The Dietary Supplement Protandim® Decreases Plasma Osteopontin and Improves Markers of Oxidative Stress in Muscular Dystrophy Mdx Mice

REFERENCES

• Armstrong D, Browne R. The analysis of free radicals, lipid peroxides, antioxidant enzymes and compounds related to oxidative stress as applied to the clinical chemistry laboratory. Adv Exp Med Biol. 1994;366:43–58.
   PubMedGoogle Scholar
• Aviram M, Rosenblat M, Billecke S, Erogul J, Sorenson E, Bisgaier C, Human serum paraoxonase (PON 1) is inactivated by oxidized low density lipoprotein and preserved by antioxidants. Free Radic Biol Med. 1999;26:892–904.
   PubMed Web of Science ®Google Scholar
• Bia B, Cassidy P, Young M, Rafael J, Leighton B, Davies K, Decreased myocardial nNOS, increased iNOS and abnormal ECGs in mouse models of Duchenne muscular dystrophy. J Mol Cell Cardiol. 1999;31:1857–1862.
   PubMed Web of Science ®Google Scholar
• Bogaard H, Natarajan R, Henderson S, Long C, Kraskauskas D, Smithson L, Chronic pulmonary artery pressure elevation is insufficient to explain right heart failure. Circulation. 2009;120:1951–1960.
   PubMed Web of Science ®Google Scholar
• Buetler TM, Renard M, Offord EA, Schneider H, Ruegg UT. Green tea extract decreases muscle necrosis in mdx mice and protects against reactive oxygen species. Am J Clin Nutr. 2002 April 1, 2002;75(4):749–753.
   PubMed Web of Science ®Google Scholar
• Bulfield G, Siller WG, Wight PA, Moore KJ. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA. 1984;81(4):1189–1192.
   PubMed Web of Science ®Google Scholar
• Call J, Voelker K, Wolff A, McMillan R, Evans N, Hulver M, Endurance capacity in maturing mdx mice is markedly enhanced by combined voluntary wheel running and green tea extract. J Appl Physiol. 2008;105(3):923–932.
   PubMed Web of Science ®Google Scholar
• Chang WJ, Iannaccone ST, Lau KS, Masters BS, McCabe TJ, McMillan K, Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc Natl Acad Sci USA. 1996;93(17):9142–9147.
   PubMed Web of Science ®Google Scholar
• Chen X, Dodd G, Thomas S, Zhang X, Wasserman MA, Rovin BH, Activation of Nrf2/ARE pathway protects endothelial cells from oxidant injury and inhibits inflammatory gene expression. Am J Physiol Heart Circ Physiol. 2006;290:H1862–H1870.
   PubMed Web of Science ®Google Scholar
• Chi M, Hintz C, McKee D, Felder S, Grant N, Kaiser K, Effect of Duchenne muscular dystrophy on enzymes of energy metabolism in individual muscle fibers. Metabolism. 1987;36:761–767.
   PubMed Web of Science ®Google Scholar
• Davis J, Murphy E, Carmichael M, Zielinski M, Groschwitz C, Brown A, Curcumin effects on inflammation and performance recovery following eccentric exercise-induced muscle damage. Am J Physiol – Regul Integr Comp Physiol. 2007;292(6):R2168–R2173.
   PubMed Web of Science ®Google Scholar
• Disatnik M, Chamberlain J, Rando T. Dystrophin mutations predict cellular susceptibility to oxidative stress. Muscle & Nerve. 2000;23(5):784–792.
   PubMed Web of Science ®Google Scholar
• Donatella Degl’Innocenti APFRGR. Oxidative stress and calcium homeostasis in dystrophic skin fibroblasts. IUBMB Life. 1999;48(4):391–396.
   PubMed Web of Science ®Google Scholar
• Dorchies OM, Wagner S, Vuadens O, Waldhauser K, Buetler TM, Kucera P, Green tea extract and its major polyphenol (-)-epigallocatechin gallate improve muscle function in a mouse model for Duchenne muscular dystrophy. Am J Physiol Cell Physiol. 2006;290(2):C616–C625.
