Limb girdle muscular dystrophies


Authors: L. Mensová;  D. Baumgartner;  V. Potočková;  R. Mazanec
Authors‘ workplace: Neurologická klinika 2. LF UK a FN Motol, Praha
Published in: Cesk Slov Neurol N 2022; 85(6): 435-448
Category: Minimonography
doi: 10.48095/cccsnn2022435

Overview

Termín pletencové svalové dystrofie (limb girdle muscular dystrophy; LGMD) byl poprvé použit v roce 1954 J. N. Waltonem a F. Nattrassem. Autoři se jím snažili vymezit další klinickou jednotku vedle častější X-vázané Duchennovy muskulární dystrofie a autozomálně dominantně dědičných myotonické a facioskapulohumerální svalové dystrofie (FSHD). V dalších letech přibývalo poznatků a publikací popisujících jednotlivé LGMD nejen s autozomálně recesivním, ale také dominantním typem dědičnosti. Bylo zjevné, že LGMD nebude jedním onemocněním, nýbrž zastřešujícím termínem pro celou skupinu velmi variabilních klinických jednotek s různým genetickým i patofyziologickým podkladem. Prudký rozvoj molekulární genetiky (zejména technik sekvenování nové generace) vedl k objevení velkého množství nových asociovaných genů. Nová klasifikace z roku 2018 definuje více než 30 subtypů LGMD a je koncipována s předpokladem, že i v budoucnosti budou přibývat další. Tato publikace přináší stručný přehled dostupných informací o LGMD a jejich epidemiologii, patogenezi, fenotypických znacích vč. popisu nejčastějších klinických jednotek, dia­gnostice, diferenciální dia­gnostice a dostupných a vyvíjených možnostech terapie.

Keywords:

limb girdle muscular dystrophies – myopathies


Sources

1. Walton NJ, Nattrass FJ. On the classification, natural history and treatment of the myopathies. Brain 1954; 77 (2): 169–231. doi: 10.1093/brain/77.2.169.

2. Bushby KMD. Dia­gnostic criteria for the limb-girdle muscular dystrophies: report of the ENMC consortium on limbgirdle dystrophies. Neuromuscular Disord 1995; 5 (1): 71–74. doi: 10.1016/0960-8966 (93) e0006- g.

3. Servián‑Morilla E, Takeuchi H, Lee TV et al. A POGLUT1 mutation causes a muscular dystrophy with reduced Notch signaling and satellite cell loss. EMBO Mol Med 2016; 8 (11): 1289–1309. doi: 10.15252/emmm.201505815.

4. Straub V, Murphy A, Udd B et al. 229th ENMC international workshop: limb girdle muscular dystrophies – Nomenclature and reformed classification Naarden, the Netherlands, 17–19 March 2017. Neuromuscular Disord 2018; 28 (8): 702–710. doi: 10.1016/j.nmd.2018.05.007.

5. van der Kooi AJ, Barth PG, Busch HF et al. The clinical spectrum of limb girdle muscular dystrophy. A survey in the Neatherlands. Brain 1996; 119 (Pt 5): 1471–1480. doi: 10.1093/brain/119.5.1471.

6. Norwood FLM, Harling C, Chinnery PF et al. Prevalence of genetic muscle disease in Northern England: in-depth analysis of a muscle clinic population. Brain 2009; 132 (Pt 11): 3175–3186. doi: 10.1093/brain/awp236.

7. Narayanaswami P, Weiss M, Selcen D et al. Evidence-based guideline summary. Neurology 2014; 83 (16): 1453–1463. doi: 10.1212/wnl.0000000000000892.

8. Mojbafan M, Bahmani R, Bagheri SD et al. Mutational spectrum of autosomal recessive limb-girdle muscular dystrophies in a cohort of 112 Iranian patients and reporting of a possible founder effect. Orphanet J Rare Dis 2020; 15 (1): 14. doi: 10.1186/s13023-020-1296-x.

