The embryonic myosin R672C mutation that underlies Freeman-Sheldon syndrome impairs cross-bridge detachment and cycling in adult skeletal muscle

Human Molecular Genetics

Volumn 24, Issue 12, 2015, Pages 3348-3358

  Racca, Alice W ^a   Beck, Anita E ^b,d   McMillin, Margaret J ^b   Steven Korte, F ^a   Bamshad, Michael J ^b,c,d   Regnier, Michael ^a,c  

^a University of Washington   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d SEATTLE CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; MYOSIN; MYOSIN HEAVY CHAIN; TAQ POLYMERASE; CALCIUM; CYTOSKELETON PROTEIN; MESSENGER RNA; MYH3 POLYPEPTIDE, HUMAN;

ADOLESCENT; ADULT; ANKLE; ARTHROGRYPOSIS; ARTICLE; ATPASE ACTIVITY ASSAY; BLOOD ANALYSIS; BODY POSTURE; CAMPTODACTYLY; CASE REPORT; CELL KINETICS; CLINICAL FEATURE; CONTROLLED STUDY; DEPRESSION; DISEASE DURATION; FAST MUSCLE; FEMALE; FLEXION CONTRACTURE; FOREARM; FREEMAN SHELDON SYNDROME; GENE MUTATION; HAND PALM; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MEDICAL HISTORY; MUSCLE BIOPSY; MUSCLE CELL; MUSCLE CONTRACTILITY; MUSCLE CONTRACTURE; MUSCLE FIBRIL; MYOFILAMENT; NASOLABIAL FOLD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PTOSIS; SCOLIOSIS; SKELETAL MUSCLE; WRIST DISEASE; CASE CONTROL STUDY; CELL CULTURE; CROUZON SYNDROME; GENE EXPRESSION; GENETICS; METABOLISM; MUSCLE CONTRACTION; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; CALCIUM; CASE-CONTROL STUDIES; CELLS, CULTURED; CRANIOFACIAL DYSOSTOSIS; CYTOSKELETAL PROTEINS; FEMALE; GENE EXPRESSION; HUMANS; MALE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MUTATION; MYOFIBRILS; MYOSINS; RNA, MESSENGER; YOUNG ADULT;

EID: 84929222109     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv084     Document Type: Article

References (68)

