Shells and heart: Are human laterality and chirality of snails controlled by the same maternal genes?

American Journal of Medical Genetics, Part A

Volumn 152 A, Issue 10, 2010, Pages 2419-2425

  Oliverio, Marco ^a   Digilio, Maria Cristina ^b   Versacci, Paolo ^c   Dallapiccola, Bruno ^b   Marino, Bruno ^c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Chirality; Maternal effect; Nodal; Situs ambiguus; Situs inversus; Situs solitus

Indexed keywords

LEFT RIGHT DETERMINATION FACTOR; PROTEIN NODAL; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR PITX2;

ASCIDIACEA; CHIRALITY; CONGENITAL HEART MALFORMATION; EMBRYO DEVELOPMENT; GENE CONTROL; GENE EXPRESSION; GENE IDENTIFICATION; GENE MUTATION; GENETIC CONSERVATION; HOMOZYGOSITY; HUMAN; NONHUMAN; ORTHOLOGY; PHENOTYPE; PRIORITY JOURNAL; RECURRENT ABORTION; REVIEW; SEA URCHIN; SIBLING; SIGNAL TRANSDUCTION; SNAIL; SPECIES DIFFERENCE; SYNAPOMORPHY; ANIMAL; FEMALE; GENETICS; HEMISPHERIC DOMINANCE; MALE; MESODERM; MORPHOGENESIS; MOUSE; NUCLEOTIDE SEQUENCE; PEDIGREE; PHYSIOLOGY; SITUS INVERSUS;

ANIMALIA; ASCIDIACEA; BILATERIA; ECHINOIDEA; GASTROPODA;

ANIMALS; BODY PATTERNING; CONSERVED SEQUENCE; FEMALE; FUNCTIONAL LATERALITY; HEART DEFECTS, CONGENITAL; HUMANS; MALE; MESODERM; MICE; PEDIGREE; SIGNAL TRANSDUCTION; SITUS INVERSUS; SNAILS;

EID: 78349252289     PISSN: 15524825     EISSN: 15524833     Source Type: Journal    
DOI: 10.1002/ajmg.a.33655     Document Type: Review

References (64)

