Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice

Journal of Molecular Histology

Volumn 35, Issue 5, 2004, Pages 489-499

  Nakae, Yoshiko ^a   Stoward, Peter J ^b   Kashiyama, Tatsuo ^c   Shono, Masayuki ^c   Akagi, Akiko ^d   Matsuzaki, Tetsuya ^e   Nonaka, Ikuya ^f  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

^d Kyushu University   (Japan)

^e CENTRAL INSTITUTE FOR EXPERIMENTAL ANIMALS   (Japan)

^f NATIONAL INSTITUTE OF MENTAL HEALTH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOFUSCIN; DYSTROPHIN;

ANIMAL TISSUE; ARTICLE; BICEPS BRACHII MUSCLE; CELL DEGENERATION; CELL REGENERATION; CELLULAR DISTRIBUTION; CHILD; CONTROLLED STUDY; DIAPHRAGM MUSCLE; DUCHENNE MUSCULAR DYSTROPHY; ELECTRON MICROSCOPY; HUMAN; HUMAN TISSUE; LASER MICROSCOPY; MACROPHAGE; MALE; MOUSE; MUSCLE CELL; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; ANIMAL; METABOLISM; MUSCLE FIBRIL; PATHOLOGY; PRESCHOOL CHILD; SKELETAL MUSCLE; ULTRASTRUCTURE; X CHROMOSOME LINKED MUSCULAR DYSTROPHIC MOUSE;

ANIMALIA; MURINAE;

ANIMALS; CHILD; CHILD, PRESCHOOL; DYSTROPHIN; HUMANS; LIPOFUSCIN; MACROPHAGES; MALE; MICE; MICE, INBRED MDX; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; MYOFIBRILS;

EID: 16644399758     PISSN: 15672379     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:HIJO.0000045947.83628.a7     Document Type: Article

References (42)

