Nuclei of aged myofibres undergo structural and functional changes suggesting impairment in RNA processing

European Journal of Histochemistry

Volumn 53, Issue 2, 2009, Pages 97-106

  Malatesta, Manuela ^a   Perdoni, F ^b   Muller, S ^c   Zancanaro, C ^a   Pellicciari, C ^b  

^a UNIVERSITY OF VERONA   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

^c INSTITUT DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Ageing; Cell nucleus; Sarcopenia; Skeletal muscle; Splicing; Transcription

Indexed keywords

DNA HYBRID; MESSENGER RNA PRECURSOR; RNA; CLEAVAGE STIMULATION FACTOR; DNA; MESSENGER RNA; RNA POLYMERASE II; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ADOLESCENT; AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BICEPS BRACHII MUSCLE; CELL FUNCTION; CELL STRUCTURE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FIBER; IMMUNOCYTOCHEMISTRY; MALE; MORPHOMETRICS; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE DISEASE; MUSCLE MASS; MUSCLE WEAKNESS; NONHUMAN; PROTEIN PHOSPHORYLATION; QUADRICEPS FEMORIS MUSCLE; RAT; RNA HYBRIDIZATION; RNA PROCESSING; RNA SPLICING; SKELETAL MUSCLE; ANIMAL; CELL AGING; CELL NUCLEUS; CYTOLOGY; FAST MUSCLE FIBER; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; NUCLEOLUS; PHYSIOLOGY; SLOW MUSCLE FIBER; ULTRASTRUCTURE; WISTAR RAT;

ANIMALIA; RATTUS;

ANIMALS; CELL AGING; CELL NUCLEOLUS; CELL NUCLEUS; CLEAVAGE STIMULATION FACTOR; DNA; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SKELETAL; MUSCLE FIBERS, SLOW-TWITCH; QUADRICEPS MUSCLE; RATS; RATS, WISTAR; RNA; RNA POLYMERASE II; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; SNRNP CORE PROTEINS;

EID: 70349245041     PISSN: 1121760X     EISSN: None     Source Type: Journal    
DOI: 10.4081/ejh.2009.106     Document Type: Article

References (69)

