Mammalian hibernation: A naturally reversible model for insulin resistance in man?

Diabetes and Vascular Disease Research

Volumn 5, Issue 2, 2008, Pages 76-81

  Martin, Sandra L ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Hibernation; Hibernator; Insulin resistance; Metabolic syndrome; Obesity

Indexed keywords

CARDIOVASCULAR SYSTEM; ENVIRONMENTAL TEMPERATURE; GENE EXPRESSION; HIBERNATION; INSULIN RESISTANCE; LIPID STORAGE; MAMMAL; METABOLIC SYNDROME X; NONHUMAN; OBESITY; REVIEW; SQUIRREL;

ADIPOSE TISSUE; ANIMALS; BIOLOGICAL CLOCKS; CARDIOVASCULAR SYSTEM; CUES; EATING; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; HIBERNATION; HUMANS; INSULIN RESISTANCE; METABOLIC SYNDROME X; OBESITY; PERIODICITY; PHOTOPERIOD; SEASONS;

EID: 45249112866     PISSN: 14791641     EISSN: None     Source Type: Journal    
DOI: 10.3132/dvdr.2008.013     Document Type: Review

References (75)

1. Carey HV, Andrews MT, Martin SL. Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 2003;83:1153-81.
2. Davis DE. Hibernation and circannual rhythms of food consumption in marmots and ground squirrels. Q Rev Biol 1976;51:477-514.
3. Wang LCH. Mammalian hibernation: an escape from the cold. Advances Comparative Environmental Physiology 1988;2:1-45.
4. van Breukelen F, Martin SL. Molecular adaptations in mammalian hibernators: unique adaptations or generalized responses? J Appl Physiol 2002;92:2640-7.
5. Barnes BM. Freeze avoidance in a mammal: body temperatures below 0°C in an arctic hibernator. Science 1989;244:1593-5.
6. Lyman CP, Chatfield PO. Physiology of hibernation in mammals. Physiol Rev 1955;35:403-25.
7. Geiser F. Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? J Comparative Physiology B - Biochem Systemic Environmental Physiol 1988;158(1):25-37.
8. Heldmaier G, Ruf T. Body temperature and metabolic rate during natural hypothermia in endotherms. J Comparative Physiol B 1992;162: 696-706.
9. Ortmann S, Heldmaier G. Regulation of body temperature and energy requirements of hibernating alpine marmots (Marmota marmota). Am J Physiol Regul Integr Comp Physiol 2000;278:R698-R704.
10. Heller HC, Colliver GW, Bread J. Thermoregulation during entrance into hibernation. Pflugers Arch 1977;369(1):55-9.
11. Buck CL, Barnes BM. Effects of ambient temperature on metabolic rate, respiratory quotient, and torpor in an arctic hibernator. Am J Physiol 2000;279:R255-R262.
12. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G. Physiology: hibernation in a tropical primate. Nature 2004;429:825-6.
13. Srere HK, Wang LCH, Martin SL. Central role for differential gene expression in mammalian hibernation. Proc Natl Acad Sci USA 1992; 89:7119-23.
14. Dark J. Annual lipid cycles in hibernators: integration of physiology and behavior. Ann Rev Nutrit 2005;25:469-97.
15. Cranford JA. Hibernation in the western jumping mouse (Zapus princeps). J Mamm 1978;59:496-509.
16. Concannon P, Levac K, Rawson R, Tennant B, Bensadoun A. Seasonal changes in serum leptin, food intake, and body weight in photoentrained woodchucks. Am J Physiol Regul Integr Comp Physiol 2001; 281:R951-R959.
17. Freeman DA, Zucker I. Temperature-independence of circannual variations in circadian rhythms of golden-mantled ground squirrels. J Biol Rhythms 2000;15:336-43.
18. Kondo N, Sekijima T, Kondo J, Takamatsu N, Tohya K, Ohtsu T. Circannual control of hibernation by HP complex in the brain. Cell 2006;125:161-72.
19. Wang LCH. Time patterns and metabolic rates of natural torpor in the Richardson's ground squirrel. Can J Zool 1979;57:149-55.
20. Dark J, Stern JS, Zucker I. Adipose tissue dynamics during cyclic weight loss and weight gain of ground squirrels. Am J Physiol Regul Integr Comp Physiol 1989;256(6):R1286-R1292.
21. Serkova NJ, Rose JC, Epperson LE, Carey HV, Martin SL. Quantitative analysis of liver metabolites in three stages of the circannual hibernation cycle in 13-lined ground squirrels by NMR. Physiol Genomics 2007;31:15-24.
22. Geiser F, McAllan BM, Kenagy GJ. The degree of dietary fatty acid unsaturation affects torpor patterns and lipid composition of a hibernator. J Comp Physiol [B] 1994;164:299-305.
23. Frank CL. The influence of dietary fatty acids on hibernation by golden-mantled ground squirrels. Physiological Zoology 1992;65:906-20.