9. Polavarapu K, Mathur A, Joshi A et al. A founder mutation in the GMPPB gene [c.1000G > A (p.Asp334Asn) ] causes a mild form of limb-girdle muscular dystrophy/congenital myasthenic syndrome (LGMD/CMS) in South Indian patients. Neurogenetics 2021; 22 (4): 271–285. doi: 10.1007/s10048-021-00658-1.

10. Bushby K. Report on the 12th ENMC sponsored international workshop – the “limb-girdle” muscular dystrophies. Neuromuscular Disord 1992; 2 (1): 3–5. doi: 10.1016/0960-8966 (92) 90019-3.

11. Angelini C, Giaretta L, Marozzo R. An update on dia­g­­- nostic options and considerations in limb-girdle dystrophies. Expert Rev Neurother 2018; 18 (9): 693–703. doi: 10.1080/14737175.2018.1508997.

12. Willis TA, Hollingsworth KG, Coombs A et al. Quantitative magnetic resonance imaging in limb-girdle muscular dystrophy 2I: a multinational cross-sectional study. PLoS One 2014; 9 (2): e90377. doi: 10.1371/journal.pone.0090377.

13. Sarkozy A, Hicks D, Hudson J et al. ANO5 gene analysis in a large cohort of patients with anoctaminopathy: confirmation of male prevalence and high occurrence of the common exon 5 gene mutation. Hum Mutat 2013; 34 (8): 1111–1118. doi: 10.1002/humu.22342.

14. Stehlíková K, Skálová D, Zídková J et al. Autosomal recessive limb-girdle muscular dystrophies in the Czech Republic. BMC Neurol 2014; 14: 154. doi: 10.1186/s12883-014-0154-7.

15. Richard I, Roudaut C, Saenz A et al. Calpainopathy – a survey of mutations and polymorphisms. Am J Hum Genetics 1999; 64 (6): 1524–1540. doi: 10.1086/302426.

16. Murphy AP, Straub V. The classification, natural history and treatment of the limb girdle muscular dystrophies. J Neuromuscul Dis 2015; 2 (2): S7–S19. doi: 10.3233/jnd-150105.

17. Hack AA, Groh ME, McNally EM. Sarcoglycans in muscular dystrophy. Microsc Res Tech 2000; 48 (3–4): 167–180. doi: 10.1002/ (SICI) 1097-0029 (20000201/15) 48: 3/4<167:: AID-JEMT5>3.0.CO; 2-T.

18. Zrelski MM, Kustermann M, Winter L. Muscle-related plectinopathies. Cells 2021; 10 (9): 2480. doi: 10.3390/cells10092480.

19. Liu J, Aoki M, Illa I et al. Dysferlin, a novel skeletal muscle gene, is mutated in Miyoshi myopathy and limb girdle muscular dystrophy. Nat Genet 1998; 20 (1): 31–36. doi: 10.1038/1682.

20. Liewluck T, Milone M. Untangling the complexity of limb‑girdle muscular dystrophies. Muscle Nerve 2018; 58 (2): 167–177. doi: 10.1002/mus.26077.

21. Kawahara G, Guyon JR, Nakamura Y et al. Zebrafish models for human FKRP muscular dystrophies. Hum Mol Genet 2010; 19 (4): 623–633. doi: 10.1093/hmg/ddp528.

22. Herrmann R, Straub V, Blank M et al. Dissociation of the dystroglycan complex in caveolin-3-deficient limb girdle muscular dystrophy. Hum Mol Genet 2000; 9 (15): 2335–2340. doi: 10.1093/oxfordjournals.hmg.a018926.

23. Alderton JM, Steinhardt RA. How calcium influx through calcium leak channels is responsible for the elevated levels of calcium-dependent proteolysis in dystrophic myotubes. Trends Cardiovasc Med 2000; 10 (6): 268–272. doi: 10.1016/s1050-1738 (00) 00075-x.

