An MYH9 human disease model in flies: Site-directed mutagenesis of the Drosophila non-muscle myosin II results in hypomorphic alleles with dominant character

Human Molecular Genetics

Volumn 16, Issue 24, 2007, Pages 3160-3173

  Franke, Josef D ^a   Montague, Ruth A ^a   Rickoll, Wayne I ^b   Kiehart, Daniel P ^a  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF PUGET SOUND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN HEAVY CHAIN; MYOSIN II; MYOSIN IIA; MYOSIN IIB;

ALLELE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE INTERACTION; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR CLONING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SITE DIRECTED MUTAGENESIS; WILD TYPE;

ALLELES; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOOD PLATELET DISORDERS; CROSSES, GENETIC; DISEASE MODELS, ANIMAL; DROSOPHILA; DROSOPHILA PROTEINS; GENES, DOMINANT; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOLECULAR MOTOR PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MYOSIN HEAVY CHAINS; PHENOTYPE; SEQUENCE HOMOLOGY, AMINO ACID; TRANSGENES;

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 36248937191     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddm279     Document Type: Article

References (58)

1. Kelley, M.J., Jawien, W., Ortel, T.L. and Korczak, J.F. (2000) Mutation of MYR9, encoding non-muscle myosin heavy chain A, in May-Regglin anomaly. Nat. Genet., 26, 106-108.
2. Seri, M., Cusano, R., Gangarossa, S., Caridi, G., Bordo, D., Lo Nigro, C., Ghiggeri, G.M., Ravazzolo, R., Savino, M., Del Vecchio, M. et al. (2000) Mutations in MYH9 result in the May-Hegglin anomaly, and Fechtner and Sebastian syndromes. The May-Heggllin/Fechtner Syndrome Consortium. Nat. Genet., 26, 103-105.
3. Seri, M., Savino, M., Bordo, D., Cusano, R., Rocca, B., Meloni, I., Di Bari, F., Koivisto, P.A., Bolognesi, M., Gluggeri, G.M. et al. (2002) Epstein syndrome: Another renal disorder with mutations in the nonmuscle myosin heavy chain 9 gene. Hum. Genet., 110, 182-186.
4. Kunishima, S., Kojima, T., Matsushita, T., Tanaka, T., Tsurusawa, M., Furukawa, Y., Nakamura, Y., Okamura, T., Amemiya, N., Nakayama, T. et al. (2001) Mutations in the NMMHC-A gene cause autosomal dominant macrothrombocytopenia with leukocyte inclusions (May-Hegglin anomaly/ Sebastian syndrome). Blood, 97, 1147-1149.
5. Balduini, C.L., Iolascon, A. and Savoia, A. (2002) Inherited thrombocytopenias: From genes to therapy. Haematologica, 87, 860-880.
6. Seri, M., Pecci, A., Di Bari, F., Cusano, R., Savino, M., Panza, E., Nigro, A., Noris, P., Gangarossa, S., Rocca, B. et al. (2003) MYH9-Telated 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), 82, 203-215.
7. Mhatre, A.N., Kim, Y., Brodie, H.A. and Lalwani, A.K. (2003) Macrothrombocytopenia and progressive deafness is due to a mutation in MYH9. Otol. Neurotol., 24, 205-209.
8. Straussman, R., Squire, J.M., Ben-Ya'acov, A. and Ravid, S. (2005) Skip Residues and Charge Interactions in Myosin II Coiled-coils: Implications for Molecular Packing. J. Mol. Biol., 353, 613-628.
9. McLachlan, A.D. and Karn, J. (1982) Periodic charge distributions in the myosin rod amino acid sequence match cross-bridge spacings in muscle. Nature, 299, 226-231.
