Intense electroacupuncture normalizes insulin sensitivity, increases muscle GLUT4 content, and improves lipid profile in a rat model of polycystic ovary syndrome

American Journal of Physiology - Endocrinology and Metabolism

Volumn 299, Issue 4, 2010, Pages

  Johansson, Julia ^a   Feng, Yi ^b   Shao, Ruijin ^a   Lönn, Malin ^a   Billig, Håkan ^a   Stener Victorin, Elisabet ^a,c  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b FUDAN UNIVERSITY   (China)

^c HEILONGJIANG UNIVERSITY OF CHINESE MEDICINE   (China)

Author keywords

Acupuncture; Glucose transporter 4; Insulin resistance; Muscle contraction; Skeletal muscle

Indexed keywords

GLUCOSE; GLUCOSE TRANSPORTER 4; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INSULIN; LIPID; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PROTEIN KINASE B; CHOLESTEROL; SLC2A4 PROTEIN, RAT; TRIACYLGLYCEROL;

ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY WEIGHT; CONTROLLED STUDY; ELECTROACUPUNCTURE; FEMALE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HYPERANDROGENISM; IMMUNOFLUORESCENCE; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID ANALYSIS; MUSCLE TWITCH; NONHUMAN; OVARY POLYCYSTIC DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; SOLEUS MUSCLE; WESTERN BLOTTING; ACUPUNCTURE; ANIMAL; BLOOD; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE CLAMP TECHNIQUE; IMMUNOBLOTTING; LIPID METABOLISM; METABOLISM; NONPARAMETRIC TEST; PHYSIOLOGY; POLYCYSTIC OVARY SYNDROME; PROCEDURES; RANDOMIZATION; WISTAR RAT;

ACUPUNCTURE THERAPY; ANIMALS; BLOTTING, WESTERN; CHOLESTEROL; DISEASE MODELS, ANIMAL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE; GLUCOSE CLAMP TECHNIQUE; GLUCOSE TRANSPORTER TYPE 4; IMMUNOBLOTTING; INSULIN RESISTANCE; LIPID METABOLISM; MUSCLE, SKELETAL; POLYCYSTIC OVARY SYNDROME; PROTO-ONCOGENE PROTEINS C-AKT; RANDOM ALLOCATION; RATS; RATS, WISTAR; STATISTICS, NONPARAMETRIC; TRIGLYCERIDES;

EID: 77957566703     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00323.2010     Document Type: Article

References (72)