24. Fanin M, Nascimbeni AC, Fulizio L et al. Loss of calpain-3 autocatalytic activity in LGMD2A patients with normal protein expression. Am J Pathol 2003; 163 (5): 1929–1936. doi: 10.1016/s0002-9440 (10) 63551-1.

25. Wallace GQ, McNally EM. Mechanisms of muscle degeneration, regeneration, and repair in the muscular dystrophies. Annu Rev Physiol 2009; 71: 37–57. doi: 10.1146/annurev.physiol.010908.163216.

26. Darras BT, Nordli DR, Shefner JM. Limb-girdle muscular dystrophy. [online]. Available from URL: https: //www.uptodate.com/contents/limb-girdle-muscular-dystrophy.

27. Paradas C, Llauger J, Diaz-Manera J et al. Redefining dysferlinopathy phenotypes based on clinical findings and muscle imaging studies. Neurology 2010; 75 (4): 316–323. doi: 10.1212/wnl.0b013e3181ea1564.

28. Magri F, Bo RD, D’Angelo MG et al. Frequency and characterisation of anoctamin 5 mutations in a cohort of Italian limb-girdle muscular dystrophy patients. Neuromuscul Disord 2012; 22 (11): 934–943. doi: 10.1016/j.nmd.2012.05.001.

29. Bushby K. Limb-girdle muscular dystrophies. [online]. Dostupné z: https: //rarediseases.org/rare-dis­- eases/limb-girdle-muscular-dystrophies/.

30. Parmová O, Mensová L, Voháňka S et al. Celonárodní screening Pompeho nemoci u pacientů s nespecifikovanou svalovou slabostí, hyperCKémií a respirační insuficiencí. Neurol Praxi 2020; 21 (Suppl B): 3–9 doi: 10.36290/neu.2020.064.

31. Kishnani PS, Steiner RD, Bali D et al. Pompe disease dia­gnosis and management guideline. Genet Med 2006; 8 (5): 267–288. doi: 10.1097/01.gim.0000218152.87434.f3.

32. Mazanec R, Mensová L, Baumgartner D et al. Dia­gnostický algoritmus u svalových dystrofií. Neurol Praxi 2019; 20 (3): 190–194 doi: 10.36290/neu.2019.017.

33. Joyce NC, Oskarsson B, Jin L-W. Muscle bio­psy evaluation in neuromuscular disorders. Phys Med Rehabil Clin N Am 2012; 23 (3): 609–631. doi: 10.1016/j.pmr.2012.06.006.

34. Mercuri E, Bushby K, Ricci E et al. Muscle MRI findings in patients with limb girdle muscular dystrophy with calpain 3 deficiency (LGMD2A) and early contractures. Neuromuscular Disord 2005; 15 (2): 164–171. doi: 10.1016/j.nmd.2004.10.008.

35. Mercuri E, Pichiecchio A, Allsop J et al. Muscle MRI in inherited neuromuscular disorders: past, present, and future. J Magn Reson Imaging 2007; 25 (2): 433–440. doi: 10.1002/jmri.20804.

36. Zaidman CM, Holland MR, Anderson CC et al. Calibrated quantitative ultrasound imaging of skeletal muscle using backscatter analysis. Muscle Nerve 2008; 38 (1): 893–898. doi: 10.1002/mus.21052.

37. Fajkusová L, Zídková J. Pletencové svalové dystrofie. Neurol Praxi 2021; 22 (2): 100–103. doi: 10.36290/neu. 2020.107.

38. Angelini C. LGMD. Identification, description and classification. Acta Myol 2020; 39 (4): 207–217. doi: 10.36185/2532-1900-024.

39. Quick S, Schaefer J, Waessnig N et al. Evaluation of heart involvement in calpainopathy (LGMD2A) using cardiovascular magnetic resonance. Muscle Nerve 2015; 52 (4): 661–663. doi: 10.1002/mus.24717.

40. Campbell DEMP, Campbell KP. Dystrophin-glycoprotein comples: post-translational processing and dystroglycan function. J Biol Chem 2003; 278 (18): 15457–15460. doi: 10.1074/jbc.r200031200.

