A point mutation in myh10 causes major defects in heart development and body wall closure

Circulation: Cardiovascular Genetics

Volumn 7, Issue 3, 2014, Pages 257-265

  Ma, Xuefei ^a   Adelstein, Robert S ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Apoptosis; Cell adhesion; Diaphragmatic; Double outlet right ventricle; Ectopia cordis; Hernia; Nonmuscle myosin type IIA

Indexed keywords

MYOSIN IIB; MYOSIN HEAVY CHAIN; NONMUSCLE MYOSIN TYPE IIB HEAVY CHAIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ADHESION; CLEFT PALATE; CONGENITAL DIAPHRAGM HERNIA; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; ECTOPIA CORDIS; EMBRYO DEVELOPMENT; GENE; HEART DEVELOPMENT; MESENCHYME CELL; MOUSE; MUSCLE CELL; MYH10 GENE; NONHUMAN; OMPHALOCELE; POINT MUTATION; PRIORITY JOURNAL; ANIMAL; CONGENITAL MALFORMATION; EMBRYOLOGY; GENETICS; HEART; HEART VENTRICLE; HUMAN; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY;

ANIMALS; HEART; HEART DEFECTS, CONGENITAL; HEART VENTRICLES; HUMANS; MICE, KNOCKOUT; MYOSIN HEAVY CHAINS; NONMUSCLE MYOSIN TYPE IIB; POINT MUTATION;

EID: 84903581668     PISSN: 1942325X     EISSN: 19423268     Source Type: Journal    
DOI: 10.1161/CIRCGENETICS.113.000455     Document Type: Article

References (40)

1. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol. 2009;10:778-790.
2. Simons M, Wang M, McBride OW, Kawamoto S, Yamakawa K, Gdula D, et al. Human nonmuscle myosin heavy chains are encoded by two genes located on different chromosomes. Circ Res. 1991;69:530-539.
3. Toothaker LE, Gonzalez DA, Tung N, Lemons RS, Le Beau MM, Arnaout MA, et al. Cellular myosin heavy chain in human leukocytes: isolation of 5′ cDNA clones, characterization of the protein, chromosomal localization, and upregulation during myeloid differentiation. Blood. 1991;78:1826-1833.
4. Golomb E, Ma X, Jana SS, Preston YA, Kawamoto S, Shoham NG, et al. Identification and characterization of nonmuscle myosin II-C, a new member of the myosin II family. J Biol Chem. 2004;279:2800-2808.
5. Leal A, Endele S, Stengel C, Huehne K, Loetterle J, Barrantes R, et al. A novel myosin heavy chain gene in human chromosome 19q13.3. Gene. 2003;312:165-171.
6. Burt RA, Joseph JE, Milliken S, Collinge JE, Kile BT. Description of a novel mutation leading to MYH9-related disease. Thromb Res. 2008;122:861-863.
7. Seri M, Pecci A, Di Bari F, Cusano R, Savino M, Panza E, et al. MYH9-related disease: May-Hegglin anomaly, Sebastian syndrome, Fechtner syndrome, and Epstein syndrome are not distinct entities but represent a variable expression of a single illness. Medicine (Baltimore). 2003;82:203-215.
8. Donaudy F, Snoeckx R, Pfister M, Zenner HP, Blin N, Di Stazio M, et al. Nonmuscle myosin heavy-chain gene MYH14 is expressed in cochlea and mutated in patients affected by autosomal dominant hearing impairment (DFNA4). Am J Hum Genet. 2004;74:770-776.
9. Yang T, Pfister M, Blin N, Zenner HP, Pusch CM, Smith RJ. Genetic heterogeneity of deafness phenotypes linked to DFNA4. Am J Med Genet A. 2005;139:9-12.
10. Kim KY, Kovács M, Kawamoto S, Sellers JR, Adelstein RS. Diseaseassociated mutations and alternative splicing alter the enzymatic and motile activity of nonmuscle myosins II-B and II-C. J Biol Chem. 2005;280:22769-22775.
11. Ma X, Kovács M, Conti MA, Wang A, Zhang Y, Sellers JR, et al. Nonmuscle myosin II exerts tension but does not translocate actin in vertebrate cytokinesis. Proc Natl Acad Sci U S A. 2012;109:4509-4514.
12. Ma X, Kawamoto S, Hara Y, Adelstein RS. A point mutation in the motor domain of nonmuscle myosin II-B impairs migration of distinct groups of neurons. Mol Biol Cell. 2004;15:2568-2579.
13. Takeda K, Kishi H, Ma X, Yu ZX, Adelstein RS. Ablation and mutation of nonmuscle myosin heavy chain II-B results in a defect in cardiac myocyte cytokinesis. Circ Res. 2003;93:330-337.
14. Ma X, Bao J, Adelstein RS. Loss of cell adhesion causes hydrocephalus in nonmuscle myosin II-B-Ablated and mutated mice. Mol Biol Cell. 2007;18:2305-2312.
15. Cantrell JR, Haller JA, Ravitch MM. A syndrome of congenital defects involving the abdominal wall, sternum, diaphragm, pericardium, and heart. Surg Gynecol Obstet. 1958;107:602-614.
16. Tullio AN, Accili D, Ferrans VJ, Yu ZX, Takeda K, Grinberg A, et al. Nonmuscle myosin II-B is required for normal development of the mouse heart. Proc Natl Acad Sci U S A. 1997;94:12407-12412.
17. Bao J, Ma X, Liu C, Adelstein RS. Replacement of nonmuscle myosin II-B with II-A rescues brain but not cardiac defects in mice. J Biol Chem. 2007;282:22102-22111.
18. Engum SA. Embryology, sternal clefts, ectopia cordis, and Cantrell's pentalogy. Semin Pediatr Surg. 2008;17:154-160.
19. Gerashchenko BI, Murata-Hori M, Hosoya H. Myosin regulatory light chain as a critical substrate of cell death: a hypothesis. Med Hypotheses. 2000;54:850-852.
20. Mills JC, Stone NL, Erhardt J, Pittman RN. Apoptotic membrane blebbing is regulated by myosin light chain phosphorylation. J Cell Biol. 1998;140:627-636.
21. Solinet S, Vitale ML. Isoform B of myosin II heavy chain mediates actomyosin contractility during TNFalpha-induced apoptosis. J Cell Sci. 2008;121(Pt 10):1681-1692.
22. Young PE, Richman AM, Ketchum AS, Kiehart DP. Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 1993;7:29-41.
23. Ma X, Jana SS, Conti MA, Kawamoto S, Claycomb WC, Adelstein RS. Ablation of nonmuscle myosin II-B and II-C reveals a role for nonmuscle myosin II in cardiac myocyte karyokinesis. Mol Biol Cell. 2010;21:3952-3962.
24. van den Hoff MJ, Moorman AF, Ruijter JM, Lamers WH, Bennington RW, Markwald RR, et al. Myocardialization of the cardiac outflow tract. Dev Biol. 1999;212:477-490.
25. Sahai E, Marshall CJ. ROCK and Dia have opposing effects on adherens junctions downstream of Rho. Nat Cell Biol. 2002;4:408-415.
26. Sturge J, Wienke D, Isacke CM. Endosomes generate localized Rho-ROCK-MLC2-based contractile signals via Endo180 to promote adhesion disassembly. J Cell Biol. 2006;175:337-347.
27. Vicente-Manzanares M, Zareno J, Whitmore L, Choi CK, Horwitz AF. Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells. J Cell Biol. 2007;176:573-580.
28. Wei Q, Adelstein RS. Conditional expression of a truncated fragment of nonmuscle myosin II-A alters cell shape but not cytokinesis in HeLa cells. Mol Biol Cell. 2000;11:3617-3627.
29. Birnbaum S, Reutter H, Mende M, de Assis NA, Diaz-Lacava A, Herms S, et al. Further evidence for the involvement of MYH9 in the etiology of non-syndromic cleft lip with or without cleft palate. Eur J Oral Sci. 2009;117:200-203.
30. Chiquet BT, Hashmi SS, Henry R, Burt A, Mulliken JB, Stal S, et al. Genomic screening identifies novel linkages and provides further evidence for a role of MYH9 in nonsyndromic cleft lip and palate. Eur J Hum Genet. 2009;17:195-204.
31. Martinelli M, Di Stazio M, Scapoli L, Marchesini J, Di Bari F, Pezzetti F, et al. Cleft lip with or without cleft palate: implication of the heavy chain of non-muscle myosin IIA. J Med Genet. 2007;44:387-392.
32. Martinelli M, Arlotti M, Palmieri A, Scapoli L, Savoia A, Di Stazio M, et al. Investigation of MYH14 as a candidate gene in cleft lip with or without cleft palate. Eur J Oral Sci. 2008;116:287-290.
33. Conti MA, Even-Ram S, Liu C, Yamada KM, Adelstein RS. Defects in cell adhesion and the visceral endoderm following ablation of nonmuscle myosin heavy chain II-A in mice. J Biol Chem. 2004;279:41263-41266.
34. Shimizu Y, Thumkeo D, Keel J, Ishizaki T, Oshima H, Oshima M, et al. ROCK-I regulates closure of the eyelids and ventral body wall by inducing assembly of actomyosin bundles. J Cell Biol. 2005;168:941-953.
35. Doi T, Puri P, Bannigan J, Thompson J. Downregulation of ROCK-I and ROCK-II gene expression in the cadmium-induced ventral body wall defect chick model. Pediatr Surg Int. 2008;24:1297-1301.
36. Phillips HM, Murdoch JN, Chaudhry B, Copp AJ, Henderson DJ. Vangl2 acts via RhoA signaling to regulate polarized cell movements during development of the proximal outflow tract. Circ Res. 2005;96:292-299.
37. Qi CH, Zhao XQ, Ma D, Ma XJ, Zhou GM, Huang GY. Downregulation of Rho associated coiled-coil forming protein kinase 1 in the process of delayed myocardialization of cardiac proximal outflow tract septum in connexin 43 knockout mice embryo. Chin Med J (Engl). 2011;124:2021-2027.
38. Ivanov AI, Parkos CA, Nusrat A. Cytoskeletal regulation of epithelial barrier function during inflammation. Am J Pathol. 2010;177:512-524.
39. Ivanov AI, McCall IC, Parkos CA, Nusrat A. Role for actin filament turnover and a myosin II motor in cytoskeleton-driven disassembly of the epithelial apical junctional complex. Mol Biol Cell. 2004;15:2639-2651.
40. Tuzovic L, Yu L, Zeng W, Li X; Lu H, Lu HM, et al. A human de novo mutation in MYH10 phenocopies the loss of function mutation in mice. Rare Dis. 2013;1:e26144-1-e26144-5.