Impaired muscle regeneration in Ob/ob and Db/db mice

TheScientificWorldJournal

Volumn 11, Issue , 2011, Pages 1525-1535

  Nguyen, Mai Huong ^a   Cheng, Ming ^a   Koh, Timothy J ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Inflammation; Leptin; Obesity; Skeletal muscle injury; Tissue repair

Indexed keywords

CARDIOTOXIN; INSULIN; LEPTIN; RNA;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL PROLIFERATION; CLINICAL ASSESSMENT; CONTROLLED STUDY; FEEDING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMPAIRED MUSCLE REGENERATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; MACROPHAGE; MORPHOLOGY; MOUSE; MUSCLE CELL; MUSCLE INJURY; MUSCLE REGENERATION; MYOBLAST; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION;

ANIMALS; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; INSULIN; INSULIN RESISTANCE; LEPTIN; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, OBESE; MUSCLE, SKELETAL; MYOBLASTS, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; REGENERATION; SIGNAL TRANSDUCTION;

MUS;

EID: 84860406420     PISSN: None     EISSN: 1537744X     Source Type: Journal    
DOI: 10.1100/tsw.2011.137     Document Type: Article

References (55)

1. Blaak, E.E. (2004) Basic disturbances in skeletal muscle fatty acid metabolism in obesity and type 2 diabetes mellitus. Proc. Nutr. Soc. 63, 323-330.
2. Jude, E.B., Eleftheriadou, I., and Tentolouris, N. (2010) Peripheral arterial disease in diabetes - a review. Diabet. Med. 27, 4-14.
3. Nomura, T., Ikeda, Y., Nakao, S., Ito, K., Ishida, K., Suehiro, T., and Hashimoto, K. (2007) Muscle strength is a marker of insulin resistance in patients with type 2 diabetes: a pilot study. Endocr. J. 54, 791-796.
4. Park, S.W., Goodpaster, B.H., Strotmeyer, E.S., de Rekeneire, N., Harris, T.B., Schwartz, A.V., Tylavsky, F.A., and Newman, A.B. (2006) Decreased muscle strength and quality in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes 55, 1813-1818.
5. Goodpaster, B.H., Delany, J.P., Otto, A.D., Kuller, L., Vockley, J., South-Paul, J.E., Thomas, S.B., Brown, J., McTigue, K., Hames, K.C., Lang, W., and Jakicic, J.M. (2010) Effects of diet and physical activity interventions on weight loss and cardiometabolic risk factors in severely obese adults: a randomized trial. JAMA 304, 1795-1802.
6. Slentz, C.A., Houmard, J.A., and Kraus, W.E. (2009) Exercise, abdominal obesity, skeletal muscle, and metabolic risk: evidence for a dose response. Obesity (Silver Spring) 17(Suppl 3), S27-33.
7. Asp, S., Daugaard, J.R., Kristiansen, S., Kiens, B., and Richter, E.A. (1996) Eccentric exercise decreases maximal insulin action in humans: muscle and systemic effects. J. Physiol. 494(Pt 3), 891-898.
8. Del Aguila, L.F., Krishnan, R.K., Ulbrecht, J.S., Farrell, P.A., Correll, P.H., Lang, C.H., Zierath, J.R., and Kirwan, J.P. (2000) Muscle damage impairs insulin stimulation of IRS-1, PI 3-kinase, and Akt-kinase in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 279, E206-212.
9. Elmquist, J.K., Maratos-Flier, E., Saper, C.B., and Flier, J.S. (1998) Unraveling the central nervous system pathways underlying responses to leptin. Nat. Neurosci. 1, 445-450.
10. Kampfer, H., Schmidt, R., Geisslinger, G., Pfeilschifter, J., and Frank, S. (2005) Wound inflammation in diabetic ob/ob mice: functional coupling of prostaglandin biosynthesis to cyclooxygenase-1 activity in diabetes-impaired wound healing. Diabetes 54, 1543-1551.
11. Kjerrulf, M., Berke, Z., Aspegren, A., Umaerus, M., Nilsson, T., Svensson, L., and Hurt-Camejo, E. (2006) Reduced cholesterol accumulation by leptin deficient (ob/ob) mouse macrophages. Inflamm. Res. 55, 300-309.
12. Maruyama, K., Asai, J., Ii, M., Thorne, T., Losordo, D.W., and D'Amore, P.A. (2007) Decreased macrophage number and activation lead to reduced lymphatic vessel formation and contribute to impaired diabetic wound healing. Am. J. Pathol. 170, 1178-1191.
13. Siegmund, B., Lehr, H.A., and Fantuzzi, G. (2002) Leptin: a pivotal mediator of intestinal inflammation in mice. Gastroenterology 122, 2011-2025.
14. Wetzler, C., Kampfer, H., Stallmeyer, B., Pfeilschifter, J., and Frank, S. (2000) Large and sustained induction of chemokines during impaired wound healing in the genetically diabetic mouse: prolonged persistence of neutrophils and macrophages during the late phase of repair. J. Invest. Dermatol. 115, 245-253.