1. Afzelius BA. 1976. A human syndrome caused by immotile cilia. Science 193: 317-319.
2. Asami T. 1993. Genetic variation and evolution of coiling chirality in snails. Forma 8: 263-276.
3. Asami T, Gittenberger E, Falkner G. 2008. Whole-body enantiomorphy and maternal inheritance of chiral reversal in the pond snail Lymnaea stagnalis. J Hered 99: 552-557.
4. Bajolle F, Zaffran S, Kelly RG, Hadchouel J, Bonnet D, Brown NA, Buckingham ME. 2006. Rotation of the myocardial wall of the outflow tract is implicated in the normal positioning of the great arteries. Circ Res 98: 421-428.
5. Bamford RN, Roessler E, Burdine RD, Saplakoǧlu U, dela Cruz J, Splitt M, Goodship JA, Towbin J, Bowers P, Ferrero GB, 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.
6. Bisgrove BW, Yost HJ. 2001. Classification of left-right patterning defects in zebrafish, mice, and humans. Am J Med Genet 101: 315-323.
7. Boorman CJ, Shimeld SM. 2002. Pitx homeobox genes in Ciona and amphioxus show left-right asymmetry is a conserved chordate character and define the ascidian adenohypophysis. Evol Dev 4: 354-365.
8. Brusca RC, Brusca GJ. 2003. Invertebrates. 2nd edition. Sunderland, Massachusetts: Sinauer Associates, Inc. p 895.
9. Carroll SB, Grenier JK, Weatherbee SD. 2001. From DNA to diversity: Molecular genetics and the evolution of animal design. Malden, Massachusetts: Blackwell; p 214.
10. Christiaen L, Bourrat F, Joly JS. 2005. A modular cis-regulatory system controls isoform-specific pitx expression in ascidian stomodaeum. Dev Biol 277: 557-566.
11. Cipollone D, Amati F, Carsetti R, Placidi S, Biancolella M, D'Amati G, Novelli G, Siracusa G, Marino B. 2006. A multiple retinoic acid antagonist induces conotruncal anomalies, including transposition of the great arteries, in mice. Cardiovasc Pathol 15: 194-202.
12. Conlon FL, Barth KS, Robertson EJ. 1991. A novel retrovirally induced embryonic lethal mutation in the mouse: Assessment of the developmental fate of embryonic stem cells homozygous for the 413.d proviral insertion. Development 111: 969-981.
13. 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.
14. De Luca A, Sarkozy A, Consoli F, Ferese R, Guida V, Dentici ML, Mingarelli R, Bellacchio E, Tuo G, Limongelli G, Digilio MC, Marino B, Dallapiccola B. 2010. Familial transposition of great arteries caused by multiple mutations in laterality genes. Heart 96: 673-677.
15. Devriendt K, Casaer A, Van Cauter A, de Zegher F, Dumoulin M, Gewillig M, Devlieger H. 1994. Asplenia syndrome and isolated total anomalous pulmonary venous connection in siblings. Eur J Pediatr 153: 712-714.
16. Digilio MC, Casey B, Toscano A, Calabrò R, Pacileo G, Marasini M, Banaudi E, Giannotti A, Dallapiccola B, Marino B. 2001. Complete transposition of the great arteries patterns of congenital heart disease in familial precurrence. Circulation 104: 2809-2814.
17. Duboc V, Lepage TA. 2008. Conserved role for the nodal signaling pathway in the establishment of dorso-ventral and left-right axes in deuterostomes. J Exper Zool (Mol Dev Evol) 310B: 41-53.
18. Duboc V, Rottinger E, Lapraz F, Besnardeau L, Lepage T. 2005. Left-right asymmetry in the sea urchin embryo is regulated by nodal signaling on the right side. Dev Cell 9: 147-158.
19. Ehlers KH, Engle MA. 1996. Familial congenital heart disease. I. Genetic and environmeltal factors. Circulation 34: 503-516.
20. Ferrero GB, Gebbia M, Pilia G, Witte D, Peyer A, Hopkin RJ, Craigen WJ, Schaffer 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.
21. Freeman G, Lundelius J. 1982. The developmental genetics of dextrality and sinistrality in the gastropod Lymnaea peregra. Roux's Arch Dev Biol 191: 69-83.
22. Goldmuntz E, Bamford R, Karkera JD, dela Cruz J, Roessler E, Muenke M. 2002. CFC1 mutations in patients with transposition of the great arteries and double-outlet right ventricle. Am J Hum Genet 70: 776-780.
23. Goor DA, Edwards JE. 1973. The spectrum of transposition of the great arteries: With specific reference to developmental anatomy of the conus. Circulation 48: 406-415.
24. Grande C, Patel NH. 2009. Nodal signalling is involved in left-right asymmetry in snails. Nature 457: 1007-1011.
25. Hamada H, Meno C, Watanabe D, Saijoh Y. 2002. Establishment of vertebrate left-right asymmetry. Nat Rev Genet 3: 103-113.
26. Hierck BP, Witte B, Poelmann RE, Gittenberger-de Groot AC, Gittenberger E. 2005. Chirality in snails is determined by highly conserved asymmetry genes. J Molluscan Stud 71: 192-195.
27. Hozumi S, Maeda R, Taniguchi K, Kanai M, Shirakabe S, Sasamura T, Speder P, Noselli S, Aigaki T, Murakami R, Matsuno K. 2006. An unconventional myosin in Drosophila reverses the default handedness in visceral organs. Nature 440: 798-802.
28. Hurwitz RC, Caskey CT. 1982. Ivemark syndrome in siblings. Clin Genet 22: 7-11.
29. 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.
30. 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.
31. Kuroda R, Endo B, Abe M, Shimizu M. 2009. Chiral blastomere arrangement dictates zygotic left-right asymmetry pathway in snails. Nature 462: 790-795.