1. Ahmed MI, Duleba AJ, El Shahat O, Ibrahim ME, Salem A. Naltrexone treatment in clomiphene resistant women with polycystic ovary syndrome. Hum Reprod 23: 2564-2569, 2008.
2. Armstrong RB, Phelps RO. Muscle fiber type composition of the rat hindlimb. Am J Anat 171: 259-272, 1984. (Pubitemid 15189959)
3. Azziz R, Carmina E, Dewailly D, Diamanti-Kandarakis E, Escobar-Morreale HF, Futterweit W, Janssen OE, Legro RS, Norman RJ, Taylor AE, Witchel SF; Task Force on the Phenotype of the Polycystic Ovary Syndrome of The Androgen Excess and PCOS Society. The Androgen Excess and PCOS Society criteria for the polycystic ovary syndrome: the complete task force report. Fertil Steril 91: 456-488, 2009.
4. Beloosesky R, Gold R, Almog B, Sasson R, Dantes A, Land-Bracha A, Hirsh L, Itskovitz-Eldor J, Lessing JB, Homburg R, Amsterdam A. Induction of polycystic ovary by testosterone in immature female rats: Modulation of apoptosis and attenuation of glucose/insulin ratio. Int J Mol Med 14: 207-215, 2004.
5. Bonen A, Tan MH, Watson-Wright WM. Insulin binding and glucose uptake differences in rodent skeletal muscles. Diabetes 30: 702-704, 1981. (Pubitemid 11017738)
6. Cabioglu MT, Ergene N. Changes in serum leptin and beta endorphin levels with weight loss by electroacupuncture and diet restriction in obesity treatment. Am J Chin Med 34: 1-11, 2006. (Pubitemid 43231396)
7. Cabioglu MT, Ergene N. Electroacupuncture therapy for weight loss reduces serum total cholesterol, triglycerides, and LDL cholesterol levels in obese women. Am J Chin Med 33: 525-533, 2005. (Pubitemid 41194614)
8. Chang SL, Lin KJ, Lin RT, Hung PH, Lin JG, Cheng JT. Enhanced insulin sensitivity using electroacupuncture on bilateral Zusanli acupoints (ST 36) in rats. Life Sci 79: 967-971, 2006.
9. Chang SL, Lin JG, Chi TC, Liu IM, Cheng JT. An insulin-dependent hypoglycaemia induced by electroacupuncture at the Zhongwan (CV12) acupoint in diabetic rats. Diabetologia 42: 250-255, 1999.
10. Chang SL, Tsai CC, Lin JG, Hsieh CL, Lin RT, Cheng JT. Involvement of serotonin in the hypoglycemic response to 2 Hz electroacupuncture of zusanli acupoint (ST36) in rats. Neurosci Lett 379: 69-73, 2005.
11. Ciaraldi TP, Aroda V, Mudaliar S, Chang RJ, Henry RR. Polycystic ovary syndrome is associated with tissue-specific differences in insulin resistance. J Clin Endocrinol Metab 94: 157-163, 2009.
12. Ciaraldi TP, el-Roeiy A, Madar Z, Reichart D, Olefsky JM, Yen SS. Cellular mechanisms of insulin resistance in polycystic ovarian syndrome. J Clin Endocrinol Metab 75: 577-583, 1992.
13. Corbould A. Effects of androgens on insulin action in women: is androgen excess a component of female metabolic syndrome? Diabetes Metab Res Rev 24: 520-532, 2008.
14. Coviello AD, Legro RS, Dunaif A. Adolescent girls with polycystic ovary syndrome have an increased risk of the metabolic syndrome associated with increasing androgen levels independent of obesity and insulin resistance. J Clin Endocrinol Metab 91: 492-497, 2006.
15. Curry DL, Bennett LL, Li CH. Stimulation of insulin secretion by beta-endorphins (1-27 & 1-31). Life Sci 40: 2053-2058, 1987.
16. Deshmukh AS, Hawley JA, Zierath JR. Exercise-induced phosphoproteins in skeletal muscle. Int J Obes (Lond) 32, Suppl 4: S18-S23, 2008.
17. Diamond MP, Grainger D, Diamond MC, Sherwin RS, Defronzo RA. Effects of methyltestosterone on insulin secretion and sensitivity in women. J Clin Endocrinol Metab 83: 4420-4425, 1998.
18. Dunaif A. Insulin resistance and the polycystic ovary syndrome: mechanism and implications for pathogenesis. Endocr Rev 18: 774-800, 1997.
19. Dunaif A, Finegood DT. Beta-cell dysfunction independent of obesity and glucose intolerance in the polycystic ovary syndrome. J Clin Endocrinol Metab 81: 942-947, 1996.
20. Dunaif A, Segal KR, Shelley DR, Green G, Dobrjansky A, Licholai T. Evidence for distinctive and intrinsic defects in insulin action in polycystic ovary syndrome. Diabetes 41: 1257-1266, 1992.
