Pharmacological activation of PPARβ promotes rapid and calcineur-independent fiber remodeling and angiogenesis in mouse skeletal muscle

American Journal of Physiology - Endocrinology and Metabolism

Volumn 295, Issue 2, 2008, Pages

  Gaudel, Céline ^a   Schwartz, Chantal ^a   Giordano, Christian ^a   Abumrad, Nada A ^b   Grimaldi, Paul A ^a  

^a INSERM   (France)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

Metabolism; Myogenesis; Type 2 diabetes

Indexed keywords

[4 [2 (3 FLUORO 4 TRIFLUOROMETHYLPHENYL) 4 METHYL 5 THIAZOLYLMETHYLTHIO] 2 METHYLPHENOXY]ACETIC ACID; ACTIN; CALCINEURIN; CD31 ANTIGEN; CYCLOSPORIN A; MYOD1 PROTEIN; MYOGENIC FACTOR 5; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA AGONIST; SUCCINATE DEHYDROGENASE; TATA BINDING PROTEIN; TRANSCRIPTION FACTOR NFAT; VASCULOTROPIN A; CYCLOSPORIN; MYF5 PROTEIN, MOUSE; MYOD PROTEIN; MYOD1 MYOGENIC DIFFERENTIATION PROTEIN; THIAZOLE DERIVATIVE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FATTY ACID OXIDATION; HISTOLOGY; HYPERPLASIA; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; MUSCLE CAPILLARY; MUSCLE DEVELOPMENT; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSGENIC MOUSE; ANIMAL; C57BL MOUSE; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; METABOLISM; MUSCLE CELL; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; CALCINEURIN; CYCLOSPORINE; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE FIBERS; MUSCLE, SKELETAL; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; NEOVASCULARIZATION, PHYSIOLOGIC; PHYSICAL CONDITIONING, ANIMAL; PPAR-BETA; SUCCINATE DEHYDROGENASE; THIAZOLES;

EID: 52649174345     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00581.2007     Document Type: Article

References (51)