15. Charge, S.B. and Rudnicki, M.A. (2004) Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 84, 209-238.
16. Cantini, M., Giurisato, E., Radu, C., Tiozzo, S., Pampinella, F., Senigaglia, D., Zaniolo, G., Mazzoleni, F., and Vitiello, L. (2002) Macrophage-secreted myogenic factors: a promising tool for greatly enhancing the proliferative capacity of myoblasts in vitro and in vivo. Neurol. Sci. 23, 189-194.
17. Arnold, L., Henry, A., Poron, F., Baba-Amer, Y., van Rooijen, N., Plonquet, A., Gherardi, R.K., and Chazaud, B. (2007) Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 204, 1057-1069.
18. Bryer, S.C., Fantuzzi, G., Van Rooijen, N., and Koh, T.J. (2008) Urokinase-type plasminogen activator plays essential roles in macrophage chemotaxis and skeletal muscle regeneration. J. Immunol. 180, 1179-1188.
19. Summan, M., Warren, G.L., Mercer, R.R., Chapman, R., Hulderman, T., Van Rooijen, N., and Simeonova, P.P. (2006) Macrophages and skeletal muscle regeneration: a clodronate-containing liposome depletion study. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290, R1488-1495.
20. Collins, S., Martin, T.L., Surwit, R.S., and Robidoux, J. (2004) Genetic vulnerability to diet-induced obesity in the C57BL/6J mouse: physiological and molecular characteristics. Physiol. Behav. 81, 243-248.
21. Koh, T.J., Bryer, S.C., Pucci, A.M., and Sisson, T.H. (2005) Mice deficient in plasminogen activator inhibitor-1 have improved skeletal muscle regeneration. Am. J. Physiol. Cell Physiol. 289, C217-223.
22. Hawke, T.J. and Garry, D.J. (2001) Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 91, 534-551.
23. Sisson, T.H., Nguyen, M.H., Yu, B., Novak, M.L., Simon, R.H., and Koh, T.J. (2009) Urokinase-type plasminogen activator increases hepatocyte growth factor activity required for skeletal muscle regeneration. Blood 114, 5052-5061.
24. Ruiter, M.S., van Golde, J.M., Schaper, N.C., Stehouwer, C.D., and Huijberts, M.S. Diabetes impairs arteriogenesis in the peripheral circulation: review of molecular mechanisms. Clin. Sci. (Lond.) 119, 225-238.
25. Simons, M. (2005) Angiogenesis, arteriogenesis, and diabetes: paradigm reassessed? J. Am. Coll. Cardiol. 46, 835-837.
26. Flegal, K.M., Carroll, M.D., Ogden, C.L., and Curtin, L.R. (2010) Prevalence and trends in obesity among US adults, 1999-2008. JAMA 303, 235-241.
27. Kahn, C.R. (1994) Banting lecture. Insulin action, diabetogenes, and the cause of type II diabetes. Diabetes 43, 1066-1084.
28. Vignaud, A., Ramond, F., Hourde, C., Keller, A., Butler-Browne, G., and Ferry, A. (2007) Diabetes provides an unfavorable environment for muscle mass and function after muscle injury in mice. Pathobiology 74, 291-300.
29. Kellerer, M., Koch, M., Metzinger, E., Mushack, J., Capp, E., and Haring, H.U. (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.
30. Maroni, P., Bendinelli, P., and Piccoletti, R. (2003) Early intracellular events induced by in vivo leptin treatment in mouse skeletal muscle. Mol. Cell. Endocrinol. 201, 109-121.
31. Maroni, P., Bendinelli, P., and Piccoletti, R. (2005) Intracellular signal transduction pathways induced by leptin in C2C12 cells. Cell Biol. Int. 29, 542-550.
32. Solberg, R., Aas, V., Thoresen, G.H., Kase, E.T., Drevon, C.A., Rustan, A.C., and Reseland, J.E. (2005) Leptin expression in human primary skeletal muscle cells is reduced during differentiation. J. Cell. Biochem. 96, 89-96.
33. Yu, T., Luo, G., Zhang, L., Wu, J., Zhang, H., and Yang, G. (2008) Leptin promotes proliferation and inhibits differentiation in porcine skeletal myoblasts. Biosci. Biotechnol. Biochem. 72, 13-21.
34. Almond, R.E. and Enser, M. (1984) A histochemical and morphological study of skeletal muscle from obese hyperglycaemic ob/ob mice. Diabetologia 27, 407-413.
35. Purchas, R.W., Romsos, D.R., Allen, R.E., and Merkel, R.A. (1985) Muscle growth and satellite cell proliferative activity in obese (OB/OB) mice. J. Anim. Sci. 60, 644-651.
36. Stickland, N.C., Batt, R.A., Crook, A.R., and Sutton, C.M. (1994) Inability of muscles in the obese mouse (ob/ob) to respond to changes in body weight and activity. J. Anat. 184(Pt 3), 527-533.
