Effects of leptin and adiponectin on proliferation and protein metabolism of porcine myoblasts

Histochemistry and Cell Biology

Volumn 138, Issue 2, 2012, Pages 271-287

  Will, Katja ^a   Kalbe, Claudia ^a   Kuzinski, Judith ^a   Lösel, Dorothea ^a   Viergutz, Torsten ^a   Palin, Marie France ^b   Rehfeldt, Charlotte ^a  

^a LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^b SHERBROOKE RESEARCH AND DEVELOPMENT CENTRE   (Canada)

Author keywords

Adiponectin; Leptin; Pig; Receptor; Satellite cell culture; Skeletal muscle

Indexed keywords

ADIPONECTIN; ADIPONECTIN RECEPTOR; FIBROBLAST GROWTH FACTOR 2; LEPTIN; LEPTIN RECEPTOR; MESSENGER RNA;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; IN VITRO STUDY; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SEMITENDINOUS MUSCLE; SKELETAL MUSCLE;

ADIPONECTIN; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CULTURE MEDIA, SERUM-FREE; FIBROBLAST GROWTH FACTOR 2; LEPTIN; MUSCLE, SKELETAL; MYOBLASTS; RECEPTORS, ADIPONECTIN; RNA, MESSENGER; SUS SCROFA;

SUIDAE; SUS;

EID: 84867398854     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-012-0949-9     Document Type: Article

References (75)