1. Allen DL, Harrison BC, Maass A, Bell ML, Byrnes WC, Leinwand LA. Cardiac and skeletal muscle adaptations to voluntary wheel running in the mouse. J Appl Physiol 90: 1900-1908, 2001.
2. Allen DL, Sartorius CA, Sycuro LK, Leinwand LA. Different pathways regulate expression of the skeletal myosin heavy chain genes. J Biol Chem 276: 43524-43533, 2001.
3. Andersen P, Henriksson J. Training induced changes in the subgroups of human type II skeletal muscle fibres. Acta Physiol Scand 99: 123-125, 1977.
4. Armesilla AL, Lorenzo E, Gomez del Arco P, Martinez-Martinez S, Alfranca A, Redondo JM. Vascular endothelial growth factor activates nuclear factor of activated T cells in human endothelial cells: a role for tissue factor gene expression. Mol Cell Biol 19: 2032-2043, 1999.
5. Birot OJ, Koulmann N, Peinnequin A, Bigard XA. Exercise-induced expression of vascular endothelial growth factor mRNA in rat skeletal muscle is dependent on fibre type. J Physiol 552: 213-221, 2003.
6. Breen EC, Johnson EC, Wagner H, Tseng HM, Sung LA, Wagner PD. Angiogenic growth factor mRNA responses in muscle to a single bout of exercise. J Appl Physiol 81: 355-361, 1996.
7. Brown MD, Cotter MA, Hudlicka O, Vrbova G. The effects of different patterns of muscle activity on capillary density, mechanical properties and structure of slow and fast rabbit muscles. Pflügers Arch 361: 241-250, 1976.
8. Brutsaert TD, Gavin TP, Fu Z, Breen EC, Tang K, Mathieu-Costello O, Wagner PD. Regional differences in expression of VEGF mRNA in rat gastrocnemius following 1 hr exercise or electrical stimulation. BMC Physiol 2: 8-18, 2002.
9. Chakkalakal JV, Stocksley MA, Harrison MA, Angus LM, Deschenes-Furry J, St-Pierre S, Megeney LA, Chin ER, Michel RN, Jasmin BJ. Expression of utrophin A mRNA correlates with the oxidative capacity of skeletal muscle fiber types and is regulated by calcineurin/NFAT signaling. Proc Natl Acad Sci USA 100: 7791-7796, 2003.
10. Chin ER, Olson EN, Richardson JA, Yang Q, Humphries C, Shelton JM, Wu H, Zhu W, Bassel-Duby R, Williams RS. A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 12: 2499-2509, 1998.
11. Constantin D, Constantin-Teodosiu D, Layfield R, Tsintzas K, Bennett AJ, Greenhaff PL. PPARdelta agonism induces a change in fuel metabolism and activation of an atrophy programme, but does not impair mitochondrial function in rat skeletal muscle. J Physiol 583: 381-390, 2007.
12. Cooper J, Hudlicka O. Effect on muscle fatigue of the changes in the capillary bed induced by long-term stimulation [proceedings]. J Physiol 263: 155P-156P, 1976.
13. Da Silva-Azevedo L, Baum O, Zakrzewicz A, Pries AR. Vascular endothelial growth factor is expressed in endothelial cells isolated from skeletal muscles of nitric oxide synthase knockout mice during prazosin-induced angiogenesis. Biochem Biophys Res Commun 297: 1270-1276, 2002.
14. DeFronzo RA, Gunnarsson R, Bjorkman O, Olsson M, Wahren J. Effects of insulin on peripheral and splanchnic glucose metabolism in noninsulin-dependent (type II) diabetes mellitus. J Clin Invest 76: 149-155, 1985.
15. Dhawan J, Rando TA. Stem cells in postnatal myogenesis: molecular mechanisms of satellite cell quiescence, activation and replenishment. Trends Cell Biol 15: 666-673, 2005.
16. Dressel U, Allen TL, Pippal JB, Rohde PR, Lau P, Muscat GE. The peroxisome proliferator-activated receptor beta/delta agonist, GW501516, regulates the expression of genes involved in lipid catabolism and energy uncoupling in skeletal muscle cells. Mol Endocrinol 17: 2477-2493, 2003.
17. Fauconnet S, Lascombe I, Chabannes E, Adessi GL, Desvergne B, Wahli W, Bittard H. Differential regulation of vascular endothelial growth factor expression by peroxisome proliferator-activated receptors in bladder cancer cells. J Biol Chem 277: 23534-23543, 2002.
