Quantitative analysis of liver metabolites in three stages of the circannual hibernation cycle in 13-lined ground squirrels by NMR

Physiological Genomics

Volumn 31, Issue 1, 2007, Pages 15-24

  Serkova, Natalie J ^a   Rose, James C ^a   Epperson, L Elaine ^a   Carey, Hannah V ^b   Martin, Sandra L ^a  

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

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Metabolomics; Nitrogen metabolism; Osmolytes; Spermophilus tridecemlineatus; Torpor

Indexed keywords

3 HYDROXYBUTYRIC ACID; ALANINE; BETAINE; CARBOHYDRATE; GLUCOSE; GLUTAMINE; LACTIC ACID; LIPID; LIVER EXTRACT; SUCCINIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; CATABOLISM; CIRCANNUAL RHYTHM; CONTROLLED STUDY; HIBERNATION; LIVER METABOLISM; METABOLOMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PATTERN RECOGNITION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SEASONAL VARIATION; SQUIRREL;

ANIMALS; BODY TEMPERATURE; GENE EXPRESSION REGULATION; GLUCOSE; HIBERNATION; LIVER; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, BIOLOGICAL; NITROGEN; SCIURIDAE; SEASONS; TEMPERATURE; TIME FACTORS;

ANIMALIA; SPERMOPHILUS; SPERMOPHILUS TRIDECEMLINEATUS;

EID: 34548822408     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00028.2007     Document Type: Article

References (46)

