Effect of Opuntia humifusa supplementation and acute exercise on insulin sensitivity and associations with PPAR-γ and PGC-1α protein expression in skeletal muscle of rats

International Journal of Molecular Sciences

Volumn 14, Issue 4, 2013, Pages 7140-7154

  Kang, Junyong ^a   Lee, Junghun ^a   Kwon, Daekeun ^a   Song, Youngju ^a  

^a SunMoon University   (South Korea)

Author keywords

GLUT 4; Insulin sensitivity; O. humifusa; PGC 1 ; PPAR

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 4; INSULIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PLANT EXTRACT; PPARGC1A PROTEIN, RAT; TRANSCRIPTION FACTOR;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIET SUPPLEMENTATION; FORCED SWIMMING TEST; GLUCOSE BLOOD LEVEL; GLUCOSE TRANSPORT; INSULIN SENSITIVITY; MALE; NONHUMAN; OPUNTIA; OPUNTIA HUMIFUSA; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE; ANIMAL; CHEMISTRY; DRUG EFFECTS; INSULIN RESISTANCE; METABOLISM; ORGAN SIZE;

ANIMALS; BODY WEIGHT; GLUCOSE TRANSPORTER TYPE 4; INSULIN; INSULIN RESISTANCE; MUSCLE, SKELETAL; OPUNTIA; ORGAN SIZE; PHYSICAL CONDITIONING, ANIMAL; PLANT EXTRACTS; PPAR GAMMA; RATS; TRANSCRIPTION FACTORS;

EID: 84876011921     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14047140     Document Type: Article

References (56)