1. Arita Y, Kihara S, Ouchi N et al (2002) Adipocyte-derived plasma protein adiponectin acts as a platelet-derived growth factor-BB-binding protein and regulates growth factor-induced common postreceptor signal in vascular smooth muscle cell. Circulation 105:2893-2898
2. Ballard FJ (1982) Regulation of protein accumulation in cultured cells. Biochem J 208:275-287
3. Berg AH, Combs TP, Scherer PE (2002) ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism. Trends Endocrinol Metab 13:84-89
4. Blanton JR Jr, Grant AL, McFarland DC, Robinson JP, Bidwell CA (1999) Isolation of two populations of myoblasts from porcine skeletal muscle. Muscle Nerve 22:43-50
5. Bonnet M, Cassar-Malek I, Chilliard Y, Picard B (2010) Ontogenesis of muscle and adipose tissues and their interactions in ruminants and other species. Animal 4:1093-1109
6. Brochu-Gaudreau K, Rehfeldt C, Blouin R, Bordignon V, Murphy BD, Palin MF (2010) Adiponectin action from head to toe. Endocrine 37:11-32
7. Brüssow KP, Schneider F, Tuchscherer A, Egerszegi I, Ratky J (2008) Comparison of LH, leptin and progesterone levels in the systemic circulation (Vena jugularis) and near the ovarian circulation (Vena cava caudalis) during the oestrous cycle in Mangalica and Landrace gilts. J Reprod Dev 54:431-438
8. Buechler C, Wanninger J, Neumeier M (2010) Adiponectin receptor binding proteins-recent advances in elucidating adiponectin signalling pathways. FEBS Lett 584:4280-4286
9. Cameron ND, Penman JC, McCullough E (2000) Serum leptin concentration in pigs selected for high or low daily food intake. Genet Res 75:209-213
10. Carbo N, Ribas V, Busquets S, Alvarez B, Lopez-Soriano FJ, Argiles JM (2000) Short-term effects of leptin on skeletal muscle protein metabolism in the rat. J Nutr Biochem 11:431-435
11. Ceddia RB, Somwar R, Maida A, Fang X, Bikopoulos G, Sweeney G (2005) Globular adiponectin increases GLUT4 translocation and glucose uptake but reduces glycogen synthesis in rat skeletal muscle cells. Diabetologia 48:132-139
12. Delaigle AM, Jonas JC, Bauche IB, Cornu O, Brichard SM (2004) Induction of adiponectin in skeletal muscle by inflammatory cytokines: in vivo and in vitro studies. Endocrinology 145:5589-5597
13. Ding ST, Liu BH, Ko YH (2004) Cloning and expression of porcine adiponectin and adiponectin receptor 1 and 2 genes in pigs. J Anim Sci 82:3162-3174
14. Ding Q, Wang Z, Chen Y (2009) Endocytosis of adiponectin receptor 1 through a clathrin-and Rab5-dependent pathway. Cell Res 19:317-327
15. Doumit ME, Cook DR, Merkel RA (1993) Fibroblast growth factor, epidermal growth factor, insulin-like growth factors, and platelet-derived growth factor-BB stimulate proliferation of clonally derived porcine myogenic satellite cells. J Cell Physiol 157:326-332
16. Doumit ME, Cook DR, Merkel RA (1996) Testosterone up-regulates androgen receptors and decreases differentiation of porcine myogenic satellite cells in vitro. Endocrinology 137:1385-1394
17. Du M, Shen QW, Zhu MJ, Ford SP (2007) Leucine stimulates mammalian target of rapamycin signaling in C2C12 myoblasts in part through inhibition of adenosine monophosphate-activated protein kinase. J Anim Sci 85:919-927
18. Erkens T, van Poucke M, Vandesompele J, Goossens K, van Zeveren A, Peelman LJ (2006) Development of a new set of reference genes for normalization of real-time RT-PCR data of porcine backfat and longissimus dorsi muscle, and evaluation with PPARGCIA. BMC Biotechnol 6:41
19. Fiaschi T, Tedesco FS, Giannoni E, Diaz-Manera J, Parri M, Cossu G, Chiarugi P (2010) Globular adiponectin as a complete mesoangioblast regulator: role in proliferation, survival, motility, and skeletal muscle differentiation. Mol Biol Cell 21:848-859
20. Fonseca-Alaniz MH, Takada J, Alonso-Vale MI, Lima FB (2007) Adipose tissue as an endocrine organ: from theory to practice. J Pediatr (Rio J) 83:S192-S203
21. Frühbeck G (2006) Intracellular signalling pathways activated by leptin. Biochem J 393:7-20
22. Frühbeck G (2008) Overview of adipose tissue and its role in obesity and metabolic disorders. Methods Mol Biol 456:1-22
23. Gimeno RE, Klaman LD (2005) Adipose tissue as an active endocrine organ: recent advances. Curr Opin Pharmacol 5:122-128
24. Guerra B, Santana A, Fuentes T, Delgado-Guerra S, Cabrera-Socorro A, Dorado C, Calbet JA (2007) Leptin receptors in human skeletal muscle. J Appl Physiol 102:1786-1792
25. Harper JM, Soar JB, Buttery PJ (1987) Changes in protein metabolism of ovine primary muscle cultures on treatment with growth hormone, insulin, insulin-like growth factor I or epidermal growth factor. J Endocrinol 112:87-96