41. Mercuri E, Brockington M, Straub V et al. Phenotypic spectrum associated with mutations in the fukutin‑related protein gene. Ann Neurol 2003; 53 (4): 537–542. doi: 10.1002/ana.10559.

42. Wicklund MP, Kissel JT. The limb-girdle muscular dystrophies. Neurol Clin 2014; 32 (3): 729–749. doi: 10.1016/ j.ncl.2014.04.005.

43. Matsumura K, Tomé FMS, Collin H et al. Deficiency of the 50K dystrophin-associated glycoprotein in severe childhood autosomal recessive muscular dystrophy. Nature 1992; 359 (6393): 320–322. doi: 10.1038/359320a0.

44. Tarakci H, Berger J. The sarcoglycan complex in skeletal muscle. Front Biosci 2016; 21 (4): 744–756. doi: 10.2741/4418.

45. Nallamilli BRR, Chakravorty S, Kesari A et al. Genetic landscape and novel disease mechanisms from a large LGMD cohort of 4656 patients. Ann Clin Transl Neurol 2018; 5 (12): 1574–1587. doi: 10.1002/acn3.649.

46. Wicklund MP. The limb-girdle muscular dystrophies. Continuum 2019; 25 (6): 1599–1618. doi: 10.1212/ con.0000000000000809.

47. Kirschner J, Lochmüller H. Sarcoglycanopathies. Handb Clin Neurol 2011; 101: 41–46. doi: 10.1016/b978-0-08-045031-5.00003-7.

48. Cagliani R, Comi GP, Tancredi L et al. Primary beta-sarcoglycanopathy manifesting as recurrent exercise-induced myoglobinuria. Neuromuscul Disord 2001; 11 (4): 389–394. doi: 10.1016/s0960-8966 (00) 00207-8.

49. Mongini T, Doriguzzi C, Bosone I et al. Alpha-sarcoglycan deficiency featuring exercise intolerance and myoglobinuria. Neuropediatrics 2002; 33 (2): 109–111. doi: 10.1055/s-2002-32374.

50. Pena L, Kim K, Charrow J. Episodic myoglobinuria in a primary gamma-sarcoglycanopathy. Neuromuscul Disord 2010; 20 (5): 337–339. doi: 10.1016/j.nmd.2010.02.015.

51. Angelini C, Fanin M, Menegazzo E et al. Homozygous a‑sarcoglycan mutation in two siblings: one asymptomatic and one steroid‑responsive mild limb-girdle muscular dystrophy patient. Muscle Nerve 1998; 21 (6): 769–775. doi: 10.1002/ (sici) 1097-4598 (199806) 21: 6<769:: aid-mus9>3.0.co; 2-5.

52. Fanin M, Nascimbeni AC, Aurino S et al. Frequency of LGMD gene mutations in Italian patients with distinct clinical phenotypes. Neurology 2009; 72 (16): 1432–1435. doi: 10.1212/wnl.0b013e3181a1885e.

53. Fanin M, Duggan DJ, Mostacciuolo ML et al. Genetic epidemiology of muscular dystrophies resulting from sarcoglycan gene mutations. J Med Genet 1997; 34 (12): 973–977. doi: 10.1136/jmg.34.12.973.

54. Lancioni A, Rotundo IL, Kobayashi YM et al. Combined deficiency of alpha and epsilon sarcoglycan disrupts the cardiac dystrophin complex. Hum Mol Genet 2011; 20 (23): 4644–4654. doi: 10.1093/hmg/ddr398.

55. Tasca G, Monforte M, Díaz-Manera J et al. MRI in sarcoglycanopathies: a large international cohort study. J Neurology Neurosurg Psychiatry 2018; 89 (1): 72–77. doi: 10.1136/jnnp-2017-316736.