   PubMed Web of Science ®Google Scholar
• Dudley RWR, Khairallah M, Mohammed S, Lands L, Des Rosiers C, Petrof BJ. Dynamic responses of the glutathione system to acute oxidative stress in dystrophic mouse (mdx) muscles. Am J Physiol Regul Integr Comp Physiol. 2006;291(3):R704–R710.
   PubMed Web of Science ®Google Scholar
• Eckerson HW, Wyte CM, LaDu BN. The human serum paraoxonase/arylesterase polymorphism. Am J Human Fenet. 1983;35(6):1126–38.
   Web of Science ®Google Scholar
• Emery A. Population frequencies of inherited neuromuscular diseases: a world survey. Neuromusc Disord. 1991;1:19–29.
   PubMedGoogle Scholar
• Faist V, Koenig J, Hoeger H, Elmadfa I. Mitochondrial oxygen consumption, lipid peroxidation and antioxidant enzyme systems in skeletal muscle of senile dystrophic mice. Pflügers Arch Eur J Physiol. 1998;437(1):168–171.
   PubMed Web of Science ®Google Scholar
• Gerstenfeld L. Osteopontin in skeletal tissue homeostasis: an emerging picture of the autocrine/paracrine functions of the extracellular matrix. J Bone Miner Res. 1999;14:850–855.
   PubMed Web of Science ®Google Scholar
• Gravallese E. Osteopontin: a bridge between bone and the immune system. J Clin Invest. 2003;112:147–149.
   PubMed Web of Science ®Google Scholar
• Hara H, Nolan P, Scott M, Bucan M, Wakayama Y, Fischbeck K. Running endurance abnormality in mdx mice. Muscle & Nerve. 2002;25(2):207–211.
   PubMed Web of Science ®Google Scholar
• Haycock J, Mac N, Mantle D. Differential protein oxidation in Duchenne and Becker muscular dystrophy. Neuroreport. 1998;9(10):2201–2207.
   PubMed Web of Science ®Google Scholar
• Higashikawa F, Eboshida A, Yokosaki Y. Enhanced biological activity of polymeric osteopontin. FEBS Lett. 2007;581:2697–2701.
   PubMed Web of Science ®Google Scholar
• Hinoi E, Takarada T, Fujimori S, Wang L, Lenato M, Uno K, Nuclear factor E2 p45-related factor 2 negatively regulates chondrogenesis. Bone. 2007;40:337–344.
   PubMed Web of Science ®Google Scholar
• Hunter MIS, Mohamed JB. Plasma antioxidants and lipid peroxidation products in Duchenne muscular dystrophy. Clin Chim Acta. 1986;155(2):123–131.
   PubMed Web of Science ®Google Scholar
• Jackson M, Jones D, Edwards R. Techniques for studying free radical damage in muscular dystrophy. Med Biol. 1984;62(2):135–138.
   PubMedGoogle Scholar
• Joe B, Vijaykumar M, Lokesh B. Biological properties of curcumin-cellular and molecular mechanisms of action. Crit Rev Food Sci Nutr. 2004;44(2):97–111.
   PubMed Web of Science ®Google Scholar
• Johnson K, Polewski M, Terkeltaub R. Transglutaminase 2 is central to induction of the arterial calcification program by smooth muscle cells. Circ Res 2008;102:529–537.
   PubMed Web of Science ®Google Scholar
• Kaartinen M, Pirhonen A, Linnala-Kankkunen A, Maenpaa P. Cross-linking of osteopontin by tissue transglutaminase increases its collagen binding properties. J Biol Chem. 1999;274:1729–1735.
   PubMed Web of Science ®Google Scholar
• Kar N, Pearson C. Catalase, superoxide dismutase, glutathione reductase and thiobarbituric acid-reactive products in normal and dystrophin human muscle. Clin Chim Acta 1979;94:277–280.
