Age-dependent regulation of skeletal muscle mitochondria by the thrombospondin-1 receptor CD47

Matrix Biology

Volumn 30, Issue 2, 2011, Pages 154-161

  Frazier, Elfaridah P ^a   Isenberg, Jeff S ^b   Shiva, Sruti ^b   Zhao, Lei ^a   Schlesinger, Paul ^a   Dimitry, Julie ^a   Abu Asab, Mones S ^c   Tsokos, Maria ^c   Roberts, David D ^c   Frazier, William A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

CD47 receptor; Fast twitch fibers; Mitochondria; Mitochondrial biogenesis; Skeletal muscles; Slow twitch fibers

Indexed keywords

CD47 ANTIGEN; MESSENGER RNA; MYOGLOBIN; MYOSIN HEAVY CHAIN; REACTIVE OXYGEN METABOLITE; THROMBOSPONDIN 1;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRON TRANSPORT; GASTROCNEMIUS MUSCLE; MITOCHONDRIAL VOLUME DENSITY; MOUSE; MUSCLE MASS; MUSCLE MITOCHONDRION; MUSCLE TWITCH; NONHUMAN; PHYSICAL PERFORMANCE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; TREADMILL; WILD TYPE;

AGING; ANIMALS; ANTIGENS, CD47; BODY COMPOSITION; BODY WEIGHT; CYTOCHROMES B; CYTOCHROMES C; ENERGY METABOLISM; FEMALE; GENE EXPRESSION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; MYOCYTES, SMOOTH MUSCLE; MYOSIN HEAVY CHAINS; NUCLEAR RESPIRATORY FACTOR 1; PHYSICAL ENDURANCE; PROTEIN ISOFORMS; REACTIVE OXYGEN SPECIES; SUPEROXIDES; THROMBOSPONDIN 1; TRANS-ACTIVATORS; VOLTAGE-DEPENDENT ANION CHANNEL 1;

MUS;

EID: 79952101222     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2010.12.004     Document Type: Article

References (66)