24. Florant GL. Lipid metabolism in hibernators: the importance of essential fatty acids. Amer Zool 1998;38:331-40.
25. Florant GL, Hester L, Ameenuddin S, Rintoul DA. The effect of a low essential fatty acid diet on hibernation in marmots. Am J Physiol 1993;264(4 Pt 2):R747-R753.
26. Hiebert SM, Thomas EM, Lee TM, Pelz KM, Yellon SM, Zucker I. Photic entrainment of circannual rhythms in golden-mantled ground squirrels: role of the pineal gland. J Biol Rhythms 2000;15:126-34.
27. Ruby N, Dark J, Heller H, Zucker I. Suprachiasmatic nucleus: role in circannual body mass and hibernation rhythms of ground squirrels. Brain Res 1998;782:63-72.
28. Ruby NF, Dark J, Burns DE, Heller HC, Zucker I. The suprachiasmatic nucleus is essential for circadian body temperature rhythms in hibernating ground squirrels. J Neurosci 2002;22:357-64.
29. Ruby NF, Dark J, Heller HC, Zucker I. Ablation of suprachiasmatic nucleus alters timing of hibernation in ground squirrels. Proc Natl Acad Sci USA 1996;93:9864-8.
30. Dark J, Kilduff TS, Heller HC, Licht P, Zucker I. Suprachiasmatic nuclei influence hibernation rhythms of golden-mantled ground squirrels. Brain Res 1990;509:111-18.
31. Rawson RE, Concannon PW, Roberts PJ, Tennant BC. Seasonal differences in resting oxygen consumption, respiratory quotient, and free thyroxine in woodchucks. Am J Physiol 1998;274:R963-R969.
32. Concannon PW, Castracane VD, Rawson RE, Tennant BC. Circannual changes in free thyroxine, prolactin, testes, and relative food intake in woodchucks, Marmota monax. Am J Physiol 1999;277:R1401-R1409.
33. Forger NG, Dark J, Barnes BM, Zucker I. Fat ablation and food restriction influence reproductive development and hibernation in ground squirrels. Biol Reprod 1986;34:831-40.
34. Wilson BE, Deeb S, Florant CL. Seasonal changes in hormone-sensitive and lipoprotein lipase mRNA concentrations in marmot white adipose tissue. Am J Physiol 1992;262:R177-R181.
35. Mostafa N, Everett DC, Chou SC, Kong PA, Florant GL, Coleman RA. Seasonal changes in critical enzymes of lipogenesis and triacylglycerol synthesis in the marmot (Marmota flaviventris). J Comp Physiol [B] 1993;163:463-9.
36. Wang P, Walter RD, Bhat BG, Florant GL, Coleman RA. Seasonal changes in enzymes of lipogenesis and triacylglycerol synthesis in the golden-mantled ground squirrel (Spermophilus lateralis). Comp Biochem Physiol B Biochem Mol Biol 1997;118:261-7.
37. Florant GL, Porst H, Peiffer A et al. Fat-cell mass, serum leptin and adiponectin changes during weight gain and loss in yellow-bellied marmots (Marmota flaviventris). J Comp Physiol [B] 2004;174:633-9.
38. Mrosovsky N, Sherry DF. Animal anorexias. Science 1980;207:837-42.
39. Hoehn KL, Hudachek SF, Summers SA, Florant GL. Seasonal, tissue-specific regulation of Akt/protein kinase B and glycogen synthase in hibernators. Am J Physiol Regul Integr Comp Physiol 2004;286:R498-R504.
40. Lyman CP, Willis JS, Malan A, Wang LCH. Hibernation and torpor in mammals and birds. New York: Academic Press; 1982.
41. Florant GL, Lawrence AK, Williams K, Bauman WA. Seasonal changes in pancreatic B-cell function in euthermic yellow-bellied marmots. Am J Physiol Regul Integr Comp Physiol 1985;249(2):R159-R165.
42. Buck MJ, Squire TL, Andrews MT. Coordinate expression of the PDK4 gene: a means of regulating fuel selection in a hibernating mammal. Physiol Genomics 2002;8:5-13.
43. Zatzman ML, Thornhill GV. Seasonal variation of cardiovascular function in the marmot, Marmota flaviventris. Cryobiology 1987;24:376-85.
44. Frerichs KU, Kennedy C, Sokoloff L, Hallenbeck JM. Local cerebral blood flow during hibernation, a model of natural tolerance to cerebral ischemia. J Cereb Blood Flow Metab 1994;14:193-205.
45. Ma YL, Zhu X, Rivera PM et al. Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels. Am J Physiol Regul Integr Comp Physiol 2005;289:R1297-R1306.
46. Fishman AP, Lyman CP. Hibernation in mammals. Circulation 1961;24: 434-45.
47. Svihla A, Bowman H, Ritenour R. Relation of prothrombin to the prolongation of clotting time in aestivating ground squirrels. Science 1952; 115:306-07.
48. Lechler E, Penick GD. Blood clotting defect in hibernating ground squirrels (Citellus tridecemlineatus). Am J Physiol 1963;205:985- 8.
