Glucose homoeostasis in rats exposed to acute intermittent hypoxia

Acta Physiologica

Volumn 209, Issue 1, 2013, Pages 77-89

  Rafacho, A ^a   Goncalves Neto L M ^a   Ferreira, F B D ^a   Protzek, A O P ^b   Boschero, A C ^b   Nunes, E A ^a   Zoccal, D B ^a,c  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^b UNIVERSITY OF CAMPINAS   (Brazil)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Blood glucose; Glucose tolerance; Insulin sensitivity; Intermittent hypoxia; Propranolol; Sympathetic activity

Indexed keywords

GLUCOSE; GLYCOGEN; INSULIN; LACTIC ACID; LIPID; PROPRANOLOL; PROTEIN KINASE B; GLUCOSE BLOOD LEVEL;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; GLYCOGEN LIVER LEVEL; HEART RATE; HYPERLIPIDEMIA; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; INSULINEMIA; INTERMITTENT HYPOXIA; LACTATE BLOOD LEVEL; LIPID BLOOD LEVEL; LIVER; MALE; MEAN ARTERIAL PRESSURE; METABOLIC PARAMETERS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SKELETAL MUSCLE; SYMPATHETIC FUNCTION; ADRENERGIC SYSTEM; ANIMAL; ANOXIA; BLOOD; HOMEOSTASIS; HYPERGLYCEMIA; INSULIN RESISTANCE; METABOLISM; PHYSIOLOGY; WISTAR RAT;

ANIMALS; ANOXIA; BLOOD GLUCOSE; HOMEOSTASIS; HYPERGLYCEMIA; INSULIN; INSULIN RESISTANCE; MALE; MUSCLE, SKELETAL; RATS, WISTAR; SYMPATHETIC NERVOUS SYSTEM;

EID: 84881545277     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/apha.12118     Document Type: Article

References (48)