1. Bauer, E.M., Qin, Y., Miller, T.W., Bandle, R.W., Csanyi, G., Pagano, P.J., Bauer, P.M., Schnermann, J., Roberts, D.D., and Isenberg, J.S., 2010. Thrombospondin-1 supports blood pressure by limiting eNOS activation and endothelial-dependent vasorelaxation. Cardiovasc. Res.
2. Benton C.R., Wright D.C., Bonen A. PGC-1alpha-mediated regulation of gene expression and metabolism: implications for nutrition and exercise prescriptions. Appl. Physiol. Nutr. Metab. 2008, 33:843-862.
3. Booth F.W., Chakravarthy M.V., Spangenburg E.E. Exercise and gene expression: physiological regulation of the human genome through physical activity. J. Physiol. 2002, 543:399-411.
4. Bordone L., Cohen D., Robinson A., Motta M.C., van Veen E., Czopik A., Steele A.D., Crowe H., Marmor S., Luo J., et al. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 2007, 6:759-767.
5. Carlezon W.A., Duman R.S., Nestler E.J. The many faces of CREB. Trends Neurosci. 2005, 28:436-445.
6. Chang C.R., Blackstone C. Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J. Biol. Chem. 2007, 282:21583-21587.
7. Chung J., Wang X.Q., Lindberg F.P., Frazier W.A. Thrombospondin-1 acts via IAP/CD47 to synergize with collagen in alpha2beta1-mediated platelet activation. Blood 1999, 94:642-648.
8. Corsetti G., Pasini E., D'Antona G., Nisoli E., Flati V., Assanelli D., Dioguardi F.S., Bianchi R. Morphometric changes induced by amino acid supplementation in skeletal and cardiac muscles of old mice. Am. J. Cardiol. 2008, 101:26E-34E.
9. Cribbs J.T., Strack S. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 2007, 8:939-944.
10. Duncan J.G., Fong J.L., Medeiros D.M., Finck B.N., Kelly D.P. Insulin-resistant heart exhibits a mitochondrial biogenic response driven by the peroxisome proliferator-activated receptor-alpha/PGC-1alpha gene regulatory pathway. Circulation 2007, 115:909-917.
11. Feige J.N., Auwerx J. Transcriptional coregulators in the control of energy homeostasis. Trends Cell Biol. 2007, 17:292-301.
12. Feige J.N., Auwerx J. Transcriptional targets of sirtuins in the coordination of mammalian physiology. Curr. Opin. Cell Biol. 2008, 20:303-309.
13. Feige J.N., Lagouge M., Canto C., Strehle A., Houten S.M., Milne J.C., Lambert P.D., Mataki C., Elliott P.J., Auwerx J. Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metab. 2008, 8:347-358.
14. Finck B.N., Kelly D.P. Peroxisome proliferator-activated receptor gamma coactivator-1 (PGC-1) regulatory cascade in cardiac physiology and disease. Circulation 2007, 115:2540-2548.
15. Frazier W.A., Gao A.-G., Dimitry J., Chung J., Lindberg F.P., Brown E.J., Linder M.E. The thrombospondin receptor integrin-associated protein (CD47) functionally couples to heterotrimeric Gi. J. Biol. Chem. 1999, 274:8554-8560.
16. Guarente L. Mitochondria-a nexus for aging, calorie restriction, and sirtuins?. Cell 2008, 132:171-176.
17. Holloszy J.O. Regulation by exercise of skeletal muscle content of mitochondria and GLUT4. J. Physiol. Pharmacol. 2008, 59(Suppl. 7):5-18.
18. Isenberg J.S., Calzada M.J., Zhou L., Guo N., Lawler J., Wang X.Q., Frazier W.A., Roberts D.D. Endogenous thrombospondin-1 is not necessary for proliferation but is permissive for vascular smooth muscle cell responses to platelet-derived growth factor. Matrix Biol. 2005, 24:110-123.
19. Isenberg J.S., Ridnour L.A., Dimitry J., Frazier W.A., Wink D.A., Roberts D.D. CD47 is necessary for inhibition of nitric oxide-stimulated vascular cell responses by thrombospondin-1. J. Biol. Chem. 2006, 281:26069-26080.
20. Isenberg J.S., Wink D.A., Roberts D.D. Thrombospondin-1 antagonizes nitric oxide-stimulated vascular smooth muscle cell responses. Cardiovasc. Res. 2006, 71:785-793.
21. Isenberg J.S., Hyodo F., Matsumoto K., Romeo M.J., Abu-Asab M., Tsokos M., Kuppusamy P., Wink D.A., Krishna M.C., Roberts D.D. Thrombospondin-1 limits ischemic tissue survival by inhibiting nitric oxide-mediated vascular smooth muscle relaxation. Blood 2007, 109:1945-1952.
22. Isenberg J.S., Hyodo F., Pappan L.K., Abu-Asab M., Tsokos M., Krishna M.C., Frazier W.A., Roberts D.D. Blocking thrombospondin-1/CD47 signaling alleviates deleterious effects of aging on tissue responses to ischemia. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2582-2588.
