Dystrophic changes in extraocular muscles after gamma irradiation in mdx:utrophin+/- mice

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  McDonald, Abby A ^a   Kunz, Matthew D ^a   McLoon, Linda K ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; COLLAGEN TYPE 1; COLLAGEN TYPE 4; MUSCLE PROTEIN; PROTEIN MDX; TRANSCRIPTION FACTOR PAX7; TRANSCRIPTION FACTOR PITX2; UNCLASSIFIED DRUG; UTROPHIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL PROLIFERATION; CONTROLLED STUDY; ENUCLEATION; EXTRAOCULAR MUSCLE; GAMMA IRRADIATION; INHIBITION KINETICS; MOUSE; MUSCULAR DYSTROPHY; NONHUMAN; SKELETAL MUSCLE SATELLITE CELL;

ANIMALS; CELL PROLIFERATION; EXTREMITIES; GAMMA RAYS; HOMEODOMAIN PROTEINS; MICE; MICE, INBRED C57BL; MICE, INBRED MDX; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; OCULOMOTOR MUSCLES; PAX7 TRANSCRIPTION FACTOR; PHENOTYPE; SATELLITE CELLS, SKELETAL MUSCLE; STEM CELLS; TRANSCRIPTION FACTORS; UTROPHIN;

EID: 84898886030     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086424     Document Type: Article

References (66)

1. Mauro A. (1961) Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9: 493-495.
2. Carlson BM, Faulkner JA (1983) The regeneration of skeletal muscle fibers following injury: a review. Med Sci Sports Exerc 15: 187-198. (Pubitemid 13010547)
3. Seale P, Sabourin LA, Girgis-Garbado A, Mansouri A, Gruss P, et al. (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102: 777-786.
4. Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, et al. (2006) Pax7 and myogenic progression in skeletal muscle satellite cells. J Cell Sci 119: 1824-1832. (Pubitemid 43811008)
5. Renault V, Piron-Hamelin G, Forestier C, DiDonna S, Decary S, et al. (2000) Skeletal muscle regeneration and the mitotic clock. Exp Gerontol 35: 711-719.
6. Taylor-Jones JM, McGehee RE, Rando TA, Lecka-Czernik B, Lipschitz DA, et al. (2002) Activation of an adipogenic program in adult myoblasts with age. Mech Ageing Dev 123: 649-661. (Pubitemid 34159230)
7. Mouly V, Aamiri A, Bigot A, Cooper RN, Di Donna S, et al.(2005) The mitotic clock in skeletal muscle regeneration, disease and cell medicated gene therapy. Acta Physiol Scand 184: 3-15. (Pubitemid 40646734)
8. Brack A, Rando RA (2007) Intrinsic changes and extrinsic influences of myogenic stem cell function during aging. Stem Cell Rev 3: 226-237. (Pubitemid 350129709)
9. Wallace GQ, McNally EM (2009) Mechanisms of muscle degeneration, regeneration, and repair in the muscular dystrophies. Annu Rev Physiol 71: 37-57.
10. Marques MJ, Ferretti R, Vomero VU, Minatel E, Neto HS (2007) Intrinsic laryngeal muscles are spared from myonecrosis in the mdx model of Duchenne muscular dystrophy. Muscle Nerve 35: 349-353. (Pubitemid 46364090)
11. Karpati G, Carpenter S. (1986) Small caliber skeletal muscle fibers do not suffer deleterious consequences of dystrophic gene expression. Am J Med Genet 25: 653-658. (Pubitemid 17191439)
12. Lucas CA, Hoh JF (1997) Extraocular fast myosin heavy chain expression in the levator palpebrae and retractor bulbi muscles. Invest Ophthalmol Vis Sci 38: 2817-2825. (Pubitemid 28009404)
13. Kaminski HJ, al-Hakim M, Leigh RJ, Katirji MB, Ruff RL. (1992) Extraocular muscles are spared in advanced Duchenne dystrophy. Ann Neurol 32: 586-588.