   PubMed Web of Science ®Google Scholar
• Kelly HW, Van Natta ML, Covar RA, Tonascia J, Green RP, Strunk RC, Effect of long-term corticosteroid use on bone mineral density in children: a prospective longitudinal assessment in the childhood asthma management program (CAMP) study. Pediatrics. 2008;122(1):e53–e61.
   PubMed Web of Science ®Google Scholar
• Kim B, Jeon W, Hong H, Jeon KB, Hahn JH, Kim YM, The anti-inflammatory activity of Phellinus linteus (Berk. & M.A. Curt.) is mediated through the PKCdelta/Nrf2/ARE signaling to up-regulation of heme oxygenase-1. J Ethnopharmacol. 2007(113):240–247.
   Google Scholar
• Kishore K, Singh M. Effect of bacosides, alcoholic extract of Bacopa monniera Linn. (brahmi), on experimental amnesia in mice. Indian J Exp Biol. 2005;43(7):640–645.
   PubMedGoogle Scholar
• Kramer F, Sandner P, Klein M, Krahn T. Plasma concentrations of matrix metalloproteinase-2, tissue inhibitor of metalloproteinase-1 and osteopontin reflect severity of heart failure in DOCA-salt hypertensive rat. Biomarkers. 2008;13:270–281.
   PubMed Web of Science ®Google Scholar
• Lang I, Deak G, Muzes G, Pronai L, Feher J. Effect of the natural bioflavonoid antioxidant silymarin on superoxide dismutase (SOD) activity and expression in vitro. Biotechnol Ther. 1993;4(3–4):263–270.
   PubMedGoogle Scholar
• Liu J, Gu X, Robbins D, Li G, Shi R, McCond JM, Protandim, a fundamentally new antioxidant approach in chemoprevention using mouse two-stage skin carcinogenesis as a model. PLoS ONE. 2009;4:e5284.
   Web of Science ®Google Scholar
• Mandel S, Weinreb O, Amit T, Youdim M. Cell signaling pathways in the neuroprotective actions of the green tea polyphenol (-)-epigallocatechin-3-gallate: implications for neurodegenerative diseases. J Neurochem. 2004;88(6):1555–1569.
   PubMed Web of Science ®Google Scholar
• Manzur A, Kuntzer T, Pike M, Swan A. Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane Database Syst Rev. 2004;2:CD003725.
   Google Scholar
• McArdle A, Helliwell TR, Beckett GJ, Catapano M, Davis A, Jackson MJ. Effect of propylthiouracil-induced hypothyroidism on the onset of skeletal muscle necrosis in dystrophin-deficient mdx mice. Clin Sci. 1998;95(1):83–89.
   Web of Science ®Google Scholar
• Mendell JR, Engel WK, Derrer EC. Duchenne muscular dystrophy: functional ischemia reproduces its characteristic lesions. Science. 1971;172(3988):1143–1145.
   PubMed Web of Science ®Google Scholar
• Mendell JR, Moxley RT, Griggs RC, Brooke MH, Fenichel GM, Miller JP, Randomized, double-blind six-month trial of prednisone in Duchenne's muscular dystrophy. N Engl J Med. 1989;320(24):1592–1597.
   PubMed Web of Science ®Google Scholar
• Mizuno Y. Changes in superoxide dismutase, catalase, glutathione peroxidase, and glutathione reductase activities and thiobarbituric acid-reactive products levels in early stages of development in dystrophic chickens. Exp Neurol. 1984;84(1):58–73.
   PubMed Web of Science ®Google Scholar
• Mohr S, Hallak H, de Boitte A, Lapetina EG, Brune B. Nitric Oxide-induced S-Glutathionylation and Inactivation of Glyceraldehyde-3-phosphate Dehydrogenase. J Biol Chem. 1999;274(14):9427–9430.
   PubMed Web of Science ®Google Scholar
• Mori R, Shaw T, Martin P. Molecular mechanisms linking wound inflammation and fibrosis: knockdown of osteopontin leads to rapid repair and reduced scarring. J Exp Med. 2008.