1. Beregi E, Regius O, Hüttl T, Göbl Z (1988) Age-related changes in the skeletal muscle cells. Z Gerontol 21: 83-86.
2. Brenman JE, Chao DS, Xia H, Aldape K, Bredt DS (1995) Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 82: 743-752.
3. Bulfield G, Siller WG, Wight PAL, Moore KJ (1984) X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81: 1189-1192.
4. Chang W-J, Iannaccone ST, Lau KS, Masters BSS, McCabe TJ, McMillan K, Padre RC, Spencer MJ, Tidball JG, Stull JT (1996) Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc Natl Acad Sci USA 93: 9142-9147.
5. Chao DS, Silvagno F, Bredt DS (1998) Muscular dystrophy in mdx mice despite lack of neuronal nitric oxide synthase. J Neurochem 71: 784-789.
6. Crosbie RH, Straub V, Yun H-Y, Lee JC, Rafael JA, Chamberlain JS, Dawson VL, Dawson TM, Campbell KP (1998) Mdx muscle pathology is independent of nNOS perturbation. Hum Mol Genet 7: 823-829.
7. Darley-Usmar V, Wiseman H, Halliwell B (1995) Nitric oxide and oxygen radicals: A question of balance. FEBS Lett 369: 131-135.
8. Disatnik M-H, Dhawan J, Yu Y, Beal MF, Whirl MM, Franco AA, Rando TA (1998) Evidence of oxidative stress in mdx mouse muscle: Studies of the pre-necrotic state. J Neurol Sci 161: 77-84.
9. Disatnik M-H, Chamberlain JS, Rando TA (2000) Dystrophin mutations predict cellular susceptibility to oxidative stress. Muscle Nerve 23: 784-792.
10. Dupont-Versteegden EE, McCarter RJ (1992) Differential expression of muscular dystrophy in diaphragm versus hindlimb muscles of mdx mice. Muscle Nerve 15: 1105-1110.
11. Engel AG, Banker BQ (1994) Ultrastructural changes in diseased muscle. In: Engel AG, Franzini-Armstrong C, eds. Myology: Basic and Clinical. Vol. 1, 2nd edn. New York: McGraw-Hill, pp. 889-1017.
12. Faist V, Koenig J, Hoeger H, Elmadfa I (1998) Mitochondrial oxygen consumption, lipid peroxidation and antioxidant enzyme systems in skeletal muscle of senile dystrophic mice. Pflügers Arch-Eur J Physiol 437: 168-171.
13. Faist V, König J, Höger H, Elmadfa I (2001) Decreased mitochondrial oxygen consumption and antioxidant enzyme activities in skeletal muscle of dystrophic mice after low-intensity exercise. Ann Nutr Metab 45: 58-66.
14. Grozdanovic Z, Gosztonyi G, Gossrau R (1996) Nitric oxide synthase I (NOS-I) is deficient in the sarcolemma of striated muscle fibres in patients with Duchenne muscular dystrophy, suggesting an association with dystrophin. Acta Histochem 98: 61-69.
15. Haycock JW, Neil SM, Jones P, Harris JB, Mantle D (1996) Oxidative damage to muscle protein in Duchenne muscular dystrophy. NeuroReport 8: 357-361.
16. Hoffman EP, Brown RH, Kunkel LM (1987) Dystrophin: The protein product of the Duchenne muscular dystrophy locus. Cell 51: 919-928.
17. Ikeda H, Tauchi H, Sato T (1985) Fine structural analysis of lipofuscin in various issues of rats of different ages. Mech Ageing Dev 33: 77-93.
18. Kameya S, Miyagoe Y, Nonaka I, Ikemoto T, Endo M, Hanaoka K, Nabeshima Y, Takeda S (1999) α1-syntrophin gene disruption results in the absence of neuronal-type nitric-oxide synthase at the sarcolemma but does not induce muscle degeneration. J Biol Chem 274: 2193-2200.
19. Kárpáti G, Carpenter S, Wolfe LS (1988) Clinical and experimental studies on lipofuscin in skeletal muscle fibres. In: Zs-Nagy I, ed. Lipofuscin - 1987: State of the Art, Budapest: Akadémiai Kiadó and Amsterdam: Elsevier Science Publishers, pp. 227-244.
20. Kelley EE, Wagner BA, Buettner GR, Burns CP (1999) Nitric oxide inhibits iron-induced lipid peroxidation in HL-60 cells. Arch Biochem Biophys 370: 97-104.
21. Laule S, Bornemann A (2001) Ultrastructural findings at the satellite cell-myofibre border in normal and diseased human muscle biopsy specimens. Acta Neuropathol 101: 435-439.
22. Louboutin JP, Fichter-Gagnepain V, Thaon E, Fardeau M (1993) Morphometric analysis of mdx diaphragm muscle fibres. Comparison with hindlimb muscles. Neuromuscul Disord 3: 463-469.
23. Louboutin J-P, Rouger K, Tinsley JM, Halldorson J, Wilson JM (2001) iNOS expression in dystrophinopathies can be reduced by somatic gene transfer of dystrophin or utrophin. Mol Med 7: 355-364.
24. Mastaglia FL, Papadimitriou JM, Kakulas BA (1970) Regeneration of muscle in Duchenne muscular dystrophy: An electron microscope study. J Neurol Sci 11: 425-444.
25. McKelvie P, Friling R, Davey K, Kowal L (1999) Changes as the result of ageing in extraocular muscles: A post-mortem study. Aust NZ J Ophthalmol 27: 420-425.
26. Murphy ME, Kehrer JP (1989) Oxidative stress and muscular dystrophy. Chem Biol Interact 69: 101-173.
27. Nakae Y, Stoward PJ, Shono M, Matsuzaki T (1999) Localisation and quantification of dehydrogenase activities in single muscle fibres of mdx gastrocnemius. Histochem Cell Biol 112: 427-436.
28. Nakae Y, Stoward PJ, Shono M, Matsuzaki T (2001) Most apoptotic cells in mdx diaphragm muscle contain accumulated lipofuscin. Histochem Cell Biol 115: 205-214.
29. Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL (1993) Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 90: 3710-3714.
30. 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.
31. Rando TA, Disatnik M-H, Yu Y, Franco A (1998) Muscle cells from mdx mice have an increased susceptibility to oxidative stress. Neuromuscul Disord 8: 14-21.
32. Roth SM, Martel GF, Ivey FM, Lemmer JT, Metter EJ, Hurley BF, Rogers MA (2000) Skeletal muscle satellite cell populations in healthy young and older men and women. Anat Rec 260: 351-358.
33. Schnell SA, Staines WA, Wessendorf MW (1999) Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J Histochem Cytochem 47: 719-730.
34. Schultz E (1976) Fine structure of satellite cells in growing skeletal muscle. Am J Anat 147: 49-70.
35. Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, Petrof B, Narusawa M, Leferovich JM, Sladky JT, Kelly AM (1991) The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352: 536-539.
36. Terman A, Brunk UT (1998a) Lipofuscin: Mechanisms of formation and increase with age. APMIS 106: 265-276.
37. Terman A, Brunk UT (1998b) On the degradability and exocytosis of ceroid/lipofuscin in cultured rat cardiac myocytes. Mech Ageing Dev 100: 145-156.
38. 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.
39. Wehling M, Spencer MJ, Tidball JG (2001) A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 155: 123-131.
40. Wink DA, Hanbauer I, Krishna MC, DeGraff W, Gamson J, Mitchell JB (1993) Nitric oxide protects against cellular damage and cytotoxicity from reactive oxygen species. Proc Natl Acad Sci USA 90: 9813-9817.
41. Yin D (1996) Biochemical basis of lipofuscin, ceroid, and age pigment-like fluorophores. Free Rad Biol Med 21: 871-888.
42. Zhuang W, Eby JC, Cheong M, Mohapatra PK, Bredt DS, Disatnik M-H, Rando TA (2001) The susceptibility of muscle cells to oxidative stress is independent of nitric oxide synthase expression. Muscle Nerve 24: 502-511.