10. McLachlan, A.D. and Karn, J. (1983) Periodic features in the amino acid sequence of nematode myosin rod. J. Mol. Biol., 164, 605-626.
11. Atkinson, S.J. and Stewart, M. (1992) Molecular interactions in myosin assembly. Role of the 28-residue charge repeat in the rod. J. Mol. Biol., 226, 7-13.
12. Ikebe, M., Komatsu, S., Woodhead, J.L., Mabuchi, K., Ikebe, R., Saito, J., Craig, R. and Higashihara, M. (2001) The tip of the coiled-coil rod determines the filament formation of smooth muscle and nonmuscle myosin. J. Biol. Chem., 276, 30293-30300.
13. Dong, F., Li, S., Pujol-Moix, N., Luban, N.L., Shin, S.W., Seo, J.H., Ruiz-Saez, A., Demeter, J., Langdon, S. and Kelley, M.J. (2005) Genotype-phenotype correlation in MYH9-related thrombocytopenia. Br. J. Haematol., 130, 620-627.
14. Heath, K.E., Campos-Barros, A., Toren, A., Rozenfeld-Granot, G., Carlsson, L.E., Savige, J., Denison, J.C., Gregory, M.C., White, J.G., Barker, D.F. et al. (2001) Nonmuscle myosin heavy chain IIA mutations define a spectrum of autosomal dominant macrothrombocytopenias: May-Hegglin anomaly and Fechtner, Sebastian, Epstein, and Alport-like syndromes. Am. J. Hum. Genet., 69, 1033-1045.
15. Deutsch, S., Rideau, A., Bochaton-Piallat, M.L., Merla, G., Geinoz, A., Gabbiani, G, Schwede, T., Matthes, T., Antonarakis, S.E. and Beris, P. (2003) Asp1424Asn MYH9 mutation results in an unstable protein responsible for the phenotypes in May-Hegglin anomaly/Fechtner syndrome. Blood, 102, 529-534.
16. Pecci, A., Canobbio, I., Balduini, A., Stefanini, L., Cisterna, B., Marseglia, C., Noris, P., Savoia, A., Balduini, C.L. and Torti, M. (2005) Pathogenetic mechanisms of hematological abnormalities of patients with MYH9 mutations. Hum. Mol. Genet., 14, 3169-3178.
17. Hu, A., Wang, F. and Sellers, J.R. (2002) Mutations in human nonmuscle myosin IIA found in patients with May-Hegglin anomaly and Fechtner syndrome result in impaired enzymatic function. J. Biol. Chem., 277, 46512-46517.
18. Kim, K.Y., Kovacs, M., Kawamoto, S., Sellers, J.R. and Adelstein, R.S. (2005) Disease-associated mutations and alternative splicing alter the enzymatic and motile activity of nonmuscle myosins II-B and II-C. J. Biol. Chem., 280, 22769-22775.
19. Franke, J.D., Dong, F., Rickoll, W.L., Kelley, M.J. and Kiehart, D.P. (2005) Rod mutations associated with MYH9-related disorders disrupt nonmuscle myosin-IIA assembly. Blood, 105, 161-169.
20. Oldfors, A., Tajsharghi, H., Darin, N. and Lindberg, C. (2004) Myopathies associated with myosin heavy chain mutations. Acta Myol. 23, 90-96.
21. Kiehart, D.P., Lutz, M.S., Chan, D., Ketchum, A.S., Laymon, R.A., Nguyen, B. and Goldstein, L.S.B. (1989) Identification of the gene for fly non-muscle myosin heavy chain: Drosophila myosin heavy chains are encoded by a gene family. EMBO J, 8, 913-922.
22. Karess, R.E., Chang, X., Edwards, K.A., Kulkarni, S., Aguilera, I. and Kiehart, D.P. (1991) The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell, 65, 1177-1189.
23. Edwards, K.A., Chang, X.-J. and Kiehart, D.P. (1995) Essential light chain of Drosophila nonmuscle myosin II. J. Muscle Res. Cell Motil., 16, 491-498.
24. Barros, C.S, Phelps, C.B. and Brand, A.H. (2003) Drosophila nonmuscle myosin II promotes the asymmetric segregation of cell fate determinants by cortical exclusion rather than active transport. Dev. Cell, 5, 829-840.
