Dystrophin and utrophin "double knockout" dystrophic mice exhibit a spectrum of degenerative musculoskeletal abnormalities

Journal of Orthopaedic Research

Volumn 31, Issue 3, 2013, Pages 343-349

  Isaac, Christian ^a,b   Wright, Adam ^a,b   Usas, Arvydas ^a   Li, Hongshuai ^a   Tang, Ying ^a   Mu, Xiaodong ^a   Greco, Nicholas ^a,b   Dong, Qing ^b   Vo, Nam ^b   Kang, James ^b   Wang, Bing ^a,b   Huard, Johnny ^a,b  

^a UNIVERSITY OF PITTSBURGH   (United States)

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

Author keywords

bone healing; ectopic calcification; muscular dystrophy; osteopenia; proteoglycans

Indexed keywords

DYSTROPHIN; UTROPHIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTICULAR CARTILAGE; CARDIOMYOPATHY; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; FRACTURE HEALING; HETEROTOPIC OSSIFICATION; HINDLIMB; INTERVERTEBRAL DISK; KNOCKOUT MOUSE; MICRO-COMPUTED TOMOGRAPHY; MOUSE; MUSCLE ATROPHY; NONHUMAN; PRIORITY JOURNAL; SOFT TISSUE CALCIFICATION; SPINE MALFORMATION;

AGING, PREMATURE; ANIMALS; BONE DISEASES, METABOLIC; CALCINOSIS; CARDIOMYOPATHIES; CARTILAGE, ARTICULAR; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DYSTROPHIN; FRACTURE HEALING; INTERVERTEBRAL DISC; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MICE, KNOCKOUT; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; MUSCULAR DYSTROPHY, DUCHENNE; TIBIAL FRACTURES; UTROPHIN;

EID: 84872796985     PISSN: 07360266     EISSN: 1554527X     Source Type: Journal    
DOI: 10.1002/jor.22236     Document Type: Article

References (54)

