Continuous myofiber remodeling in uninjured extraocular myofibers: Myonuclear turnover and evidence for apoptosis

Muscle and Nerve

Volumn 29, Issue 5, 2004, Pages 707-715

  McLoon, Linda K ^a   Rowe, Jocelyn ^a   Wirtschafter, Jonathan ^a   McCormick, Kathleen M ^b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Apopotosis; Extraocular muscles; Mitosis; Myofibers; Satellite cells

Indexed keywords

BIOLOGICAL MARKER; BROXURIDINE; CASPASE 3; DYSTROPHIN; KI 67 ANTIGEN; LAMININ; MYOGENIC FACTOR; SCATTER FACTOR; TRANSCRIPTION FACTOR PAX7;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL FUSION; CONTROLLED STUDY; CYTOPLASM; ENZYME LOCALIZATION; EXTRAOCULAR MUSCLE; IMMUNOHISTOCHEMISTRY; MUSCLE CELL; MUSCLE EXCITATION; MYOPATHY; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RABBIT; SATELLITE CELL; SKELETAL MUSCLE;

ANIMALS; APOPTOSIS; CELL NUCLEUS; MUSCLE FIBERS; MUSCLE, SKELETAL; RABBITS; REGENERATION;

EID: 1642398604     PISSN: 0148639X     EISSN: None     Source Type: Journal    
DOI: 10.1002/mus.20012     Document Type: Article

References (52)