   Web of Science ®Google Scholar
• Nakae Y, Hirasaka K, Goto J, Nikawa T, Shono M, Yoshida M, Subcutaneous injection, from birth, of epigallocatechin-3-gallate, a component of green tea, limits the onset of muscular dystrophy in mdx mice: a quantitative histological, immunohistochemical and electrophysiological study. Histochem Cell Biol. 2008;129(4):489–501.
   PubMed Web of Science ®Google Scholar
• Nakae Y, Stoward P, Kashiyama T, Shono M, Akagi A, Matsuzaki T, Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice. J Mol Histol. 2004;35(5):489–499.
   PubMed Web of Science ®Google Scholar
• Nelson S, Bose S, Grunwald G, Myhill P, McCord J. The induction of human superoxide dismutase and catalase in vivo: a fundamentally new approach to antioxidant therapy. Free Radic Biol Med. 2006;40(2):341–347.
   PubMed Web of Science ®Google Scholar
• Nguyen S, Sok D. Oxidative inactivation of paraoxonase1, an antioxidant protein and its effect on antioxidant action. Free Radic Res. 2003;37:1319–1330.
   PubMed Web of Science ®Google Scholar
• Ohkawa H, Ohishi N, Yagi K. Reaction of linoleic acid hydroperoxide with thiobarbituric acid. J Lipid Res. 1978;19(8):1053–1057.
   PubMed Web of Science ®Google Scholar
• Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351–358.
   PubMed Web of Science ®Google Scholar
• Ohta K, Mizuno Y. Studies on pathogenesis of muscular dystrophy: levels of thiobarbituric acid-reactive products in avian muscular dystrophy. No To Shinkei. 1984;36(4):333–337.
   PubMedGoogle Scholar
• Okamoto H. Osteopontin and cardiovascular system. Mol Cell Biochem 2007;300:1–7.
   PubMed Web of Science ®Google Scholar
• Pardo A, Gibson K, Cisneros J, Richards TJ, Yang Y, Becerril C, Up-regulation and profibrotic role of osteopontin in human idiopathic pulmonary fibrosis. PLoS Med. 2005;2:e251.
   PubMed Web of Science ®Google Scholar
• Pockwinse S, JL S, Lian J, Stein G. Developmental stage-specific cellular responses to vitamin D and glucocorticoids during differentiation of the osteoblast phenotype: interrelationship of morphology and gene expression by in situ hybridization. Exp Cell Res. 1995;216:244–260.
   PubMedGoogle Scholar
• Porter J, Khanna S, Kaminski H, Rao JS, Merriam AP, Richmonds CR, A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum Mol Genet. 2002;11:263–272.
   PubMedGoogle Scholar
• Ragusa RJ, Chow CK, Porter JD. Oxidative stress as a potential pathogenic mechanism in an animal model of Duchenne muscular dystrophy. Neuromuscul Disord. 1997;7(6–7):379–386.
   Web of Science ®Google Scholar
• Rando TA, Disatnik M-H, Yu Y, Franco A. Muscle cells from mdx mice have an increased susceptibility to oxidative stress. Neuromuscul Disord. 1998;8(1):14–21.
   PubMed Web of Science ®Google Scholar
• Rasool M, Varalakshmi P. Protective effect of Withania somnifera root powder in relation to lipid peroxidation, antioxidant status, glycoproteins and bone collagen on adjuvant-induced arthritis in rats. Fundam Clin Pharmacol. 2007;21(2):157–164.
   PubMed Web of Science ®Google Scholar
• Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB. 2008;22:659–661.
   PubMed Web of Science ®Google Scholar
• Rodriguez M, Tarnopolsky M. Patients with dystrophinopathy show evidence of increased oxidative stress. Free Radic Biol Med. 2003;34(9):1217–1220.
   PubMed Web of Science ®Google Scholar
• Rosenberg M, Zugck C, Nelles M, Jvenger C, Fronk D, Remppis A, Osteopontin, a new prognostic biomarker in patients with chronic heart failure. Circ Heart Fail. 2008;1:43–49.