14. Khurana TS, Prendergast RA, Alameddine HS, Tome FM, Fardeau M, et al. (1995) Absence of extraocular muscle pathology in Duchenne's muscular dystrophy: role for calcium homeostasis in extraocular muscle sparing. J Exp Med 182: 467-475.
15. Ragusa RJ, Chow CK, Porter JD (1997) Oxidative stress as a potential pathogenic mechanism in an animal model of Duchenne muscular dystrophy. Neuromuscul Disord 7: 379-386. (Pubitemid 27445322)
16. Wehling M, Stull JT, McCabe TJ, Tidball JG (1998) Sparing of mdx extraocular muscles from dystrophic pathology is not attributable to normalized concentration or distribution of neuronal nitric oxide synthase. Neuromuscul Disord 8: 22-29. (Pubitemid 28174931)
17. Porter JD, Merriam AP, Khanna S, Andrade FH, Richmonds CR, et al. (2003) Constitutive properties, not molecular adaptations, mediate extraocular muscle sparing in dystrophic mdx mice. FASEB J 17: 893-919.
18. McLoon LK, Wirtschafter JD (2002) Continuous myonuclear addition to single extraocular myofibers in uninjured adult rabbits. Muscle Nerve 25: 348-358. (Pubitemid 34203211)
19. McLoon LK, Wirtschafter JD (2002) Activated satellite cells are present in uninjured extraocular muscles of mature mice. Trans. Am Ophthalmol Soc 100: 119-123.
20. McLoon LK, Rowe J, Wirtschafter J, McCormick KM (2004) Continuous myofiber remodeling in uninjured extraocular myofibers: myonuclear turnover and evidence for apoptosis. Muscle Nerve 29: 707-715. (Pubitemid 38620013)
21. McLoon LK, Wirtschafter J (2003) Activated satellite cells in extraocular muscles of normal adult monkeys and humans. Invest Ophthalmol Vis Sci 44: 1927-1932. (Pubitemid 36520281)
22. Ugalde I, Christiansen SP, McLoon LK (2005) Botulinum toxin treatment of extraocular muscles in rabbit results in increased myofiber remodeling. Invest Ophthalmol Vis Sci 46: 4114-4120. (Pubitemid 44264612)
23. Kallestad KM, Hebert SL, McDonald AA, Daniel ML, Cu SR, McLoon LK (2011) Sparing of extraocular muscle in aging and muscular dystrophies: A myogenic precursor cell hypothesis. Exp Cell Res 317: 873-885.
24. Hebert SL, Daniel ML, McLoon LK (2013) The role of Pitx2 in maintaining the phenotype of myogenic precursor cells in the extraocular muscles. PLoS One 8: e58405.
25. Weller B, Karpati G, Lehnert S, Carpenter S (1991) Major alteration of the pathological phenotype in gamma irradiated mdx soleus muscles. J Neuropathol Exp Neurol 50: 419-431.
26. McGeachie JK, Grounds MD, Partridge TA, Morgan JE (1993) Age-related changes in replication of myogenic cells in mdx mice: quantitative autoradiographic studies. J Neurol Sci 119: 169-179. (Pubitemid 23343055)
27. Quinlan JG, Lyden SOP, Cambier DM, Johnson SR, Michaels SE, Denman DL (1995) Radiation inhibition of mdx mouse muscle regeneration: Dose and age factors. Muscle Nerve 18: 201-206.
28. Granata Al, Vecchi C, Graciotti L, Fulgenzi G, Maggi S, Corsi A (1998) Gamma irradiation can reduce muscle damage in mdx dystrophic mice. Acta Neuropathol 96: 564-568.
