PPARδ regulates satellite cell proliferation and skeletal muscle regeneration

Springer Science and Business Media LLC - Tập 1 Số 1 - 2011
Alison Rae Angione1, Chunhui Jiang1, Dongning Pan2, Yong‐Xu Wang2, Shihuan Kuang3
1Department of Animal Sciences, Purdue University, 901 West State Street, West Lafayette, IN, 47907, USA
2Program in Gene Function and Expression and Program in Molecular Medicine, University of Massachusetts Medical School, 364 Plantation Street, Worcester, 01605, USA
3Center for Cancer Research, Purdue University, 201 S. University Street, West Lafayette, IN, 47907, USA

Tóm tắt

Abstract Peroxisome proliferator-activated receptors (PPARs) are a class of nuclear receptors that play important roles in development and energy metabolism. Whereas PPARδ has been shown to regulate mitochondrial biosynthesis and slow-muscle fiber types, its function in skeletal muscle progenitors (satellite cells) is unknown. Since constitutive mutation of Pparδ leads to embryonic lethality, we sought to address this question by conditional knockout (cKO) of Pparδ using Myf5-Cre/Pparδ flox/flox alleles to ablate PPARδ in myogenic progenitor cells. Although Pparδ-cKO mice were born normally and initially displayed no difference in body weight, muscle size or muscle composition, they later developed metabolic syndrome, which manifested as increased body weight and reduced response to glucose challenge at age nine months. Pparδ-cKO mice had 40% fewer satellite cells than their wild-type littermates, and these satellite cells exhibited reduced growth kinetics and proliferation in vitro. Furthermore, regeneration of Pparδ-cKO muscles was impaired after cardiotoxin-induced injury. Gene expression analysis showed reduced expression of the Forkhead box class O transcription factor 1 (FoxO1) gene in Pparδ-cKO muscles under both quiescent and regenerating conditions, suggesting that PPARδ acts through FoxO1 in regulating muscle progenitor cells. These results support a function of PPARδ in regulating skeletal muscle metabolism and insulin sensitivity, and they establish a novel role of PPARδ in muscle progenitor cells and postnatal muscle regeneration.

Từ khóa


Tài liệu tham khảo

Zierath JR, Hawley JA: Skeletal muscle fiber type: influence on contractile and metabolic properties. PLoS Biol. 2004, 2: e348-10.1371/journal.pbio.0020348.

Rana ZA, Gundersen K, Buonanno A: Activity-dependent repression of muscle genes by NFAT. Proc Natl Acad Sci USA. 2008, 105: 5921-5926. 10.1073/pnas.0801330105.

Serrano AL, Murgia M, Pallafacchina G, Calabria E, Coniglio P, Lømo T, Schiaffino S: Calcineurin controls nerve activity-dependent specification of slow skeletal muscle fibers but not muscle growth. Proc Natl Acad Sci USA. 2001, 98: 13108-13113. 10.1073/pnas.231148598.

Bassel-Duby R, Olson EN: Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem. 2006, 75: 19-37. 10.1146/annurev.biochem.75.103004.142622.

Glass DJ: PI3 kinase regulation of skeletal muscle hypertrophy and atrophy. Curr Top Microbiol Immunol. 2010, 346: 267-278. 10.1007/82_2010_78.

Pavlath GK, Horsley V: Cell fusion in skeletal muscle: central role of NFATC2 in regulating muscle cell size. Cell Cycle. 2003, 2: 420-423.

Tedesco FS, Dellavalle A, Diaz-Manera J, Messina G, Cossu G: Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J Clin Invest. 2010, 120: 11-19. 10.1172/JCI40373.

Charge SB, Rudnicki MA: Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004, 84: 209-238. 10.1152/physrev.00019.2003.

Kuang S, Rudnicki MA: The emerging biology of satellite cells and their therapeutic potential. Trends Mol Med. 2008, 14: 82-91. 10.1016/j.molmed.2007.12.004.

Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA: Pax7 is required for the specification of myogenic satellite cells. Cell. 2000, 102: 777-786. 10.1016/S0092-8674(00)00066-0.

Halevy O, Piestun Y, Allouh MZ, Rosser BW, Rinkevich Y, Reshef R, Rozenboim I, Wleklinski-Lee M, Yablonka-Reuveni Z: Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn. 2004, 231: 489-502. 10.1002/dvdy.20151.

Olguin HC, Olwin BB: Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev Biol. 2004, 275: 375-388. 10.1016/j.ydbio.2004.08.015.

Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR: Muscle satellite cells adopt divergent fates: a mechanism for self-renewal?. J Cell Biol. 2004, 166: 347-357. 10.1083/jcb.200312007.

