1H-NMR metabolomic biomarkers of poor outcome after hemorrhagic shock are absent in hibernators

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Bogren, Lori K ^a   Murphy, Carl J ^a   Johnston, Erin L ^a   Sinha, Neeraj ^b   Serkova, Natalie J ^c,d   Drew, Kelly L ^a  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^b SANJAY GANDHI POSTGRADUATE INSTITUTE OF MEDICAL SCIENCES   (India)

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

^d UNIVERSITY OF COLORADO CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; LIPID;

ANAEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY TEMPERATURE; CONTROLLED STUDY; DISEASE MARKER; FEMALE; GLUCOSE METABOLISM; GLYCOLYSIS; HEMORRHAGIC SHOCK; HIBERNATION; LIPID METABOLISM; MALE; METABOLIC REGULATION; METABOLITE; METABOLOMICS; NONHUMAN; ORGAN INJURY; PROGNOSIS; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; REPERFUSION INJURY; SCIURIDAE; SEASON; SPECIES DIFFERENCE; ANIMAL; BLOOD; METABOLOME; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SHOCK, HEMORRHAGIC; SPRAGUE DAWLEY RAT; TREATMENT OUTCOME;

ANIMALS; BIOMARKERS; HIBERNATION; LIPIDS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLOME; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; SCIURIDAE; SHOCK, HEMORRHAGIC; TREATMENT OUTCOME;

EID: 84960193863     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107493     Document Type: Article

References (71)

