Intermittent hypoxia impairs glucose homeostasis in C57BL6/J mice: Partial improvement with Cessation of the exposure

Sleep

Volumn 36, Issue 10, 2013, Pages 1483-1490

  Polak, Jan ^a,b   Shimoda, Larissa A ^a   Drager, Luciano F ^a,c   Undem, Clark ^a   McHugh, Holly ^a   Polotsky, Vsevolod Y ^a   Punjabi, Naresh M ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CHARLES UNIVERSITY   (Czech Republic)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Glucose intolerance; Insulin resistance; Intermittent hypoxia; Obstructive sleep apnea

Indexed keywords

GLUCOSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; EXPOSURE; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; GLYCOGEN LIVER LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; INTERMITTENT HYPOXIA; LIVER CELL; LIVER METABOLISM; MOUSE; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PRIORITY JOURNAL;

GLUCOSE INTOLERANCE; INSULIN RESISTANCE; INTERMITTENT HYPOXIA; OBSTRUCTIVE SLEEP APNEA;

ANIMALS; ANOXIA; BLOOD GLUCOSE; DISEASE MODELS, ANIMAL; GLUCOSE; GLUCOSE TOLERANCE TEST; HOMEOSTASIS; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; SLEEP APNEA, OBSTRUCTIVE;

EID: 84885155381     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.5665/sleep.3040     Document Type: Article

References (43)