56. Lodi R, Muntoni F, Taylor J et al. Correlative MR imaging and 31P-MR spectroscopy study in sarcoglycan deficient limb girdle muscular dystrophy. Neuromuscul Disord 1997; 7 (8): 505–511. doi: 10.1016/s0960-8966 (97) 00108-9.

57. Penttilä S, Palmio J, Suominen T et al. Eight new mutations and the expanding phenotype variability in muscular dystrophy caused by ANO5. Neurology 2012; 78 (12): 897–903. doi: 10.1212/wnl.0b013e31824c4682.

58. Vázquez J, Lefeuvre C, Escobar RE et al. Phenotypic spectrum of myopathies with recessive anoctamin-5 mutations. J Neuromuscul Dis 2020; 7 (4): 443–451. doi: 10.3233/jnd-200515.

59. Christiansen J, Güttsches A-K, Schara-Schmidt U et al. ANO5-related muscle diseases: from clinics and genetics to pathology and research strategies. Genes Dis 2022; 9 (6): 1506–1520. doi: 10.1016/j.gendis.2022.01.001.

60. Vinit J, Samson M, Gaultier J-B et al. Dysferlin deficiency treated like refractory polymyositis. Clin Rheumatol 2009; 29 (1): 103–106. doi: 10.1007/s10067-009-1273-1.

61. Barresi R. From proteins to genes: immunoanalysis in the dia­gnosis of muscular dystrophies. Skelet Muscle 2011; 1 (1): 24. doi: 10.1186/2044-5040-1-24.

62. Rowin J, Meriggioli MN, Cochran EJ et al. Prominent inflammatory changes on muscle bio­psy in patients with Miyoshi myopathy. Neuromuscular Disord 1999; 9 (6–7): 417–420. doi: 10.1016/s0960-8966 (99) 00041-3.

63. Rosenfeld A. Spinal muscular atrophy. [online]. Avail­able from URL: https: //emedicine.medscape.com/article/1181436-overview.

64. Neuromuskulární sekce České neurologické společnosti. [online]. Dostupné z URL: https: //www.neuromuskularni-sekce.cz/

65. Sveen M-L, Jeppesen TD, Hauerslev S et al. Endurance training. Neurology 2007; 68 (1): 59–61. doi: 10.1212/01.wnl.0000250358.32199.24.

66. Sveen M, Andersen SP, Ingelsrud LH et al. Resistance training in patients with limb‑girdle and becker muscular dystrophies. Muscle Nerve 2013; 47 (2): 163–169. doi: 10.1002/mus.23491.

67. Harvey LA, Katalinic OM, Herbert RD et al. Stretch for the treatment and prevention of contractures. Cochrane Database Syst Rev 2017; 1 (1): CD007455. doi: 10.1002/14651858.cd007455.pub3.

68. Feingold B, Mahle WT, Auerbach S et al. Management of cardiac involvement associated with neuromuscular diseases: a scientific statement from the American Heart Association. Circulation 2017; 136 (13): e200–231. doi: 10.1161/cir.0000000000000526.

69. Norwood F, Visser M de, Eymard B et al. EFNS guideline on dia­gnosis and management of limb girdle muscular dystrophies. Eur J Neurol 2007; 14 (12): 1305–1312. doi: 10.1111/j.1468-1331.2007.01979.x.

70. Margeta M, Connolly AM, Winder TL et al. Cardiac pathology exceeds skeletal muscle pathology in two cases of limb‑girdle muscular dystrophy type 2I. Muscle Nerve 2009; 40 (5): 883–889. doi: 10.1002/mus. 21432.

71. D’Amico A, Petrini S, Parisi F et al. Heart transplantation in a child with LGMD2I presenting as isolated dilated cardiomyopathy. Neuromuscul Disord 2008; 18 (2): 153–155. doi: 10.1016/j.nmd.2007.09.013.

72. Nikhanj A, Yogasundaram H, Nichols BM et al. Cardiac intervention improves heart disease and clinical outcomes in patients with muscular dystrophy in a multidisciplinary care setting. J Am Heart Assoc 2020; 9 (2): e014004. doi: 10.1161/jaha.119.014004.