1. Scribner DM, Witowski NE, Mulier KE, Lusczek ER, Wasiluk KR, et al. (2010) Liver metabolomic changes identify biochemical pathways in hemorrhagic shock. J Surg Res 164: e131-139.
2. Lee JH, Kim SC, Lee TH, Chung SW, No HW, et al. (2008) Preliminary study on physiological changes of hemorrhagic shock in rats. Conf Proc IEEE Eng Med Biol Soc 2008: 4891-4894.
3. Mongardon N, Dumas F, Ricome S, Grimaldi D, Hissem T, et al. (2011) Postcardiac arrest syndrome: from immediate resuscitation to long-term outcome. Ann Intensive Care 1: 45.
4. Raedschelders K, Ansley DM, Chen DD (2012) The cellular and molecular origin of reactive oxygen species generation during myocardial ischemia and reperfusion. Pharmacol Ther 133: 230-255.
5. Kurtz CC, Lindell SL, Mangino MJ, Carey HV (2006) Hibernation confers resistance to intestinal ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol 291: G895-901.
6. Martin SL, Epperson LE, Rose JC, Kurtz CC, Ane C, et al. (2008) Proteomic analysis of the winter-protected phenotype of hibernating ground squirrel intestine. Am J Physiol Regul Integr Comp Physiol 295: R316-328.
7. Lindell SL, Klahn SL, Piazza TM, Mangino MJ, Torrealba JR, et al. (2005) Natural resistance to liver cold ischemia-reperfusion injury associated with the hibernation phenotype. Am J Physiol Gastrointest Liver Physiol 288: G473- 480.
8. Jani A, Epperson E, Martin J, Pacic A, Ljubanovic D, et al. (2011) Renal protection from prolonged cold ischemia and warm reperfusion in hibernating squirrels. Transplantation 92: 1215-1221.
9. Dave KR, Prado R, Raval AP, Drew KL, Perez-Pinzon MA (2006) The arctic ground squirrel brain is resistant to injury from cardiac arrest during euthermia. Stroke 37: 1261-1265.
10. Dave KR, Anthony Defazio R, Raval AP, Dashkin O, Saul I, et al. (2009) Protein kinase C epsilon activation delays neuronal depolarization during cardiac arrest in the euthermic arctic ground squirrel. J Neurochem 110: 1170-1179.
11. Bogren LKOJ, Carpluk J, Moore JT, Drew KL (2014) Resistance to systemic inflammation and multi organ damage after global ischemia/reperfusion in the arctic ground squirrel. Submitted to PLOS ONE.
12. Epperson LE, Rose JC, Carey HV, Martin SL (2009) Seasonal proteomic changes reveal molecular adaptations to preserve and replenish liver proteins during ground squirrel hibernation. Am J Physiol Regul Integr Comp Physiol.
13. Serkova NJ, Rose JC, Epperson LE, Carey HV, Martin SL (2007) Quantitative analysis of liver metabolites in three stages of the circannual hibernation cycle in 13-lined ground squirrels by NMR. Physiol Genomics 31: 15-24.
14. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83: 1153-1181.
15. Dark J (2005) Annual lipid cycles in hibernators: integration of physiology and behavior. Annu Rev Nutr 25: 469-497.
16. Epperson LE, Karimpour-Fard A, Hunter LE, Martin SL (2011) Metabolic cycles in a circannual hibernator. Physiol Genomics 43: 799-807.
17. Epperson LE, Rose JC, Russell RL, Nikrad MP, Carey HV, et al. (2010) Seasonal protein changes support rapid energy production in hibernator brainstem. J Comp Physiol B 180: 599-617.
18. Williams CT, Goropashnaya AV, Buck CL, Fedorov VB, Kohl F, et al. (2011) Hibernating above the permafrost: effects of ambient temperature and season on expression of metabolic genes in liver and brown adipose tissue of arctic ground squirrels. J Exp Biol 214: 1300-1306.
19. Nelson CJ, Otis JP, Carey HV (2010) Global analysis of circulating metabolites in hibernating ground squirrels. Comp Biochem Physiol Part D Genomics Proteomics 5: 265-273.
20. Jani A, Orlicky DJ, Karimpour-Fard A, Epperson LE, Russell RL, et al. (2012) Kidney proteome changes provide evidence for a dynamic metabolism and regional redistribution of plasma proteins during torpor-arousal cycles of hibernation. Physiol Genomics 44: 717-727.
21. Hindle AG, Karimpour-Fard A, Epperson LE, Hunter LE, Martin SL (2011) Skeletal muscle proteomics: carbohydrate metabolism oscillates with seasonal and torpor-arousal physiology of hibernation. Am J Physiol Regul Integr Comp Physiol 301: R1440-1452.
22. Hampton M, Melvin RG, Kendall AH, Kirkpatrick BR, Peterson N, et al. (2011) Deep sequencing the transcriptome reveals seasonal adaptive mechanisms in a hibernating mammal. PLoS One 6: e27021.
23. Chaffin CL, Vandevoort CA (2013) Follicle growth, ovulation, and luteal formation in primates and rodents: a comparative perspective. Exp Biol Med (Maywood) 238: 539-548.
