Of mice and men: Dissecting the genetic pathway that controls left-right asymmetry in mice and humans

American Journal of Medical Genetics - Seminars in Medical Genetics

Volumn 97, Issue 4, 2000, Pages 258-270

  Schneider, Heike ^b   Brueckner, Martina ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NONE

Author keywords

Cilia; Dynein; Heterotaxy; Laterality; Mouse mutations; Situs inversus

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; KINESIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; EMBRYO DEVELOPMENT; GENE FUNCTION; GENE MUTATION; GENETIC ANALYSIS; MOUSE; NEURAL TUBE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PSEUDOPODIUM; REVIEW; SITUS INVERSUS;

ABNORMALITIES, MULTIPLE; ANIMALS; BODY PATTERNING; CILIA; DYNEIN ATPASE; ECTODERM; EMBRYONIC AND FETAL DEVELOPMENT; ENDODERM; FETAL PROTEINS; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES; GENES, HOMEOBOX; GENES, LETHAL; HOMEODOMAIN PROTEINS; HUMANS; KINESIN; MICE; MICE, MUTANT STRAINS; MUTATION; NOTOCHORD; PHENOTYPE; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 0034443891     PISSN: 01487299     EISSN: None     Source Type: Journal    
DOI: 10.1002/1096-8628(200024)97:4<258::AID-AJMG1276>3.0.CO;2-8     Document Type: Review

References (73)