1. Haring, H.U.; Mehnert, H. Pathogenesis of Type 2 diabetes mellitus: Candidates for a signal transmitter defect causing insulin resistance of the skeletal muscle. Diabetologia 1993, 36, 176-182.
2. DeFronzo, R.A.; Ferrannini, E. Insulin resistance: A multifaceted syndrome responsible for NIDDM, obesity, hypertension dyslipidemia and atherosclerotic cardiovascular disease. Diabetes Care 1991, 14, 173-194.
3. DeFronzo, R.A.; Bonadonna, R.C.; Ferrannini, E. Pathogenesis of NIDDM. A balanced overview. Diabetes Care 1992, 15, 318-368.
4. Ford, E.S.; Williamson, D.F.; Liu, S. Weight change and diabetes incidence: Findings from a national cohort of US adults. Am. J. Epidemiol. 1997, 146, 214-222.
5. Resnick, H.E.; Valsania, P.; Halter, J.B.; Lin, X. Relation of weight gain and weight loss on subsequent diabetes risk in overweight adults. J. Epidemiol. Commun. Health 2000, 54, 596-602.
6. Picard, F.; Auwerx, J. PPAR (gamma) and glucose homeostasis. Annu. Rev. Nutr. 2002, 22, 167-197.
7. Wilson, T.M.; Brown, P.J.; Sternbach, D.D.; Henke, B.R. The PPARs: From orphan receptors to drug discovery. J. Med. Chem. 2000, 43, 527-550.
8. Miyazaki, Y.; He, H.; Mandarino, L.J.; de Fronzo, R.A. Resiglitazone improves downstream insulin receptor signaling in type 2 diabetic patients. Diabetes 2003, 52, 1943-1950.
9. Kawaguchi, H.; Akune, T.; Yamaguchi, M.; Ohba, S.; Ogata, N.; Chung, U.I.; Kubota, N.; Terauchi, Y.; Kadowaki, T.; Nakamura, K. Distinct effects of PPAR gamma insufficiency on bone marrow cells, osteoblast, and osteoclastic cells. J. Bone Miner. Metab. 2005, 23, 275-279.
10. Lefebvre, A.M.; Chen, I.; Desteumaux, P.; Najib, J.; Fruchart, J.C.; Geboes, K.; Btiggs, M.; Heyman, R.; Auwerx, J. Activation of the peroxisome proliferator-activated receptor gamma promotes the development of colon tumors in C57BL/6JAPCMin/+mice. Nat. Med. 1998, 4, 1053-1057.
11. Song, Y.J.; Sawamura, M.; Ikeda, K.; Igawa, S.; Yamori, Y. Soluble dietary fibre improves insulin sensitivity by increasing muscle glut-4 content in stroke-prone spontaneously hypertensive rats. Clin. Exp. Pharmacol. Physiol. 2000, 27, 41-45.
12. Lee, S.H.; Lee, H.J.; Lee, Y.H.; Lee, B.W.; Cha, B.S.; Kang, E.S.; Ahn, C.W.; Park, J.S.; Kim, H.J.; Lee, E.Y.; et al. Korean red ginseng (Panax ginseng) improves insulin sensitivity in high fat fed Sprague-Dawley rats. Phytother. Res. 2012, 26, 142-147.
13. Goldstein, G.; Nobel, P.S. Water relations and low temperature acclimation for cactus species varying in freezing tolerance. Plant Physiol. 1994, 104, 675-681.
14. Kang, J.; Park, J.; Choi, S.H.; Igawa, S.; Song, Y. Opuntia humifusa supplementation increased bone density by regulating parathyroid hormone and osteocalcin in male growing rats. Int. J. Mol. Sci. 2012, 13, 6747-6756.
15. Cho, J.Y.; Park, S.C.; Kim, T.W.; Kim, K.S.; Song, J.C.; Kim, S.K.; Lee, H.M.; Sung, H.J.; Park, H.J.; Song, Y.B.; et al. Radical scavenging and anti-inflammatory activity of extracts from Opuntia humifusa Raf. J. Pharm. Pharmacol. 2006, 58, 113-119.
16. Park, E.H.; Kahng, J.H.; Lee, S.H.; Shin, K.H. An anti-inflammatory principles from cactus. Fitoterapia 2001, 72, 288-290.
17. Chavez-Santoscoy, R.A.; Gutierrez-Uribe, J.A.; Serna-Saldivar, S.O. Phenolic composition, antioxidant capacity and in vitro cancer cell cytotoxicity of nine prickly pear (Opuntia spp.) juices. Plant Foods Hum. Nutr. 2009, 64, 146-152.
18. Butera, D.; Tesoriere, L.; Di Gaudio, F.; Bongiorno, A.; Allegra, M.; Pintaudi, A.M.; Kohen, R.; Livrea, M.A. Antioxidant activities of sicilian prickly pear (Opuntia ficus indica) fruit extracts and reducing properties of its betalains: Betanin and indicaxanthin. J. Agric. Food Chem. 2002, 50, 6895-6901.
19. Hahm, S.W.; Park, J.; Son, Y.S. Opuntia humifusa stems lower blood glucose and cholesterol levels in streptozotocin-induced diabetic rats. Nutr. Res. 2011, 31, 479-487.
20. Hamada, T.; Arias, E.B.; Cartee, G.D. Increased submaximal insulin-stimulated glucose uptake in mouse skeletal muscle after treadmill exercise. J. Appl. Physiol. 2006, 101, 1368-1376.