23. Isenberg J.S., Romeo M.J., Abu-Asab M., Tsokos M., Oldenborg A., Pappan L., Wink D.A., Frazier W.A., Roberts D.D. Increasing survival of ischemic tissue by targeting CD47. Circ. Res. 2007, 100:712-720.
24. Isenberg J.S., Frazier W.A., Krishna M.C., Wink D.A., Roberts D.D. Enhancing cardiovascular dynamics by inhibition of thrombospondin-1/CD47 signaling. Curr. Drug Targets 2008, 9:833-841.
25. Isenberg J.S., Frazier W.A., Roberts D.D. Thrombospondins: from structure to therapeutics: thrombospondin-1: a physiological regulator of nitric oxide signaling. Cell. Mol. Life Sci. 2008, 65:728-742.
26. Isenberg J.S., Maxhimer J.B., Hyodo F., Pendrak M.L., Ridnour L.A., DeGraff W.G., Tsokos M., Wink D.A., Roberts D.D. Thrombospondin-1 and CD47 limit cell and tissue survival of radiation injury. Am. J. Pathol. 2008, 173:1100-1112.
27. Isenberg J.S., Maxhimer J.B., Powers P., Tsokos M., Frazier W.A., Roberts D.D. Treatment of liver ischemia-reperfusion injury by limiting thrombospondin-1/CD47 signaling. Surgery 2008, 144:752-761.
28. Isenberg J.S., Pappan L.K., Romeo M.J., Abu-Asab M., Tsokos M., Wink D.A., Frazier W.A., Roberts D.D. Blockade of thrombospondin-1-CD47 interactions prevents necrosis of full thickness skin grafts. Ann. Surg. 2008, 247:180-190.
29. Isenberg J.S., Roberts D.D., Frazier W.A. CD47: a new target in cardiovascular therapy. Arterioscler. Thromb. Vasc. Biol. 2008, 28:615-621.
30. Isenberg J.S., Romeo M.J., Yu C., Yu C.K., Nghiem K., Monsale J., Rick M.E., Wink D.A., Frazier W.A., Roberts D.D. Thrombospondin-1 stimulates platelet aggregation by blocking the antithrombotic activity of nitric oxide/cGMP signaling. Blood 2008, 111:613-623.
31. Isenberg J.S., Qin Y., Maxhimer J.B., Sipes J.M., Despres D., Schnermann J., Frazier W.A., Roberts D.D. Thrombospondin-1 and CD47 regulate blood pressure and cardiac responses to vasoactive stress. Matrix Biol. 2009, 28:110-119.
32. Jin G., Tsuji K., Xing C., Yang Y.G., Wang X., Lo E.H. CD47 gene knockout protects against transient focal cerebral ischemia in mice. Exp. Neurol. 2009, 217:165-170.
33. Katic M., Kennedy A.R., Leykin I., Norris A., McGettrick A., Gesta S., Russell S.J., Bluher M., Maratos-Flier E., Kahn C.R. Mitochondrial gene expression and increased oxidative metabolism: role in increased lifespan of fat-specific insulin receptor knock-out mice. Aging Cell 2007, 6:827-839.
34. Lagouge M., Argmann C., Gerhart-Hines Z., Meziane H., Lerin C., Daussin F., Messadeq N., Milne J., Lambert P., Elliott P., et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006, 127:1109-1122.
35. Lai L., Leone T.C., Zechner C., Schaeffer P.J., Kelly S.M., Flanagan D.P., Medeiros D.M., Kovacs A., Kelly D.P. Transcriptional coactivators PGC-1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev. 2008, 22:1948-1961.
36. Le Gouill E., Jimenez M., Binnert C., Jayet P.Y., Thalmann S., Nicod P., Scherrer U., Vollenweider P. Endothelial nitric oxide synthase (eNOS) knockout mice have defective mitochondrial beta-oxidation. Diabetes 2007, 56:2690-2696.
37. Leone T.C., Lehman J.J., Finck B.N., Schaeffer P.J., Wende A.R., Boudina S., Courtois M., Wozniak D.F., Sambandam N., Bernal-Mizrachi C., et al. PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 2005, 3:e101.
38. Lin J., Wu H., Tarr P.T., Zhang C.Y., Wu Z., Boss O., Michael L.F., Puigserver P., Isotani E., Olson E.N., et al. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 2002, 418:797-801.
39. Lin J., Handschin C., Spiegelman B.M. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 2005, 1:361-370.
40. Lindberg F.P., Bullard D.C., Caver T.E., Gresham H.D., Beaudet A.L., Brown E.J. Decreased resistance to bacterial infection and granulocyte defects in IAP-deficient mice. Science 1996, 274:795-798.
41. Lira V.A., Benton C.R., Yan Z., Bonen A. PGC-1alpha regulation by exercise training and its influences on muscle function and insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E145-161.
42. Lira V.A., Brown D.L., Lira A.K., Kavazis A.N., Soltow Q.A., Zeanah E.H., Criswell D.S. Nitric oxide and AMPK cooperatively regulate PGC-1 in skeletal muscle cells. J. Physiol. 2010, 588:3551-3566.
43. Lopez-Lluch G., Hunt N., Jones B., Zhu M., Jamieson H., Hilmer S., Cascajo M.V., Allard J., Ingram D.K., Navas P., et al. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc. Natl Acad. Sci. USA 2006, 103:1768-1773.
