Linkage of cardiac left-right asymmetry and dorsal-anterior development in Xenopus. Development 1995, 121:1467-1474.
21. Davidson B.P., Kinder S.J., Steiner K., Schoenwolf G.C., Tam P.P. Impact of node ablation on the morphogenesis of the body axis and the lateral asymmetry of the mouse embryo during early organogenesis. Developmental Biology 1999, 211:11-26.
22. Duboc V., Lepage T. A conserved role for the nodal signaling pathway in the establishment of dorso-ventral and left-right axes in deuterostomes. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 2008, 310:41-53.
23. Elinson R.P., Pasceri P. Two UV-sensitive targets in dorsoanterior specification of frog embryos. Development 1989, 106:511-518.
24. Essner J.J., Vogan K.J., Wagner M.K., Tabin C.J., Yost H.J., Brueckner M. Conserved function for embryonic nodal cilia. Nature 2002, 418:37-38.
25. Essner J.J., Amack J.D., Nyholm M.K., Harris E.B., Yost H.J. 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 2005, 132:1247-1260.
26. Fan M.J., Sokol S.Y. A role for Siamois in Spemann organizer formation. Development 1997, 124:2581-2589.
27. Fliegauf M., Benzing T., Omran H. When cilia go bad: cilia defects and ciliopathies. Nature Reviews Molecular Cell Biology 2007, 8:880-893.
28. Fukumoto T., Kema I.P., Levin M. Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos. Current Biology 2005, 15:794-803.
29. Gaio U., Schweickert A., Fischer A., Garratt A.N., Muller T., Ozcelik C., Lankes W., Strehle M., Britsch S., Blum M., et al. A role of the cryptic gene in the correct establishment of the left-right axis. Current Biology 1999, 9:1339-1342.
30. Gerhart J., Danilchik M., Doniach T., Roberts S., Rowning B., Stewart R. Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. Development 1989, 107(Suppl):37-51.
31. Grande C., Patel N.H. Nodal signalling is involved in left-right asymmetry in snails. Nature 2009, 457:1007-1011.
32. Hamada H. Breakthroughs and future challenges in left-right patterning. Development, Growth and Differentiation 2008, 50(Suppl 1):S71-78.
33. Hashimoto H., Rebagliati M., Ahmad N., Muraoka O., Kurokawa T., Hibi M., Suzuki T. The Cerberus/Dan-family protein Charon is a negative regulator of Nodal signaling during left-right patterning in zebrafish. Development 2004, 131:1741-1753.
34. Hashimoto M., Hamada H. Translation of anterior-posterior polarity into left-right polarity in the mouse embryo. Current Opinion in Genetics and Development 2010, 20:433-437.
35. Hibino T., Ishii Y., Levin M., Nishino A. Ion flow regulates left-right asymmetry in sea urchin development. Development Genes and Evolution 2006, 216:265-276.
36. Hojo M., Takashima S., Kobayashi D., Sumeragi A., Shimada A., Tsukahara T., Yokoi H., Narita T., Jindo T., Kage T., et al. Right-elevated expression of charon is regulated by fluid flow in medaka Kupffer's vesicle. Development, Growth and Differentiation 2007, 49:395-405.
37. Kawasumi A., Nakamura T., Iwai N., Yashiro K., Saijoh Y., Belo J.A., Shiratori H., Hamada H. Left-right asymmetry in the level of active Nodal protein produced in the node is translated into left-right asymmetry in the lateral plate of mouse embryos. Developmental Biology 2011, 353:321-330.
38. Kramer-Zucker A.G., Olale F., Haycraft C.J., Yoder B.K., Schier A.F., Drummond I.A. Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 2005, 132:1907-1921.
39. Kuroda R., Endo B., Abe M., Shimizu M. Chiral blastomere arrangement dictates zygotic left-right asymmetry pathway in snails. Nature 2009, 462:790-794.
40. Levin M. Motor protein control of ion flux is an early step in embryonic left-right asymmetry. Bioessays 2003, 25:1002-1010.