29. McGeachie JK, Grounds MD (1999) The timing between skeletal muscle myoblast replication and fusion into myotubes, and the stability of regenerated dystrophic myofibers: an autoradiographic study in mdx mice. J Anat 194: 287-295. (Pubitemid 29191848)
30. Pagel CN, Partridge TA (1999) Covert persistence of mdx mouse myopathy is revealed by acute and chronic effects of irradiation. J Neurol Sci 164: 103-116. (Pubitemid 29288639)
31. Gross JG, Morgan JE (1999) Muscle precursor cells injected into irradiated mdx mouse muscle persist after serial injury. Muscle Nerve 22: 174-185. (Pubitemid 29070391)
32. Heslop L, Morgan JE, Partridge TA (2000) Evidence for a myogenic stem cell that is exhausted in dystrophic muscle. J Cell Sci 113: 2299-2308. (Pubitemid 30426843)
33. Zhou L, Rafael-Fortney JA, Huang P, Zhao XS, Cheng G et al., (2008) Haploinsufficiency of utrophin gene worsens skeletal muscle inflammation and fibrosis in mdx mice. J Neurol Sci 264: 106-111. (Pubitemid 350186318)
34. Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS et al. (1997) Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90: 729-738. (Pubitemid 27357964)
35. Mu X, Usas A, Lu A, Wang B, Weiss K, et al. (2013) RhoA mediates defective stem cell function and heterotopic ossification in dystrophic muscle of mice. FASEB J 27: 3619-3631.
36. DiMario JX, Uzman A, Strohman RC (1991) Fiber regeneration is not persistent in dystrophic (mdx) mouse skeletal muscle. Dev Biol 148: 314-321. (Pubitemid 121004770)
37. Stedman HH, Sweeney HL, Shrager JC, Maguire HC, Panettieri RA et al. (1991) The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352: 536-539.
38. Deconinck N, Tinsley J, De Backer F, Fisher R, Kahn D et al. (1997) Expression of truncated utrophin leads to major functional improvements in dystrophin-deficient muscles of mice. Nat Med 3: 1216-1221. (Pubitemid 27508821)
39. Huang P, Cheng G, Lu H, Aronica M, Ransohoff RM et al. (2011) Impaired respiratory function in mdx and mdx/utrophin+/- mice. Muscle Nerve 43: 263-267.
40. Morgan JE, Hoffman EP, Partridge TA (1990) Normal myogenic cells from newborn mice restore normal histology to degenerating muscles of the mdx mouse. J Cell Biol 111: 2437-2449. (Pubitemid 120014528)
41. Wakeford S, Watt DJ, Partridge TA (1991) X-irradiation improves mdx mouse muscle as a model of myofiber loss in DMD. Muscle Nerve 14: 42-50.
42. Rosenblatt JD, Parry DJ (1992) Gamma irradiation prevents compensatory hypertrophy of overloaded mouse extensor digitorum longus muscle. J Appl Physiol 73: 2538-2543. (Pubitemid 23019667)
43. Phalen JN, Gonyea WJ (1997) Effect of radiation on satellite cell activity and protein expression in overloaded mammalian skeletal muscle. Anat Rec 247: 179-188.
44. Mitchell PO, Pavlath GK. (2001) A muscle precursor cell-dependent pathway contributes to muscle growth after atrophy. Am J Physiol Cell Physiol 281: C1706-1715.
45. Lowe DA, Alway SE (1999) Stretch-induced myogenin, MyoD, and MRF4 expression and acute hypertroph in quail slow-tonic muscle are not dependent upon satellite cell proliferation. Cell Tissue Res 296: 531-539. (Pubitemid 29253684)
46. McCarthy JJ, Mula J, Miyazaki M, Erfani R, Garrison K, et al. (2011) Effective fiber hypertrophy in satellite cell-depleted skeletal muscle. Development 138: 3657-3666.
47. Jackson JR, Mula J, Kirby TJ, Fry CS, Lee JD, et al. (2012) Satellite cell depletion does not inhibit adult skeletal muscle regrowth following unloading-induced atrophy. Am J Physiol Cell Physiol 303: C854-861.
48. Zhou Y, Cheng G, Dieter L, Hjalt TA, Andrade FH, et al. (2009) An altered phenotype in conditional knockout of Pitx2 in extraocular muscle. Invest Ophthalmol Vis Sci 50: 4531-4541.