1. Allen DL, Monke SR, Talmadge RJ, Roy RR, Edgerton VR. Plasticity of myonuclear number in hypertrophied and atrophied mammalian skeletal muscle fibers. J Appl Physiol 1995;78:1969-1976.
2. Allen DL, Linderman JK, Roy RR, Bigbee AJ, Grindeland RE, Mukku V, Edgerton VR. Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. Am J Physiol 1997;273:C579-C587.
3. Barton-Davis ER, Shoturma DI, Musaro A, Rosenthal N, Sweeney HL. Viral mediated expression of insulin-like growth factor I blocks the aging-related loss of skeletal muscle function. Proc Natl Acad Sci USA 1998;95:15603-15607.
4. Beauchamp JR, Heslop L, Yu DS, Tajbakhsh S, Kelly RG, Wernig A, Buckingham ME, Partridge TA, Zammit PS. Expression of CD34 and Myf5 defines the majority of quiescent adult skeletal muscle satellite cells. J Cell Biol 2000;151:1221-1233.
5. Blaveri K, Heslop L, Yu DS, Rosenblatt JD, Gross JG, Partridge TA, Morgan JE. Patterns of repair of dystrophic mouse muscle: studies on isolated fibers. Dev Dynam 1999;216:244-256.
6. Borisov AB, Carlson BM. Cell death in denervated skeletal muscle is distinct from classical apoptosis. Anat Rec 2000;258:305-318.
7. Decary S, Ben Hamida C, Mouly V, Barbet JP, Hentati F, Butler-Browne GS. Shorter telomeres in dystrophic muscle consistent with extensive regeneration in young children. Neuromuscul Disord 2000;10:113-120.
8. Dee K, Freer M, Mei Y, Weyman CM. Apoptosis coincident with the differentiation of skeletal myoblasts is delayed by caspase 3 inhibition and abrogated by MEK-independent constitutive Ras signaling. Cell Death Differ 2002;9:209-218.
9. Fernando P, Kelly JF, Balazsi K, Slack RS, Megeney LA. Caspase 3 activity is required for skeletal muscle differentiation. Proc Natl Acad Sci USA 2002;99:11025-11030.
10. Fischer MD, Gorospe JR, Felder E, Bogdanovich S, Pedrosa-Domellof F, Ahima RS, Rubinstein NA, Hoffman EP, Khurana TS. Expression profiling reveals metabolic and structural components of extraocular muscles. Physiol Genomics 2002;9:71-84.
11. Friden J, Lieber RL. Segmental muscle fiber lesions after repetitive eccentric contractions. Cell Tissue Res 1998;293:165-171.
12. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 1992;119:493-501.
13. Goldberg SJ, Shall MS. Motor units of extraocular muscles: recent findings. Progr Brain Res 1999;123:221-232.
14. Gussoni E, Bennett RR, Muskiewicz KR, Meyerrose T, Nolta JA, Gilgoff I, Stein J, Chan Y, Lidov HG, Bonnemann CG, von Moers A, Morris GE, den Dunnen JT, Chamberlain JS, Kunkel LM, Weinberg K. Long-term persistence of donor nuclei in a Duchenne muscular dystrophy patient receiving bone marrow transplantation. J Clin Invest 2002;110:807-814.
15. Hack AA, Chantal TL, Jiang F, Clendenin CJ, Sigrist KS, Wollman RL, McNally EM. γ-sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin. J Cell Biol 1998;142:1279-1287.
16. Henson C, Staunton H, Brett FM. Does ageing have an effect on midbrain premotor nuclei for vertical eye movements? Mov Disord 2005;18:688-694.
17. Horton RM, Manfredi AA, Conti-Tronconi BM. The embryonic gamma subunit of the nicotinic acetylcholine receptor is expressed in adult extraocular muscle. Neurology 1993;43:983-986.
18. Karpati G, Carpenter S. Small-caliber skeletal muscle fibers do not suffer deleterious consequences of dystrophic gene expression. Am J Med Genet 1986;25:653-658.
19. Koga M, Hiromatsu Y, Jimi A, Inoue Y, Nonaka K. Possible involvement of Fas-mediated apoptosis in eye muscle tissue from patients with thyroid-associated ophthalmopathy. Thyroid 1998;8:311-318.
20. Kong J, Anderson JE. Dynamic restoration of dystrophin to dystrophin-deficient myotubes. Muscle Nerve 2001;24:77-88.
21. Lucas CA, Hoh JF. Extraocular fast myosin heavy chain expression in the levator palpebrae and retractor bulbi muscles. Invest Ophthalmol Vis Sci 1997;38:2817-2825.
22. Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 1961;9:493-495.
23. McLoon LK, Christiansen SP. A novel approach to treatment of strabismus: increasing extraocular muscle strength in rabbits with insulin growth factor II. Invest Ophthalmol Vis Sci 2003;44:3866-3872.
24. McLoon LK, Rios L, Wirtschafter JD. Complex three-dimensional patterns of myosin isoform expression: differences between and within specific extraocular muscles. J Muscle Res Cell Motil 1999;20:771-783.
25. McLoon LK, Wirtschafter JD. NCAM is expressed in mature extraocular muscles. Invest Ophthalmol Vis Sci 1996;37:318-327.
26. McLoon LK, Wirtschafter JD. Continuous myonuclear addition to single extraocular myofibers of uninjured adult rabbits. Muscle Nerve 2002;25:348-358.