73. Simonds AK. Recent advances in respiratory care for neuromuscular disease. Chest 2006; 130 (6): 1879–1886. doi: 10.1378/chest.130.6.1879.

74. Bartoli M, Roudaut C, Martin S et al. Safety and efficacy of AAV-mediated calpain 3 gene transfer in a mouse model of limb-girdle muscular dystrophy type 2A. Mol Ther 2006; 13 (2): 250–259. doi: 10.1016/j.ymthe.2005.09.017.

75. Griffin DA, Pozsgai ER, Heller KN et al. Preclinical syste-mic delivery of adeno-associated a-sarcoglycan gene transfer for limb-girdle muscular dystrophy. Hum Gene Ther 2021; 32 (7–8): 390–404. doi: 10.1089/hum.2019.199.

76. Israeli D, Cosette J, Corre G et al. An AAV-SGCG dose-response study in a g-sarcoglycanopathy mouse model in the context of mechanical stress. Mol Ther Methods Clin Dev 2019; 13: 494–502. doi: 10.1016/ j.omtm.2019.04.007.

77. Lostal W, Bartoli M, Bourg N et al. Efficient recovery of dysferlin deficiency by dual adeno-associated vector-mediated gene transfer. Hum Mol Genet 2010; 19 (10): 1897–1907. doi: 10.1093/hmg/ddq065.

78. Xu L, Lu PJ, Wang C-H et al. Adeno-associated virus 9 mediated FKRP gene therapy restores functional glycosylation of a-dystroglycan and improves muscle functions. Mol Ther 2013; 21 (10): 1832–1840. doi: 10.1038/mt.2013.156.

79. Vannoy CH, Leroy V, Lu QL. Dose-dependent effects of FKRP gene-replacement therapy on functional rescue and longevity in dystrophic mice. Mol Ther Methods Clin Dev 2018; 11: 106–120. doi: 10.1016/j.omtm.2018.10.004.

80. Birnkrant DJ, Bushby K, Bann CM et al. Dia­gnosis and management of Duchenne muscular dystrophy, part 1: dia­gnosis, and neuromuscular, rehabilitation, endocrine, and gastrointestinal and nutritional management. Lancet Neurol 2018; 17 (3): 251–267. doi: 10.1016/s1474-4422 (18) 30024-3.

81. Wong-Kisiel LC, Kuntz NL. Two siblings with limb-girdle muscular dystrophy type 2E responsive to deflazacort. Neuromuscular Disord 2010; 20 (2): 122–124. doi: 10.1016/j.nmd.2009.11.005.

82. Bogdanovich S, McNally EM, Khurana TS. Myostatin blockade improves function but not histopathology in a murine model of limb‑girdle muscular dystrophy 2C. Muscle Nerve 2008; 37 (3): 308–316. doi: 10.1002/mus.20920.

83. Mariot V, Joubert R, Hourdé C et al. Downregulation of myostatin pathway in neuromuscular diseases may explain challenges of anti-myostatin therapeutic approaches. Nat Commun 2017; 8 (1): 1859. doi: 10.1038/s41467-017-01486-4.

84. Piñol-Jurado P, Suárez-Calvet X, Fernández-Simón E et al. Nintedanib decreases muscle fibrosis and improves muscle function in a murine model of dystrophinopathy. Cell Death Dis 2018; 9 (7): 776. doi: 10.1038/s41419-018-0792-6.

85. REaDY. [online]. Dostupné z URL: https: //ready.registry.cz/.

Labels
Paediatric neurology Neurosurgery Neurology

Article was published in

Czech and Slovak Neurology and Neurosurgery

Issue 6

2022 Issue 6

Most read in this issue
Login
Forgotten password

Don‘t have an account?  Create new account

Forgotten password

Enter the email address that you registered with. We will send you instructions on how to set a new password.

Login

Don‘t have an account?  Create new account