1. Young T, Palta M, Dempsey J, Skatrud J, Weber S, Badr S. The occurrence of sleep-disordered breathing among middle-aged adults. N Engl J Med 1993;328:1230-5.
2. Young T, Peppard PE, Gottlieb DJ. Epidemiology of obstructive sleep apnea: a population health perspective. Am J Respir Crit Care Med 2002;165:1217-39.
3. Peppard PE, Young T, Palta M, Skatrud J. Prospective study of the association between sleep-disordered breathing and hypertension. N Engl J Med 2000;342:1378-84.
4. Cano-Pumarega I, Duran-Cantolla J, Aizpuru F, et al. Obstructive sleep apnea and systemic hypertension: longitudinal study in the general population: the Vitoria Sleep Cohort. Am J Respir Crit Care Med 2011;184:1299-304.
5. Marin JM, Agusti A, Villar I, et al. Association between treated and untreated obstructive sleep apnea and risk of hypertension. JAMA 2012;307:2169-76.
6. Gottlieb DJ, Yenokyan G, Newman AB, et al. Prospective study of obstructive sleep apnea and incident coronary heart disease and heart failure: the sleep heart health study. Circulation 2010;122:352-60.
7. Yeboah J, Redline S, Johnson C, et al. Association between sleep apnea, snoring, incident cardiovascular events and all-cause mortality in an adult population: MESA. Atherosclerosis 2011;219:963-8.
8. Arzt M, Young T, Finn L, Skatrud JB, Bradley TD. Association of sleepdisordered breathing and the occurrence of stroke. Am J Respir Crit Care Med 2005;172:1447-51.
9. Redline S, Yenokyan G, Gottlieb DJ, et al. Obstructive sleep apneahypopnea and incident stroke: the sleep heart health study. Am J Respir Crit Care Med 2010;182:269-77.
10. Yaggi HK, Concato J, Kernan WN, Lichtman JH, Brass LM, Mohsenin V. Obstructive sleep apnea as a risk factor for stroke and death. N Engl J Med 2005;353:2034-41.
11. Marshall NS, Wong KK, Liu PY, Cullen SR, Knuiman MW, Grunstein RR. Sleep apnea as an independent risk factor for all-cause mortality: the Busselton Health Study. Sleep 2008;31:1079-85.
12. Young T, Finn L, Peppard PE, et al. Sleep disordered breathing and mortality: eighteen-year follow-up of the Wisconsin sleep cohort. Sleep 2008;31:1071-8.
13. Punjabi NM, Caffo BS, Goodwin JL, et al. Sleep-disordered breathing and mortality: a prospective cohort study. PLoS Med 2009;6:e1000132.
14. Marshall NS, Delling L, Grunstein RR, et al. Self-reported sleep apnoea and mortality in patients from the Swedish Obese Subjects study. Eur Respir J 2011;38:1349-54.
15. Punjabi NM. Do sleep disorders and associated treatments impact glucose metabolism? Drugs 2009;69(Suppl 2):13-27.
16. Tasali E, Mokhlesi B, Van Cauter E. Obstructive sleep apnea and type 2 diabetes: interacting epidemics. Chest 2008;133:496-506.
17. Strohl KP, Novak RD, Singer W, et al. Insulin levels, blood pressure and sleep apnea. Sleep 1994;17:614-8.
18. Ip MS, Lam B, Ng MM, Lam WK, Tsang KW, Lam KS. Obstructive sleep apnea is independently associated with insulin resistance. Am J Respir Crit Care Med 2002;165:670-6.
19. Punjabi NM, Sorkin JD, Katzel LI, Goldberg AP, Schwartz AR, Smith PL. Sleep-disordered breathing and insulin resistance in middle-aged and overweight men. Am J Respir Crit Care Med 2002;165:677-82.
20. Punjabi NM, Shahar E, Redline S, Gottlieb DJ, Givelber R, Resnick HE. Sleep-disordered breathing, glucose intolerance, and insulin resistance: the Sleep Heart Health Study. Am J Epidemiol 2004;160:521-30.
21. Polotsky VY, Li J, Punjabi NM, et al. Intermittent hypoxia increases insulin resistance in genetically obese mice. J Physiol 2003;552(Pt 1):253-64.
22. Iiyori N, Alonso LC, Li J, et al. Intermittent hypoxia causes insulin resistance in lean mice independent of autonomic activity. Am J Respir Crit Care Med 2007;175:851-7.
23. O'Donnell CP. Metabolic consequences of intermittent hypoxia. Adv Exp Med Biol 2007;618:41-9.
24. Yokoe T, Alonso LC, Romano LC, et al. Intermittent hypoxia reverses the diurnal glucose rhythm and causes pancreatic beta-cell replication in mice. J Physiol 2008;586:899-911.
25. Xu J, Long YS, Gozal D, Epstein PN. Beta-cell death and proliferation after intermittent hypoxia: role of oxidative stress. Free Radic Biol Med 2009;46:783-90.
26. Drager LF, Li J, Reinke C, Bevans-Fonti S, Jun. JC, Polotsky VY. Intermittent hypoxia exacerbates metabolic effects of diet-induced obesity. Obesity (Silver Spring) 2011;11:2167-74.
27. Louis M, Punjabi NM. Effects of acute intermittent hypoxia on glucose metabolism in awake healthy volunteers. J Appl Physiol 2009;106:1538-44.
28. Bonadonna RC, De Fronzo RA. Glucose metabolism in obesity and type 2 diabetes. Diabetes Metab 1991;17(1 Pt 2):112-35.
29. Zierler K. Whole body glucose metabolism. Am J Physiol 1999;276(3 Pt 1):E409-26.
30. Tagaito Y, Polotsky V Y, Campen MJ, et al. A model of sleep-disordered breathing in the C57BL/6J mouse. J Appl Physiol 2001;91:2758-66.
31. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28:412-9.
32. Wahren J, Ekberg K. Splanchnic regulation of glucose production. Annu Rev Nutr 2007;27:329-45.
33. Chiu LL, Chou SW, Cho YM, et al. Effect of prolonged intermittent hypoxia and exercise training on glucose tolerance and muscle GLUT4 protein expression in rats. J Biomed Sci 2004;11:838-46.
34. Ling Q, Sailan W, Ran J, et al. The effect of intermittent hypoxia on bodyweight, serum glucose and cholesterol in obesity mice. Pak J Biol Sci 2008;11:869-75.
35. Chen CY, Tsai YL, Kao CL, et al. Effect of mild intermittent hypoxia on glucose tolerance, muscle morphology and AMPK-PGC-1alpha signaling. Chin J Physiol 2010;53:62-71.
36. Carreras A, Kayali F, Zhang J, Hirotsu C, Wang Y, Gozal D. Metabolic effects of intermittent hypoxia in mice: steady versus high-frequency applied hypoxia daily during the rest period. Am J Physiol Regul Integr Comp Physiol 2012;303:R700-9.
37. Fenik VB, Singletary T, Branconi JL, Davies RO, Kubin L. Glucoregulatory consequences and cardiorespiratory parameters in rats exposed to chronic-intermittent hypoxia: effects of the duration of exposure and losartan. Front Neurol 2012;3:51.
38. Li J, Bosch-Marce M, Nanayakkara A, et al. Altered metabolic responses to intermittent hypoxia in mice with partial defciency of hypoxiainducible factor-1alpha. Physiol Genomics 2006;25:450-7.
39. Baum D, Griepp R, Porte D, Jr. Glucose-induced insulin release during acute and chronic hypoxia. Am J Physiol 1979;237:E45-50.
40. Dionne KE, Colton CK, Yarmush ML. Effect of hypoxia on insulin secretion by isolated rat and canine islets of Langerhans. Diabetes 1993;42:12-21.
41. Grankvist K, Marklund SL, Taljedal IB. CuZn-superoxide dismutase, Mnsuperoxide dismutase, catalase and glutathione peroxidase in pancreatic islets and other tissues in the mouse. Biochem J 1981;199:393-8.
42. Lee EJ, Alonso LC, Stefanovski D, et al. Time-dependent changes in glucose and insulin regulation during intermittent hypoxia and continuous hypoxia. Eur J Appl Physiol 2013;113:467-78.
43. Toye AA, Lippiat JD, Proks P, et al. A genetic and physiological study of impaired glucose homeostasis control in C57BL/6J mice. Diabetologia 2005;48:675-86.