Conboy MJ, Karasov AO, Rando TA: High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biol. 2007, 5: e102-10.1371/journal.pbio.0050102.

Kuang S, Kuroda K, Le Grand F, Rudnicki MA: Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell. 2007, 129: 999-1010. 10.1016/j.cell.2007.03.044.

Shinin V, Gayraud-Morel B, Gomes D, Tajbakhsh S: Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol. 2006, 8: 677-687. 10.1038/ncb1425.

Buckingham M, Bajard L, Chang T, Daubas P, Hadchouel J, Meilhac S, Montarras D, Rocancourt D, Relaix F: The formation of skeletal muscle: from somite to limb. J Anat. 2003, 202: 59-68. 10.1046/j.1469-7580.2003.00139.x.

Ustanina S, Carvajal J, Rigby P, Braun T: The myogenic factor Myf5 supports efficient skeletal muscle regeneration by enabling transient myoblast amplification. Stem Cells. 2007, 25: 2006-2016. 10.1634/stemcells.2006-0736.

Gayraud-Morel B, Chrétien F, Flamant P, Gomès D, Zammit PS, Tajbakhsh S: A role for the myogenic determination gene Myf5 in adult regenerative myogenesis. Dev Biol. 2007, 312: 13-28. 10.1016/j.ydbio.2007.08.059.

Seale P, Bjork B, Yang W, Kajimura S, Chin S, Kuang S, Scimè A, Devarakonda S, Conroe HM, Erdjument-Bromage H, Tempst P, Rudnicki MA, Beier DR, Spiegelman BM: PRDM16 controls a brown fat/skeletal muscle switch. Nature. 2008, 454: 961-967. 10.1038/nature07182.

Wang YX: PPARs: diverse regulators in energy metabolism and metabolic diseases. Cell Res. 2010, 20: 124-137. 10.1038/cr.2010.13.

Lefebvre P, Chinetti G, Fruchart JC, Staels B: Sorting out the roles of PPARα in energy metabolism and vascular homeostasis. J Clin Invest. 2006, 116: 571-580. 10.1172/JCI27989.

Semple RK, Chatterjee VK, O'Rahilly S: PPARγ and human metabolic disease. J Clin Invest. 2006, 116: 581-589. 10.1172/JCI28003.

Barish GD, Narkar VA, Evans RM: PPARδ: a dagger in the heart of the metabolic syndrome. J Clin Invest. 2006, 116: 590-597. 10.1172/JCI27955.

Girroir EE, Hollingshead HE, He P, Zhu B, Perdew GH, Peters JM: Quantitative expression patterns of peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) protein in mice. Biochem Biophys Res Commun. 2008, 371: 456-461. 10.1016/j.bbrc.2008.04.086.

Escher P, Braissant O, Basu-Modak S, Michalik L, Wahli W, Desvergne B: Rat PPARs: quantitative analysis in adult rat tissues and regulation in fasting and refeeding. Endocrinology. 2001, 142: 4195-4202. 10.1210/en.142.10.4195.

Michalik L, Auwerx J, Berger JP, Chatterjee VK, Glass CK, Gonzalez FJ, Grimaldi PA, Kadowaki T, Lazar MA, O'Rahilly S, Palmer CNA, Plutzky J, Reddy JK, Spiegelman BM, Staels B, Wahli W: International Union of Pharmacology. LXI. Peroxisome proliferator-activated receptors. Pharmacol Rev. 2006, 58: 726-741. 10.1124/pr.58.4.5.

Shearer BG, Hoekstra WJ: Recent advances in peroxisome proliferator-activated receptor science. Curr Med Chem. 2003, 10: 267-280.

Oliver WR, 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 δ agonist promotes reverse cholesterol transport. Proc Natl Acad Sci USA. 2001, 98: 5306-5311. 10.1073/pnas.091021198.

Napal L, Marrero PF, Haro D: An intronic peroxisome proliferator-activated receptor-binding sequence mediates fatty acid induction of the human carnitine palmitoyltransferase 1A. J Mol Biol. 2005, 354: 751-759. 10.1016/j.jmb.2005.09.097.

Luquet S, Lopez-Soriano J, Holst D, Fredenrich A, Melki J, Rassoulzadegan M, Grimaldi PA: Peroxisome proliferator-activated receptor δ controls muscle development and oxidative capability. FASEB J. 2003, 17: 2299-2301.

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 PPARδ. PLoS Biol. 2004, 2: e294-10.1371/journal.pbio.0020294.