1. Alway SE, Siu PM. Nuclear apoptosis contributes to sarcopenia. Exerc Sport Sci Rev 2008; 36:51-57
2. Ansved T, Larsson L. Effects of ageing on enzyme-histochemical, morphometrical and contractile properties of the soleus muscle in the rat. J Neurol Sci 1989;93:105-124 (Pubitemid 19244012)
3. Attaix D, Mosoni L, Dardevet D, Combaret L, Patureau Mirand P, Grizard J. Altered responses in skeletal muscle protein turnover during aging in anabolic and catabolic periods. Int J Biochem Cell Biol 2005; 37:1962-1973
4. Bernhard W. A new staining procedure for electron microscopic cytology. J Ultrastruct Res 1969;27:250-265
5. Biggiogera M, Bottone MG, Scovassi AI, Soldani C, Vecchio L, Pellicciari C. Rearrangement of nuclear ribonucleoprotein (RNP)-containing structures during apoptosis and transcriptional arrest. Biol Cell 2004; 96: 603-615 (Pubitemid 39562235)
6. Biggiogera M, Cisterna B, Spedito A, Vecchio L, Malatesta M. Perichromatin fibrils as early markers of transcriptional alterations. Differentiation 2007;76:57-65.
7. Borisov AB, Carlson BM. Cell death in denervated skeletal muscle is distinct from classical apoptosis. Anat Rec 2000; 258:305-318 (Pubitemid 30146013)
8. Brooks NE, Schuenke MD, Hikida RS. Ageing influences myonuclear domain size differently in fast and slow skeletal muscle of rats. Acta Physiologica 2009; doi: 10.1111/j.1748-1716.2009.01983.x.
9. Bruunsgaard H, Pedersen M, Pedersen BK. Aging and proinflammatory cytokines. Curr Opin Hematol 2001;8:131-136
10. Bruusgaard JC, Liestøl K, Gundersen K. Distribution of myonuclei and microtubules in live muscle fibers of young, middle-aged, and old mice. J Appl Physiol 2006; 100:2024-2030 (Pubitemid 43845878)
11. Cardani R, Mancinelli E, Rotondo G, Sansone V, Meola G. Muscleblind-like protein 1 nuclear sequestration is a molecular pathology marker of DM1 and DM2. Eur J Histochem 2006;50:177-182
12. Cisterna B, Flach F, Vecchio L, Barabino SML, Battistelli S, Martin TE, et al. Can a GMO-containing diet influence embryo development? A preliminary study on pre-implantation mouse embryos. Eur J Histochem 2008;52:263-267
13. Combaret L, Dardevet D, Béchet D, Taillandier D, Mosoni L, Attaix D. Skeletal muscle proteolysis in aging. Curr Opin Clin Nutr Metab Care 2009;12:37-41.
14. Deschenes MR. Effects of aging on muscle fibre type and size. Sports Med 2004; 34:809-824
15. Dirks A, Leeuwenburgh C. The role of apoptosis in age-related skeletal muscle atrophy. Sports Med 2005;35:473-483 (Pubitemid 41002968)
16. Doherty TJ. Invited review: Aging and sarcopenia. J Appl Physiol 2003;95:1717-1727
17. Dupont-Versteegden EE. Apoptosis in muscle atrophy: relevance to sarcopenia. Exp Gerontol 2005; 40:473-481 (Pubitemid 40884500)
18. Edström E, Ulfhake B. Sarcopenia is not due to lack of regenerative drive in senescent skeletal muscle. Aging Cell 2005;4:65-77. (Pubitemid 41632905)
19. Fakan S. Ultrastructural cytochemical analyses of nuclear functional architecture. Eur J Histochem 2004; 48:5-14. (Pubitemid 38524331)
20. Gallegly JC, Turesky NA, Strotman BA, Gurley CM, Peterson CA, Dupont-Versteegden EE. Satellite cell regulation of muscle mass is altered at old age. J Appl Physiol 2004; 97: 1082-1090
21. Gundersen K, Bruusgaard JC. Nuclear domains during muscle atrophy: nuclei lost or paradigm lost? J Physiol 2008; 586.11: 2675-2681
22. Hallen A. Accumulation of insoluble protein and ageing. Biogerontol 2002;3:307-315
23. Hepple RT. Sarcopenia: a critical perspective. Sci Aging Knowledge Environ 2003; 2003:pe31.
24. Hughes VA, Frontera WR, Roubenoff R, Evans WJ, Singh MA. Longitudinal changes in body composition in older men and women: role of body weight change and physical activity. Am J Clin Nutr 2002;76:473-481 (Pubitemid 34804075)
25. Jameson CW. Towards a unified and interdisciplinary model of ageing. Med Hypotheses 2004;63:83-86 (Pubitemid 38887116)
26. Kadi F, Charifi N, Denis C, Lexell J. Satellite cells and myonuclei in young and elderly women and men. Muscle Nerve 2004: 29:120-127 (Pubitemid 38040565)
27. Karakelides H, Sreekumaran Nair K. Sarcopenia of aging and its metabolic impact. Curr Top Dev Biol 2005;68:123-148
28. Kim JH, Choy HE, Nam KH, Park SC. Transglutaminase-mediated cross-linking of specific core histone subunits and cellular senescence. Ann N Y Acad Sci 2001;928:65-70.
29. Koopman R, van Loon LJC. Aging, exercise and muscle protein metabolism. J Appl Physiol (January 8, 2009). doi:10.1152/japplphysiol.91551.2008.
30. Lafarga M, Berciano MT, Andres MA. Protein-synthesis inhibition induces perichromatin granule accumulation and intranuclear rodlet formation in osmotically stimulated supraoptic neurons. Anat Embryol 1993;187:363-369 (Pubitemid 23183696)
31. Larsson L, Sjodin B, Karlsson J. Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, ages 22-65 years. Acta Physiol Scand 1978;103:31-39 (Pubitemid 8349314)
32. Leeuwenburgh C. Role of apoptosis in sarcopenia. J Gerontol 2003;58A: 999-1001.
33. Lesnefsky EJ, Hoppel CL. Oxidative phosphorylation and aging. Ageing Res Rev 2006;5:402-433
34. Lexell J. Human aging, muscle mass, and fibre type composition. J Gerontol A Biol Sci Med Sci 1995;50:11-16
35. Lührmann R, Kastner B, Bach M. Structure of spliceosomal snRNPs and their role in pre-mRNA splicing. Biochim Biophys Acta 1990;1087:265-292 (Pubitemid 20377575)
