Skeletal muscle α-actin diseases (actinopathies): Pathology and mechanisms

Acta Neuropathologica

Volumn 125, Issue 1, 2013, Pages 19-32

  Nowak, Kristen J ^a,b   Ravenscroft, Gianina ^a,b   Laing, Nigel G ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b PATHWEST LABORATORY MEDICINE   (Australia)

Author keywords

Clinical phenotype; Future directions; Genetics; Pathobiology; Pathology; Skeletal muscle gene (ACTA1) diseases

Indexed keywords

ALPHA ACTININ 1; TYROSINE;

ACTIN FILAMENT AGGREGATE MYOPATHY; AUTOSOMAL DOMINANT DISORDER; AUTOSOMAL RECESSIVE DISORDER; CAP MYOPATHY; CELL AGGREGATION; CLINICAL FEATURE; CONGENITAL FIBRE TYPE DISPROPORTION; CORE LIKE AREA MYOPATHY; DYSTROPHIC MYOPATHY; FRAMESHIFT MUTATION; GENE; GENE THERAPY; HUMAN; INTRANUCLEAR ROD MYOPATHY; MINIMAL CHANGE MYOPATHY; MISSENSE MUTATION; MOLECULAR PATHOLOGY; MOSAICISM; MUSCLE BIOPSY; MYOPATHY; NEMALINE MYOPATHY; NONHUMAN; NONSENSE MUTATION; PRIORITY JOURNAL; REVIEW; SKELETAL MUSCLE ALPHA ACTININ 1 GENE; SKELETAL MUSCLE ALPHA ACTININ 1 GENE DISEASE; STOP CODON; ZEBRA BODY MYOPATHY;

ACTINS; ANIMALS; HUMANS; MUSCLE CONTRACTION; MUSCLE WEAKNESS; MUTATION; MYOPATHIES, NEMALINE; PHENOTYPE;

EID: 84872360566     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-012-1019-z     Document Type: Review

References (86)