41. Levin M. Left-right asymmetry in embryonic development: a comprehensive review. Mechanisms of Development 2005, 122:3-25.
42. Levin M. Is the early left-right axis like a plant, a kidney, or a neuron? The integration of physiological signals in embryonic asymmetry. Birth Defects Research Part C: Embryo Today 2006, 78:191-223.
43. Levin M., Thorlin T., Robinson K.R., Nogi T., Mercola M. Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 2002, 111:77-89.
44. Lin X., Xu X. Distinct functions of Wnt/beta-catenin signaling in KV development and cardiac asymmetry. Development 2009, 136:207-217.
45. Long S., Ahmad N., Rebagliati M. The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development 2003, 130:2303-2316.
46. Lowe L.A., Supp D.M., Sampath K., Yokoyama T., Wright C.V., Potter S.S., Overbeek P., Kuehn M.R. Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature 1996, 381:158-161.
47. Lustig K.D., Kroll K., Sun E., Ramos R., Elmendorf H., Kirschner M.W. A Xenopus nodal-related gene that acts in synergy with noggin to induce complete secondary axis and notochord formation. Development 1996, 122:3275-3282.
48. Maisonneuve C., Guilleret I., Vick P., Weber T., Andre P., Beyer T., Blum M., Constam D.B. Bicaudal C, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow. Development 2009, 136:3019-3030.
49. Marjoram L., Wright C. Rapid differential transport of Nodal and Lefty on sulfated proteoglycan-rich extracellular matrix regulates left-right asymmetry in Xenopus. Development 2011, 138:475-485.
50. Marques S., Borges A.C., Silva A.C., Freitas S., Cordenonsi M., Belo J.A. The activity of the Nodal antagonist Cerl-2 in the mouse node is required for correct L/R body axis. Genes and Development 2004, 18:2342-2347.
51. Marshall W.F., Nonaka S. Cilia: tuning in to the cell's antenna. Current Biology 2006, 16. R604-614.
52. May-Simera H.L., Kai M., Hernandez V., Osborn D.P., Tada M., Beales P.L. Bbs8, together with the planar cell polarity protein Vangl2, is required to establish left-right asymmetry in zebrafish. Developmental Biology 2010, 345:215-225.
53. Mayer B. Über das Regulations- und Induktionsvermögen der halbseitigen oberen Urmundlippe von Triton. Wilhelm Roux's Archiv für EntwMech Org 1935, 133:518-581.
54. McGrath J., Somlo S., Makova S., Tian X., Brueckner M. Two populations of node monocilia initiate left-right asymmetry in the mouse. Cell 2003, 114:61-73.
55. Meinhardt H. Models for organizer and notochord formation. C R Acad Sci III, Sci Vie 2000, 323:23-30.
56. Meinhardt H. Organizer and axes formation as a self-organizing process. International Journal of Developmental Biology 2001, 45:177-188.
57. Meinhardt H. Models of biological pattern formation: from elementary steps to the organization of embryonic axes. Current Topics in Develpomental Biology 2008, 81:1-63.
58. Moody S.A., Kline M.J. Segregation of fate during cleavage of frog (Xenopus laevis) blastomeres. Anatomy and Embryology (Berlin) 1990, 182:347-362.
59. Muller J.K., Prather D.R., Nascone-Yoder N.M. Left-right asymmetric morphogenesis in the Xenopus digestive system. Develpmental Dynamics 2003, 228:672-682.
60. Nakamura T., Mine N., Nakaguchi E., Mochizuki A., Yamamoto M., Yashiro K., Meno C., Hamada H. Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateral-inhibition system. DevelopmentalCell 2006, 11:495-504.
61. Nakaya M.A., Biris K., Tsukiyama T., Jaime S., Rawls J.A., Yamaguchi T.P. Wnt3a links left-right determination with segmentation and anteroposterior axis elongation. Development 2005, 132:5425-5436.