21. Dunaif A, Wu X, Lee A, Diamanti-Kandarakis E. Defects in insulin receptor signaling in vivo in the polycystic ovary syndrome (PCOS). Am J Physiol Endocrinol Metab 281: E392-E399, 2001. (Pubitemid 33774558)
22. Elbers JM, Asscheman H, Seidell JC, Megens JA, Gooren LJ. Long-term testosterone administration increases visceral fat in female to male transsexuals. J Clin Endocrinol Metab 82: 2044-2047, 1997. (Pubitemid 27287559)
23. Feng Y, Johansson J, Shao R, Mannerås L, Fernandez-Rodriguez J, Billig H, Stener-Victorin E. Hypothalamic neuroendocrine functions in rats with dihydrotestosterone-induced polycystic ovary syndrome: effects of low-frequency electro-acupuncture. PLoS One 4: e6638, 2009.
24. Fruzzetti F, Bersi C, Parrini D, Ricci C, Genazzani AR. Effect of long-term naltrexone treatment on endocrine profile, clinical features, and insulin sensitivity in obese women with polycystic ovary syndrome. Fertil Steril 77: 936-944, 2002. (Pubitemid 34497160)
25. Goodyear LJ, Kahn BB. Exercise, glucose transport, and insulin sensitivity. Annu Rev Med 49: 235-261, 1998.
26. Han JS. Acupuncture: neuropeptide release produced by electrical stimulation of different frequencies. Trends Neurosci 26: 17-22, 2003.
27. Harris WS. n-3 fatty acids and serum lipoproteins: animal studies. Am J Clin Nutr 65: 1611S-1616S, 1997.
28. Henriksen EJ, Bourey RE, Rodnick KJ, Koranyi L, Permutt MA, Holloszy JO. Glucose transporter protein content and glucose transport capacity in rat skeletal muscles. Am J Physiol Endocrinol Metab 259: E593-E598, 1990.
29. Higashimura Y, Shimoju R, Maruyama H, Kurosawa M. Electroacupuncture improves responsiveness to insulin via excitation of somatic afferent fibers in diabetic rats. Auton Neurosci 150: 100-103, 2009.
30. Holmang A, Niklasson M, Rippe B, Lonnroth P. Insulin insensitivity and delayed transcapillary delivery of insulin in oophorectomized rats treated with testosterone. Acta Physiol Scand 171: 427-438, 2001. (Pubitemid 33757313)
31. Holmang A, Svedberg J, Jennische E, Bjorntorp P. Effects of testosterone on muscle insulin sensitivity and morphology in female rats. Am J Physiol Endocrinol Metab 259: E555-E560, 1990. (Pubitemid 20340374)
32. Højlund K, Glintborg D, Andersen NR, Birk JB, Treebak JT, Frøsig C, Beck-Nielsen H, Wojtaszewski JF. Impaired insulin-stimulated phosphorylation of Akt and AS160 in skeletal muscle of women with polycystic ovary syndrome is reversed by pioglitazone treatment. Diabetes 57: 357-366, 2008.
33. Ishizaki N, Okushi N, Yano T, Yamamura Y. Improvement in glucose tolerance as a result of enhanced insulin sensitivity during electroacupuncture in spontaneously diabetic Goto-Kakizaki rats. Metabolism 58: 1372-1378, 2009.
34. Kagitani F, Uchida S, Hotta H, Aikawa Y. Manual acupuncture needle stimulation of the rat hindlimb activates groups I, II, III and IV single afferent nerve fibers in the dorsal spinal roots. Jpn J Physiol 55: 149-155, 2005.
35. Kang Y, Li M, Yan W, Li X, Kang J, Zhang Y. Electroacupuncture alters the expression of genes associated with lipid metabolism and immune reaction in liver of hypercholesterolemia mice. Biotechnol Lett 29: 1817-1824, 2007.
36. Kaufman MP, Waldrop TG, Rybycki KJ, Ordway GA, Mitchell JH. Effects of static and rythmic twitch contractions on the discharge of group III and IV muscle afferents. Cardiovasc Res 18: 663-668, 1984.
37. Kim SK, Lee G, Shin M, Han JB, Moon HJ, Park JH, Kim KJ, Ha J, Park DS, Min BI. The association of serum leptin with the reduction of food intake and body weight during electroacupuncture in rats. Pharmacol Biochem Behav 83: 145-149, 2006.
38. Kramer HF, Witczak CA, Fujii N, Jessen N, Taylor EB, Arnolds DE, Sakamoto K, Hirshman MF, Goodyear LJ. Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle. Diabetes 55: 2067-2076, 2006.