25. Franke, J.D., Montague, R.A. and Kiehart, D.P. (2005) Nonmuscle Myosin II Generates Forces that Transmit Tension and Drive Contraction in Multiple Tissues during Dorsal Closure. Curr. Biol., 15, 2208-2221.
26. Bertet, C., Sulak, L. and Lecuit, t. (2004) Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature, 429, 667-671.
27. Edwards, K.A. and Kiehart, D.P. (1996) Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis. Development, 122, 1499-1511.
28. Halsell, S.R. and Kiehart, D.P. (1998) Second-site noncomplementation identities genomic regions required for Drosophila nonmuscle-myosin function during morphogenesis. Genetics, 148 1845-1863.
29. Hawley, R.S. and Walker, M.Y. (2003) Advanced Genetic Analysis: Finding Meaning in a Genome, Blackwell Science Ltd, Oxford.
30. Halsell, S.R., Chu, B. and Kiehart, D.P. (2000) Genetic analysis demonstrates a direct link between Rho signaling and nonmuscle myosin function during Drosophila morphogenesis. Genetics, 155 1253-1265.
31. Brand, A.H. and Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401-415.
32. Young, P.E., Richman, A.M., Ketchum, A.S. and Kiehart, D.P. (1993) Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev., 7, 29-41.
33. Stafford, W.F., III (1985) Effect of various anions on the stability of the coiled coil of skeletal muscle myosin. Biochemistry, 24, 3314-3321.
34. St Johnston, D. (2002) The art and dosign of genetic screens: Drosophila melanogaster. Nat. Rev. Genet., 3, 176-188.
35. Simon, M.A. (1994) Signal transduction during the development of the Drosophila R7 photoreceptor. Dev. Biol., 166, 431-442.
36. Takeda, K., Kishi, H., Ma, X., Yu, Z.X. and Adelstein, R.S. (2003) Ablation and mutation of nonmuscle myosin heavy chain II-B results in a defect in cardiac myocyte cytokinesis. Circ. Res., 93, 330-337.
37. Ma, X., Kawamoto, S., Hara, Y. and Adelstein, R.S. (2004) A point mutation in the motor domain of nonmuscle myosin II-B impairs migration of distinct groups of neurons. Mol. Biol. Cell, 15, 2568-2579.
38. Berg, J.S., Powell, B.C. and Cheney, R.E. (2001) A millennial myosin census. Mol. Biol. Cell, 12, 780-794.
39. Bejsovec, A. and Anderson, P. (1990) Functions of the myosin ATP and actin binding sites are required for C. elegans thick filament assembly. Cell, 60, 133-140.
40. Ketchum, A.S., Stewart, C.T., Stewart, M. and Kiehart, D.P. (1990) Complete sequence of the Drosophila nonmuscle myosin heavy-chain transcript: Conserved sequences in the myosin tail and differential splicing in the 5′ untranslated sequence. Proc. Natl Acad. Sci. USA 87, 6316-6320.
41. Brown, N.H. and Kafatos, P.C. (1988) Functional cDNA libraries from Drosophila embryos. J. Mol. Biol., 203, 425-437.
42. Ashburner, M. (1989) Drosophila, A Laboratory Handbook, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, p. 11724.
43. Kiehart, D., Galbraith, C., Edwards, K., Rickoll, W. and Montague, R. (2000) Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol., 149, 471-490.
44. Franke, J.D., Boury, A.L., Gerald, N.J. and Kiehart, D.P. (2006) Native nonmuscle myosin II stability and light chain binding in Drosophila melanogaster. Cell Motil. Cytoskeleton, 63, 604-622.
45. Kiehart, D.P. and Feghali, R. (1986) Cytoplasmic myosin from Drosophila melanogaster. J. Cell Biol., 103, 1517-1525.