1. Afzelius BA. 1976. A human syndrome caused by immotile cilia. Science 193:317-319.
2. Ang SL, Rossant J. 1994. HNF-3 beta is essential for node and notochord formation in mouse development. Cell 78:561-574.
3. Bamford RN, Roessler E, Burdine RD, Saplakoglu U, dela Cruz J, Splitt M, Towbin J, Bowers P, Marino B, Schier AF, Shen MM, Muenke M, Casey B. 2000. Loss-of-function mutations in the EGF-CFC gene CFC1 are associated with human left-right laterality defects. Nat Genet 26:365-369.
4. Beddington RS. 1994. Induction of a second neural axis by the mouse node. Development 120:613-620.
5. Beddington RS, Rashbass P, Wilson V. 1992. Brachyury: a gene affecting mouse gastrulation and early organogenesis. Dev Suppl 157-165.
6. 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.
7. Carrel T, Purandare SM, Harrison W, Elder F, Fox T, Casey B, Herman GE. 2000. The X-linked mouse mutation bent tail is associated with a deletion of the Zic3 locus. Hum Mol Genet 9:1937-1942.
8. Casey B, Devoto M, Jones KL, Ballabio A. 1993. Mapping a gene for familial situs abnormalities to human chromosome Xq24-q27.1. Nat Genet 5:403-407.
9. Chang H, Huylebroeck D, Verschueren K, Guo Q, Matzuk MM, Zwijsen A. 1999. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 126:1631-1642.
10. Chang H, Zwijsen A, Vogel H, Huylebroeck D, Matzuk MM. 2000. Smad5 is essential for left-right asymmetry in mice. Dev Biol 219:71-78.
11. 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.
12. Chen JN, van Eeden FJ, Warren KS, Chin A, Nusslein-Volhard C, Haffter P, Fishman MC. 1997. Left-right pattern of cardiac BMP4 may drive asymmetry of the heart in zebrafish. Development 124:4373-4382.
13. Chiang C, Litingtung Y, Lee E, Young KE, Corden JL, Westphal H, Beachy PA. 1996. Cyclopia and defective axial patterning in mice lacking sonic hedgehog gene function. Nature 383:407-413.
14. Cole DG, Diener DR, Himelblau AL, Beech PL, Fuster JC, Rosenbaum JL. 1998. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J Cell Biol 141:993-1008.
15. Collignon J, Varlet I, Robertson EJ. 1996. Relationship between asymmetric nodal expression and the direction of embryonic turning [see Comments]. Nature 381:155-158.
16. Conlon FL, Lyons KM, Takaesu N, Barth KS, Kispert A, Herrmann B, Robertson EJ. 1994. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120:1919-1928.
17. Constam DB, Robertson EJ. 2000. Tissue-specific requirements for the proprotein convertase furin/SPC1 during embryonic turning and heart looping. Development 127:245-254.
18. Danos MC, Yost HJ. 1996. Role of notochord in specification of cardiac left-right orientation in zebrafish and Xenopus. Dev Biol 177:96-103.
19. Davidson BP, Kinder SJ, Steiner K, Schoenwolf GC, Tam PP. 1999. Impact of node ablation on the morphogenesis of the body axis and the lateral asymmetry of the mouse embryo during early organogenesis. Dev Biol 211: 11-26.
20. Dufort D, Schwartz L, Harpal K, Rossant J. 1998. The transcription factor HNF3beta is required in visceral endoderm for normal primitive streak morphogenesis. Development 125:3015-3025.
21. Ferrero GB, Gebbia M, Pilia G, Witte D, Peier A, Hopkin RJ, Craigen WJ, Shaffer LG, Schlessinger D, Ballabio A, Casey B. 1997. A submicroscopic deletion in Xq26 associated with familial situs ambiguus. Am J Hum Genet 61:395-401.
22. Gage PJ, Camper SA. 1997. Pituitary homeobox 2, a novel member of the bicoid-related family of homeobox genes, is a potential regulator of anterior structure formation. Hum Mol Genet 6:457-464.
23. Gaio U, Schweickert A, Fischer A, Garratt AN, Muller T, Ozcelik C, Lankes W, Strehle M, Britsch S, Blum M, Birchmeier C. 1999. A role of the cryptic gene in the correct establishment of the left-right axis. Curr Biol 9:1339-1342.
24. Gebbia M, Ferrero GB, Pilia G, Bassi MT, Aylsworth A, Penman-Splitt M, Bird LM, Bamforth JS, Burn J, Schlessinger D, Nelson DL, Casey B. 1997. X-linked situs abnormalities result from mutations in Z1C3 [see Comments]. Nat Genet 17: 305-308.
25. Heymer J, Kuehn M, Ruther U. 1997. The expression pattern of nodal and lefty in the mouse mutant Ft suggests a function in the establishment of handedness. Mech Dev 66:5-11.
26. Hummel KP, Chapman DB. 1959. Visceral inversion and associated anomalies in the mouse. J Hered 50:9-13.
27. Hyatt BA, Lohr JL, Yost HJ. 1996. Initiation of vertebrate left-right axis formation by maternal Vgl. Nature 384:62-65.
28. Ioffe E, Stanley P. 1994. Mice lacking N-acetyl-glucosaminyltransferase I activity die at midgestation, revealing an essential role for complex or hybrid N-linked carbohydrates. Proc Natl Acad Sci U S A 91:728-732.
29. Izraeli S, Lowe LA, Bertness VL, Good DJ, Dorward DW, Kirsch IR, Kuehn MR. 1999. The SIL gene is required for mouse embryonic axial development and left-right specification. Nature 399:691-694.
30. King T, Beddington RS, Brown NA. 1998. The role of the brachyury gene in heart development and left-right specification in the mouse. Mech Dev 79:29-37.
31. Kispert A, Koschorz B, Herrmann BG. 1995. The T protein encoded by brachyury is a tissue-specific transcription factor. EMBO J 14:4763-4772.
32. Kosaki K, Bassi MT, Kosaki R, Lewin M, Belmont J, Schauer G, Casey B. 1999a. Characterization and mutation analysis of human LEFTY A and LEFTY B, homologues of murine genes implicated in left-right axis development. Am J Hum Genet 64:712-721.
33. Kosaki R, Gebbia M, Kosaki K, Lewin M, Bowers P, Towbin JA, Casey B. 1999b. Left-right axis malformations associated with mutations in ACVR2B, the gene for human activin receptor type IIB. Am J Med Genet 82:70-76.
34. 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.
35. Levin M, Roberts DJ, Holmes LB, Tabin C. 1996. Laterality defects in conjoined twins [Letter]. Nature 384:321.
36. Lin CR, Kioussi C, O'Connell S, Briata P, Szeto D, Liu F, Izpisua-Belmonte JC, Rosenfeld MG. 1999. Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 401:279-282.
37. Lohr JL, Danos MC, Yost HJ. 1997. Left-right asymmetry of a nodal-related gene is regulated by dursoanterior midline structures during Xenopus development. Development 124:1465-1472.