21. Ruschke, K.; Fishbein, L.; Dietrich, A.; Klöting, N.; Tönjes, A.; Oberbach, A.; Fasshauer, M.; Jenkner, J.; Schön, M.R.; Stumvoll, M.; et al. Gene expression of PPARgamma and PGC-1alpha in human omental and subcutaneous adipose tissues is related to insulin resistance markers and mediates beneficial effects of physical training. Eur. J. Endocrinol. 2010, 162, 515-523.
22. Hevener, A.L.; He, W.; Barak, Y.; Le, J.; Bandyopadhyay, G.; Olson, P.; Wilkes, J.; Evans, R.M.; Olefsky, J. Muscle-specific Pparg deletion causes insulin resistance. Nat. Med. 2003, 9, 1491-1497.
23. Shih, C.C.; Lin, C.H.; Lin, W.L.; Wu, J.B. Momordica charantia extract on insulin resistance and the skeletal muscle GLUT4 protein in fructose-fed rats. J. Ethnopharmacol. 2009, 123, 82-90.
24. Patti, M.E.; Butte, A.J.; Crunkhorn, S.; Cusi, K.; Berria, R.; Kashyap, S.; Miyazaki, Y.; Kohane, I.; Costello, M.; Saccone, R.; et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc. Natl. Acad. Sci. USA 2003, 100, 8466-8471.
25. Michael, L.F.; Wu, Z.; Cheatham, R.B.; Puigserver, P.; Adelmant, G.; Lehman, J.J.; Kelly, D.P.; Spiegelman, B.M. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc. Natl. Acad. Sci. USA 2001, 98, 3820-3825.
26. De Munter, J.S.; Hu, F.B.; Spiegelman, D.; Franz, M.; van Dam, R.M. Whole grain, bran, and germ intake and risk of type 2 diabetes: A prospective cohort study and systematic review. PLoS Med. 2007, 4, 1385-1395.
27. Pittas, A.G.; Lau, J.; Hu, F.B.; Dawson-Hughes, B. The role of vitamin D and calcium in type 2 diabetes: A systemic review and meta-analysis. J. Clin. Endocrinol. Metab. 2007, 92, 2017-2029.
28. Takaya, J.; Higashino, H.; Kobayashi, Y. Intracellular magnesium and insulin resistance. Magnes. Res. 2004, 17, 126-136.
29. Lopez-Ridaura, R.; Willett, W.C.; Rimm, E.B.; Liu, S.; Stampfer, M.J.; Manson, J.E.; Hu, F.B. Magnesium intake and risk of type 2 diabetes in men and women. Diabetes Care 2004, 27, 134-140.
30. Suarez, A.; Pulido, N.; Casla, A.; Casanova, B.; Arrieta, F.J.; Rovira, A. Impaired tyrosin-kinase activity of muscle insulin receptors from hypomagnesaemic rats. Diabetologia 1995, 38, 1262-1270.
31. Berger, J.; Bailey, P.; Biswas, C.; Cullinan, C.A.; Doebber, T.W.; Hayes, N.S.; Saperstein, R.; Smith, R.G.; Leibowitz, M.D. Thiazolidinediones produce a conformational change in peroxisomal proliferator-activated receptor-gamma: Binding and activation correlate with antidiabetic actions in db/db mice. Endocrinology 1996, 137, 4189-4195.
32. Guerrero-Romero, F.; Rodríguez-Morán, M. Pioglitazone increases serum magnesium levels in glucose-intolerant subjects. A randomized, controlled trial. Exp. Clin. Endocrinol. Diabetes 2003, 111, 91-96.
33. Emoto, M.; Nishizawa, Y. Diabetes Mellitus and Magnesium. In New Perspectives in Magnesium Research; Nishizawa, Y., Morii, H., Durlach, J., Eds.; Springer-Verlag: London, UK, 2007; pp. 197-212.
34. Garvey, W.T.; Maianu, L.; Hancock, J.A.; Golichowski, A.M.; Baron, A. Gene expression of GLUT4 in skeletal muscle from insulin-resistant patients with obesity, IGT, GDM, and NIDDM. Diabetes 1992, 41, 465-475.
35. Begum, N.; Leitner, W.; Reusch, J.E.; Sussman, K.E.; Draznin, B. GLUT-4 phosphorylation and its intrinsic activity. Mechanism of Ca2+ induced inhibition of insulin-stimulated glucose transport. J. Biol. Chem. 1993, 268, 3352-3356.
36. Hellman, B.; Berne, C.; Grapengiesser, E.; Grill, V.; Gylfe, E.; Lund, P.E. The cytoplasmic Ca2+ response to glucose as an indicator of impairment of the pancreatic beta-cell function. Eur. J. Clin. Invest. 1990, 20, S10-S17.
37. Pershadsingh, H.A.; Shade, D.L.; Delfert, D.M.; McDonald, J.M. Chelation of intracellular calcium blocks insulin action in the adipocyte. Proc. Natl. Acad. Sci. USA 1987, 84, 1025-1029.
38. Pikilidou, M.I.; Lasaridis, A.N.; Sarafidism, P.A.; Befani, C.D.; Koliakos, G.G.; Tziolas, I.M.; Kazakos, K.A.; Yovos, J.G.; Nilsson, P.M. Insulin sensitivity increase after calcium supplementation and change in intraplatelet calcium and sodium-hydrogen exchange in hypertensive patients with Type 2 diabetes. Diabet. Med. 2009, 26, 211-219.
39. Sánchez, M.; de la Sierra, A.; Coca, A.; Poch, E.; Giner, V.; Urbano-Márquez, A. Oral calcium supplementation reduces intraplatelet free calcium concentration and insulin resistance in essential hypertensive patients. Hypertension 1997, 29, 531-536.