49. Zhou Y, Liu D, Kaminski HJ. (2011) Pitx2 regulates myosin heavy chain isoform expression and multi-innervation in extraocular muscle. J Physiol 589: 4601-4614.
50. Duchen LW (1970) Changes in motor innervation and cholinesterase localization induced by botulinum toxin in skeletal muscle of the mouse: differences between fast and slow muscles. J Neurol Neurosurg Psychiat 33: 40-54.
51. Hassan SM, Jennekens FGI, Veldman H (1995) Botulinum-toxin induced myopathy in the rat. Brain 118: 533-545.
52. Spencer RF, McNeer KW (1987) Botulinum toxin paralysis of adult extraocular muscle. Structural alterations in orbital, singly innervated muscle fibers. Arch Ophthalmol 105: 1703-1711. (Pubitemid 18009197)
53. Ahmad M, Liu JX, Brännström T, Andersen PM, Stål P, Pedrosa-Domellöf F (2010) Human extraocular muscles in ALS. Invest Ophthalmol Vis Sci 51: 3494-3591.
54. Valdez G, Tapia JC, Lichtman JW, Fox MA, Sanes JR (2012) Shared resistance to aging and ALS in neuromuscular junctions of specific muscles. PLoS One 7(4): e34640.
55. Christiansen SP, Antunes-Foschini RS, McLoon LK (2010) Effects of recession versus tenotomy surgery without recession in adult rabbit extraocular muscle. Invest Ophthalmol Vis Sci 51: 5646-5656.
56. Fischer MD, Gorospe JR, Felder E, Bogdanovich S, Pedrosa-Domellöf F, et al. (2002) Expression profiling reveals metabolic and structural components of extraocular muscles. Physiol Genomics 9: 71-84. (Pubitemid 135707414)
57. Anderson BC, Christiansen SP, Grandt S, Grange RW, McLoon LK (2006) Increased extraocular muscle strength with direct injection of insulin-like growth factor-I. Invest Ophthalmol Vis Sci 47: 2461-2467. (Pubitemid 351639828)
58. Christiansen SP, McLoon LK (2006) The effect of resection on satellite cell activity in rabbit extraocular muscle. Invest Ophthalmol Vis Sci 47: 605-613. (Pubitemid 46768387)
59. Sakurai T, Ueda T, Kawai M, Tobita H, Miyakoshi J (2009) Protective effects of insulin-like growth factor-I on the decrease in myogenic differentiation by ionizing radiation. Int J Radiat Biol 85: 153-157.
60. Yang SY, Hoy M, Fuller B, Sales KM, Seifalian AM, et al. (2010) Pretreatment with insulin-like growth factor I protects skeletal muscle cells against oxidative damage via PI3K/Akt and ERK1/2 MAPK pathways. Lab Invest 90: 391-401.
61. Kallestad KM, McLoon LK (2009) Defining the heterogeneity of skeletal-muscle derived side and main population cells isolated immediately ex vivo. J Cellul Physiol 222: 676-684.
62. Kovanen V (2002) Intramuscular extracellular matrix: complex environment of muscle cells. Exerc Sport Sci Rev 30: 20-25.
63. Ricard-Blum S, Ruggiero F (2005) The collagen superfamily: from the extracellular matrix to the cell membrane. Pathol Biol (Paris) 53: 430-442. (Pubitemid 41112079)
64. Stager D Jr, McLoon LK, Felius J (2013) Postulating a role for connective tissue elements in inferior oblique overaction. Trans Am Ophthalmol Soc 111: 70-81.
65. van Putten M, Kumar D, Hulsker M, Hoogaars WMH, Plomp JJ, et al. (2012) Comparison of skeletal muscle pathology and motor function of dystrophin and utrophin deficient mouse strains. Neuromuscul Disord 22: 406-417.
66. Becher UM, Breitbach M, Sassa P, Garbe S, van der Ven PFM, et al. (2009) Enrichment and terminal differentiation of striated muscle progenitors in vitro. Exp Cell Res 315: 2741-2751.