38. Lowe LA, Supp DM, Sampath K, Yokoyama T, Wright CV, Potter SS, Overbeek P, Kuehn MR. 1996. Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus [see Comments]. Nature 381:158-161.
39. Lu MF, Pressman C, Dyer R, Johnson RL, Martin JF. 1999. Function of Rieger syndrome gene in left-right asymmetry and craniofacial development. Nature 401:276-278.
40. Marszalek JR, Ruiz-Lozano P, Roberts E, Chien KR, Goldstein LS. 1999. Situs inversus and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc Natl Acad Sci U S A 96:5043-5048.
41. Melloy PG, Ewart JL, Cohen MF, Desmond ME, Kuehn MR, Lo CW. 1998. No turning, a mouse mutation causing left-right and axial patterning defects. Dev Biol 193: 77-89.
42. Meno C, Gritsman K, Ohishi S, Ohfuji Y, Heckscher E, Mochida K, Shimono A, Kondoh H, Talbot WS, Robertson EJ, Schier AF, Hamada H. 1999. Mouse Lefty2 and zebrafish antivin are feedback inhibitors of nodal signaling during vertebrate gastrulation. Mol Cell 4:287-298.
43. Meno C, Ito Y, Saijoh Y, Matsuda Y, Tashiro K, Kuhara S, Hamada H. 1997. Two closely-related left-right asymmetrically expressed genes, lefty-1 and lefty-2: their distinct expression domains, chromosomal linkage and direct neuralizing activity in Xenopus embryos. Genes Cells 2:513-524.
44. 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 [see Comments]. Nature 381:151-155.
45. 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.
46. Metzler M, Gertz A, Sarkar M, Schachter H, Schrader JW, Marth JD. 1994. Complex asparagine-linked oligosaccharides are required for morphogenic events during post-implantation development. EMBO J 13:2056-2065.
47. Meyers EN, Martin GR. 1999. Differences in left-right axis pathways in mouse and chick: functions of FGF8 and SHH. Science 285:403-406.
48. Mochizuki T, Saijoh Y, Tsuchiya K, Shirayoshi Y, Takai S, Taya C, Yonekawa H, Yamada K, Nihei H, Nakatsuji N, Overbeek PA, Hamada H, Yokoyama T. 1998. Cloning of inv, a gene that controls left/right asymmetry and kidney development. Nature 395: 177-181.
49. Morgan D, Turnpenny L, Goodship J, Dai W, Majumder K, Matthews L, Gardner A, Schuster G, Vien L, Harrison W, Elder FF, Penman-Splitt M, Overbeek P, Strachan T. 1998. Inversin, a novel gene in the vertebrate left-right axis pathway, is partially deleted in the inv mouse [published erratum appears in Nat Genet 1998;20(3):312]. Nat Genet 20:149-156.
50. Morris RL, Scholey JM. 1997. Heterotrimeric kinesin-II is required for the assembly of motile 9 + 2 ciliary axonemes on sea urchin embryos. J Cell Biol 138:1009-1022.
51. 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.
52. Nascone N, Mercola M. 1997. Organizer induction determines left-right asymmetry in Xenopus. Dev Biol 189:68-78.
53. Nomura M, Li E. 1998. Smad2 role in mesoderm formation, left-right patterning and craniofacial development [see Comments]. Nature 393:786-790.
54. 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 [published erratum appears in Cell 1999;99(1):117]. Cell 95: 829-837.
55. Oh SP, Li E. 1997. The signaling pathway mediated by the type IIB activin receptor controls axial patterning and lateral asymmetry in the mouse. Genes Dev 11:1812-1826.
56. 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.
57. Pazour GJDB, Vucica Y, Seeley ES, Rosenbaum JL, Witman GB, Cole DG. 2000. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J Cell Biol 151:709-718.
58. Pennarun G, Escudier E, Chapelin C, Bridoux AM, Cacheux V, Roger G, Clement A, Goossens M, Amselem S, Duriez B. 1999. Loss-of-function mutations in a human gene related to Chlamydomonas reinhardtii dynein IC78 result in primary ciliary dyskinesia. Am J Hum Genet 65:1508-1519.
59. Rankin CT, Bunton T, Lawler AM, Lee SJ. 2000. Regulation of left-right patterning in mice by growth/differentiation factor-1. Nat Genet 24:262-265.
60. Ryan AK, Blumberg B, Rodriguez-Esteban C, Yonei-Tamura S, Tamura K, Tsukui T, de la Pena J, Sabbagh W, Greenwald J, Choe S, Norris DP, Robertson EJ, Evans RM, Rosenfeld MG, Izpisua Belmonte JC. 1998. Pitx2 determines left-right asymmetry of internal organs in vertebrates. Nature 394:545-551.
61. Schneider A, Mijalski T, Schlange T, Dai W, Overbeek P, Arnold HH, Brand T. 1999. The homeobox gene NKX3.2 is a target of left-right signalling and is expressed on opposite sides in chick and mouse embryos. Curr Biol 9:911-914.
62. Sefton M, Sanchez S, Nieto MA. 1998. Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo. Development 125:3111-3121.
63. Semina EV, Reiter R, Leysens NJ, Alward WL, Small KW, Datson NA, Siegel-Bartelt J, Bierke-Nelson D, Bitoun P, Zabel BU, Carey JC, Murray JC. 1996. Cloning and characterization of a novel bicoid-related homeobox transcription factor gene, RIEG, involved in Rieger syndrome. Nat Genet 14:392-399.
64. Sun X, Meyers EN, Lewandoski M, Martin GR. 1999. Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev 13:1834-1846.
65. 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 asym-metries. Development 126:5495-5504.
66. Supp DM, Witte DP, Potter SS, Brueckner M. 1997. Mutation of an axonemal dynein affects left-right asymmetry in inversus viscerum mice. Nature 389:963-966.
67. 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.
68. 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.
69. 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.
70. Yamazaki H, Nakata T, Okada Y, Hirokawa N. 1995. KIF3A/B: a heterodimeric kinesin superfamily protein that works as a microtubule plus end-directed motor for membrane organelle transport. J Cell Biol 130:1387-1399.
71. Yan YT, Gritsman K, Ding J, Burdine RD, Corrales JD, Price SM, Talbot WS, Schier AF, Shen MM. 1999. Conserved requirement for EGF-CFC genes in vertebrate left-right axis formation. Genes Dev 13:2527-2537.
72. Yashiro K, Saijoh Y, Sakuma R, Tada M, Tomita N, Amano K, Matsuda Y, Monden M, Okada S, Hamada H. 2000. Distinct transcriptional regulation and phylogenetic divergence of human LEFTY genes. Genes Cells 5:343-357.
73. Yokoyama T, Copeland NG, Jenkins NA, Montgomery CA, Elder FF, Overbeek PA. 1993. Reversal of left-right asymmetry: a situs inversus mutation [see Comments]. Science 260:679-682.