32. Levin M. 2005. Left-right asymmetry in embryonic development: A comprehensive review. Mech Dev 122: 3-25.
33. Levin M, Johnson RL, Stern CD, Kuehn M, Tabin C. 1995. A molecular pathway determining left-right asymmetry in chick embryogenesis. Cell 82: 801-814.
34. Lin AE, Ticho BA, Houde K, Westgate M-N, Holmes LB. 2000. Heterotaxy: Associated conditions and hospital-based prevalence in newborns. Genet Med 2: 157-172.
35. 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. Nature 381: 158-161.
36. Marino B, Corno AF. 2003. Spiral pattern: Universe, normal heart, and complex congenital defects. J Thorac Cardiovasc Surg 126: 1225-1226.
37. Marino B, Capolino R, Digilio MC, Di Donato R. 2002a. Transposition of the great arteries in asplenia and polysplenia phenotypes. Am J Med Genet 110: 292-294.
38. Marino B, Digilio MC, Versacci P, Anaclerio S, Dallapiccola B. 2002b. Transposition of great arteries. Understanding its pathogenesis. Ital Heart J Suppl 3: 154-160.
39. Mohapatra B, Casey B, Li H, Ho-Dawson T, Smith L, Fernbach SD, Molinari L, Niesh SR, Jefferies JL, Craigen WJ, Towbin JA, Belmont JW, Ware SM. 2009. Identification and functional characterization of NODAL rare variants in heterotaxy and isolated cardiovascular malformations. Hum Mol Genet 18: 861-871.
40. Morokuma J, Ueno M, Kawanishi H, Saiga H, Nishida H. 2002. HrNodal, the ascidian nodal-related gene, is expressed in the left side of the epidermis, and lies upstream of HrPitx. Dev Genes Evol 212: 439-446.
41. Nakamura T, Mine N, Nakaguchi E, Mochizuki A, Yanamoto M, Yashiro K, Meno C, Hamada H. 2006. Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateral-inhibition. Syst Dev Cell 11: 495-504.
42. Niikawa N, Kohsaka S, Mizumoto M, Hamada I, Kaji T. 1983. Familial clustering of situs inversus totalis, and asplenia and polysplenia syndromes. Am J Med Genet 16: 43-47.
43. Nora JJ, Nora AH. 1987. Maternal transmission of congenital heart disease: New recurrence risk figures and the question of cytoplasmic inheritance and vulnerability to teratogens. Am J Cardiol 59: 459-465.
44. Nora JJ, Berg K, Nora AH. 1991. Cardiovascular diseases. Genetics, epidemiology, and prevention. New York: Oxford University Press.
45. 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.
46. Okumura T, Utsuno H, Kuroda J, Gittenberger E, Asami T, Matsuno K. 2008. The development and evolution of left-right asymmetry in invertebrates: Lessons from Drosophila and snails. Dev Dyn 237: 3497-3515.
47. Øyen N, Poulsen G, Boyd HA, Wohlfahrt J, Jensen PKA, Melbye M. 2009. Recurrence of congenital heart defects in families. Circulation 120: 295-301.
48. Palmer RA. 2004. Symmetry breaking and the evolution of development. Science 306: 828-833.
49. Peeters H, Devriendt P. 2006. Human laterality disorders. Eur J Med Genet 49: 349-362.
50. Richardson MK. 1995. Heterochrony and the phylotypic period. Dev Biol 172: 412-421.
51. Roessler E, Ouspenskaia MV, Karkera JD, Vélez JI, Kantipong A, Lacbawan F, Bowers P, Belmont JW, Towbin JA, Goldmuntz E, Feldman B, Muenke M. 2008. Reduced NODAL signaling strength via mutation of several pathway members including FOXH1 is linked to human heart defects and holoprosencephaly. Am J Hum Genet 83: 18-29.
52. Ruppert EE, Fox RS, Barnes RD. 2004. Invertebrate zoology: A functional evolutionary approach. 7th edition. Belmont, California: Brooks/Cole Thompson Learning. XVII+ 962+I-26 pp.
53. Schier AF. 2003. Nodal signaling in vertebrate development. Annu Rev Cell Dev Biol 19: 589-621.
54. Shibazaki Y, Shimizu M, Kuroda R. 2004. Body handedness is directed by genetically determined cytoskeletal dynamics in the early embryo. Curr Biol 14: 1462-1467.
55. Shilthuizen M, Davison A. 2005. The convoluted evolution of snail chirality. Naturwissenschaften 92: 504-515.
56. Sturtevant AH. 1923. Inheritance of direction of coiling in Limnaea. Science 58: 269-270.
57. Utsuno H, Asami T. 2010. Maternal inheritance of racemism in the terrestrial snail Bradybaena similaris. J Hered 101: 11-19.
58. Ware SM, Peng J, Zhu L, Fernbach S, Colicos S, Casey B, Towbin J, Belmont JW. 2004. Identification and functional analysis of ZIC3 mutations in heterotaxy and related congenital heart defects. Am J Hum Genet 74: 93-105.
59. Wood WB. 1997. Left-right asymmetry in animal development. Annu Rev Cell Dev Biol 13: 53-82.
60. Yasui H, Morishima M, Nakazawa M, Aikawa E. 1998. Anomalous looping, atrioventricular cushion dysplasia, and unilateral ventricular hypoplasia in the mouse embryos with right isomerism induced by retinoic acid. Anat Rec 250: 210-219.
61. Yoshida K, Saiga H. 2008. Left-right asymmetric expression of Pitx is regulated by the asymmetric Nodal signaling through an intronic enhancer in Ciona intestinalis. Dev Genes Evol 218: 353-360.
62. Yost HJ. 1999. Diverse initiation in a conserved left-right pathway? Curr Opin Gen Dev 9: 422-426.
63. Zhou X, Sasaki H, Lowe L, Hogan BLM, Kuehn MR. 1993. Nodal is a novel TGFβ-like gene expressed in the mouse node during gastrulation. Nature 361: 543-547.
64. Zlotogora J, Elian E. 1981. Asplenia and polysplenia syndromes with abnormalities of lateralisation in a sibship. J Med Genet 18: 301-302.