44. Malek M.H., Olfert I.M. Global deletion of thrombospondin-1 increases cardiac and skeletal muscle capillarity and exercise capacity in mice. Exp. Physiol. 2009, 94:749-760.
45. Manna P.P., Frazier W.A. The mechanism of CD47-dependent killing of T cells: heterotrimeric Gi-dependent inhibition of protein kinase A. J. Immunol. 2003, 170:3544-3553.
46. Maxhimer J.B., Shih H.B., Isenberg J.S., Miller T.W., Roberts D.D. Thrombospondin-1/CD47 blockade following ischemia-reperfusion injury is tissue protective. Plast. Reconstr. Surg. 2009, 124:1880-1889.
47. Miller T.W., Isenberg J.S., Roberts D.D. Thrombospondin-1 is an inhibitor of pharmacological activation of soluble guanylate cyclase. Br. J. Pharmacol. 2010, 159:1542-1547.
48. Nemoto S., Fergusson M.M., Finkel T. SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1{alpha}. J. Biol. Chem. 2005, 280:16456-16460.
49. Nisoli E., Carruba M.O. Nitric oxide and mitochondrial biogenesis. J. Cell Sci. 2006, 119:2855-2862.
50. Nisoli E., Falcone S., Tonello C., Cozzi V., Palomba L., Fiorani M., Pisconti A., Brunelli S., Cardile A., Francolini M., et al. Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proc. Natl Acad. Sci. USA 2004, 101:16507-16512.
51. Oh M., Rybkin I.I., Copeland V., Czubryt M.P., Shelton J.M., van Rooij E., Richardson J.A., Hill J.A., De Windt L.J., Bassel-Duby R., et al. Calcineurin is necessary for the maintenance but not embryonic development of slow muscle fibers. Mol. Cell. Biol. 2005, 25:6629-6638.
52. Rodgers J.T., Lerin C., Haas W., Gygi S.P., Spiegelman B.M., Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 2005, 434:113-118.
53. Salminen A., Kaarniranta K. SIRT1: regulation of longevity via autophagy. Cell. Signal. 2009, 21:1356-1360.
54. Scherz-Shouval R., Elazar Z. ROS, mitochondria and the regulation of autophagy. Trends Cell Biol. 2007, 17:422-427.
55. Scherz-Shouval R., Shvets E., Fass E., Shorer H., Gil L., Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J. 2007, 26:1749-1760.
56. Schmidt R.E., Green K.G., Snipes L.L., Feng D. Neuritic dystrophy and neuronopathy in Akita (Ins2(Akita)) diabetic mouse sympathetic ganglia. Exp. Neurol. 2009, 216:207-218.
57. Shiva S., Sack M.N., Greer J.J., Duranski M., Ringwood L.A., Burwell L., Wang X., MacArthur P.H., Shoja A., Raghavachari N., et al. Nitrite augments tolerance to ischemia/reperfusion injury via the modulation of mitochondrial electron transfer. J. Exp. Med. 2007, 204:2089-2102.
58. Spangenburg E.E., Booth F.W. Molecular regulation of individual skeletal muscle fibre types. Acta Physiol. Scand. 2003, 178:413-424.
59. Timmers H.J., Pacak K., Huynh T.T., Abu-Asab M., Tsokos M., Merino M.J., Baysal B.E., Adams K.T., Eisenhofer G. Biochemically silent abdominal paragangliomas in patients with mutations in the succinate dehydrogenase subunit B gene. J. Clin. Endocrinol. Metab. 2008, 93:4826-4832.
60. Uldry M., Yang W., St-Pierre J., Lin J., Seale P., Spiegelman B.M. Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab. 2006, 3:333-341.
61. Uluckan O., Becker S.N., Deng H., Zou W., Prior J.L., Piwnica-Worms D., Frazier W.A., Weilbaecher K.N. CD47 regulates bone mass and tumor metastasis to bone. Cancer Res. 2009, 69:3196-3204.
62. Wang X.Q., Lindberg F.P., Frazier W.A. Integrin-associated protein stimulates alpha2beta1-dependent chemotaxis via Gi-mediated inhibition of adenylate cyclase and extracellular-regulated kinases. J. Cell Biol. 1999, 147:389-400.
63. Wenz T., Rossi S.G., Rotundo R.L., Spiegelman B.M., Moraes C.T. Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging. Proc. Natl Acad. Sci. USA 2009, 106:20405-20410.
64. Wozniak A.C., Anderson J.E. Nitric oxide-dependence of satellite stem cell activation and quiescence on normal skeletal muscle fibers. Dev. Dyn. 2007, 236:240-250.
65. Wu Z., Huang X., Feng Y., Handschin C., Feng Y., Gullicksen P.S., Bare O., Labow M., Spiegelman B., Stevenson S.C. Transducer of regulated CREB-binding proteins (TORCs) induce PGC-1alpha transcription and mitochondrial biogenesis in muscle cells. Proc. Natl Acad. Sci. USA 2006, 103:14379-14384.
66. Yao, M., Roberts, D.D., and Isenberg, J.S., 2011. Thrombospondin-1 inhibition of vascular smooth muscle cell responses occurs via modulation of both cAMP and cGMP. Pharmacol Res. 63, 13-22.