1. Agrawal PB, Strickland CD, Midgett C, Morales A, Newburger DE et al (2004) Heterogeneity of nemaline myopathy cases with skeletal muscle alpha-actin gene mutations. Ann Neurol 56(1):86-96
2. Bauer DE, Orkin SH (2011) Update on fetal hemoglobin gene regulation in hemoglobinopathies. Curr Opin Pediatr 23(1):1-8
3. Beall CJ, Sepanski MA, Fyrberg EA (1989) Genetic dissection of Drosophila myofibril formation: effects of actin and myosin heavy chain null alleles. Gene Dev 3(2):131-140
4. Bing W, Razzaq A, Sparrow J, Marston S (1998) Tropomyosin and troponin regulation of wild type and E93K mutant actin filaments from Drosophila flight muscle. Charge reversal on actin changes actin-tropomyosin from on to off state. J Biol Chem 273(24):15016-15021
5. Bornemann A, Petersen MB, Schmalbruch H (1996) Fatal congenital myopathy with actin filament deposits. Acta Neuropathol 92(1):104-108
6. Clarke NF, Ilkovski B, Cooper S, Valova VA, Robinson PJ et al (2007) The pathogenesis of ACTA1-related congenital fiber type disproportion. Ann Neurol 61(6):552-561
7. Clarke NF, North KN (2003) Congenital fiber type disproportion-30 years on. J Neuropath Exp Neur 62(10):977-989
8. Conen PE, Murphy EG, Donohue WL (1963) Light and electron microscopic studies of "myogranules" in a child with hypotonia and muscle weakness. Canad Med Assoc J 89:983-986
9. Costa CF, Rommelaere H, Waterschoot D, Sethi KK, Nowak KJ et al (2004) Myopathy mutations in α-skeletal-muscle actin cause a range of molecular defects. J Cell Sci 117(15):3367-3377
10. Crawford K, Flick R, Close L, Shelly D, Paul R et al (2002) Mice lacking skeletal muscle actin show reduced muscle strength and growth deficits and die during the neonatal period. Mol Cell Biol 22(16):5887-5896
11. Cripps RM, Ball E, Stark M, Lawn A, Sparrow JC (1994) Recovery of dominant, autosomal flightless mutants of Drosophila melanogaster and identification of a new gene required for normal muscle structure and function. Genetics 137(1):151-164
12. D'Amico A, Graziano C, Pacileo G, Petrini S, Nowak KJ et al (2006) Fatal hypertrophic cardiomyopathy and nemaline myopathy associated with ACTA1 K336E mutation. Neuromuscular Disord 16(9-10):548-552
13. De Paula AM, Franques J, Fernandez C, Monnier N, Lunardi J et al (2009) A TPM3 mutation causing cap myopathy. Neuromuscular Disord 19(10):685-688
14. Domazetovska A, Ilkovski B, Cooper ST, Ghoddusi M, Hardeman EC et al (2007) Mechanisms underlying intranuclear rod formation. Brain 130(12):3275-3284
15. Domazetovska A, Ilkovski B, Kumar V, Valova VA, Vandebrouck A et al (2007) Intranuclear rod myopathy: molecular pathogenesis and mechanisms of weakness. Ann Neurol 62(6):597-608
16. dos Remedios CG, Chhabra D, Kekic M, Dedova IV, Tsubakihara M et al (2003) Actin binding proteins: regulation of cytoskeletal microfilaments. Physiol Rev 83(2):433-473
17. Drummond DR, Hennessey ES, Sparrow JC (1991) Characterisation of missense mutations in the Act88F gene of Drosophila melanogaster. Mol Gen Genet 226(1-2):70-80
18. Dubowitz V, Sewry CA (2007) Muscle biopsy: a practical approach, 3rd edn. Saunders Elsevier, Philadelphia
19. Feng JJ, Marston S (2009) Genotype-phenotype correlations in ACTA1 mutations that cause congenital myopathies. Neuromuscular Disord 19(1):6-16
20. Fidzianska A, Badurska B, Ryniewicz B, Dembek I (1981) "Cap disease": new congenital myopathy. Neurol 31(9):1113-1120
21. Goebel HH, Anderson JR, Hubner C, Oexle K, Warlo I (1997) Congenital myopathy with excess of thin myofilaments. Neuromuscular Disord 7:160-168
22. Goebel HH, Laing NG (2009) Actinopathies and myosinopathies. Brain Pathol 19(3):516-522
23. Goebel HH, Lenard HG (1992) Congenital myopathies. In: Rowland LP, DiMauro S (eds) Myopathies - handbook of clinical neurology, vol 18(62). Elsevier Science, Amsterdam, pp 331-367