18. Ferrara N. Role of vascular endothelial growth factor in regulation of physiological angiogenesis. Am J Physiol Cell Physiol 280: C1358-C1366, 2001.
19. Fritz T, Kramer DK, Karlsson HK, Galuska D, Engfeldt P, Zierath JR, Krook A. Low-intensity exercise increases skeletal muscle protein expression of PPARdelta and UCP3 in type 2 diabetic patients. Diabetes Metab Res Rev 22: 492-498, 2006.
20. Funk WD, Ouellette M, Wright WE. Molecular biology of myogenic regulatory factors. Mol Biol Med 8: 185-195, 1991.
21. Goodyear LJ, Kahn BB. Exercise, glucose transport, and insulin sensitivity. Annu Rev Med 49: 235-261, 1998.
22. Graef IA, Chen F, Chen L, Kuo A, Crabtree GR. Signals transduced by Ca(2+)/calcineurin and NFATc3/c4 pattern the developing vasculature. Cell 105: 863-875, 2001.
23. Graham TL, Mookherjee C, Suckling KE, Palmer CN, Patel L. The PPARdelta agonist GW0742X reduces atherosclerosis in LDLR(-/-) mice. Atherosclerosis 181: 29-37, 2005.
24. Grimaldi PA. Regulatory role of peroxisome proliferator-activated receptor delta (PPAR delta) in muscle metabolism. A new target for metabolic syndrome treatment? Biochimie 87: 5-8, 2005.
25. Gute D, Fraga C, Laughlin MH, Amann JF. Regional changes in capillary supply in skeletal muscle of high-intensity endurance-trained rats. J Appl Physiol 81: 619-626, 1996.
26. Hernandez GL, Volpert OV, Iniguez MA, Lorenzo E, Martinez-Martinez S, Grau R, Fresno M, Redondo JM. Selective inhibition of vascular endothelial growth factor-mediated angiogenesis by cyclosporin A: roles of the nuclear factor of activated T cells and cyclooxygenase 2. J Exp Med 193: 607-620, 2001.
27. Holst D, Luquet S, Nogueira V, Kristiansen K, Leverve X, Grimaldi PA. Nutritional regulation and role of peroxisome proliferator-activated receptor delta in fatty acid catabolism in skeletal muscle. Biochim Biophys Acta 1633: 43-50, 2003.
28. Jansson E, Kaijser L. Muscle adaptation to extreme endurance training in man. Acta Physiol Scand 100: 315-324, 1977.
29. Leibowitz MD, Fievet C, Hennuyer N, Peinado-Onsurbe J, Duez H, Bergera J, Cullinan CA, Sparrow CP, Baffic J, Berger GD, Santini C, Marquis RW, Tolman RL, Smith RG, Moller DE, Auwerx J. Activation of PPARdelta alters lipid metabolism in db/db mice. FEBS Lett 473: 333-336, 2000.
30. Lloyd PG, Prior BM, Yang HT, Terjung RL. Angiogenic growth factor expression in rat skeletal muscle in response to exercise training. Am J Physiol Heart Circ Physiol 284: H1668-H1678, 2003.
31. Luquet S, Lopez-Soriano J, Holst D, Fredenrich A, Melki J, Rassoulzadegan M, Grimaldi PA. Peroxisome proliferator-activated receptor delta controls muscle development and oxidative capability. FASEB J 17: 2299-2301, 2003.
32. McCullagh KJ, Calabria E, Pallafacchina G, Ciciliot S, Serrano AL, Argentini C, Kalhovde JM, Lomo T, Schiaffino S. NFAT is a nerve activity sensor in skeletal muscle and controls activity-dependent myosin switching. Proc Natl Acad Sci USA 101: 10590-10595, 2004.
33. Mercier J, Perez-Martin A, Bigard X, Ventura R. Muscle plasticity and metabolism: effects of exercise and chronic diseases. Mol Aspects Med 20: 319-373, 1999.
34. Miniou P, Tiziano D, Frugier T, Roblot N, Le Meur M, Melki J. Gene targeting restricted to mouse striated muscle lineage. Nucleic Acids Res 27: e27, 1999.
35. Namgaladze D, Shcherbyna I, Kienhofer J, Hofer HW, Ullrich V. Superoxide targets calcineurin signaling in vascular endothelium. Biochem Biophys Res Commun 334: 1061-1067, 2005.