39. Larance M, Ramm G, Stöckli J, van Dam EM, Winata S, Wasinger V, Simpson F, Graham M, Junutula JR, Guilhaus M, James DE. Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J Biol Chem 280: 37803-37813, 2005.
40. Legro RS. Polycystic ovary syndrome. Phenotype to genotype. Endocrinol Metab Clin North Am 28: 379-396, 1999.
41. Li M, Zhang Y. Modulation of gene expression in cholesterol-lowering effect of electroacupuncture at Fenglong acupoint (ST40): a cDNA microarray study. Int J Mol Med 19: 617-629, 2007.
42. Li X, Zhu J, Huo H. Profile of differentially expressed genes in blood vessels and blood cells of hyperlipidemia rats using suppression subtractive hybridization. J Nanosci Nanotechnol 5: 1287-1291, 2005. (Pubitemid 44502145)
43. Lin JG, Chen WC, Hsieh CL, Tsai CC, Cheng YW, Cheng JT, Chang SL. Multiple sources of endogenous opioid peptide involved in the hypoglycemic response to 15 Hz electroacupuncture at the Zhongwan acupoint in rats. Neurosci Lett 366: 39-42, 2004.
44. Lin JG, Chang SL, Cheng JT. Release of beta-endorphin from adrenal gland to lower plasma glucose by the electroacupuncture at Zhongwan acupoint in rats. Neurosci Lett 326: 17-20, 2002.
45. Lin RT, Tzeng CY, Lee YC, Ho WJ, Cheng JT, Lin JG, Chang SL. Acute effect of electroacupuncture at the Zusanli acupoints on decreasing insulin resistance as shown by lowering plasma free fatty acid levels in steroid-background male rats. BMC Complement Altern Med 9: 26, 2009.
46. Lund S, Holman GD, Schmitz O, Pedersen O. Contraction stimulates translocation of glucose transporter GLUT4 in skeletal muscle through a mechanism distinct from that of insulin. Proc Natl Acad Sci USA 92: 5817-5821, 1995.
47. Lund S, Holman GD, Schmitz O, Pedersen O. Glut 4 content in the plasma membrane of rat skeletal muscle: comparative studies of the subcellular fractionation method and the exofacial photolabelling technique using ATB-BMPA. FEBS Lett 330: 312-318, 1993. (Pubitemid 23276346)
48. Lund S, Holman GD, Zierath JR, Rincon J, Nolte LA, Clark AE, Schmitz O, Pedersen O, Wallberg-Henriksson H. Effect of insulin on GLUT4 cell surface content and turnover rate in human skeletal muscle as measured by the exofacial bis-mannose photolabeling technique. Diabetes 46: 1965-1969, 1997.
49. Macut D, Panidis D, Glisić B, Spanos N, Petakov M, Bjekić J, Stanojlović O, Rousso D, Kourtis A, Bozić I, Damjanović S. Lipid and lipoprotein profile in women with polycystic ovary syndrome. Can J Physiol Pharmacol 86: 199-204, 2008.
50. Mannerås L, Cajander S, Holmäng A, Seleskovic Z, Lystig T, Lönn M, Stener-Victorin E. A new rat model exhibiting both ovarian and metabolic characteristics of polycystic ovary syndrome. Endocrinology 148: 3781-3791, 2007.
51. Mannerås L, Cajander S, Lönn M, Stener-Victorin E. Acupuncture and exercise restore adipose tissue expression of sympathetic markers and improve ovarian morphology in rats with dihydrotestosterone-induced PCOS. Am J Physiol Regul Integr Comp Physiol 296: R1124-R1131, 2009.
52. Mannerås L, Jonsdottir IH, Holmäng A, Lönn M, Stener-Victorin E. Low-frequency electro-acupuncture and physical exercise improve metabolic disturbances and modulate gene expression in adipose tissue in rats with dihydrotestosterone-induced polycystic ovary syndrome. Endocrinology 149: 3559-3568, 2008.
53. Manni L, Lundeberg T, Holmäng A, Aloe L, Stener-Victorin E. Effect of electro-acupuncture on ovarian expression of alpha (1)- and beta (2)-adrenoceptors, and p75 neurotrophin receptors in rats with steroid-induced polycystic ovaries. Reprod Biol Endocrinol 3: 21, 2005. (Pubitemid 41529036)
54. Marcondes FK, Bianchi FJ, Tanno AP. Determination of the estrous cycle phases of rats: some helpful considerations. Braz J Biol 62: 609-614, 2002.
55. Moran LJ, Pasquali R, Teede HJ, Hoeger KM, Norman RJ. Treatment of obesity in polycystic ovary syndrome: a position statement of the Androgen Excess and Polycystic Ovary Syndrome Society. Fertil Steril 92: 1966-1982, 2008.