62. Nieuwkoop P.D., Faber J. Normal Table of Xenopus laevis (Daudin) 1967, North Holland Publishing Co., Amsterdam.
63. Nonaka S., Shiratori H., Saijoh Y., Hamada H. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 2002, 418:96-99.
64. Nonaka S., Yoshiba S., Watanabe D., Ikeuchi S., Goto T., Marshall W.F., Hamada H. De novo formation of left-right asymmetry by posterior tilt of nodal cilia. PLoS Biology 2005, 3:e268.
65. Ohi Y., Wright C.V. Anteriorward shifting of asymmetric Xnr1 expression and contralateral communication in left-right specification in Xenopus. Developmental Biology 2007, 301:447-463.
66. Okada Y., Nonaka S., Tanaka Y., Saijoh Y., Hamada H., Hirokawa N. Abnormal nodal flow precedes situs inversus in iv and inv mice. Molecular Cell 1999, 4:459-468.
67. Okada Y., Takeda S., Tanaka Y., Belmonte J.C., Hirokawa N. Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 2005, 121:633-644.
68. Oki S., Hashimoto R., Okui Y., Shen M.M., Mekada E., Otani H., Saijoh Y., Hamada H. Sulfated glycosaminoglycans are necessary for Nodal signal transmission from the node to the left lateral plate in the mouse embryo. Development 2007, 134:3893-3904.
69. Olbrich H., Haffner K., Kispert A., Volkel A., Volz A., Sasmaz G., Reinhardt R., Hennig S., Lehrach H., Konietzko N., et al. Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry. Nature Genetics 2002, 30:143-144.
70. Onuma Y., Yeo C.Y., Whitman M. XCR2, one of three Xenopus EGF-CFC genes, has a distinct role in the regulation of left-right patterning. Development 2006, 133:237-250.
71. Oteiza P., Koppen M., Krieg M., Pulgar E., Farias C., Melo C., Preibisch S., Muller D., Tada M., Hartel S., et al. Planar cell polarity signalling regulates cell adhesion properties in progenitors of the zebrafish laterality organ. Development 2010, 137:3459-3468.
72. Pohl B.S., Knochel W. Isolation and developmental expression of Xenopus FoxJ1 and FoxK1. Develpment Genes and Evolution 2004, 214:200-205.
73. Pohl C. Left-right patterning in the C. elegans embryo: unique mechanisms and common principles. Communicative and Integrative Biology 2011, 4:34-40.
74. Qiu D., Cheng S.M., Wozniak L., McSweeney M., Perrone E., Levin M. Localization and loss-of-function implicates ciliary proteins in early, cytoplasmic roles in left-right asymmetry. Develpmental Dynamics 2005, 234:176-189.
75. Ramsdell A.F., Bernanke J.M., Trusk T.C. Left-right lineage analysis of the embryonic Xenopus heart reveals a novel framework linking congenital cardiac defects and laterality disease. Development 2006, 133:1399-1410.
76. Sampath K., Cheng A.M., Frisch A., Wright C.V. Functional differences among Xenopus nodal-related genes in left-right axis determination. Development 1997, 124:3293-3302.
77. Scharf S.R., Gerhart J.C. Determination of the dorsal-ventral axis in eggs of Xenopus laevis: complete rescue of UV-impaired eggs by oblique orientation before first cleavage. Developmental Biology 1980, 79:181-198.
78. Schier A.F. Nodal signaling in vertebrate development. Annual Review of Cell and Developmental Biology 2003, 19:589-621.
79. Schier A.F. Nodal morphogens. Cold Spring Harbor Perspectives in Biology 2009, 1:a003459.
80. Schweickert A., Weber T., Beyer T., Vick P., Bogusch S., Feistel K., Blum M. Cilia-driven leftward flow determines laterality in Xenopus. Current Biology 2007, 17:60-66.
81. Schweickert A., Vick P., Getwan M., Weber T., Schneider I., Eberhardt M., Beyer T., Pachur A., Blum M. The nodal inhibitor coco is a critical target of leftward flow in Xenopus. Current Biology 2010.
82. Shen M.M. Nodal signaling: developmental roles and regulation. Development 2007, 134:1023-1034.
83. Shimeld S.M., Levin M. Evidence for the regulation of left-right asymmetry in Ciona intestinalis by ion flux. Develpmental Dynamics 2006, 235:1543-1553.