36. Oliver WR Jr, Shenk JL, Snaith MR, Russell CS, Plunket KD, Bodkin NL, Lewis MC, Winegar DA, Sznaidman ML, Lambert MH, Xu HE, Sternbach DD, Kliewer SA, Hansen BC, Willson TM. A selective peroxisome proliferator-activated receptor delta agonist promotes reverse cholesterol transport. Proc Natl Acad Sci USA 98: 5306-5311, 2001.
37. Olson EN, Williams RS. Calcineurin signaling and muscle remodeling. Cell 101: 689-692, 2000.
38. Peeters LL, Vigne JL, Tee MK, Zhao D, Waite LL, Taylor RN. PPARgamma represses VEGF expression in human endometrial cells: implications for uterine angiogenesis. Angiogenesis 8: 373-379, 2005.
39. Piqueras L, Reynolds AR, Hodivala-Dilke KM, Alfranca A, Redondo JM, Hatae T, Tanabe T, Warner TD, Bishop-Bailey D. Activation of PPARbeta/delta induces endothelial cell proliferation and angiogenesis. Arterioscler Thromb Vasc Biol 27: 63-69, 2007.
40. Rafiee P, Heidemann J, Ogawa H, Johnson NA, Fisher PJ, Li MS, Otterson MF, Johnson CP, Binion DG. Cyclosporin A differentially inhibits multiple steps in VEGF induced angiogenesis in human microvascular endothelial cells through altered intracellular signaling. Cell Commun Signal 2: 3, 2004.
41. Schuler M, Ali F, Chambon C, Duteil D, Bornert JM, Tardivel A, Desvergne B, Wahli W, Chambon P, Metzger D. PGC1alpha expression is controlled in skeletal muscles by PPARbeta, whose ablation results in fiber-type switching, obesity, and type 2 diabetes. Cell Metab 4: 407-414, 2006.
42. Schulz RA, Yutzey KE. Calcineurin signaling and NFAT activation in cardiovascular and skeletal muscle development. Dev Biol 266: 1-16, 2004.
43. Sprecher DL, Massien C, Pearce G, Billin AN, Perlstein I, Willson TM, Hassall DG, Ancellin N, Patterson SD, Lobe DC, Johnson TG. Triglyceride:high-density lipoprotein cholesterol effects in healthy subjects administered a peroxisome proliferator activated receptor delta agonist. Arterioscler Thromb Vasc Biol 27: 359-365, 2007.
44. Stephen RL, Gustafsson MC, Jarvis M, Tatoud R, Marshall BR, Knight D, Ehrenborg E, Harris AL, Wolf CR, Palmer CN. Activation of peroxisome proliferator-activated receptor delta stimulates the proliferation of human breast and prostate cancer cell lines. Cancer Res 64: 3162-3170, 2004.
45. Stewart CE, Rittweger J. Adaptive processes in skeletal muscle: molecular regulators and genetic influences. J Musculoskelet Neuronal Interact 6: 73-86, 2006.
46. Tanaka T, Yamamoto J, Iwasaki S, Asaba H, Hamura H, Ikeda Y, Watanabe M, Magoori K, Ioka RX, Tachibana K, Watanabe Y, Uchiyama Y, Sumi K, Iguchi H, Ito S, Doi T, Hamakubo T, Naito M, Auwerx J, Yanagisawa M, Kodama T, Sakai J. Activation of peroxisome proliferator-activated receptor delta induces fatty acid beta-oxidation in skeletal muscle and attenuates metabolic syndrome. Proc Natl Acad Sci USA 100: 15924-15929, 2003.
47. Tanner CJ, Barakat HA, Dohm GL, Pories WJ, MacDonald KG, Cunningham PR, Swanson MS, Houmard JA. Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 282: E1191-E1196, 2002.
48. Vissing K, Andersen JL, Schjerling P. Are exercise-induced genes induced by exercise? FASEB J 19: 94-96, 2005.
49. Wang YX, Zhang CL, Yu RT, Cho HK, Nelson MC, Bayuga-Ocampo CR, Ham J, Kang H, Evans RM. Regulation of muscle fiber type and running endurance by PPARdelta. PLoS Biol 2: e294, 2004.
50. Watt MJ, Southgate RJ, Holmes AG, Febbraio MA. Suppression of plasma free fatty acids upregulates peroxisome proliferator-activated receptor (PPAR) alpha and delta and PPAR coactivator 1alpha in human skeletal muscle, but not lipid regulatory genes. J Mol Endocrinol 33: 533-544, 2004.
51. Yang Y, Creer A, Jemiolo B, Trappe S. Time course of myogenic and metabolic gene expression in response to acute exercise in human skeletal muscle. J Appl Physiol 98: 1745-1752, 2005.