24. Goebel HH, Piirso A, Warlo I, Schofer O, Kehr S et al (1997) Infantile intranuclear rod myopathy. J Child Neurol 12:22-30
25. Goebel HH, Warlo I (1997) Nemaline myopathy with intranuclear rods - intranuclear rod myopathy. Neuromuscular Disord 7:13-19
26. Haigh SE, Salvi SS, Sevdali M, Stark M, Goulding D et al (2010) Drosophila indirect flight muscle specific Act88F actin mutants as a model system for studying congenital myopathies of the human ACTA1 skeletal muscle actin gene. Neuromuscular Disord 20(6):363-374
27. Hennessey ES, Harrison A, Drummond DR, Sparrow JC (1992) Mutant actin: a dead end? J Musc Res Cell Motil 13:127-131
28. Hung RM, Yoon G, Hawkins CE, Halliday W, Biggar D et al (2010) Cap myopathy caused by a mutation of the skeletal alpha-actin gene ACTA1. Neuromuscular Disord 20(4):238-240
29. Hutchinson DO, Charlton A, Laing NG, Ilkovski B, North KN (2006) Autosomal dominant nemaline myopathy with intranuclear rods due to mutation of the skeletal muscle ACTA1 gene: clinical and pathological variability within a kindred. Neuromuscular Disord 16(2):113-121
30. Huxley AF, Niedergerke R (1954) Structural changes during contraction: interference microscopy of living muscle fibres. Nature 173:971-973
31. Ilkovski B, Clement S, Sewry C, North KN, Cooper ST (2005) Defining alpha-skeletal and alpha-cardiac actin expression in human heart and skeletal muscle explains the absence of cardiac involvement in ACTA1 nemaline myopathy. Neuromuscular Disord 15(12):829-835
32. Ilkovski B, Cooper ST, Nowak K, Ryan MM, Yang N et al (2001) Nemaline myopathy caused by mutations in the muscle α-skeletal-actin gene. Am J Hum Genet 68(6):1333-1343
33. Ilkovski B, Nowak KJ, Domazetovska A, Maxwell AL, Clement S et al (2004) Evidence for a dominant-negative effect in ACTA1 nemaline myopathy caused by abnormal folding, aggregation and altered polymerization of mutant actin isoforms. Hum Mol Genet 13(16):1727-1743
34. Jain RK, Jayawant S, Squier W, Muntoni F, Sewry CA et al (2012) Nemaline myopathy with stiffness and hypertonia associated with an ACTA1 mutation. Neurol 78(14):1100-1103
35. Jungbluth H, Sewry CA, Brown SC, Nowak KJ, Laing NG et al (2001) Mild phenotype of nemaline myopathy with sleep hypoventilation due to mutation in the skeletal muscle alpha-actin (ACTA1) gene. Neuromuscular Disord 11:35-40
36. Kaindl AM, Ruschendorf F, Krause S, Goebel HH, Koehler K et al (2004) Missense mutations of ACTA1 cause dominant congenital myopathy with cores. J Med Genet 41(11):842-848
37. Kalita D (1989) Nonprogressive nemaline myopathy. J Orthomolec Med 4:70-74
38. Karpati G, Carpenter S (1992) Skeletal muscle in neuromuscular diseases. In: Rowland LP, DiMauro S (eds) Myopathies - handbook of clinical neurology, vol 18(62). Elsevier Science, Amsterdam, pp 1-48
39. Laing NG (1995) Inherited disorders of contractile proteins in skeletal and cardiac muscle. Curr Opin Neurol 8:391-396
40. Laing NG, Clarke NF, Dye DE, Liyanage K, Walker KR et al (2004) Actin mutations are one cause of congenital fibre type disproportion. Ann Neurol 56(5):689-694
41. Laing NG, Dye DE, Wallgren-Pettersson C, Richard G, Monnier N et al (2009) Mutations and polymorphisms of the skeletal muscle alpha-actin gene (ACTA1). Hum Mutat 30(9):1267-1277
42. Laing NG, Wilton SD, Akkari PA, Dorosz S, Boundy K et al (1995) A mutation in the α-tropomyosin gene TPM3 associated with autosomal dominant nemaline myopathy. Nat Genet 9:75-79
43. Lake BD, Wilson J (1975) Zebra body myopathy. Clinical, histochemical and ultrastructural studies. J Neurol Sci 24(4):437-446
44. Lehtokari VL, Ceuterick-de Groote C, de Jonghe P, Marttila M, Laing NG et al (2007) Cap disease caused by heterozygous deletion of the beta-tropomyosin gene TPM2. Neuromuscular Disord 17:433-442