27. McLoon LK, Wirtschafter JD. Activated satellite cells are present in uninjured extraocular muscles of mature mice. Trans Am Ophthalmol Soc 2002;100:119-124.
28. McLoon LK, Wirtschafter JD. Activated satellite cens in extraocular muscles of normal adult monkeys and humans. Invest Ophthalmol Vis Sci 2003;44:1927-1932.
29. Melone MAB, Peluso G, Petillo O, Galderisi U, Cotrufo R. 1999. Defective growth in vitro in Duchenne muscular dystrophy myoblasts: the molecular and biochemical basis. J Cell Biochem 1999;76:118-132.
30. Mootoosamy RC, Dietrich S. Distinct regulatory cascades for head and trunk myogenesis. Development 2002;129:573-583.
31. Muhlendyck H. Age-dependent changes in transverse sections of muscle fibers from the exterior eye muscles in man. Z Gerontol 1979;12:46-59.
32. Oh SY, Poukens V, Cohen MS, Demer JL. Structure-function correlation in laminar vascularity in human rectus extraocular muscles. Invest Ophthalmol Vis Sci 2001;42:17-22.
33. Olwin BB, Hauschka SD. Cell surface fibroblast growth factor and epidermal growth factor receptors are permanently lost during skeletal muscle terminal differentiation in culture. J Cell Biol 1988;107:761-769.
34. Paul AC, Rosenthal N. Different modes of hypertrophy in skeletal muscle fibers. J Cell Biol 2002;156:751-760.
35. Porter JD, Baker RS. Muscles of a different 'color': the unusual properties of the extraocular muscles may predispose or protect them in neurogenic and myogenic disease. Neurology 1996;46:30-37.
36. Putman CT, Dusterhoft S, Pette D. Satellite cell proliferation in low frequency-stimulated fast muscle of hypothyroid rat. Am J Physiol Cell Physiol 2000;279:C682-C690.
37. Reiner A, Medina L, Figueredo-Cardenas G, Anfinson S. Brain-stem motoneuron pools that are selectively resistant in amyotrophic lateral sclerosis are preferentially enriched in parvalbumin: evidence from monkey brainstem for a calcium-mediated mechanism in sporadic ALS. Exp Neurol 1995;131:239-250.
38. Richard I, Roudaut C, Marchand S, Baghdiguian S, Herasse M, Stockholm D, Ono Y, Suel L, Bourge N, Sorimachi H, Lefranc G, Fardeau M, Sebille A, Beckmann JS. Loss of calpain 3 proteolytic activity leads to muscular dystrophy and to apoptosis-associated IκBα/nuclear factor κB pathway perturbation in mice. J Cell Biol 2000;151:1583-1590.
39. Rodrigues AD, Schmalbruch H. Satellite cells and myonuclei in long-term denervated rat muscles. Anat Rec 1995;243:430-437.
40. Ruest LB, Marcotte R, Wang E. Peptide elongation factor eEF1A-2S1 expression in cultured differentiated myotubes and its protective effect against caspase-3-mediated apoptosis. J Biol Chem 2002;277:5418-5425.
41. Schmalbruch H. Segmental fiber breakdown and defects of the plasmalemma in diseased human muscles. Acta Neuropathol 1975;33:129-141.
42. Schultz E, McCormick KM. Skeletal muscle satellite cells. Rev Physiol Biochem Pharmacol 1994;123:213-257.
43. Schulze-Osthoff K, Walczak H, Droge W, Krammer P. Cell nucleus and DNA fragmentation are not required for apoptosis. J Cell Biol 1994;127:15-20.
44. Schwartz LM, Smith SW, Jones ME, Osborne BA. Do all programmed cell deaths occur via apoptosis? Proc Natl Acad Sci USA 1993;90:980-984.
45. Seale P, Sabourin LA, Girgis-Garbardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells. Cell 2000;15:777-786.
46. Silvestrini R, Costa A, Verneroni S, Del Bino G, Persici P. Comparative analysis of different approaches to investigate cell kinetics. Cell Tissue Kinet 1988;21:123-131.
47. Smith HK, Maxwell L, Rodgers CD, McKee NH, Phyley MJ. Exercise-enhanced satellite cell proliferation and new myonuclear addition in rat skeletal muscle. J Appl Physiol 2001;90:1407-1414.
48. Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and myf-5 act upstream of MyoD. Cell 1997;89:127-138.
49. Taoka T, Iwasaki S, Uchida H, Fukusumi A, Kichikawa K, Nakagawa H, Takayama K, Sakamoto M, Ohishi H. Enhancement pattern of normal extraocular muscles in dynamic contrast-enhanced MR imaging with fat suppression. Acta Radiol 2000;41:211-216.
50. Tatsumi R, Anderson JE, Nevoret CJ, Halevy O, Allen RE. HGF/SF is present in normal adult skeletal muscle and is capable of activating satellite cells. Devel Biol 1998;194:114-128.
51. Tidball JG, Albrecht DE, Lokensgard BE, Spencer MJ. Apoptosis precedes necrosis of dystrophic-deficient muscle. J Cell Sci 1995;108:2197-2204.
52. Wieczorek DF, Periasamy M, Butler-Browne GS, Whalen RG, Nadal-Ginard B. Co-expression of multiple myosin heavy chain genes, in addition to a tissue-specific one, in extraocular muscles. J Cell Biol 1985;101:618-629.