40. Dudley, G.A.; Terjung, R.L. Influence of acidosis on AMP deaminase activity in contracting fast-twitch muscle. Am. J. Physiol. 1985, 248, C43-C50.
41. Hutber, C.A.; Hardie, D.G.; Winder, W.W. Electrical stimulation inactivates muscle acetyl-CoA carboxylase and increases AMP-activated protein kinase. Am. J. Physiol. 1997, 272, E262-E266.
42. Tarada, S.; Kawanaka, K.; Goto, M.; Shimokawa, T.; Tabata, I. Effect of high-intensity intermittent swimming on PGC-1α protein expression in rat skeletal muscle. Acta Physiol. Scand. 2005, 184, 59-65.
43. Calvo, J.A.; Daniels, T.G.; Wang, X.; Paul, A.; Lin, J.; Spiegelman, B.M.; Stevenson, S.C.; Rangwala, S.M. Muscle specific expression of PPARγ coactivator-1α improves exercise performance and increases peak oxygen uptake. J. Appl. Physiol. 2008, 104, 1304-1324.
44. Kawamura, T.; Yoshida, K.; Sugawara, A.; Nagasaka, M.; Mori, N.; Takeuchi, K.; Kohzuki, M. Regulation of skeletal muscle peroxisome proliferator-activated receptor gamma expression by exercise and angiotensin-converting enzyme inhibition in fructose-fed hypertensive rats. Hypertens. Res. 2004, 27, 61-70.
45. Russell, A.P.; Feilchenfeldt, J.; Schreiber, S.; Praz, M.; Crettenand, A.; Gobelet, C.; Meier, C.A.; Bell, D.R.; Kralli, A.; Giacobino, J.P.; et al. Endurance training in humans leads to fiber type specific increases in levels of peroxisome proliferator activated receptor gamma coactivator 1 and peroxisome proliferator activated receptor alpha in skeletal muscle. Diabetes 2003, 52, 2874-2881.
46. De Filippis, E.; Alvarez, G.; Berria, R.; Cusi, K.; Everman, S.; Meyer, C.; Mandarino, L.J. Insulin-resistant muscle is exercise resistant: Evidence for reduced response of nuclear-encoded mitochondrial genes to exercise. Am. J. Physiol. Endocrinol. Metab. 2008, 294, 607-614.
47. Baar, K.; Wende, A.R.; Jones, T.E.; Marison, M.; Nolte, L.A.; Chen, M.; Kelly, D.P.; Holloszy, J.O. Adaptations of skeletal muscle to exercise: Rapid increase in the transcriptional coactivator PGC-1. FASEB J. 2002, 16, 1879-1886.
48. Russell, A.P.; Hessenlink, M.K.; Lo, S.K.; Schrauwen, P. Regulation of metabolic transcriptional co-activators and transcription factors with acute exercise. FASEB J. 2005, 19, 986-988.
49. Tunstall, R.J.; Mehan, K.A.; Wadley, G.D.; Collier, G.R.; Bonen, A.; Hargreaves, M.; Cameron-Smith, D. Exercise training increases lipid metabolism gene expression in human skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2002, 283, E66-E72.
50. Loviscach, M.; Rehman, N.; Carter, L.; Mudaliar, S.; Mohadeen, P.; Ciaraldi, T.P.; Veerkamp, J.H.; Henry, R.R. Distribution of peroxisome proliferator-activated receptors (PPARs) in human skeletal muscle and adipose tissue: Relation to insulin action. Diabetologia 2000, 43, 304-311.
51. Baron, A.D.; Brechtel, G. Insulin differentially regulates systemic and skeletal muscle vascular resistance. Am. J. Physiol. 1993, 265, E61-E67.
52. Puigserver, P.; Spiegelman, B.M. Peroxisome proliferator-activated receptor-gamma coactivator 1alpha (PGC-1 alpha): Transcriptional coactivator and metabolic regulator. Endocr. Rev. 2003, 24, 78-90.
53. Ling, C.; Poulsen, P.; Carlsson, E.; Ridderstråle, M.; Almgren, P.; Wojtaszewski, J.; Beck-Nielsen, H.; Groop, L.; Vaag, A. Multiple environmental and genetic factors influence skeletal muscle PGC-1α and PGC-1β gene expression in twins. J. Clin. Invest. 2004, 114, 1518-1526.
54. Crunkhorn, S.; Dearie, F.; Mantzoros, C.; Gami, H.; da Silva, W.S.; Espinoza, D.; Faucette, R.; Barry, K.; Bianco, A.C.; Patti, M.E. Peroxisome proliferator activator receptor gamma coactivator-1 expression is reduced in obesity: Potential pathogenic role of saturated fatty acids and p38 mitogen-activated protein kinase activation. J. Biol. Chem. 2007, 282, 15439-15450.
55. Association of Official Analytical Chemists (AOAC). Official Methods of Analysis of the Association of Analytical Chemists, 16th ed.; AOAC: Washington, DC, USA, 1998.
56. Kim, Y.J.; Park, T.S. Genes are differentially expressed in the epididymal fat of rats rendered obese by a high-fat diet. Nutr. Res. 2008, 28, 414-422.