Aging-associated oxidative stress modulates the acute inflammatory response in skeletal muscle after contusion injury

Experimental Gerontology

Volumn 45, Issue 5, 2010, Pages 381-388

  Ghaly, Ahmed ^a   Marsh, Daniel R ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Chemokines; Contusion injury; Lipid peroxidation; Macrophage; Myeloperoxidase; TGF 1

Indexed keywords

CD68 ANTIGEN; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; GLUTATHIONE; GLUTATHIONE DISULFIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYELOPEROXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TRANSFORMING GROWTH FACTOR BETA1;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNOMODULATION; INFLAMMATION; LIPID PEROXIDATION; MACROPHAGE; MALE; MUSCLE INJURY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SKELETAL MUSCLE;

AGING; ANIMALS; CONTUSIONS; GLUTATHIONE; GLUTATHIONE DISULFIDE; INFLAMMATION; LIPID PEROXIDATION; MALE; MUSCLE, SKELETAL; NEUTROPHIL INFILTRATION; OXIDATIVE STRESS; PEROXIDASE; RATS; RATS, INBRED BN; RATS, INBRED F344; TRANSFORMING GROWTH FACTOR BETA1;

RATTUS;

EID: 77951093548     PISSN: 05315565     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exger.2010.03.004     Document Type: Article

References (39)