1. Abe, H., Minokoshi, Y. & Shimazu, T. 1993. Effect of beta 3-adrenergic agonist, BRL35135A, on glucose uptake in rat skeletal muscle in vivo and in vitro. J Endocrinol 139, 479-486.
2. Barros, R.C.H., Bonagamba, L.G.H., Okamoto-Canesin, R., de Oliveira, M., Branco, L.G.S. & Machado, B.H. 2002. Cardiovascular responses to chemoreflex activation with potassium cyanide or hypoxic hypoxia in awake rats. Auton Neurosci 97, 110-115.
3. Buren, J., Lai, Y.C., Lundgren, M., Eriksson, J.W. & Jensen, J. 2008. Insulin action and signalling in fat and muscle from dexamethasone-treated rats. Arch Biochem Biophys 474, 91-101.
4. Dehvari, N., Hutchinson, D.S., Nevzorova, J., Dallner, O.S., Sato, M., Kocan, M., Merlin, J., Evans, B.A., Summers, R.J. & Bengtsson, T. 2012. β(2)-adrenoceptors increase translocation of GLUT4 via GPCR kinase sites in the receptor C-terminal tail. Br J Pharmacol 165, 1442-1456.
5. Dick, T.E., Hsieh, Y.H., Wang, N. & Prabhakar, N. 2007. Acute intermittent hypoxia increases both phrenic and sympathetic nerve activities in the rat. Exp Physiol 92, 87-97.
6. Drager, L.F., Jun, J.C. & Polotsky, V.Y. 2010. Metabolic consequences of intermittent hypoxia: relevance to obstructive sleep apnea. Best Pract Res Clin Endocrinol Metab 24, 843-851.
7. Drager, L.F., Li, J., Reinke, C., Bevans-Fonti, S., Jun, J.C. & Polotsky, V.Y. 2011. Intermittent hypoxia exacerbates metabolic effects of diet-induced obesity. Obesity (Silver Spring) 19, 2167-2174.
8. Fenik, V.B., Singletary, T., Branconi, J.L., Davies, R.O. & Kubin, L. 2012. Glucoregulatory consequences and cardiorespiratory parameters in rats exposed to chronic-intermittent hypoxia: effects of the duration of exposure and losartan. Front Neurol 3, 51.
9. Filiputti, E., Rafacho, A., Araujo, E.P., Silveira, L.R., Trevisan, A., Batista, T.M., Curi, R., Velloso, L.A., Quesada, I., Boschero, A.C. & Carneiro, E.M. 2010. Augmentation of insulin secretion by leucine supplementation in malnourished rats: possible involvement of the phosphatidylinositol 3-phosphate kinase/mammalian target protein of rapamycin pathway. Metabolism 59, 635-644.
10. Fujii, N., Jessen, N. & Goodyear, L.J. 2006. AMP-activated protein kinase and the regulation of glucose transport. Am J Physiol Endocrinol Metab 291, E867-E877.
11. Gamboa, J.L., Garcia-Cazarin, M.L. & Andrade, F.H. 2011. Chronic hypoxia increases insulin-stimulated glucose uptake in mouse soleus muscle. Am J Physiol Regul Integr Comp Physiol 300, R85-R91.
12. Giozzet, V.A., Rafacho, A., Boschero, A.C., Carneiro, E.M. & Bosqueiro, J.R. 2008. Dexamethasone treatment in vivo counteracts the functional pancreatic islet alterations caused by malnourishment in rats. Metabolism 57, 617-624.
13. Guerrero-Romero, F., Simental-Mendia, L.E., Gonzalez-Ortiz, M., Martinez-Abundis, E., Ramos-Zavala, M.G., Hernandez-Gonzalez, S.O., Jacques-Camarena, O. & Rodriguez-Moran, M. 2010. The product of triglycerides and glucose, a simple measure of insulin sensitivity. Comparison with the euglycemic-hyperinsulinemic clamp. J Clin Endocrinol Metab 95, 3347-3351.
14. Iiyori, N., Alonso, L.C., Li, J., Sanders, M.H., Garcia-Ocana, A., O'Doherty, R.M., Polotsky, V.Y. & O'Donnell, C.P. 2007. Intermittent hypoxia causes insulin resistance in lean mice independent of autonomic activity. Am J Respir Crit Care Med 175, 851-857.
15. Järhult, J., Falck, B., Ingemansson, S. & Nobin, A. 1979. The functional importance of sympathetic nerves to the liver and endocrine pancreas. Ann Surg 189, 96-100.
16. Jun, J. & Polotsky, V.Y. 2007. Sleep disordered breathing and metabolic effects: evidence from animal models. Sleep Med Clin 2, 263-277.
17. Jun, J. & Polotsky, V.Y. 2009. Metabolic consequences of sleep-disordered breathing. ILAR J 50, 289-306.
18. Jun, J.C., Shin, M.K., Yao, Q., Bevans-Fonti, S., Poole, J., Drager, L.F. & Polotsky, V.Y. 2012. Acute hypoxia induces hypertriglyceridemia by decreasing plasma triglyceride clearance in mice. Am J Physiol Endocrinol Metab 303, E377-E388.
19. Kara, T., Narkiewicz, K. & Somers, V.K. 2003. Chemoreflexes-physiology and clinical implications. Acta Physiol Scand 177, 377-384.
20. Leuenberger, U.A., Hogeman, C.S., Quraishi, S., Linton-Frazier, L. & Gray, K.S. 2007. Short-term intermittent hypoxia enhances sympathetic responses to continuous hypoxia in humans. J Appl Physiol 103, 835-842.
21. Levy, B., Desebbe, O., Montemont, C. & Gibot, S. 2008. Increased aerobic glycolysis through beta2 stimulation is a common mechanism involved in lactate formation during shock states. Shock 30, 417-421.
22. Li, J., Bosch-Marce, M., Nanayakkara, A., Savransky, V., Fried, S.K., Semenza, G.L. & Polotsky, V.Y. 2006. Altered metabolic responses to intermittent hypoxia in mice with partial deficiency of hypoxia-inducible factor-1alpha. Physiol Genomics 25, 450-457.
23. Liu, Y.L. & Stock, M.J. 1995. Acute effects of the beta 3-adrenoreceptor agonist, BRL 35135, on tissue glucose utilisation. Br J Pharmacol 114, 888-894.
24. Lo, S., Russell, J.C. & Taylor, A.W. 1970. Determination of glycogen in small tissue samples. J Appl Physiol 28, 234-236.