1. Larson CM, Henderson RC,. 2000. Bone mineral density and fractures in boys with Duchenne muscular dystrophy. J Pediatr Orthop 20: 71-74.
2. Sussman M,. 2002. Duchenne muscular dystrophy. J Am Acad Orthop Surg 10: 138-151.
3. Koenig M, Hoffman EP, Bertelson CJ, et al. 1987. Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50: 509-517.
4. Hoffman EP, Fischbeck KH, Brown RH, et al. 1988. Characterization of dystrophin in muscle-biopsy specimens from patients with Duchenne's or Becker's muscular dystrophy. N Engl J Med 318: 1363-1368.
5. Infante JP, Huszagh VA,. 1999. Mechanisms of resistance to pathogenesis in muscular dystrophies. Mol Cell Biochem 195: 155-167.
6. Sacco A, Mourkioti F, Tran R, et al. 2010. Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell 143: 1059-1071.
7. Morgan JE, Zammit PS,. 2010. Direct effects of the pathogenic mutation on satellite cell function in muscular dystrophy. Exp Cell Res 316: 3100-3108.
8. Cornelison DD, Wilcox-Adelman SA, Goetinck PF, et al. 2004. Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev 18: 2231-2236.
9. Collins CA, Olsen I, Zammit PS, et al. 2005. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122: 289-301.
10. Montarras D, Morgan J, Collins C, et al. 2005. Direct isolation of satellite cells for skeletal muscle regeneration. Science 309: 2064-2067.
11. Kuang S, Kuroda K, Le Grand F, et al. 2007. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 129: 999-1010.
12. Sacco A, Doyonnas R, Kraft P, et al. 2008. Self-renewal and expansion of single transplanted muscle stem cells. Nature 456: 502-506.
13. Webster C, Blau HM,. 1990. Accelerated age-related decline in replicative life-span of Duchenne muscular dystrophy myoblasts: implications for cell and gene therapy. Somat Cell Mol Genet 16: 557-565.
14. Hsu JD,. 1982. Skeletal changes in children with neuromuscular disorders. Prog Clin Biol Res 101: 553-557.
15. McDonald DG, Kinali M, Gallagher AC, et al. 2002. Fracture prevalence in Duchenne muscular dystrophy. Dev Med Child Neurol 44: 695-698.
16. Bothwell JE, Gordon KE, Dooley JM, et al. 2003. Vertebral fractures in boys with Duchenne muscular dystrophy. Clin Pediatr 42: 353-356.
17. Soderpalm AC, Magnusson P, Ahlander AC, et al. 2008. Bone markers and bone mineral density in Duchenne muscular dystrophy. J Musculoskel Neuron Interact 8: 24.
18. Karol LA,. 2007. Scoliosis in patients with Duchenne muscular dystrophy. J Bone Joint Surg Am 89: 155-162.
19. Boot AM, de Ridder MA, Pols HA, et al. 1997. Bone mineral density in children and adolescents: relation to puberty, calcium intake, and physical activity. J Clin Endocrinol Metab 82: 57-62.
20. Ward K, Alsop C, Caulton J, et al. 2004. Low magnitude mechanical loading is osteogenic in children with disabling conditions. J Bone Miner Res 19: 360-369.
21. Wang Q, Alen M, Nicholson P, et al. 2007. Weight-bearing, muscle loading and bone mineral accrual in pubertal girls-A 2-year longitudinal study. Bone 40: 1196-1202.
22. McKay H, Smith E,. 2008. Winning the battle against childhood physical inactivity: the key to bone strength? J Bone Miner Res 23: 980-985.
23. Anderson JE, Lentz DL, Johnson RB,. 1993. Recovery from disuse osteopenia coincident to restoration of muscle strength in mdx mice. Bone 14: 625-634.
24. Montgomery E, Pennington C, Isales CM, et al. 2005. Muscle-bone interactions in dystrophin-deficient and myostatin-deficient mice. Anat Rec A Discov Mol Cell Evol Biol 286: 814-822.
25. Nakagaki WR, Bertran CA, Matsumura CY, et al. 2011. Mechanical, biochemical and morphometric alterations in the femur of mdx mice. Bone 48: 372-379.
26. Novotny SA, Warren GL, Lin AS, et al. 2011. Bone is functionally impaired in dystrophic mice but less so than skeletal muscle. Neuromuscul Disord 21: 183-193.
27. Rufo A, Del Fattore A, Capulli M, et al. 2011. Mechanisms inducing low bone density in Duchenne muscular dystrophy in mice and humans. J Bone Miner Res 26: 1891-1903.
28. Bulfield G, Siller WG, Wight PA, et al. 1984. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81: 1189-1192.
29. Sicinski P, Geng Y, Ryder-Cook AS, et al. 1989. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244: 1578-1580.
30. Carnwath JW, Shotton DM,. 1987. Muscular dystrophy in the mdx mouse: histopathology of the soleus and extensor digitorum longus muscles. J Neurol Sci 80: 39-54.
31. Torres LF, Duchen LW,. 1987. The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates. Brain J Neurol 110: 269-299.
32. Coulton GR, Morgan JE, Partridge TA, et al. 1988. The mdx mouse skeletal muscle myopathy: I. A histological, morphometric and biochemical investigation. Neuropathol Appl Neurobiol 14: 53-70.
33. DiMario JX, Uzman A, Strohman RC,. 1991. Fiber regeneration is not persistent in dystrophic (MDX) mouse skeletal muscle. Dev Biol 148: 314-321.
34. Deconinck AE, Rafael JA, Skinner JA, et al. 1997. Utrophin-dystrophin- deficient mice as a model for Duchenne muscular dystrophy. Cell 90: 717-727.
35. Grady RM, Teng H, Nichol MC, et al. 1997. Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90: 729-738.
36. Mankin HJ,. 1971. Biochemical and metabolic aspects of osteoarthritis. Orthop Clin North Am 2: 19-31.
37. Lyons G, Eisenstein SM, Sweet MB,. 1981. Biochemical changes in intervertebral disc degeneration. Biochim Biophys Acta 673: 443-453.
38. Bianchi ML, Mazzanti A, Galbiati E, et al. 2003. Bone mineral density and bone metabolism in Duchenne muscular dystrophy. Osteoporos Int 14: 761-767.
39. Soderpalm AC, Magnusson P, Ahlander AC, et al. 2007. Low bone mineral density and decreased bone turnover in Duchenne muscular dystrophy. Neuromuscul Disord 17: 919-928.
40. Winder SJ,. 1997. The membrane-cytoskeleton interface: the role of dystrophin and utrophin. J Muscle Res Cell Motil 18: 617-629.
41. Kamel HK,. 2003. Sarcopenia and aging. Nutr Rev 61: 157-167.
42. Crepaldi G, Maggi S,. 2005. Sarcopenia and osteoporosis: a hazardous duet. J Endocrinol Invest 28: 66-68.
43. Schoenfeld AJ, Nelson JH, Burks R, et al. 2011. Incidence and risk factors for lumbar degenerative disc disease in the United States military 1999-2008. Mil Med 176: 1320-1324.
44. Bohatirchuk F,. 1957. Aging and osteoarthritis. Can Med Assoc J 76: 106-114.
45. Sinusas K,. 2012. Osteoarthritis: diagnosis and treatment. Am Fam Physician 85: 49-56.
46. Hsu JD, Furumasu J,. 1993. Gait and posture changes in the Duchenne muscular dystrophy child. Clin Orthop Relat Res 288: 122-125.
47. Madigan L, Vaccaro AR, Spector LR, et al. 2009. Management of symptomatic lumbar degenerative disk disease. J Am Acad Orthop Surg 17: 102-111.
48. Lammers AR, German RZ, Lightfoot PS,. 1998. The impact of muscular dystrophy on limb bone growth and scaling in mice. Acta anatomica 162: 199-208.
49. Garris DR, Burkemper KM, Garris BL,. 2007. Influences of diabetes (db/db), obese (ob/ob) and dystrophic (dy/dy) genotype mutations on hind limb bone maturation: a morphometric, radiological and cytochemical indices analysis. Diabetes Obes Metabol 9: 311-322.
50. Loeser RF,. 2010. Age-related changes in the musculoskeletal system and the development of osteoarthritis. Clin Geriatr Med 26: 371-386.
51. Adams MA, Roughley PJ,. 2006. What is intervertebral disc degeneration, and what causes it? Spine (PhilaPa 1976) 31: 2151-2161.
52. Johnell O, Kanis J,. 2005. Epidemiology of osteoporotic fractures. Osteoporos Int 16: S3-S7.
53. Rossi DJ, Jamieson CH, Weissman IL,. 2008. Stems cells and the pathways to aging and cancer. Cell 132: 681-696.
54. Lavasani M, Robinson AR, Lu A, et al. 2012. Muscle-derived stem/progenitor cell dysfunction limits healthspan and lifespan in a murine progeria model. Nat Commun 3: 608.