   PubMedGoogle Scholar
• Rozenberg O, Aviram M. S-Glutathionylation regulates HDL-associated paraoxonase 1 (PON1) activity. Biochem Biophys Res Commun. 2006;351:492–498.
   PubMed Web of Science ®Google Scholar
• Saito Y, Kon S, Fujiwara Y, Nakayama Y, Kurotaki D, Fukudo N, Osteopontin small interfering RNA protects mice from fulminant hepatitis. Hum Gene Ther. 2007;18:1205–1214.
   PubMed Web of Science ®Google Scholar
• Sander M, Chavoshan B, Harris SA, Iannaccone ST, Stull JT, Thomas GD, Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc Natl Acad Sci USA. 2000;97(25):13818–13823.
   PubMed Web of Science ®Google Scholar
• Scatena M, Liaw L, Giachelli C. Osteopontin: a multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler Thromb Vasc Biol 2007;27:2302–2309.
   PubMedGoogle Scholar
• Senger D, Wirth D, Hynes R. Transformed mammalian cells secrete specific proteins and phosphoproteins. Cell. 1979;16:885–893.
   PubMed Web of Science ®Google Scholar
• Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, Barnard PJ. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science. 1989;244(4912):1578–1580.
   PubMed Web of Science ®Google Scholar
• Soran H, Younis N, Charlton-Menys V, Durrington P. Variation in paraoxonase-1 activity and atherosclerosis. Curr Opin Lipidol. 2009;20:265–274.
   PubMed Web of Science ®Google Scholar
• Stamler JS, Singel DJ, Loscalzo J. Biochemistry of nitric oxide and its redox-activated forms. Science. 1992;258(5090):1898–1902.
   PubMed Web of Science ®Google Scholar
• Thomas GD, Sander M, Lau KS, Huang PL, Stull JT, Victor RG. Impaired metabolic modulation of adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc Natl Acad Sci USA. 1998;95(25):15090–15095.
   PubMed Web of Science ®Google Scholar
• Turk R, Sterrenburg E, Van Der Wees C, de Megjer EJ, de Menezes RX, Groh S, Common pathological mechanisms in mouse models for muscular dystrophies. FASEB. 2006;20:127–129.
   PubMedGoogle Scholar
• Velmurugan K, Alam J, McCord J, Pugazhenthi S. Synergistic induction of heme oxygenase-1 by the components of the antioxidant supplement Protandim. Free Radic Biol Med. 2009;46:430–440.
   PubMed Web of Science ®Google Scholar
• Vetrone S, Montecino-Rodriguez E, Kudryashova E, Kranerovo I, Hoffman EP, Liv SD, Osteopontin promotes fibrosis in dystrophic mouse muscle by modulating immune cell subsets and intramuscular TGF-beta. J Clin Invest. 2009;119:1583–1594.
   PubMed Web of Science ®Google Scholar
• Voisin V, Sébrié C, Matecki S, Yu H, Gillet B, Ramonatxo M, l-arginine improves dystrophic phenotype in mdx mice. Neurobiol Dis. 2005;20(1):123–130.
   PubMed Web of Science ®Google Scholar
• Walter M, Jacob R, Jeffers B, Ghadanfar M, Preston G, Buch J, Serum levels of thiobarbituric acid reactive substances predict cardiovascular events in patients with stable coronary artery disease: a longitudinal analysis of the PREVENT study. J Am Coll Cardiol. 2004;44:1996–2002.
   PubMed Web of Science ®Google Scholar
• Wehling M, Spencer MJ, Tidball JG. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol. 2001;155(1):123–132.
   PubMed Web of Science ®Google Scholar
• Wong BLY, Christopher C. Corticosteroids in Duchenne muscular dystrophy: a reappraisal. J Child Neurol. 2002;17(3):183–190.
   PubMed Web of Science ®Google Scholar
• Wu C, Wu M, Chiang E, Wu CC, Chen YJ, Chen CJ, Elevated plasma osteopontin associated with gastric cancer development, invasion and survival. Gut. 2007(56):782–789.
   PubMedGoogle Scholar