24. Ostadal B, Netuka I, Maly J, Besik J, Ostadalova I (2009) Gender differences in cardiac ischemic injury and protection-experimental aspects. Exp Biol Med (Maywood) 234: 1011-1019.
25. Barnes BM, Kretzmann M, Zucker I, Licht P (1988) Plasma androgen and gonadotropin levels during hibernation and testicular maturation in goldenmantled ground squirrels. Biol Reprod 38: 616-622.
26. Buck CL, Barnes BM (2003) Androgen in free-living arctic ground squirrels: seasonal changes and influence of staged male-male aggressive encounters. Horm Behav 43: 318-326.
27. Serkova N, Fuller TF, Klawitter J, Freise CE, Niemann CU (2005) H-NMRbased metabolic signatures of mild and severe ischemia/reperfusion injury in rat kidney transplants. Kidney Int 67: 1142-1151.
28. Stringer KA, Serkova NJ, Karnovsky A, Guire K, Paine R, et al. (2011) Metabolic consequences of sepsis-induced acute lung injury revealed by plasma 1H-nuclear magnetic resonance quantitative metabolomics and computational analysis. Am J Physiol Lung Cell Mol Physiol 300: L4-L11.
29. Kriat M, Vion-Dury J, Confort-Gouny S, Favre R, Viout P, et al. (1993) Analysis of plasma lipids by NMR spectroscopy: application to modifications induced by malignant tumors. J Lipid Res 34: 1009-1019.
30. Nicholson JK, Foxall PJ, Spraul M, Farrant RD, Lindon JC (1995) 750 MHz 1H and 1H-13C NMR spectroscopy of human blood plasma. Anal Chem 67: 793-811.
31. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS (2012) MetaboAnalyst 2.0-a comprehensive server for metabolomic data analysis. Nucleic Acids Res 40: W127-133.
32. Xia J, Psychogios N, Young N, Wishart DS (2009) MetaboAnalyst: a web server for metabolomic data analysis and interpretation. Nucleic Acids Res 37: W652- 660.
33. Rohrig R, Wegewitz C, Lendemans S, Petrat F, de Groot H (2014) Superiority of acetate compared with lactate in a rodent model of severe hemorrhagic shock. J Surg Res 186: 338-345.
34. Almac E, Aksu U, Bezemer R, Jong W, Kandil A, et al. (2012) The acute effects of acetate-balanced colloid and crystalloid resuscitation on renal oxygenation in a rat model of hemorrhagic shock. Resuscitation 83: 1166-1172.
35. Umeda K, Takahashi T, Inoue K, Shimizu H, Maeda S, et al. (2009) Prevention of hemorrhagic shock-induced intestinal tissue injury by glutamine via heme oxygenase-1 induction. Shock 31: 40-49.
36. Yang R, Martin-Hawver L, Woodall C, Thomas A, Qureshi N, et al. (2007) Administration of glutamine after hemorrhagic shock restores cellular energy, reduces cell apoptosis and damage, and increases survival. JPEN J Parenter Enteral Nutr 31: 94-100.
37. Mulier KE, Lexcen DR, Luzcek E, Greenberg JJ, Beilman GJ (2012) Treatment with beta-hydroxybutyrate and melatonin is associated with improved survival in a porcine model of hemorrhagic shock. Resuscitation 83: 253-258.
38. Angele MK, Schneider CP, Chaudry IH (2008) Bench-to-bedside review: latest results in hemorrhagic shock. Crit Care 12: 218.
39. Wilson M, Davis DP, Coimbra R (2003) Diagnosis and monitoring of hemorrhagic shock during the initial resuscitation of multiple trauma patients: a review. J Emerg Med 24: 413-422.
40. Cohen MJ, Serkova NJ, Wiener-Kronish J, Pittet JF, Niemann CU (2010) 1H- NMR-based metabolic signatures of clinical outcomes in trauma patients- beyond lactate and base deficit. J Trauma 69: 31-40.
41. Serkova NJ, Standiford TJ, Stringer KA (2011) The emerging field of quantitative blood metabolomics for biomarker discovery in critical illnesses. Am J Respir Crit Care Med 184: 647-655.
42. Niemann CU, Hirose R, Liu T, Behrends M, Brown JL, et al. (2005) Ischemic preconditioning improves energy state and transplantation survival in obese Zucker rat livers. Anesth Analg 101: 1577-1583.
43. Niemann CU, Choi S, Behrends M, Hirose R, Noh J, et al. (2006) Mild hypothermia protects obese rats from fulminant hepatic necrosis induced by ischemia-reperfusion. Surgery 140: 404-412.
44. Serkova NJ, Jackman M, Brown JL, Liu T, Hirose R, et al. (2006) Metabolic profiling of livers and blood from obese Zucker rats. J Hepatol 44: 956-962.
45. Andrews MT (2007) Advances in molecular biology of hibernation in mammals. Bioessays 29: 431-440.
46. Andrews MT, Russeth KP, Drewes LR, Henry PG (2009) Adaptive mechanisms regulate preferred utilization of ketones in the heart and brain of a hibernating mammal during arousal from torpor. Am J Physiol Regul Integr Comp Physiol 296: R383-393.
47. Carey HV, Potter KT, Peters TL, Epperson LE, Rose JC, et al. (2006) Hibernating mammals have enhanced survival and reduced gut damage after hemorrhage. Faseb Journal 20: A1382-A1382.