56. Norman RJ, Dewailly D, Legro RS, Hickey TE. Polycystic ovary syndrome. Lancet 370: 685-697, 2007.
57. Ploug T, van Deurs B, Ai H, Cushman SW, Ralston E. Analysis of GLUT4 distribution in whole skeletal muscle fibers: identification of distinct storage compartments that are recruited by insulin and muscle contractions. J Cell Biol 142: 1429-1446, 1998. (Pubitemid 28452594)
58. Rincon J, Holmäng A, Wahlström EO, Lönnroth P, Björntorp P, Zierath JR, Wallberg-Henriksson H. Mechanisms behind insulin resistance in rat skeletal muscle after oophorectomy and additional testosterone treatment. Diabetes 45: 615-621, 1996.
59. Rockl KS, Witczak CA, Goodyear LJ. Signaling mechanisms in skeletal muscle: acute responses and chronic adaptations to exercise. IUBMB Life 60: 145-153, 2008.
60. Rosenbaum D, Haber RS, Dunaif A. Insulin resistance in polycystic ovary syndrome: decreased expression of GLUT-4 glucose transporters in adipocytes. Am J Physiol Endocrinol Metab 264: E197-E202, 1993.
61. Sano H, Kane S, Sano E, Mîinea CP, Asara JM, Lane WS, Garner CW, Lienhard GE. Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J Biol Chem 278: 14599-14602, 2003. (Pubitemid 36799780)
62. Seow KM, Juan CC, Hsu YP, Hwang JL, Huang LW, Ho LT. Amelioration of insulin resistance in women with PCOS via reduced insulin receptor substrate-1 Ser312 phosphorylation following laparoscopic ovarian electrocautery. Hum Reprod 22: 1003-1010, 2007.
63. Shao R, Weijdegård B, Fernandez-Rodriguez J, Egecioglu E, Zhu C, Andersson N, Thurin-Kjellberg A, Bergh C, Billig H. Ciliated epithelial- specific and regional-specific expression and regulation of the estrogen receptor-β2 in the fallopian tubes of immature rats: a possible mechanism for estrogen-mediated transport process in vivo. Am J Physiol Endocrinol Metab 293: E147-E158, 2007.
64. Shepherd PR, Kahn BB. Glucose transporters and insulin action - implications for insulin resistance and diabetes mellitus. N Engl J Med 341: 248-257, 1999.
65. Shimoju-Kobayashi R, Maruyama H, Yoneda M, Kurosawa M. Responses of hepatic glucose output to electro-acupuncture stimulation of the hindlimb in anaesthetized rats. Auton Neurosci 115: 7-14, 2004. (Pubitemid 39420995)
66. Slot J, Geuze H, Gigengack S, Lienhard G, James D. Immunolocalization of the insulin regulatable glucose transporter in brown adipose tissue of the rat. J Cell Biol 113: 123-135, 1991.
67. Song XM, Ryder JW, Kawano Y, Chibalin AV, Krook A, Zierath JR. Muscle fiber type specificity in insulin signal transduction. Am J Physiol Regul Integr Comp Physiol 277: R1690-R1696, 1999.
68. Stener-Victorin E, Fujisawa S, Kurosawa M. Ovarian blood flow responses to electroacupuncture stimulation depend on estrous cycle and on site and frequency of stimulation in anesthetized rats. J Appl Physiol 101: 84-91, 2006. (Pubitemid 44035352)
69. Stener-Victorin E, Kobayashi R, Kurosawa M. Ovarian blood flow responses to electro-acupuncture stimulation at different frequencies and intensities in anaesthetized rats. Auton Neurosci 108: 50-56, 2003. (Pubitemid 37386263)
70. Stener-Victorin E, Kobayashi R, Watanabe O, Lundeberg T, Kurosawa M. Effect of electro-acupuncture stimulation of different frequencies and intensities on ovarian blood flow in anaesthetized rats with steroid-induced polycystic ovaries. Reprod Biol Endocrinol 2: 16, 2004. (Pubitemid 39130563)
71. Stener-Victorin E, Lundeberg T, Cajander S, Aloe L, Manni L, Waldenström U, Janson PO. Steroid-induced polycystic ovaries in rats: effect of electro-acupuncture on concentrations of endothelin-1 and nerve growth factor (NGF), and expression of NGF mRNA in the ovaries, the adrenal glands, and the central nervous system. Reprod Biol Endocrinol 1: 33, 2003. (Pubitemid 39130491)
72. Wang YT, An H. The acupuncture at Fenglong acupoint for treatment of 49 cases of hypercholestrolemia. Chin Acupunct Moxibust 3: 21-23, 1990.