Schuler M, Ali F, Chambon C, Duteil D, Bornert JM, Tardivel A, Desvergne B, Wahli W, Chambon P, Metzger D: PGC1α expression is controlled in skeletal muscles by PPARβ, whose ablation results in fiber-type switching, obesity, and type 2 diabetes. Cell Metab. 2006, 4: 407-414. 10.1016/j.cmet.2006.10.003.

Han JK, Lee HS, Yang HM, Hur J, Jun SI, Kim JY, Cho CH, Koh GY, Peters JM, Park KW, Cho HJ, Lee HY, Kang HJ, Oh BH, Park YB, Kim HS: Peroxisome proliferator-activated receptor-δ agonist enhances vasculogenesis by regulating endothelial progenitor cells through genomic and nongenomic activations of the phosphatidylinositol 3-kinase/Akt pathway. Circulation. 2008, 118: 1021-1033. 10.1161/CIRCULATIONAHA.108.777169.

Kim YH, Han HJ: High-glucose-induced prostaglandin E2 and peroxisome proliferator-activated receptor δ promote mouse embryonic stem cell proliferation. Stem Cells. 2008, 26: 745-755. 10.1634/stemcells.2007-0786.

Peters JM, Gonzalez FJ: Sorting out the functional role(s) of peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) in cell proliferation and cancer. Biochim Biophys Acta. 2009, 1796: 230-241.

Simonini MV, Polak PE, Boullerne AI, Peters JM, Richardson JC, Feinstein DL: Regulation of oligodendrocyte progenitor cell maturation by PPARδ: effects on bone morphogenetic proteins. ASN Neuro. 2010, 2: e00025-10.1042/AN20090051.

Wang D, Wang H, Guo Y, Ning W, Katkuri S, Wahli W, Desvergne B, Dey SK, DuBois RN: Crosstalk between peroxisome proliferator-activated receptor δ and VEGF stimulates cancer progression. Proc Natl Acad Sci USA. 2006, 103: 19069-19074. 10.1073/pnas.0607948103.

Barak Y, Liao D, He W, Ong ES, Nelson MC, Olefsky JM, Boland R, Evans RM: Effects of peroxisome proliferator-activated receptor δ on placentation, adiposity, and colorectal cancer. Proc Natl Acad Sci USA. 2002, 99: 303-308. 10.1073/pnas.012610299.

Tallquist MD, Weismann KE, Hellström M, Soriano P: Early myotome specification regulates PDGFA expression and axial skeleton development. Development. 2000, 127: 5059-5070.

Rosenblatt JD, Lunt AI, Parry DJ, Partridge TA: Culturing satellite cells from living single muscle fiber explants. In vitro Cell Dev Biol Anim. 1995, 31: 773-779. 10.1007/BF02634119.

Nahlé Z, Hsieh M, Pietka T, Coburn CT, Grimaldi PA, Zhang MQ, Das D, Abumrad NA: CD36-dependent regulation of muscle FoxO1 and PDK4 in the PPAR δ/β-mediated adaptation to metabolic stress. J Biol Chem. 2008, 283: 14317-14326. 10.1074/jbc.M706478200.

Wagner KD, Wagner N: Peroxisome proliferator-activated receptor β/δ (PPARβ/δ) acts as regulator of metabolism linked to multiple cellular functions. Pharmacol Ther. 2010, 125: 423-435. 10.1016/j.pharmthera.2009.12.001.

Kitamura T, Kitamura YI, Funahashi Y, Shawber CJ, Castrillon DH, Kollipara R, DePinho RA, Kitajewski J, Accili D: A Foxo/Notch pathway controls myogenic differentiation and fiber type specification. J Clin Invest. 2007, 117: 2477-2485. 10.1172/JCI32054.

Wang LC, Kernell D: Recovery of type I fiber regionalization in gastrocnemius medialis of the rat after reinnervation along original and foreign paths, with and without muscle rotation. Neuroscience. 2002, 114: 629-640. 10.1016/S0306-4522(02)00315-9.

Waddell JN, Zhang P, Wen Y, Gupta SK, Yevtodiyenko A, Schmidt JV, Bidwell CA, Kumar A, Kuang S: Dlk1 is necessary for proper skeletal muscle development and regeneration. PLoS One. 2010, 5: e15055-10.1371/journal.pone.0015055.

He T, Lu T, d'Uscio LV, Lam CF, Lee HC, Katusic ZS: Angiogenic function of prostacyclin biosynthesis in human endothelial progenitor cells. Circ Res. 2008, 103: 80-88. 10.1161/CIRCRESAHA.108.176057.