37. Wang, X., Hu, Z., Hu, J., Du, J., and Mitch, W.E. (2006) Insulin resistance accelerates muscle protein degradation: activation of the ubiquitin-proteasome pathway by defects in muscle cell signaling. Endocrinology 147, 4160-4168.
38. Warmington, S.A., Tolan, R., and McBennett, S. (2000) Functional and histological characteristics of skeletal muscle and the effects of leptin in the genetically obese (ob/ob) mouse. Int. J. Obes. Relat. Metab. Disord. 24, 1040-1050.
39. Almond, R.E. and Enser, M. (1989) Effects of adrenalectomy on muscle fibre growth and fibre-type composition in obese-hyperglycaemic (ob/ob) and lean mice. Int. J. Obes. 13, 791-800.
40. Saito, M. and Bray, G.A. (1984) Adrenalectomy and food restriction in the genetically obese (ob/ob) mouse. Am. J. Physiol. 246, R20-25.
41. Ceddia, R.B., William, W.N., Jr., and Curi, R. (2001) The response of skeletal muscle to leptin. Front. Biosci. 6, D90-97.
42. Steinberg, G.R., Parolin, M.L., Heigenhauser, G.J., and Dyck, D.J. (2002) Leptin increases FA oxidation in lean but not obese human skeletal muscle: evidence of peripheral leptin resistance. Am. J. Physiol. Endocrinol. Metab. 283, E187-192.
43. Suzuki, A., Okamoto, S., Lee, S., Saito, K., Shiuchi, T., and Minokoshi, Y. (2007) Leptin stimulates fatty acid oxidation and peroxisome proliferator-activated receptor alpha gene expression in mouse C2C12 myoblasts by changing the subcellular localization of the alpha2 form of AMP-activated protein kinase. Mol. Cell. Biol. 27, 4317-4327.
44. Hamrick, M.W., Herberg, S., Arounleut, P., He, H.Z., Shiver, A., Qi, R.Q., Zhou, L., Isales, C.M., and Mi, Q.S. (2010) The adipokine leptin increases skeletal muscle mass and significantly alters skeletal muscle miRNA expression profile in aged mice. Biochem. Biophys. Res. Commun. 400, 379-383.
45. Gruen, M.L., Hao, M., Piston, D.W., and Hasty, A.H. (2007) Leptin requires canonical migratory signaling pathways for induction of monocyte and macrophage chemotaxis. Am. J. Physiol. Cell Physiol. 293, C1481-1488.
46. Loffreda, S., Yang, S.Q., Lin, H.Z., Karp, C.L., Brengman, M.L., Wang, D.J., Klein, A.S., Bulkley, G.B., Bao, C., Noble, P.W., Lane, M.D., and Diehl, A.M. (1998) Leptin regulates proinflammatory immune responses. FASEB J. 12, 57-65.
47. Sanchez-Margalet, V., Martin-Romero, C., Santos-Alvarez, J., Goberna, R., Najib, S., and Gonzalez-Yanes, C. (2003) Role of leptin as an immunomodulator of blood mononuclear cells: mechanisms of action. Clin. Exp. Immunol. 133, 11-19.
48. Santos-Alvarez, J., Goberna, R., and Sanchez-Margalet, V. (1999) Human leptin stimulates proliferation and activation of human circulating monocytes. Cell. Immunol. 194, 6-11.
49. Frank, S., Stallmeyer, B., Kampfer, H., Kolb, N., and Pfeilschifter, J. (2000) Leptin enhances wound re-epithelialization and constitutes a direct function of leptin in skin repair. J. Clin. Invest. 106, 501-509.
50. Murad, A., Nath, A.K., Cha, S.T., Demir, E., Flores-Riveros, J., and Sierra-Honigmann, M.R. (2003) Leptin is an autocrine/paracrine regulator of wound healing. FASEB J. 17, 1895-1897.
51. Ring, B.D., Scully, S., Davis, C.R., Baker, M.B., Cullen, M.J., Pelleymounter, M.A., and Danilenko, D.M. (2000) Systemically and topically administered leptin both accelerate wound healing in diabetic ob/ob mice. Endocrinology 141, 446-449.
52. El-Haschimi, K., Pierroz, D.D., Hileman, S.M., Bjorbaek, C., and Flier, J.S. (2000) Two defects contribute to hypothalamic leptin resistance in mice with diet-induced obesity. J. Clin. Invest. 105, 1827-1832.
53. Van Heek, M., Compton, D.S., France, C.F., Tedesco, R.P., Fawzi, A.B., Graziano, M.P., Sybertz, E.J., Strader, C.D., and Davis, H.R., Jr. (1997) Diet-induced obese mice develop peripheral, but not central, resistance to leptin. J. Clin. Invest. 99, 385-390.
54. Dyck, D.J. (2005) Leptin sensitivity in skeletal muscle is modulated by diet and exercise. Exerc. Sport Sci. Rev. 33, 189-194.
55. Steinberg, G.R., McAinch, A.J., Chen, M.B., O'Brien, P.E., Dixon, J.B., Cameron-Smith, D., and Kemp, B.E. (2006) The suppressor of cytokine signaling 3 inhibits leptin activation of AMP-kinase in cultured skeletal muscle of obese humans. J. Clin. Endocrinol. Metab. 91, 3592-3597.