1. Yang, H.Y., Chung, C.S. and Nemechek, R.W. (1987) A genetic analysis of clubfoot in Hawaii. Genet. Epidemiol., 4, 299-306.
2. Wang, J.H., Palmer, R.M. and Chung, C.S. (1988) The role of major gene in clubfoot. Am. J. Hum. Genet., 42, 772-776.
3. Hall, J. (1992) Arthrogryposis. In Principles and Practice of Medical Genetics. Churchill Livingstone, Edinburgh, pp. 989-1035.
4. Rebbeck, T.R., Dietz, F.R., Murray, J.C. and Buetow, K.H. (1993) A single-gene explanation for the probability of having idiopathic talipes equinovarus. Am. J. Hum. Genet., 53, 1051-1063.
5. De Andrade, M., Barnholtz, J.S., Amos, C.I., Lochmiller, C., Scott, A., Risman, M. and Hecht, J.T. (1998) Segregation analysis of idiopathic talipes equinovarus in a Texan population. Am. J. Med. Genet., 79, 97-102.
6. Lochmiller, C., Johnston, D., Scott, A., Risman, M. and Hecht, J.T. (1998) Genetic epidemiology study of idiopathic talipes equinovarus. Am. J. Med. Genet., 79, 90-96.
7. Chapman, C., Stott, N.S., Port, R.V. and Nicol, R.O. (2000) Genetics of club foot in Maori and Pacific people. J. Med. Genet., 37, 680-683.
8. Honein, M.A., Paulozzi, L.J. and Moore, C.A. (2000) Family history, maternal smoking, and clubfoot: an indication of a geneenvironment interaction. Am. J. Epidemiol., 152, 658-665.
9. Dietz, F. (2002) The genetics of idiopathic clubfoot. Clin. Orthop. Relat. Res., 39-48.
10. Bale, J.R., Stoll, B.J. and Lucas, A.O., Committee on Improving Birth Outcomes (eds) (2003) Reducing Birth Defects: Meeting the Challenge in the Developing World. The National Academies Press, Washington, DC.
11. Bamshad, M., Jorde, L.B. and Carey, J.C. (1996) A revised and extended classification of the distal arthrogryposes. Am. J. Med. Genet., 65, 277-281.
12. Sung, S.S., Brassington, A.-M.E., Grannatt, K., Rutherford, A., Whitby, F.G., Krakowiak, P.A., Jorde, L.B., Carey, J.C. and Bamshad, M. (2003) Mutations in genes encoding fast-twitch contractile proteins cause distal arthrogryposis syndromes. Am. J. Hum. Genet., 72, 681-690.
13. Sung, S.S., Brassington, A.-M.E., Krakowiak, P.A., Carey, J.C., Jorde, L.B. and Bamshad, M. (2003) Mutations in TNNT3 cause multiple congenital contractures: a second locus for distal arthrogryposis type 2B. Am. J. Hum. Genet., 73, 212-214.
14. 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.
15. Toydemir, R.M., Chen, H., Proud, V.K., Martin, R., van Bokhoven, H., Hamel, B.C.J., 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., 140, 2387-2393.
16. Shrimpton, A.E. and Hoo, J.J. (2006) A TNNI2 mutation in a family with distal arthrogryposis type 2B. Eur. J. Med. Genet., 49, 201-206.
17. Jiang, M., Zhao, X., Han,W., Bian, C., Li, X.,Wang, G., Ao, Y., Li, Y., Yi, D., Zhe, Y. et al. (2006) A novel deletion in TNNI2 causes distal arthrogryposis in a large Chinese family with marked variability of expression. Hum. Genet., 120, 238-242.
18. Kimber, E., Tajsharghi, H., Kroksmark, A.-K., Oldfors, A. and Tulinius, M. (2006) A mutation in the fast skeletal muscle troponin I gene causes myopathy and distal arthrogryposis. Neurology, 67, 597-601.
19. Tajsharghi, H., Kimber, E., Kroksmark, A.-K., Jerre, R., Tulinius, M. and Oldfors, A. (2008) Embryonic myosin heavy-chain mutations cause distal arthrogryposis and developmental myosin myopathy that persists postnatally. Arch. Neurol., 65, 1083-1090.
20. Tajsharghi, H., Kimber, E., Holmgren, D., Tulinius, M. and Oldfors, A. (2007) Distal arthrogryposis and muscleweakness associated with a beta-tropomyosin mutation. Neurology, 68, 772-775.
21. 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.
22. Gurnett, C.A., Desruisseau, D.M., McCall, K., Choi, R., Meyer, Z.I., Talerico, M., Miller, S.E., Ju, J.-S., Pestronk, A., Connolly, A.M. et al. (2010) Myosin binding protein C1: a novel gene for autosomal dominant distal arthrogryposis type 1. Hum. Mol. Genet., 19, 1165-1173.
23. Robinson, P., Lipscomb, S., Preston, L.C., Altin, E.,Watkins, H., Ashley, C.C. and Redwood, C.S. (2007) Mutations in fast skeletal troponin I, troponin T, and beta-tropomyosin that cause distal arthrogryposis all increase contractile function. FASEB J. Off. Publ. Fed. Am. Soc. Exp. Biol., 21, 896-905.
24. Ochala, J., Li, M., Tajsharghi, H., Kimber, E., Tulinius, M., Oldfors, A. and Larsson, L. (2007) Effects of a R133W beta-tropomyosin mutation on regulation of muscle contraction in single human muscle fibres. J. Physiol., 581, 1283-1292.