Piqueras L, Reynolds AR, Hodivala-Dilke KM, Alfranca A, Redondo JM, Hatae T, Tanabe T, Warner TD, Bishop-Bailey D: Activation of PPARβ/δ induces endothelial cell proliferation and angiogenesis. Arterioscler Thromb Vasc Biol. 2007, 27: 63-69. 10.1161/01.ATV.0000250972.83623.61.

Kannan-Thulasiraman P, Seachrist DD, Mahabeleshwar GH, Jain MK, Noy N: Fatty acid-binding protein 5 and PPARβ/δ are critical mediators of epidermal growth factor receptor-induced carcinoma cell growth. J Biol Chem. 2010, 285: 19106-19115. 10.1074/jbc.M109.099770.

Zaveri NT, Sato BG, Jiang F, Calaoagan J, Laderoute KR, Murphy BJ: A novel peroxisome proliferator-activated receptor δ antagonist, SR13904, has anti-proliferative activity in human cancer cells. Cancer Biol Ther. 2009, 8: 1252-1261. 10.4161/cbt.8.13.8691.

Wagner KD, Benchetrit M, Bianchini L, Michiels JF, Wagner N: Peroxisome proliferator-activated receptor β/δ (PPARβ/δ) is highly expressed in liposarcoma and promotes migration and proliferation. J Pathol. 2011, 224: 575-588. 10.1002/path.2910.

Ramaswamy S, Nakamura N, Vazquez F, Batt DB, Perera S, Roberts TM, Sellers WR: Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc Natl Acad Sci USA. 1999, 96: 2110-2115. 10.1073/pnas.96.5.2110.

Kandel ES, Skeen J, Majewski N, Di Cristofano A, Pandolfi PP, Feliciano CS, Gartel A, Hay N: Activation of Akt/protein kinase B overcomes a G2/M cell cycle checkpoint induced by DNA damage. Mol Cell Biol. 2002, 22: 7831-7841. 10.1128/MCB.22.22.7831-7841.2002.

Chakravarthy MV, Abraha TW, Schwartz RJ, Fiorotto ML, Booth FW: Insulin-like growth factor-I extends in vitro replicative life span of skeletal muscle satellite cells by enhancing G1/S cell cycle progression via the activation of phosphatidylinositol 3'-kinase/Akt signaling pathway. J Biol Chem. 2000, 275: 35942-35952. 10.1074/jbc.M005832200.

Foreman JE, Sharma AK, Amin S, Gonzalez FJ, Peters JM: Ligand activation of peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) inhibits cell growth in a mouse mammary gland cancer cell line. Cancer Lett. 2010, 288: 219-225. 10.1016/j.canlet.2009.07.006.

Adhikary T, Kaddatz K, Finkernagel F, Schönbauer A, Meissner W, Scharfe M, Jarek M, Blöcker H, Müller-Brüsselbach S, Müller R: Genomewide analyses define different modes of transcriptional regulation by peroxisome proliferator-activated receptor-β/δ (PPARβ/δ). PLoS One. 2011, 6: e16344-10.1371/journal.pone.0016344.

Giordano C, Rousseau AS, Wagner N, Gaudel C, Murdaca J, Jehl-Piétri C, Sibille B, Grimaldi PA, Lopez P: Peroxisome proliferator-activated receptor β activation promotes myonuclear accretion in skeletal muscle of adult and aged mice. Pflügers Arch. 2009, 458: 901-913. 10.1007/s00424-009-0676-9.

Bois PRJ, Grosveld GC: FKHR (FOXO1a) is required for myotube fusion of primary mouse myoblasts. EMBO J. 2003, 22: 1147-1157. 10.1093/emboj/cdg116.

Hoffman EP, Brown RH, Kunkel LM: Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell. 1987, 51: 919-928. 10.1016/0092-8674(87)90579-4.

Zubrzycka-Gaarn EE, Bulman DE, Karpati G, Burghes AH, Belfall B, Klamut HJ, Talbot J, Hodges RS, Ray PN, Worton RG: The Duchenne muscular dystrophy gene product is localized in sarcolemma of human skeletal muscle. Nature. 1988, 333: 466-469. 10.1038/333466a0.

Miura P, Chakkalakal JV, Lunde J, Shaver A, Belanger G, Jasmin BJ: Activation of PPARδ stimulates utrophin A expression in skeletal muscle cells. FASEB J. 2007, 21: A1301-A1302.

Miura P, Chakkalakal JV, Boudreault L, Bélanger G, Hébert RL, Renaud JM, Jasmin BJ: Pharmacological activation of PPARβ/δ stimulates utrophin A expression in skeletal muscle fibers and restores sarcolemmal integrity in mature mdx mice. Hum Mol Genet. 2009, 18: 4640-4649. 10.1093/hmg/ddp431.

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