1. Avila MA, Berasain C, Prieto J, Mato JM, Garcia-Trevijano ER, Corrales FJ. Influence of impaired liver methionine metabolism on the development of vascular disease and inflammation. Curr Med Chem Cardiovasc Hematol Agents 3: 267-281, 2005.
2. Behrends M, Hirose R, Serkova NJ, Coatney JL, Bedolli M, Yardi J, Park YH, Niemann CU. Mild hypothermia reduces the inflammatory response and hepatic ischemia/reperfusion injury in rats. Liver Int 26: 734-741, 2006.
3. Brauch KM, Dhruv ND, Hanse EA, Andrews MT. Digital transcriptome analysis indicates adaptive mechanisms in the heart of a hibernating mammal. Physiol Genomics 23: 227-234, 2005.
4. 13C NMR analysis reveals a link between L-glutamine metabolism, D-glucose metabolism and gamma-glutamyl cycle activity in a clonal pancreatic beta-cell line. Diabetologia 46: 1512-1521, 2003.
5. Carey HV, Andrews MT, Martin SL. Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83: 1153-1181, 2003.
6. Carey HV, Frank CL, Seifert JP. Hibernation induces oxidative stress and activation of NK-κB in ground squirrel intestine. J Comp Physiol 170: 551-559, 2000.
7. Carey HV, Rhoads CA, Aw TY. Hibernation induces glutathione redox imbalance in ground squirrel intestine. J Comp Physiol 173: 269-276, 2003.
8. Dark J. Annual lipid cycles in hibernators: integration of physiology and behavior. Annu Rev Nutr 25: 469-497, 2005.
9. 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 37: 1261-1265, 2006.
10. Drew KL, Osborne PG, Frerichs KU, Hu Y, Koren RE, Hallenbeck JM, Rice ME. Ascorbate and glutathione regulation in hibernating ground squirrels. Brain Res 851: 1-8, 1999.
11. Epperson LE, Dahl T, Martin SL. Quantitative analysis of liver protein expression during hibernation in the golden-mantled ground squirrel. Mol Cell Proteomics 3: 920-933, 2004.
12. Essex-Fraser PA, Steele SL, Bernier NJ, Murray BW, Stevens ED, Wright PA. Expression of four glutamine synthetase genes in the early stages of development of rainbow trout (Oncorhynchus mykiss) in relationship to nitrogen excretion. J Biol Chem 280: 20268-20273, 2005.
13. Fisher KC. On the mechanism of periodic arousal in the hibernating ground squirrel. Ann Acad Sci Fenn Ser A IV Biol 71: 141-156, 1964.
14. Fleck CC, Carey HV. Modulation of apoptotic pathways in intestinal mucosa during hibernation. Am J Physiol Regul Integr Comp Physiol 289: R586-R595, 2005.
15. Frerichs KU, Hallenbeck JM. Hibernation in ground squirrels induces state and species-specific tolerance to hypoxia and aglycemia: an in vitro study in hippocampal slices. J Cereb Blood Flow Metab 18: 168-175, 1998.
16. 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 14: 193-205, 1994.
17. Frerichs KU, Smith CB, Brenner M, DeGracia DJ, Krause GS, Marrone L, Dever TE, Hallenbeck JM. Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc Natl Acad Sci USA 95: 14511-14516, 1998.
18. Galster W, Morrison P. Gluconeogenesis in arctic ground squirrels between periods of hibernation. Am J Physiol 228: 325-330, 1975.
19. Glantzounis GK, Salacinski HJ, Yang W, Davidson BR, Seifalian AM. The contemporary role of antioxidant therapy in attenuating liver ischemia-reperfusion injury: a review. Liver Transpl 11: 1031-1047, 2005.
20. Gonzales S, Polizio AH, Erario MA, Tomaro ML. Glutamine is highly effective in preventing in vivo cobalt-induced oxidative stress in rat liver. World J Gastroenterol 11: 3533-3538, 2005.
21. Gonzalez-Correa JA, De La Cruz JP, Martin-Aurioles E, Lopez-Egea MA, Ortiz P, Sanchez de la Cuesta F. Effects of S-adenosyl-L-methionine on hepatic and renal oxidative stress in an experimental model of acute biliary obstruction in rats. Hepatology 26: 121-127, 1997.
22. Heldmaier G, Ortmann S, Elvert R. Natural hypometabolism during hibernation and daily torpor in mammals. Respir Physiol Neurobiol 141: 317-329, 2004.
23. 1H MRS study of a hibernating mammal. J Neurochem 101: 1505-1515, 2007.
24. Kurtz CC, Carey HV. Seasonal changes in the intestinal immune system of hibernating ground squirrels. Dev Comp Immunol 31: 415-428, 2007.
25. Kurtz CC, Lindell SL, Mangino MJ, Carey HV. Hibernation confers resistance to intestinal ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 291: G895-G901, 2006.
26. Lindell SL, Klahn SL, Piazza TM, Mangino MJ, Torrealba JR, Southard JH, Carey HV. Natural resistance to liver cold ischemia-reperfusion injury associated with the hibernation phenotype. Am J Physiol Gastrointest Liver Physiol 288: G473-G480, 2005.
27. Lyman CP, Willis JS, Malan A, Wang LCH. Hibernation and Torpor in Mammals and Birds. New York: Academic, 1982.
28. Ma YL, Zhu X, Rivera PM, Toien O, Barnes BM, LaManna JC, Smith MA, Drew KL. Absence of cellular stress in brain after hypoxia induced by arousal from hibernation in Arctic ground squirrels. Am J Physiol Regul Integr Comp Physiol 289: R1297-R1306, 2005.
29. Nicholson JK, Lindon JC, Holmes E. "Metabonomics": understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 29: 1181-1189, 1999.
30. Niemann CU, Hirose R, Liu T, Behrends M, Brown JL, Kominsky DF, Roberts JP, Serkova N. Ischemic preconditioning improves energy state and transplantation survival in obese Zucker rat livers. Anesth Analg 101: 1577-1583, 2005.
31. Robinson PM, Roberts MF. Effects of osmolyte precursors on the distribution of compatible solutes in Methanohalophilus portucalensis. Appl Environ Microbiol 63: 4032-4038, 1997.
32. Roderick SL, Chan WW, Agate DS, Olsen LR, Vetting MW, Rajashankar KR, Cohen DE. Structure of human phosphatidylcholine transfer protein in complex with its ligand. Nat Struct Biol 9: 507-511, 2002.
33. Rolfe DFS, Brown GC. Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77: 731-758, 1997.
34. Serkova N, Fuller TF, Klawitter J, Freise CE, Niemann CU. H-NMR-based metabolic signatures of mild and severe ischemia/reperfusion injury in rat kidney transplants. Kidney Int 67: 1142-1151, 2005.
35. Serkova NJ, Jackman M, Brown JL, Liu T, Hirose R, Roberts JP, Maher JJ, Niemann CU. Metabolic profiling of livers and blood from obese Zucker rats. J Hepatol 44: 956-962, 2006.
36. 1H-NMR-based metabolomics. Expert Rev Mol Diagn 6: 717-731, 2006.
37. Shirasawa K, Takabe T, Kishitani S. Accumulation of glycinebetaine in rice plants that overexpress choline monooxygenase from spinach and evaluation of their tolerance to abiotic stress. Ann Bot (Lond) 98: 565-571, 2006.
38. Street TO, Bolen DW, Rose GD. A molecular mechanism for osmolyte-induced protein stability. Proc Natl Acad Sci USA 103: 13997-14002, 2006.
39. 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 281: R572-R583, 2001.
40. Treberg JR, Speers-Roesch B, Piermarini PM, Ip YK, Ballantyne JS, Driedzic WR. The accumulation of methylamine counteracting solutes in elasmobranchs with differing levels of urea: a comparison of marine and freshwater species. J Exp Biol 209: 860-870, 2006.
41. van Breukelen F, Martin SL. Translational initiation is uncoupled from elongation at 18°C during mammalian hibernation. Am J Physiol Regul Integr Comp Physiol 281: R1374-R1379, 2001.
42. van Breukelen F, Sonenberg N, Martin SL. Seasonal and state-dependent changes of eIF4E and 4E-BP1 during mammalian hibernation: implications for the control of translation during torpor. Am J Physiol Regul Integr Comp Physiol 287: R349-R353, 2004.
43. Williams DR, Epperson LE, Li W, Hughes MA, Taylor R, Rogers J, Martin SL, Cossins AR, Gracey AY. Seasonally hibernating phenotype assessed through transcript screening. Physiol Genomics 24: 13-22, 2005.
44. Yan J, Burman A, Nichols C, Alila L, Showe LC, Showe MK, Boyer BB, Barnes BM, Marr TG. The detection of differential gene expression in brown adipose tissue of hibernating arctic ground squirrels with mouse microarrays. Physiol Genomics 25: 346-353, 2006.
45. Zhegunov GF, Mikulinsky YE, Kudokotseva EV. Hyperactivation of protein synthesis in tissues of hibernating animals on arousal. Cryo Lett 9: 236-245, 1988.
46. Zimny ML, Gregory R. High energy phosphates during hibernation and arousal in the ground squirrel. Am J Physiol 195: 233-236, 1958.