26. Hauner H (2005) Secretory factors from human adipose tissue and their functional role. Proc Nutr Soc 64:163-169
27. Huber K, Petzold J, Rehfeldt C, Ender K, Fiedler I (2007) Muscle energy metabolism: structural and functional features in different types of porcine striated muscles. J Muscle Res Cell Motil 28:249-258
28. Hug C, Wang J, Ahmad NS, Bogan JS, Tsao TS, Lodish HF (2004) T-cadherin is a receptor for hexameric and high-molecularweight forms of Acrp30/adiponectin. Proc Natl Acad Sci USA 101:10308-10313
29. Jacobi SK, Gabler NK, Ajuwon KM, Davis JE, Spurlock ME (2006) Adipocytes, myofibers, and cytokine biology: new horizons in the regulation of growth and body composition. J Anim Sci 84(Suppl):E140-E149
30. Jurimae J, Jurimae T (2007) Plasma adiponectin concentration in healthy pre-and postmenopausal women: relationship with body composition, bone mineral, and metabolic variables. Am J Physiol Endocrinol Metab 293:E42-E47
31. Kadowaki T, Yamauchi T (2005) Adiponectin and adiponectin receptors. Endocr Rev 26:439-451
32. Kalbe C, Mau M, Rehfeldt C (2008) Developmental changes and the impact of isoflavones on mRNA expression of IGF-I receptor, EGF receptor and related growth factors in porcine skeletal muscle cell cultures. Growth Horm IGF Res 18:424-433
33. Kellerer M, Koch M, Metzinger E, Mushack J, Capp E, Haring HU (1997) Leptin activates PI-3 kinase in C2C12 myotubes via janus kinase-2 (JAK-2) and insulin receptor substrate-2 (IRS-2) dependent pathways. Diabetologia 40:1358-1362
34. Kosel D, Heiker JT, Juhl C, Wottawah CM, Bluher M, Morl K, Beck-Sickinger AG (2010) Dimerization of adiponectin receptor 1 is inhibited by adiponectin. J Cell Sci 123:1320-1328
35. Krause MP, Liu Y, Vu V, Chan L, Xu A, Riddell MC, Sweeney G, Hawke TJ (2008) Adiponectin is expressed by skeletal muscle fibers and influences muscle phenotype and function. Am J Physiol Cell Physiol 295:C203-C212
36. Kupchak BR, Garitaonandia I, Villa NY, Smith JL, Lyons TJ (2009) Antagonism of human adiponectin receptors and their membrane progesterone receptor paralogs by TNFalpha and a ceramidase inhibitor. Biochemistry 48:5504-5506
37. Laemmli UK (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 227:680-685
38. Lamosova D, Zeman M (2001) Effect of leptin and insulin on chick embryonic muscle cells and hepatocytes. Physiol Res 50:183-189
39. Ledoux S, Campos DB, Lopes FL, Dobias-Goff M, Palin MF, Murphy BD (2006) Adiponectin induces periovulatory changes in ovarian follicular cells. Endocrinology 147:5178-5186
40. Lin J, Barb CR, Matteri RL, Kraeling RR, Chen X, Meinersmann RJ, Rampacek GB (2000) Long form leptin receptor mRNA expression in the brain, pituitary, and other tissues in the pig. Domest Anim Endocrinol 19:53-61
41. Liu BH, Wang PH, Wang YC, Cheng WM, Mersmann HJ, Ding ST (2008) Fasting regulates the expression of adiponectin receptors in young growing pigs. J Anim Sci 86:3377-3384
42. Lord E, Ledoux S, Murphy BD, Beaudry D, Palin MF (2005) Expression of adiponectin and its receptors in swine. J Anim Sci 83:565-578
43. Maroni P, Bendinelli P, Piccoletti R (2003) Early intracellular events induced by in vivo leptin treatment in mouse skeletal muscle. Mol Cell Endocrinol 201:109-121
44. Maroni P, Bendinelli P, Piccoletti R (2005) Intracellular signal transduction pathways induced by leptin in C2C12 cells. Cell Biol Int 29:542-550
45. Matsubara M, Katayose S, Maruoka S (2003) Decreased plasma adiponectin concentrations in nondiabetic women with elevated homeostasis model assessment ratios. Eur J Endocrinol 148:343-350
46. Mau M, Oksbjerg N, Rehfeldt C (2008) Establishment and conditions for growth and differentiation of a myoblast cell line derived from the semimembranosus muscle of newborn piglets. In Vitro Cell Dev Biol Anim 44:1-5
47. Milligan G (2008) A day in the life of a G protein-coupled receptor: the contribution to function of G protein-coupled receptor dimerization. Br J Pharmacol 153(Suppl 1):S216-S229
48. Miner JL (2004) The adipocyte as an endocrine cell. J Anim Sci 82:935-941
49. Minokoshi Y, Kim YB, Peroni OD, Fryer LG, Muller C, Carling D, Kahn BB (2002) Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase. Nature 415:339-343
50. Nakashima K, Yakabe Y (2007) AMPK activation stimulates myofibrillar protein degradation and expression of atrophyrelated ubiquitin ligases by increasing FOXO transcription factors in C2C12 myotubes. Biosci Biotechnol Biochem 71:1650-1656
51. Novikoff AB, Shin WY, Drucker J (1961) Mitochondrial localization of oxidative enzymes: staining results with two tetrazolium salts. J Biophys Biochem Cytol 9:47-61
52. Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346-356