36. Malatesta M, Bertoni-Freddari C, Fattoretti P, Baldelli B, Fakan S, Gazzanelli G. Aging and vitamin E deficiency are responsible for altered RNA pathways. Ann N Y Acad Sci 2004; 1019:379-382 (Pubitemid 38951340)
37. Malatesta M, Bertoni-Freddari C, Fattoretti P, Caporaloni C, Fakan S, Gazzanelli G. Altered RNA structural constituents in aging and vitamin E deficiency. Mech Ageing Dev 2003;124:175-181 (Pubitemid 36293926)
38. Malatesta M, Perdoni F, Battistelli S, Muller S, Zancanaro C. The cell nuclei of skeletal muscle cells are transcriptionally active in hibernating edible dormice. BMC Cell Biol 2009;10:19.
39. Malatesta M, Perdoni F, Santin G, Battistelli S, Muller S, Biggiogera M. Hepatoma tissue culture (HTC) cells as a model for investigating the effects of low concentrations of herbicide on cell structure and function. Toxicol in vitro 2008; 22:1853-1860.
40. Manta P, Vassilopoulos D, Spengos M. Nucleo-cytoplasmic ratio in ageing skeletal muscle. Eur Arch Psychiatry Neurol Sci 1987;236:235-236 (Pubitemid 17054827)
41. Marbaix G, Huez G, Burny A, Cleuter Y, Hubert E, Leclercq M, et al. Absence of polyadenylate segment in globin messenger RNA accelerates its degradation in Xenopus oocytes. Proc Natl Acad Sci USA 1975;72:3065-3067
42. Payne GW, Bearden SE. The microcirculation of skeletal muscle in aging. Microcirculation 2006; 13:275-277
43. Pujol G, Soderqvist H, Radu A. Age-associated reduction of nuclear protein import in human fibroblast. Biochem Biophys Res Comm 2002; 274:354-358 (Pubitemid 34694102)
44. Puvion E, Puvion-Dutilleul F. Ultrastructure of the nucleus in relation to transcription and splicing: roles of perichromatin fibrils and interchromatin granules. Exp Cell Res 1996; 229:217-225 (Pubitemid 27026908)
45. Puvion E, Viron A, Bernhard W. Unusual accumulation of ribonucleoprotein constituents in the nucleus of cultured rat liver cells after hypothermal shock. Biol Cell 1977; 29:81-88 (Pubitemid 8211468)
46. Puvion-Dutilleul F, Puvion E. Relationship between chromatin and perichromatin granules in cadmium-treated isolated hepatocytes. J. Ultrastruct. Res. 1981; 7:341-350
47. Rodrigues Ade C, Schmalbruch H. Satellite cells and myonuclei in long-term denervated rat muscles. Anat Rec 1995;243:430-437
48. Roijkind M, Dominguez-Rosales JA, Nieto N, Greenweld P. Role of hydrogen peroxide and oxidative stress in healing responses. Cell Mol Life Sci 2002; 59:1872-1891 (Pubitemid 36015861)
49. Roubenoff R. Sarcopenia and its implications for the elderly. Eur J Clin Nutr 2000; 54:S40-7.
50. Ryall JG, Schertzer JD, Lynch GS. Cellular and molecular mechanisms underlying age-related skeletal muscle wasting and weakness. Biogerontol 2008;9:213-228
51. Schwarzacher HG, Wachtler F. The nucleolus. Anat Embryol 1993;188:515-536
52. Shaw PJ, Jordan EG. The nucleolus. Ann Rev Cell Dev Biol 1995;11:93-121.
53. Shorey CD, Manning LA, Everitt AV. Morphometrical analysis of skeletal muscle fibre ageing and the effect of hypophysectomy and food restriction in the rat. Gerontol 1988; 34:97-109.
54. Soreq H, Nudel U, Salomon R, Revel M, Littauer UZ. In vitro translation of polyadenylic acid-free rabbit globin messenger RNA. J Mol Biol 1974;88:233-245
55. Spector DL. Nuclear organization and gene expression. Exp Cell Res 1996;229:189-197
56. Stadtman ER. Protein oxidation and aging. Free Radic Res 2006;40:1250-1258
57. Stadtman ER. Role of oxidant species in aging. Curr Med Chem 2004;11:1105-1112
58. Szulc P, Beck TJ, Marchand F, Delmas PD. Low skeletal muscle mass is associated with poor structural parameters of bone and impaired balance in elderly men: the MINOS study. J Bone Miner Res 2005;20:721-729 (Pubitemid 40571628)
59. Tenover JL. Testosterone and the aging male. J Androl 1997;18:103-106
60. Testillano PS, Gorab E, Risueno MC. A new approach to map transcription sites at the ultrastructural level. J Histochem Cytochem 1994; 42:1-10. (Pubitemid 24006628)
61. Thompson LD. Age-related muscle dysfunction. Exp Gerontol 2009;44:106-111
62. Tomonaga M. Histochemical and ultrastructural changes in senile human skeletal muscle. J Am Geriatr Soc 1977; 25:125-131 (Pubitemid 8061236)
63. Veraldi KL, Arhin GK, Martincic K, Chung-Ganster LH, Wilusz J, Milcarek C. HnRNP F influences binding of a 64-kilodalton subunit of cleavage stimulation factor to mRNA precursors in mouse B cells. Mol Cell Biol 2001; 21:1228-1238 (Pubitemid 32114971)
64. Verdijk LB, Koopman R, Schaart G, Meijer K, Savelberg HH, van Loon LJ. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab 2007;292:E151-7.
65. Wada KI, Katsuta S, Soya H. Natural occurrence of myofiber cytoplasmic enlargement accompanied by decrease in myonuclear number. Japanese J Physiol 2003; 53:145-150 (Pubitemid 36950540)
66. Wheeler TM, Thornton CA. Myotonic dystrophy: RNA-mediated muscle disease. Curr Opin Neurol 2007; 20:572-576
67. Wilson MM, Morley JE. Invited review: Aging and energy balance. J Appl Physiol 2003;95:1728-1736
68. Zancanaro C, Malatesta M, Vogel P, Osculati F, Fakan S. Ultrastructural and morphomentrical analyses of the brown adipocyte nucleus in a hibernating dormouse. Biol Cell 1993;79:55-61. (Pubitemid 24009533)
69. Zancanaro C, Mariotti R, Perdoni F, Nicolato E, Malatesta M. Physical training is associated with changes in NMR and morphometrical parameters of the skeletal muscle in senescent mice. Eur J Histochem 2007; 51: 305-310