49. 2Macroglobulin gene expression is independent of acute phase response during hibernation in ground squirrels. Am J Physiol Regul Integr Comp Physiol 1995;268: R1507-R1512.
50. Sheikh AM, Chauhan V, Tsiouris JA et al. Elevated levels of serum alpha2 macroglobulin in wild black bears during hibernation. Biochimie 2003;85:1027-32.
51. Epperson LE, Martin SL. Quantitative assessment of ground squirrel RNA levels in multiple stages of hibernation. Physiol Genomics 2002; 10:93-102.
52. Mominoki K, Morimatsu M, Karjalainen M, Hohtola E, Hissa R, Saito M. Elevated plasma concentrations of haptoglobin in European brown bears during hibernation. Comp Biochem Physiol A Mol Integr Physiol 2005;142:472-7.
53. Toien O, Drew KL, Chao ML, Rice ME. Ascorbate dynamics and oxygen consumption during arousal from hibernation in Arctic ground squirrels. Am J Physiol Regul Integr Comp Physiol 2001;281:R572-R583.
54. Lindell SL, Klahn SL, Piazza TM et al. Natural resistance to liver cold ischemia-reperfusion injury associated with the hibernation phenotype. Am J Physiol Gastrointest Liver Physiol 2005;288:G473-G480.
55. Dave KR, Prado R, Raval AP, Drew KL, Perez-Pinzon MA. The arctic ground squirrel brain is resistant to injury from cardiac arrest during euthermia. Stroke 2006;37:1261-5.
56. Kurtz CC, Lindell SL, Mangino MJ, Carey HV. Hibernation confers resistance to intestinal ischemia-reperfusion injury. Am J Physiol Gastroint Liver Physiol 2006;291:G895-G901.
57. Drew KL, Harris MB, LaManna JC, Smith MA, Zhu XW, Ma YL. Hypoxia tolerance in mammalian heterotherms. J Exp Biol 2004;207:3155-62.
58. Andrews MT. Advances in molecular biology of hibernation in mammals. Bioessays 2007;29:431-40.
59. Carey HV, Rhoads CA, Aw TY. Hibernation induces glutathione redox imbalance in ground squirrel intestine. J Comp Physiol [B] 2003;173: 269-76.
60. Andrews MT, Squire TL, Bowen CM, Rollins MB. Low-temperature carbon utilization is regulated by novel gene activity in the heart of a hibernating mammal. Proc Natl Acad Sci USA 1998;95:8392-7.
61. O'Hara BF, Watson FL, Srere HK et al. Gene expression in the brain across the hibernation cycle. J Neurosci 1999;19:3781-90.
62. Brauch KM, Dhruv ND, Hanse EA, Andrews MT. Digital transcriptome analysis indicates adaptive mechanisms in the heart of a hibernating mammal. Physiol Genomics 2005;23:227-34.
63. Yan J, Burman A, Nichols C et al. The detection of differential gene expression in brown adipose tissue of hibernating arctic ground squirrels using mouse microarrays. Physiol Genomics 2006;25:346-53.
64. Williams DR, Epperson LE, Li W et al. Seasonally hibernating phenotype assessed through transcript screening. Physiol Genomics 2005; 24(1):13-22.
65. Epperson LE, Dahl T, Martin SL. Quantitative analysis of liver protein expression during hibernation in the golden-mantled ground squirrel. Mol Cell Proteomics 2004;3:920-33.
66. Lee YJ, Miyake SI, Wakita H et al. Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells. J Cereb Blood Flow Metab 2007;27:950-62.
67. Ohtsuki T, Jaffe H, Brenner M et al. Stimulation of tyrosine phosphorylation of a brain protein by hibernation. J Cereb Blood Flow Metab 1998;18:1040-5.
68. Chen Y, Matsushita M, Nairn AC et al. Mechanisms for increased levels of phosphorylation of elongation factor-2 during hibernation in ground squirrels. Biochemistry 1998;40:11565-70.
69. Frerichs KU, Smith CB, Brenner M et al. Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc Natl Acad Sci USA 1998;95:14511-16.
70. van Breukelen F, Sonenberg N, Martin SL. Seasonal and state-dependent changes of elF4E and 4E-BP1 during mammalian hibernation: implications for the control of translation during torpor. Am J Physiol Regul Integr Comp Physiol 2004;287:R349-R353.
71. Storey KB. Regulation of liver metabolism by enzyme phosphorylation during mammalian hibernation. J Biol Chem 1987;262:1670-3.
72. Neel JV. Diabetes mellitus: a "thrifty" genotype rendered detrimental by "progress"? Am J Hum Genet 1962;14:353- 62.
73. Diamond J. The double puzzle of diabetes. Nature 2003;423:599-602.
74. Speakman JR. Thrifty genes for obesity and the metabolic syndrome - time to call off the search? Diabetes Vasc Dis Res 2006;3(1):7-11, doi: 10.3132/dvdr.2006.010.
75. Grant PJ. Obesity, diabetes and cardiovascular disease: is the fat lady singing? Diabetes Vasc Dis Res 2006;3(1):5-6, doi: 10.3132/dvdr.2006. 007.