84. Shiratori H., Hamada H. The left-right axis in the mouse: from origin to morphology. Development 2006, 133:2095-2104.
85. Shook D.R., Majer C., Keller R. Pattern and morphogenesis of presumptive superficial mesoderm in two closely related species, Xenopus laevis and Xenopus tropicalis. Developmental Biology 2004, 270:163-185.
86. Smith J.C., Price B.M., Green J.B., Weigel D., Herrmann B.G. Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 1991, 67:79-87.
87. Sokol S., Christian J.L., Moon R.T., Melton D.A. Injected Wnt RNA induces a complete body axis in Xenopus embryos. Cell 1991, 67:741-752.
88. Song H., Hu J., Chen W., Elliott G., Andre P., Gao B., Yang Y. Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 2010, 466:378-382.
89. Spemann H., Mangold H. Über Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren. Archiv f Mikrosk Anat u Entwicklungsmech 1924, 100:599-638.
90. Stewart R.M., Gerhart J.C. The anterior extent of dorsal development of the Xenopus embryonic axis depends on the quantity of organizer in the late blastula. Development 1990, 109:363-372.
91. Stubbs J.L., Oishi I., Izpisua Belmonte J.C., Kintner C. The forkhead protein Foxj1 specifies node-like cilia in Xenopus and zebrafish embryos. Nature Genetics 2008, 40:1454-1460.
92. Tabin C. Do we know anything about how left-right asymmetry is first established in the vertebrate embryo?. Journal of Molecular Histology 2005, 36:317-323.
93. Vandenberg L.N., Levin M. Far from solved: a perspective on what we know about early mechanisms of left-right asymmetry. Develpmental Dynamics 2010, 239:3131-3146.
94. Vandenberg L.N., Levin M. Consistent left-right asymmetry cannot be established by late organizers in Xenopus unless the late organizer is a conjoined twin. Development 2010, 137:1095-1105.
95. Vick P., Schweickert A., Weber T., Eberhardt M., Mencl S., Shcherbakov D., Beyer T., Blum M. Flow on the right side of the gastrocoel roof plate is dispensable for symmetry breakage in the frog Xenopus laevis. Developmental Biology 2009, 331:281-291.
96. Vonica A., Brivanlou A.H. The left-right axis is regulated by the interplay of Coco, Xnr1 and derriere in Xenopus embryos. Developmental Biology 2007, 303:281-294.
97. Wang X., Yost H.J. Initiation and propagation of posterior to anterior (PA) waves in zebrafish left-right development. Develpmental Dynamics 2008, 237:3640-3647.
98. Weaver C., Kimelman D. Move it or lose it: axis specification in Xenopus. Development 2004, 131:3491-3499.
99. Yamamoto M., Mine N., Mochida K., Sakai Y., Saijoh Y., Meno C., Hamada H. Nodal signaling induces the midline barrier by activating nodal expression in the lateral plate. Development 2003, 130:1795-1804.
100. Yan Y.T., Gritsman K., Ding J., Burdine R.D., Corrales J.D., Price S.M., Talbot W.S., Schier A.F., Shen M.M. Conserved requirement for EGF-CFC genes in vertebrate left-right axis formation. Genes and Development 1999, 13:2527-2537.
101. Yin Y., Bangs F., Paton I.R., Prescott A., James J., Davey M.G., Whitley P., Genikhovich G., Technau U., Burt D.W., et al. The Talpid3 gene (KIAA0586) encodes a centrosomal protein that is essential for primary cilia formation. Development 2009, 136:655-664.
102. Yu X., Ng C.P., Habacher H., Roy S. Foxj1 transcription factors are master regulators of the motile ciliogenic program. Nature Genetics 2008, 40:1445-1453.
103. Zhang M., Bolfing M.F., Knowles H.J., Karnes H., Hackett B.P. Foxj1 regulates asymmetric gene expression during left-right axis patterning in mice. Biochemical and Biophysical Research Communications 2004, 324:1413-1420.