25. Louis, M. & Punjabi, N.M. 2009. Effects of acute intermittent hypoxia on glucose metabolism in awake healthy volunteers. J Appl Physiol 106, 1538-1544.
26. Lui, M.M. & Ip, M.S. 2010. Disorders of glucose metabolism in sleep-disordered breathing. Clin Chest Med 31, 271-285.
27. Matthews, D.R., Hosker, J.P., Rudenski, A.S., Naylor, B.A., Treacher, D.F. & Turner, R.C. 1985. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412-419.
28. Mu, J., Brozinick, J.T. Jr, Valladares, O., Bucan, M. & Birnbaum, M.J. 2001. A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7, 1085-1094.
29. Narimiya, M., Yamada, H., Matsuba, I., Ikeda, Y.U., Tanese, T. & Abe, M. 1982. The effect of hypoxia on insulin and glucagon secretion in the perfused pancreas of the rat. Endocrinology 111, 1010-1014.
30. Nevzorova, J., Evans, B.A., Bengtsson, T. & Summers, R.J. 2006. Multiple signaling pathways involved in beta2-adrenboreceptor-mediated glucose uptake in rat skeletal muscle cells. Br J Pharmacol 147, 446-454.
31. Ota, H., Tamaki, S., Itaya-Hironaka, A., Yamauchi, A., Sakuramoto-Tsuchida, S., Morioka, T., Takasawa, S. & Kimura, H. 2012. Attenuation of glucose-induced insulin secretion by intermittent hypoxia via down-regulation of CD38. Life Sci 90, 206-211.
32. Peltonen, G.L., Scalzo, R.L., Schweder, M.M., Larson, D.G., Luckasen, G.J., Irwin, D., Hamilton, K.L., Schroeder, T. & Bell, C. 2012. Sympathetic inhibition attenuates hypoxia induced insulin resistance in healthy adult humans. J Physiol 590, 2801-2809.
33. Polotsky, V.Y., Li, J., Punjabi, N.M., Rubin, A.E., Smith, P.L., Schwartz, A.R. & O'Donnell, C.P. 2003. Intermittent hypoxia increases insulin resistance in genetically obese mice. J Physiol 552, 253-264.
34. Qin, L., Xiang, Y., Song, Z., Jing, R., Hu, C. & Howard, S.T. 2010. Erythropoietin as a possible mechanism for the effects of intermittent hypoxia on bodyweight, serum glucose and leptin in mice. Regul Pept 165, 168-173.
35. Rafacho, A., Roma, L.P., Taboga, S.R., Boschero, A.C. & Bosqueiro, J.R. 2007. Dexamethasone-induced insulin resistance is associated with increased connexin 36 mRNA and protein expression in pancreatic rat islets. Can J Physiol Pharmacol 85, 536-545.
36. Rafacho, A., Giozzet, V.A., Boschero, A.C. & Bosqueiro, J.R. 2008. Functional alterations in endocrine pancreas of rats with different degrees of dexamethasone-induced insulin resistance. Pancreas 36, 284-293.
37. Rafacho, A., Quallio, S., Ribeiro, D.L., Taboga, S.R., Paula, F.M., Boschero, A.C. & Bosqueiro, J.R. 2010. The adaptive compensations in endocrine pancreas from glucocorticoid-treated rats are reversible after the interruption of treatment. Acta Physiol (Oxf) 200, 223-235.
38. Reinke, C., Bevans-Fonti, S., Drager, L.F., Shin, M.K. & Polotsky, V.Y. 2011. Effects of different acute hypoxic regimens on tissue oxygen profiles and metabolic outcomes. J Appl Physiol 111, 881-890.
39. Somers, V.K. 1995. Sympathetic neural mechanisms in obstructive sleep apnea. J Clin Invest 96, 1897-1904.
40. Tasali, E. & Ip, M.S. 2008. Obstructive sleep apnea and metabolic syndrome: alterations in glucose metabolism and inflammation. Proc Am Thorac Soc 5, 207-217.
41. Tassone, F., Lanfranco, F., Gianotti, L., Pivetti, S., Navone, F., Rossetto, R., Grottoli, S., Gai, V., Ghigo, E. & Maccario, M. 2003. Obstructive sleep apnoea syndrome impairs insulin sensitivity independently of anthropometric variables. Clin Endocrinol (Oxf) 59, 374-379.
42. Witkowski, A., Prejbisz, A., Florczak, E., Kadziela, J., Sliwinski, P., Bielen, P., Michalowska, I., Kabat, M., Warchol, E., Januszewicz, M., Narkiewicz, K., Somers, V.K., Sobotka, P.A. & Januszewicz, A. 2011. Effects of renal sympathetic denervation on blood pressure, sleep apnea course, and glycemic control in patients with resistant hypertension and sleep apnea. Hypertension 58, 559-565.
43. Xing, T. & Pilowsky, P.M. 2010. Acute intermittent hypoxia in rat in vivo elicits a robust increase in tonic sympathetic nerve activity that is independent of respiratory drive. J Physiol 588, 3075-3088.
44. Yokoe, T., Alonso, L.C., Romano, L.C., Rosa, T.C., O'Doherty, R.M., Garcia-Ocana, A., Minoguchi, K. & O'Donnell, C.P. 2008. Intermittent hypoxia reverses the diurnal glucose rhythm and causes pancreatic beta-cell replication in mice. J Physiol 586, 899-911.
45. Zierath, J.R., Tsao, T.S., Stenbit, A.E., Ryder, J.W., Galuska, D. & Charron, M.J. 1998. Restoration of hypoxia-stimulated glucose uptake in GLUT4-deficient muscles by muscle-specific GLUT4 transgenic complementation. J Biol Chem 273, 20910-20915.
46. Zoccal, D.B., Bonagamba, L.G., Oliveira, F.R., Antunes-Rodrigues, J. & Machado, B.M. 2007a. Increased sympathetic activity in rats submitted to chronic intermittent hypoxia. Exp Physiol 92, 79-85.
47. Zoccal, D.B., Bonagamba, L.G., Antunes-Rodrigues, J. & Machado, B.H. 2007b. Plasma corticosterone levels is elevated in rats submitted to chronic intermittent hypoxia. Auton Neurosci 134, 115-117.
48. Zoccal, D.B., Simms, A.E., Bonagamba, L.G.H., Braga, V.A., Pickering, A.E., Paton, J.F.R. & Machado, B.H. 2008. Increased sympathetic outflow in juvenile rats submitted to chronic intermittent hypoxia correlates with enhanced expiratory activity. J Physiol 586, 3253-3265.