46. Martinsson, T., Oldfors, A., Darin, N., Berg, K., Tajsharghi, H., Kyllerman, M. and Wahlstrom, J. (2000) Autosomal dominant myopathy: missense mutation (Glu-706 - > Lys) in the myosin heavy chain IIa gene. Proc. Natl Acad. Sci. USA, 97, 14614-14619.
47. Tajsharghi, H., Darin, N., Rekabdar, E., Kyllerman, M., Wahlstrom, J., Martinsson, T. and Oldfors, A. (2005) Mutations and sequence variation in the human myosin heavy chain IIa gene (MYH2). Eur. J. Hum. Genet. 13, 617-622.
48. Toydemir, R.M., Rutherford, A., Whitby, F.G., Jorde, L.B., Carey, J.C. and Bamshad, M.J. (2006) Mutations in embryonic myosin heavy chain (MYH3) cause Freeman-Sheldon syndrome and Sheldon-Hall syndrome. Nat. Genet., 38, 561-565.
49. Ching, Y.H., Ghosh, T.K., Cross, S.J., Packham, E.A., Honeyman, L., Loughna, S., Robinson, T.E., Dearlove, A.M., Ribas, G., Bonser, A.J. et al. (2005) Mutation in myosin heavy chain 6 causes atrial septal defect. Nat. Genet., 37, 423-428.
50. Carniel, E., Taylor, M.R., Sinagra, G., Di Lenarda, A., Ku, L., Fain, P.R., Boucek, M.M., Cavanaugh, J., Miocic, S., Slavov, D. et al. (2005) Alpha-myosin heavy chain: A sarcomeric gene associated with dilated and hypertrophic phenotypes of cardiomyopathy. Circulation 112, 54-59.
51. Tajsharghi, H., Thornell, L.E., Lindberg, C., Lindvall, B., Henriksson, K.G. and Oldfors, A. (2003) Myosin storage myopathy associated with a heterozygous missense mutation in MYH7. Ann. Neurol., 54, 494-500.
52. Kamisago, M., Sharma, S.D., DePalma, S.R., Solomon, S., Sharma, P., McDonough, B., Smoot, L., Mullen, M.P., Woolf, P.K., Wigle, E.D. et al. (2000) Mutations in sarcomere protein genes as a cause of dilated cardiomyopathy. N. Engl. J. Med., 343, 1688-1696.
53. Bohlega, S., Abu-Amero, S.N., Wakil, S.M., Carroll, P., Al-Amr, R., Lach, B., Al-Sayed, Y., Cupler, E.J. and Meyer, B.F. (2004) Mutation of the slow myosin heavy chain rod domain underlies hyaline body myopathy. Neurology, 62, 1518-1521.
54. Veugelers, M., Bressan, M., McDermott, D.A., Weremowicz, S., Morton, C.C., Mabry, C.C., Lefaivre, J.F., Zunamon, A., Destree, A., Chaudron, J.M. et al. (2004) Mutation of perinatal myosin heavy chain associated with a Carney complex variant. N. Engl. J. Med., 351 460-469.
55. Stevenson, D.A., Swoboda, K.J., Sanders, R.K. and Bamshad, M. (2006) A new distal arthrogryposis syndrome characterized by plantar flexion contractures. Am. J. Med. Genet. A, 140, 2797-2801.
56. Toydemir, R.M., Chen, H., Proud, V.K., Martin, R., van Bokhoven, H., Hamel, B.C., Tuerlings, J.H., Stratakis, C.A., Jorde, L.B. and Bamshad, M.J. (2006) Trismus-pseudocamptodactyly syndrome is caused by recurrent mutation of MYH8. Am. J. Med. Genet. A, 140, 2387-2393.
57. Zhu, L., Vranckx, R., Khau Van Kien, P., Lalande, A., Boisset, N., Mathieu F., Wegman, M., Glancy, L., Gasc, J.M., Brunotte, F. et al. (2006) Mutations in myosin heavy chain 11 cause a syndrome associating thoracic aortic aneurysm/aortic dissection and patent ductus arteriosus. Nat. Genet., 38, 343-349.
58. Donaudy, F., Snoeckx, R., Pfister, M., Zenner, H.P., Blin, N., Di Stazio, M., Ferrara, A., Lanzara, C., Ficarella, R., Declau, F. et al. (2004) 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., 74, 770-776.