53. Ramsay TG (2003) Porcine leptin inhibits protein breakdown and stimulates fatty acid oxidation in C2C12 myotubes. J Anim Sci 81:3046-3051
54. Rehfeldt C, Kalbe C, Nürnberg G, Mau M (2009) Dose-dependent effects of genistein and daidzein on protein metabolism in porcine myotube cultures. J Agric Food Chem 57:852-857
55. Rehfeldt C, Walther K (1997) A combined assay for DNA, protein, and incorporated [3H] label in cultured muscle cells. Anal Biochem 251:294-297
56. Rehfeldt C, Walther K, Albrecht E, Nurnberg G, Renne U, Bunger L (2002) Intrinsic properties of muscle satellite cells are changed in response to long-term selection of mice for different growth traits. Cell Tissue Res 310:339-348
57. Siawrys G, Kaminski T, Smolinska N, Przala J (2007) Expression of leptin and long form of leptin receptor genes and proteins in pituitary of cyclic and pregnant pigs. J Physiol Pharmacol 58:845-857
58. Smolinska N, Kaminski T, Siawrys G, Przala J (2007) Long form of leptin receptor gene and protein expression in the porcine ovary during the estrous cycle and early pregnancy. Reprod Biol 7:17-39
59. Solberg R, Aas V, Thoresen GH, Kase ET, Drevon CA, Rustan AC, Reseland JE (2005) Leptin expression in human primary skeletal muscle cells is reduced during differentiation. J Cell Biochem 96:89-96
60. Sweeney G, Keen J, Somwar R, Konrad D, Garg R, Klip A (2001) High leptin levels acutely inhibit insulin-stimulated glucose uptake without affecting glucose transporter 4 translocation in l6 rat skeletal muscle cells. Endocrinology 142:4806-4812
61. Steinberg GR, Rush JW, Dyck DJ (2003) AMPK expression and phosphorylation are increased in rodent muscle after chronic leptin treatment. Am J Physiol Endocrinol Metab 284:E648-E654
62. Su YX, Deng HC, Zhang MX, Long J, Peng ZG (2012) Adiponectin inhibits PDGF-induced mesangial cell proliferation: regulation of mammalian target of rapamycin-mediated survival pathway by adenosine 5-monophosphate-activated protein kinase. Horm Metab Res 44:21-27
63. Tajmir P, Kwan JJ, Kessas M, Mozammel S, Sweeney G (2003) Acute and chronic leptin treatment mediate contrasting effects on signaling, glucose uptake, and GLUT4 translocation in L6-GLUT4myc myotubes. J Cell Physiol 197:122-130
64. Terrillon S, Bouvier M (2004) Roles of G-protein-coupled receptor dimerization. EMBO Rep 5:30-34
65. Tomas E, Tsao TS, Saha AK, Murrey HE, Zhang CC, Itani SI, Lodish HF, Ruderman NB (2002) Enhanced muscle fat oxidation and glucose transport by ACRP30 globular domain: acetyl-CoA carboxylase inhibition and AMP-activated protein kinase activation. Proc Natl Acad Sci USA 99:16309-16313
66. Wang Y, Lam KS, Xu JY, Lu G, Xu LY, Cooper GJ, Xu A (2005) Adiponectin inhibits cell proliferation by interacting with several growth factors in an oligomerization-dependent manner. J Biol Chem 280:18341-18347
67. Whitley NC, O'Brien DJ, Quinn RW, Keisler DH, Walker EL, Brown MA (2009) Milk leptin in sows and blood leptin and growth of their offspring. J Anim Sci 87:1659-1663
68. Wylie ARG (2011) Leptin in farm animals: where are we and where can we go? Animal 5:246-267
69. Yablonka-Reuveni Z, Seger R, Rivera AJ (1999) Fibroblast growth factor promotes recruitment of skeletal muscle satellite cells in young and old rats. J Histochem Cytochem 47:23-42
70. Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K, Mori Y, Ide T, Murakami K, Tsuboyama-Kasaoka N, Ezaki O, Akanuma Y, Gavrilova O, Vinson C, Reitman ML, Kagechika H, Shudo K, Yoda M, Nakano Y, Tobe K, Nagai R, Kimura S, Tomita M, Froguel P, Kadowaki T (2001) The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med 7:941-946
71. Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T (2002) Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 8:1288-1295
72. Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M, Murakami K, Ohteki T, Uchida S, Takekawa S, Waki H, Tsuno NH, Shibata Y, Terauchi Y, Froguel P, Tobe K, Koyasu S, Taira K, Kitamura T, Shimizu T, Nagai R, Kadowaki T (2003) Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423:762-769
73. Yi Z, Hathaway MR, Dayton WR, White ME (2001) Effects of growth factors on insulin-like growth factor binding protein (IGFBP) secretion by primary porcine satellite cell cultures. J Anim Sci 79:2820-2826
74. Yu T, Luo G, Zhang L, Wu J, Zhang H, Yang G (2008) Leptin promotes proliferation and inhibits differentiation in porcine skeletal myoblasts. Biosci Biotechnol Biochem 72:13-21
75. Zhou Q, Du J, Hu Z, Walsh K, Wang XH (2007) Evidence for adipose-muscle cross talk: opposing regulation of muscle proteolysis by adiponectin and Fatty acids. Endocrinology 148:5696-5705