48. Podgoreanu MV, Qing M, Mackensen BG; Zhang Z, Smith MP, et al. (2011) The Hibernator Phenotype is Cardioprotective in the Setting of Deep Hypothermic Circulatory Arrest. American Heart Association, American Stroke Association. Orlando, FL: Duke University, University of Alaska Fairbanks.
49. Maalouf M, Rho JM, Mattson MP (2009) The neuroprotective properties of calorie restriction, the ketogenic diet, and ketone bodies. Brain Res Rev 59: 293-315.
50. Klein AH, Wendroth SM, Drewes LR, Andrews MT (2010) Small-volume dbeta- hydroxybutyrate solution infusion increases survivability of lethal hemorrhagic shock in rats. Shock 34: 565-572.
51. Tai KK, Nguyen N, Pham L, Truong DD (2008) Ketogenic diet prevents cardiac arrest-induced cerebral ischemic neurodegeneration. J Neural Transm 115: 1011-1017.
52. Al-Zaid NS, Dashti HM, Mathew TC, Juggi JS (2007) Low carbohydrate ketogenic diet enhances cardiac tolerance to global ischaemia. Acta Cardiol 62: 381-389.
53. Engel FL, Winton MG, Long CN (1943) Biochemical Studies on Shock : I. The Metabolism of Amino Acids and Carbohydrate during Hemorrhagic Shock in the Rat. J Exp Med 77: 397-410.
54. Koustova E, Rhee P, Hancock T, Chen H, Inocencio R, et al. (2003) Ketone and pyruvate Ringer's solutions decrease pulmonary apoptosis in a rat model of severe hemorrhagic shock and resuscitation. Surgery 134: 267-274.
55. Hara J, Fujimura M, Myou S, Kita T, Abo M, et al. (2008) Sputum eosinophilia, airway hyperresponsiveness and airway narrowing in young adults with former asthma. Allergol Int 57: 211-217.
56. Geiser F (1988) Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? J Comp Physiol B 158: 25-37.
57. Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66: 239-274.
58. Suzuki M, Kitamura Y, Mori S, Sato K, Dohi S, et al. (2002) Betahydroxybutyrate, a cerebral function improving agent, protects rat brain against ischemic damage caused by permanent and transient focal cerebral ischemia. Jpn J Pharmacol 89: 36-43.
59. Suzuki M, Sato K, Dohi S, Sato T, Matsuura A, et al. (2001) Effect of betahydroxybutyrate, a cerebral function improving agent, on cerebral hypoxia, anoxia and ischemia in mice and rats. Jpn J Pharmacol 87: 143-150.
60. Epperson LE, Rose JC, Carey HV, Martin SL (2010) Seasonal proteomic changes reveal molecular adaptations to preserve and replenish liver proteins during ground squirrel hibernation. Am J Physiol Regul Integr Comp Physiol 298: R329-340.
61. Park Y, Hirose R, Coatney JL, Ferrell L, Behrends M, et al. (2007) Ischemiareperfusion injury is more severe in older versus young rat livers. J Surg Res 137: 96-102.
62. Waters NJ, Waterfield CJ, Farrant RD, Holmes E, Nicholson JK (2005) Metabonomic deconvolution of embedded toxicity: application to thioacetamide hepato- and nephrotoxicity. Chem Res Toxicol 18: 639-654.
63. McNelis J, Marini CP, Jurkiewicz A, Szomstein S, Simms HH, et al. (2001) Prolonged lactate clearance is associated with increased mortality in the surgical intensive care unit. Am J Surg 182: 481-485.
64. Frerichs KU, Hallenbeck JM (1998) 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.
65. Christian SL, Ross AP, Zhao HW, Kristenson HJ, Zhan X, et al. (2008) Arctic ground squirrel (Spermophilus parryii) hippocampal neurons tolerate prolonged oxygen-glucose deprivation and maintain baseline ERK1/2 and JNK activation despite drastic ATP loss. J Cereb Blood Flow Metab 28: 1307-1319.
66. Storey KB (2010) Out cold: biochemical regulation of mammalian hibernation - a mini-review. Gerontology 56: 220-230.
67. Frerichs KU, Kennedy C, Sokoloff L, Hallenbeck JM (1994) Local cerebral blood flow during hibernation, a model of natural tolerance to ''cerebral ischemia''. J Cereb Blood Flow Metab 14: 193-205.
68. Dave KR, Christian SL, Perez-Pinzon MA, Drew KL (2012) Neuroprotection: lessons from hibernators. Comp Biochem Physiol B Biochem Mol Biol 162: 1-9.
69. Barnes BM (1989) Freeze avoidance in a mammal: body temperatures below 0 degree C in an Arctic hibernator. Science 244: 1593-1595.
70. Serkova NJ, Brown MS (2012) Quantitative analysis in magnetic resonance spectroscopy: from metabolic profiling to in vivo biomarkers. Bioanalysis 4: 321-341.
71. Barton RH, Waterman D, Bonner FW, Holmes E, Clarke R, et al. (2010) The influence of EDTA and citrate anticoagulant addition to human plasma on information recovery from NMR-based metabolic profiling studies. Mol Biosyst 6: 215-224.