25. Ackermann, M.A., Patel, P.D., Valenti, J., Takagi, Y., Homsher, E., Sellers, J.R. and Kontrogianni-Konstantopoulos, A. (2013) Loss of actomyosin regulation in distal arthrogryposis myopathy due to mutant myosin binding protein-C slow. FASEB J., 27, 3217-3228.
26. Beck, A.E., McMillin, M.J., Gildersleeve, H., Kezele, P., Shively, J., Carey, J.C., Regnier, M. and Bamshad, M.J. (2013) Spectrum of mutations that cause distal arthrogryposis types 1 and 2B. Am. J. Med. Genet., 161A, 550-555.
27. Ochala, J. (2008) Thin filament proteins mutations associated with skeletal myopathies: defective regulation of muscle contraction. J. Mol. Med., 86, 1197-1204.
28. Silberstein, L., Webster, S.G., Travis, M. and Blau, H.M. (1986) Developmental progression of myosin gene expression in cultured muscle cells. Cell, 46, 1075-1081.
29. Webster, C., Silberstein, L., Hays, A.P. and Blau, H.M. (1988) Fast muscle fibers are preferentially affected in Duchenne muscular dystrophy. Cell, 52, 503-513.
30. Gambke, B. and Rubinstein, N.A. (1984) A monoclonal antibody to the embryonic myosin heavy chain of rat skeletal muscle. J. Biol. Chem., 259, 12092-12100.
31. Racca, A.W., Beck, A.E., Rao, V.S., Flint, G.V., Lundy, S.D., Born, D.E., Bamshad, M.J. and Regnier, M. (2013) Contractility and kinetics of human fetal and human adult skeletal muscle. J. Physiol., 591, 3049-3061.
32. Resnicow, D.I., Deacon, J.C., Warrick, H.M., Spudich, J.A. and Leinwand, L.A. (2010) Functional diversity among a family of human skeletal muscle myosin motors. Proc. Natl. Acad. Sci. USA, 107, 1053-1058.
33. Brenner, B. and Yu, L.C. (1991) Characterization of radial force and radial stiffness in Ca(2+)-activated skinned fibres of the rabbit psoas muscle. J. Physiol., 441, 703-718.
34. Williams, C.D., Regnier, M. and Daniel, T.L. (2010) Axial and radial forces of cross-bridges depend on lattice spacing. PLoS Comput. Biol., 6, e1001018.
35. West, J.M., Barclay, C.J., Luff, A.R. andWalker, D.W. (1999) Developmental changes in the activation properties and ultrastructure of fast- and slow-twitch muscles from fetal sheep. J. Muscle Res. Cell Motil., 20, 249-264.
36. Tesi, C., Piroddi, N., Colomo, F. and Poggesi, C. (2002) Relaxation kinetics following sudden Ca(2+) reduction in single myofibrils from skeletal muscle. Biophys. J., 83, 2142-2151.
37. Stehle, R., Krüger, M. and Pfitzer, G. (2002) Force kinetics and individual sarcomere dynamics in cardiac myofibrils after rapid ca(2+) changes. Biophys. J., 83, 2152-2161.
38. Poggesi, C., Tesi, C. and Stehle, R. (2005) Sarcomeric determinants of striated muscle relaxation kinetics. Pflüg. Arch. Eur. J. Physiol., 449, 505-517.
39. Morgan, D.L. and Proske, U. (2006) Sarcomere popping requires stretch over a range where total tension decreases with length. J. Physiol., 574, 627-628.
40. Cuda, G., Pate, E., Cooke, R. and Sellers, J.R. (1997) In vitro actin filament sliding velocities produced by mixtures of different types of myosin. Biophys. J., 72, 1767-1779.
41. Herron, T.J., Korte, F.S. and McDonald, K.S. (2001) Loaded shortening and power output in cardiac myocytes are dependent on myosin heavy chain isoform expression. Am. J. Physiol. Heart Circ. Physiol., 281, H1217-H1222.
42. Kreutziger, K.L., Piroddi, N., McMichael, J.T., Tesi, C., Poggesi, C. and Regnier, M. (2011) Calcium binding kinetics of troponin C strongly modulate cooperative activation and tension kinetics in cardiac muscle. J. Mol. Cell. Cardiol., 50, 165-174.
43. Ochala, J., Li, M., Ohlsson, M., Oldfors, A. and Larsson, L. (2008) Defective regulation of contractile function in muscle fibres carrying an E41K beta-tropomyosin mutation. J. Physiol., 586, 2993-3004.
44. Fyrberg, E., Fyrberg, C.C., Beall, C. and Saville, D.L. (1990) Drosophila melanogaster troponin-T mutations engender three distinct syndromes of myofibrillar abnormalities. J. Mol. Biol., 216, 657-675.
45. Moreno-Gonzalez, A., Korte, F.S., Dai, J., Chen, K., Ho, B., Reinecke, H., Murry, C.E. and Regnier, M. (2009) Cell therapy enhances function of remote non-infarcted myocardium. J. Mol. Cell. Cardiol., 47, 603-613.
46. Regnier, M., Rivera, A.J., Chase, P.B., Smillie, L.B. and Sorenson, M.M. (1999) Regulation of skeletal muscle tension redevelopment by troponin C constructs with different Ca2+ affinities. Biophys. J., 76, 2664-2672.