45. Lindqvist J, Penisson-Besnier I, Iwamoto H, Li M, Yagi N et al (2012) A myopathy-related actin mutation increases contractile function. Acta Neuropathol 123(5):739-746
46. Nguyen MA, Joya JE, Kee AJ, Domazetovska A, Yang N et al (2011) Hypertrophy and dietary tyrosine ameliorate the phenotypes of a mouse model of severe nemaline myopathy. Brain 134(12):3516-3529
47. Nonaka I, Nakamura Y, Tojo M, Sugita H, Ishikawa T et al (1983) Congenital myopathy without specific features (minimal change myopathy). Neuropediatrics 14(4):237-241
48. Nowak KJ, Ravenscroft G, Jackaman C, Filipovska A, Davies SM et al (2009) Rescue of skeletal muscle alpha-actin-null mice by cardiac (fetal) alpha-actin. J Cell Biol 185(5):903-915
49. Nowak KJ, Sewry CA, Navarro C, Squier W, Reina C et al (2007) Nemaline myopathy caused by absence of alpha-skeletal muscle actin. Ann Neurol 61(2):175-184
50. Nowak KJ, Wattanasirichaigoon D, Goebel HH, Wilce M, Pelin K et al (1999) Mutations in the skeletal muscle alpha-actin gene in patients with actin myopathy and nemaline myopathy. Nat Genet 23(2):208-212
51. Ohlsson M, Fidzianska A, Tajsharghi H, Oldfors A (2009) TPM3 mutation in one of the original cases of cap disease. Neurology 72(22):1961-1963
52. Ravenscroft G, Colley SM, Walker KR, Clement S, Bringans S et al (2008) Expression of cardiac alpha-actin spares extraocular muscles in skeletal muscle alpha-actin diseases - quantification of striated alpha-actins by MRM-mass spectrometry. Neuromuscular Disord 18(12):953-958
53. Ravenscroft G, Jackaman C, Bringans S, Papadimitriou JM, Griffiths LM et al (2011) Mouse models of dominant ACTA1 disease recapitulate human disease and provide insight into therapies. Brain 134(4):1101-1115
54. Ravenscroft G, Jackaman C, Sewry CA, McNamara E, Squire SE et al (2011) Actin nemaline myopathy mouse reproduces disease, suggests other actin disease phenotypes and provides cautionary note on muscle transgene expression. PLoS One 6(12):e28699
55. Razzaq A, Schmitz S, Veigel C, Molloy JE, Geeves MA et al (1999) Actin residue glu(93) is identified as an amino acid affecting myosin binding. J Biol Chem 274(40):28321-28328
56. Reyes MG, Goldbarg H, Fresco K, Bouffard A (1987) Zebra body myopathy: a second case of ultrastructurally distinct congenital myopathy. J Child Neurol 2(4):307-310
57. Rubenstein PA, Martin DJ (1983) NH2-terminal processing of Drosophila melanogaster actin. Sequential removal of two amino acids. J Biol Chem 258(18):11354-11360
58. Russell AJ, Hartman JJ, Hinken AC, Muci AR, Kawas R et al (2012) Activation of fast skeletal muscle troponin as a potential therapeutic approach for treating neuromuscular diseases. Nat Med 18(3):452-455
59. Ryan MM, Sy C, Rudge S, Ellaway C, Ketteridge D et al (2008) Dietary l-tyrosine supplementation in nemaline myopathy. J Child Neurol 23(6):609-613
60. Saito Y, Komaki H, Hattori A, Takeuchi F, Sasaki M et al (2011) Extramuscular manifestations in children with severe congenital myopathy due to ACTA1 gene mutations. Neuromuscular Disord 21(7):489-493
61. Sanoudou D, Haslett JN, Kho AT, Guo S, Gazda HT et al (2003) Expression profiling reveals altered satellite cell numbers and glycolytic enzyme transcription in nemaline myopathy muscle. Proc Natl Acad Sci USA 100(8):4666-4671
62. Sarnat HB (1992) Vimentin and desmin in maturing skeletal muscle and developmental myopathies. Neurol 42(8):1616-1624
63. Schnell C, Kan A, North KN (2000) 'An artefact gone awry': identification of the first case of nemaline myopathy by Dr R.D.K. Reye. Neuromuscular Disord 10(4-5):307-312