1. Aoi W., Naito Y., Takanami Y., Kawai Y., Sakuma K., Ichikawa H., Yoshida N., Yoshikawa T. Oxidative stress and delayed-onset muscle damage after exercise. Free Radic. Biol. Med. 2004, 37:480-487.
2. Bartnik B.L., Juurlink B.H., Devon R.M. Macrophages: their myelinotrophic or neurotoxic actions depend upon tissue oxidative stress. Mult. Scler. 2000, 6:37-42.
3. Bondesen B.A., Mills S.T., Kegley K.M., Pavlath G.K. The COX-2 pathway is essential during early stages of skeletal muscle regeneration. Am. J. Physiol. Cell Physiol. 2004, 287:C475-C483.
4. Callejas N.A., Fernandez-Martinez A., Castrillo A., Bosca L., Martin-Sanz P. Selective inhibitors of cyclooxygenase-2 delay the activation of nuclear factor κB and attenuate the expression of inflammatory genes in murine macrophages treated with lipopolysaccharide. Mol. Pharmacol. 2003, 63:671-677.
5. Carlson B.M., Faulkner J.A. Muscle transplantation between young and old rats: age of host determines recovery. Am. J. Physiol. 1989, 256:C1262-C1266.
6. Carlson M.E., Conboy M.J., Hsu M., Barchas L., Jeong J., Agrawal A., Mikels A.J., Agrawal S., Schaffer D.V., Conboy I.M. Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell. 2009, 8:676-689.
7. Carlson M.E., Hsu M., Conboy I.M. Imbalance between pSmad3 and notch induces CDK inhibitors in old muscle stem cells. Nature 2008, 454:528-532.
8. Chung H.Y., Kim H.J., Kim K.W., Choi J.S., Yu B.P. Molecular inflammation hypothesis of aging based on the anti-aging mechanism of calorie restriction. Microsc. Res. Tech. 2002, 59:264-272.
9. Conboy I.M., Conboy M.J., Smythe G.M., Rando T.A. Notch-mediated restoration of regenerative potential to aged muscle. Science 2003, 302:1575-1577.
10. Conboy I.M., Conboy M.J., Wagers A.J., Girma E.R., Weissman I.L., Rando T.A. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005, 433:760-764.
11. Conboy I.M., Rando T.A. The regulation of notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 2002, 3:397-409.
12. Cuevas M.J., Almar M., Garcia-Glez J.C., Garcia-Lopez D., De Paz J.A., Alvear-Ordenes I., Gonzalez-Gallego J. Changes in oxidative stress markers and NF-κB activation induced by sprint exercise. Free Radic. Res. 2005, 39:431-439.
13. Foster W., Li Y., Usas A., Somogyi G., Huard J. Gamma interferon as an antifibrosis agent in skeletal muscle. J. Orthop. Res. 2003, 21:798-804.
14. Fulle S., Protasi F., Di Tano G., Pietrangelo T., Beltramin A., Boncompagni S., Vecchiet L., Fano G. The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp. Gerontol. 2004, 39:17-24.
15. Ghaly, A., Marsh, D. R. Ischemia-reperfusion modulates the inflammatory and regenerative response of muscle to contusion injury. Int. J. Exp. Pathol. 2010, in press.
16. Harman D. Free-radical theory of aging increasing the functional life span. Ann. N.Y. Acad. Sci. 1994, 717:1-15.
17. Hnia K., Gayraud J., Hugon G., Ramonatxo M., De La P.S., Matecki S., Mornet D. L-arginine decreases inflammation and modulates the nuclear factor-κB/matrix metalloproteinase cascade in MDX muscle fibers. Am. J. Pathol. 2008, 172:1509-1519.
18. Hodgson J.A., Roy R.R., Higuchi N., Monti R.J., Zhong H., Grossman E., Edgerton V.R. Does daily activity level determine muscle phenotype?. J. Exp. Biol. 2005, 208:3761-3770.
19. Javesghani D., Magder S.A., Barreiro E., Quinn M.T., Hussain S.N. Molecular characterization of a superoxide-generating NAD(P)H oxidase in the ventilatory muscles. Am. J. Respir. Crit Care Med. 2002, 165:412-418.
20. Khodr B., Khalil Z. Modulation of inflammation by reactive oxygen species: implications for aging and tissue repair. Free Radic. Biol. Med. 2001, 30:1-8.
21. Kim H.J., Kim K.W., Yu B.P., Chung H.Y. The effect of age on cyclooxygenase-2 gene expression: NF-κB activation and IκBα degradation. Free Radic. Biol. Med. 2000, 28:683-692.
22. Li Y., Foster W., Deasy B.M., Chan Y., Prisk V., Tang Y., Cummins J., Huard J. Transforming growth factor-β1 induces the differentiation of myogenic cells into fibrotic cells in injured skeletal muscle: a key event in muscle fibrogenesis. Am. J. Pathol. 2004, 164:1007-1019.
23. Liu D., Black B.L., Derynck R. TGF-β inhibits muscle differentiation through functional repression of myogenic transcription factors by Smad3. Genes Dev. 2001, 15:2950-2966.
24. Lu Y., Wahl L.M. Oxidative stress augments the production of matrix metalloproteinase-1, cyclooxygenase-2, and prostaglandin E2 through enhancement of NF-κB activity in lipopolysaccharide-activated human primary monocytes. J. Immunol. 2005, 175:5423-5429.
25. Marsh D.R., Criswell D.S., Carson J.A., Booth F.W. Myogenic regulatory factors during regeneration of skeletal muscle in young adult and old rats. J. Appl. Physiol. 1997, 83(4):1270-1275.
26. Marsh D.R., Criswell D.S., Hamilton M.T., Booth F.W. Association of insulin-like growth factor mRNA expressions with muscle regeneration in young, adult, and old rats. Am. J. Physiol. 1997, 273:R353-R358.
27. Marsh D.R., Hinds L.R., Lester W.S., Reinking B.E., Booth F.W. The force-frequency relationship is altered in regenerating and senescent rat skeletal muscle. Muscle Nerve 1998, 21:1265-1274.
28. Masszi A., Fan L., Rosivall L., McCulloch C.A., Rotstein O.D., Mucsi I., Kapus A. Integrity of cell-cell contacts is a critical regulator of TGF-β1-induced epithelial-to-myofibroblast transition: role for β-catenin. Am. J. Pathol. 2004, 165:1955-1967.
29. McGeachie J.K., Grounds M.D. Retarded myogenic cell replication in regenerating skeletal muscles of old mice. an autoradiographic study in young and old BALBc and SJL/J mice. Cell Tissue Res. 1995, 280:277-282.
30. Musaro A., McCullagh K., Paul A., Houghton L., Dobrowolny G., Molinaro M., Barton E.R., Sweeney H.L., Rosenthal N. Localized Igf-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat. Genet. 2001, 27:195-200.
31. Pluchino S., Quattrini A., Brambilla E., Gritti A., Salani G., Dina G., Galli R., Del Carro U., Amadio S., Bergami A., Furlan R., Comi G., Vescovi A.L., Martino G. Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 2003, 422:688-694.
32. Prisk V., Huard J. Muscle injuries and repair: the role of prostaglandins and inflammation. Histol. Histopathol. 2003, 18:1243-1256.
33. Sadeh M. Effects of aging on skeletal muscle regeneration. J. Neurol. Sci. 1988, 87:67-74.
34. Schafer F.Q., Buettner G.R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 2001, 30:1191-1212.
35. Shen W., Li Y., Tang Y., Cummins J., Huard J. NS-398, a cyclooxygenase-2-specific inhibitor, delays skeletal muscle healing by decreasing regeneration and promoting fibrosis. Am. J. Pathol. 2005, 167:1105-1117.
36. Shen W., Li Y., Zhu J., Schwendener R., Huard J. Interaction between macrophages, TGF-β1, and the COX-2 pathway during the inflammatory phase of skeletal muscle healing after injury. J. Cell Physiol. 2008, 214:405-412.
37. Shi H., Liu K.J. Effects of glucose concentration on redox status in rat primary cortical neurons under hypoxia. Neurosci. Lett. 2006, 410:57-61.
38. Turturro A., Witt W.W., Lewis S., Hass B.S., Lipman R.D., Hart R.W. Growth curves and survival characteristics of the animals used in the biomarkers of aging program. J. Gerontol. A Biol. Sci. Med. Sci. 1999, 54:B492-B501.
39. Wickens A.P. Ageing and the free radical theory. Respir. Physiol. 2001, 128:379-391.