47. Feest, E.R., Steven Korte, F., Tu, A.-Y., Dai, J., Razumova, M.V., Murry, C.E. and Regnier, M. (2014) Thin filament incorporation of an engineered cardiac troponin C variant (L48Q) enhances contractility in intact cardiomyocytes from healthy and infarcted hearts. J. Mol. Cell. Cardiol., 72, 219-227.
48. Korte, F.S., Dai, J., Buckley, K., Feest, E.R., Adamek, N., Geeves, M.A., Murry, C.E. and Regnier, M. (2011) Upregulation of cardiomyocyte ribonucleotide reductase increases intracellular 2 deoxy-ATP, contractility, and relaxation. J. Mol. Cell. Cardiol., 51, 894-901.
49. Nowakowski, S.G., Kolwicz, S.C., Korte, F.S., Luo, Z., Robinson-Hamm, J.N., Page, J.L., Brozovich, F., Weiss, R.S., Tian, R., Murry, C.E. et al. (2013) Transgenic overexpression of ribonucleotide reductase improves cardiac performance. Proc. Natl. Acad. Sci. USA, 110, 6187-6192.
50. Regnier, M. and Homsher, E. (1998) The effect of ATP analogs on posthydrolytic and force development steps in skinned skeletal muscle fibers. Biophys. J., 74, 3059-3071.
51. Regnier, M., Martyn, D.A. and Chase, P.B. (1998) Calcium regulation of tension redevelopment kinetics with 2-deoxy-ATP or low [ATP] in rabbit skeletal muscle. Biophys. J., 74, 2005-2015.
52. Regnier, M., Rivera, A.J., Chen, Y. and Chase, P.B. (2000) 2-Deoxy-ATP enhances contractility of rat cardiac muscle. Circ. Res., 86, 1211-1217.
53. Stevenson, D.A., Carey, J.C., Palumbos, J., Rutherford, A., Dolcourt, J. and Bamshad, M.J. (2006) Clinical characteristics and natural history of Freeman-Sheldon syndrome. Pediatrics, 117, 754-762.
54. Beck, A.E., McMillin, M.J., Gildersleeve, H.I.S., Shively, K.M.B., Tang, A. and Bamshad, M.J. (2014) Genotype-phenotype relationships in Freeman-Sheldon syndrome. Am. J. Med. Genet., 164, 2808-2813.
55. Butler-Browne, G.S. and Whalen, R.G. (1984) Myosin isozyme transitions occurring during the postnatal development of the rat soleus muscle. Dev. Biol., 102, 324-334.
56. Regnier, M., Martyn, D.A. and Chase, P.B. (1996) Calmidazolium alters Ca2+ regulation of tension redevelopment rate in skinned skeletal muscle. Biophys. J., 71, 2786-2794.
57. Ottenheijm, C.A.C.,Witt, C.C., Stienen, G.J., Labeit, S., Beggs, A. H. and Granzier, H. (2009) Thin filament length dysregulation contributes to muscle weakness in nemaline myopathy patients with nebulin deficiency. Hum. Mol. Genet., 18, 2359-2369.
58. Brenner, B. (1983) Technique for stabilizing the striation pattern in maximally calcium-activated skinned rabbit psoas fibers. Biophys. J., 41, 99-102.
59. Regnier, M., Morris, C. and Homsher, E. (1995) Regulation of the cross-bridge transition from a weakly to strongly bound state in skinned rabbit muscle fibers. Am. J. Physiol., 269, C1532-C1539.
60. Matsubara, I., Umazume, Y. and Yagi, N. (1985) Lateral filamentary spacing in chemically skinned murine muscles during contraction. J. Physiol., 360, 135-148.
61. Martyn, D.A. and Gordon, A.M. (1988) Length and myofilament spacing-dependent changes in calcium sensitivity of skeletal fibres: effects of pH and ionic strength. J. Muscle Res. Cell Motil., 9, 428-445.
62. Brenner, B. and Eisenberg, E. (1986) Rate of force generation in muscle: correlation with actomyosin ATPase activity in solution. Proc. Natl. Acad. Sci. USA, 83, 3542-3546.
63. Colomo, F., Piroddi, N., Poggesi, C., te Kronnie, G. and Tesi, C. (1997) Active and passive forces of isolated myofibrils from cardiac and fast skeletal muscle of the frog. J. Physiol., 500, 535-548.
64. Kreutziger, K.L., Piroddi, N., Scellini, B., Tesi, C., Poggesi, C. and Regnier, M. (2008) Thin filament Ca2+ binding properties and regulatory unit interactions alter kinetics of tension development and relaxation in rabbit skeletal muscle. J. Physiol., 586, 3683-3700.
65. Colomo, F., Nencini, S., Piroddi, N., Poggesi, C. and Tesi, C. (1998) Calcium dependence of the apparent rate of force generation in single striated muscle myofibrils activated by rapid solution changes. Adv. Exp. Med. Biol., 453, 373-382.
66. Tesi, C., Colomo, F., Nencini, S., Piroddi, N. and Poggesi, C. (2000) The effect of inorganic phosphate on force generation in single myofibrils fromrabbit skeletal muscle. Biophys. J., 78, 3081-3092.
67. Brandt, P.W., Colomo, F., Piroddi, N., Poggesi, C. and Tesi, C. (1998) Force regulation by Ca2+ in skinned single cardiac myocytes of frog. Biophys. J., 74, 1994-2004.
68. Dubowitz, V. and Sewry, C.A. (2007) Muscle Biopsy: A Practical Approach, 3rd ed. Elsevier Health Sciences, Philadelphia, PA.