64. Schroder JM, Durling H, Laing N (2004) Actin myopathy with nemaline bodies, intranuclear rods, and a heterozygous mutation in ACTA1 (Asp154Asn). Acta Neuropathol 108(3):250-256
65. Schroder R, Reimann J, Salmikangas P, Clemen CS, Hayashi YK et al (2003) Beyond LGMD1A: myotilin is a component of central core lesions and nemaline rods. Neuromuscular Disord 13(6):451-455
66. Sewry CA, Holton J, Dick DJ, Jacques T, Muntoni F et al (2009) Zebra body myopathy resolved. Neuromuscular Disord 19:637-638
67. Sewry CA, Jimenez-Mallebrera C, Muntoni F (2008) Congenital myopathies. Curr Opin Neurol 21(5):569-575
68. Sewry CA, Muller C, Davis M, Dwyer JS, Dove J et al (2002) The spectrum of pathology in central core disease. Neuromuscular Disord 12(10):930-938
69. Sheterline P, Clayton J, Sparrow JC (1998) Actin. In: Protein Profiles, vol 1. Oxford University Press, Oxford
70. Shy GM, Engel WK, Somers JE, Wanko T (1963) Nemaline myopathy: a new congenital myopathy. Brain 86:793-810
71. Sparrow JC, Nowak KJ, Durling HJ, Beggs AH, Wallgren-Pettersson C et al (2003) Muscle disease caused by mutations in the skeletal muscle alpha-actin gene (ACTA1). Neuromuscular Disord 13:519-531
72. Sugita H, Masaki T, Ebashi S (1974) Staining of myofibrils with fluorescent antibody against the 10S component of the original alpha-actinin preparation. J Biochem 75(3):671-673
73. Tajsharghi H, Ohlsson M, Lindberg C, Oldfors A (2007) Congenital myopathy with nemaline rods and cap structures caused by a mutation in the beta-tropomyosin gene (TPM2). Arch Neurol 64(9):1334-1338
74. Taylor A, Erba H, Muscat G, Kedes L (1988) Nucleotide sequence and expression of the human skeletal α-actin gene: evolution of functional regulatory domains. Genomics 3:323-336
75. Vandekerckhove J, Weber K (1978) At least six different actins are expressed in a higher mammal: an analysis based on the amino acid sequence of the amino-terminal tryptic peptide. J Mol Biol 126(4):783-802
76. Vandekerckhove J, Weber K (1984) Chordate muscle actins differ distinctly from invertebrate muscle actins. The evolution of the different vertebrate muscle actins. J Mol Biol 179(3):391-413
77. Vilquin JT, Catelain C, Vauchez K (2011) Cell therapy for muscular dystrophies: advances and challenges. Curr Opin Organ Transplant 16(6):640-649
78. Visegrady B, Machesky LM (2010) Myopathy-causing actin mutations promote defects in serum-response factor signalling. Biochem J 427(1):41-48
79. Voit T, Krogmann O, Lenard HG, Neuen-Jacob E, Wechsler W et al (1988) Emery-Dreifuss muscular dystrophy: disease spectrum and differential diagnosis. Neuropediatrics 19(2):62-71
80. Wallefeld W, Krause S, Nowak KJ, Dye D, Horvath R et al (2006) Severe nemaline myopathy caused by mutations of the stop codon of the skeletal muscle alpha actin gene (ACTA1). Neuromuscular Disord 16(9-10):541-547
81. Wallgren-Pettersson C (1989) Congenital nemaline myopathy: a clinical follow-up study of twelve patients. J Neurol Sci 89:1-14
82. Wallgren-Pettersson C, Laing NG (2001) Report of the 83rd ENMC International Workshop: 4th Workshop on Nemaline Myopathy, 22-24 September 2000, Naarden, The Netherlands. Neuromuscular Disord 11(6-7):589-595
83. Wallgren-Pettersson C, Laing NG (2010) Congenital myopathies. In: Karpati G, Hilton-Jones D, Bushby K, Griggs RC (eds) Disorders of voluntary muscle, 8th edn. Cambridge University Press, Cambridge, pp 282-298
84. Wallgren-Pettersson C, Sewry CA, Nowak KJ, Laing NG (2011) Nemaline myopathies. Semin Pediatr Neurol 18(4):230-238
85. Wang CH, Dowling JJ, North K, Schroth MK, Sejersen T et al (2012) Consensus statement on standard of care for congenital myopathies. J Child Neurol 27(3):363-382
86. Yamaguchi M, Robson RM, Stromer MH, Dahl DS, Oda T (1978) Actin filaments form the backbone of nemaline myopathy rods. Nature 271(5642):265-267