Glutamine metabolism drives succinate accumulation in plasma and the lung during hemorrhagic shock

Journal of Trauma and Acute Care Surgery

Volumn 81, Issue 6, 2016, Pages 1012-1019

  Slaughter, Anne L ^a   D'Alessandro, Angelo ^b   Moore, Ernest E ^a,c   Banerjee, Anirban ^a   Silliman, Christopher C ^a,d,e   Hansen, Kirk C ^b   Reisz, Julie A ^b   Fragoso, Miguel ^a,c   Wither, Matthew J ^b   Bacon, Anthony W ^a   Moore, Hunter B ^a   Peltz, Erik D ^a  

^a UNIVERSITY OF COLORADO   (United States)

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

^c DENVER HEALTH MEDICAL CENTER   (United States)

^d Nutrition Obesity Research Center at the University of Colorado   (United States)

^e Bonfils Blood Center   (United States)

Author keywords

Glutaminolysis; mass spectrometry; metabolomics; metabolopathy; Sprague Dawley rats

Indexed keywords

ADENOSINE TRIPHOSPHATE; GLUTAMINE; GLUTAMINE C 13; GLUTAMINE N 15; RADIOISOTOPE; SUCCINIC ACID; UNCLASSIFIED DRUG;

ANAEROBIC METABOLISM; ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ARTICLE; BLOOD SAMPLING; BRAIN TISSUE; CELL SURVIVAL; CONTROLLED STUDY; HEART; HEMORRHAGIC SHOCK; ISOTOPE LABELING; LUNG PARENCHYMA; MASS SPECTROMETRY; METABOLOMICS; NONHUMAN; PLASMA; PRIORITY JOURNAL; RAT; SPRAGUE DAWLEY RAT; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ANIMAL; BRAIN; CARDIAC MUSCLE; DISEASE MODEL; LIVER; LUNG; METABOLISM;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; GLUTAMINE; LIVER; LUNG; MYOCARDIUM; RATS; RATS, SPRAGUE-DAWLEY; SHOCK, HEMORRHAGIC; SUCCINIC ACID;

EID: 84986224433     PISSN: 21630755     EISSN: 21630763     Source Type: Journal    
DOI: 10.1097/TA.0000000000001256     Document Type: Article

References (39)

1. Moore FA, Moore EE. Evolving concepts in the pathogenesis of postinjury multiple organ failure. Surg Clin North Am. 1995;75(2):257-277.
2. Moore FA, Haenel JB, Moore EE, Whitehill TA. Incommensurate oxygen consumption in response to maximal oxygen availability predicts postinjury multiple organ failure. J Trauma. 1992;33(1):58-65; discussion 65-67.
3. Lenz A, Franklin GA, Cheadle WG. Systemic inflammation after trauma. Injury. 2007;38(12):1336-1345.
4. Moore FA, McKinley BA, Moore EE, Nathens AB, West M, Shapiro MB, Bankey P, Freeman B, Harbrecht BG, Johnson JL, et al. Inflammation and the host response to injury, a large-scale collaborative project: patientoriented research core-standard operating procedures for clinical care. III. Guidelines for shock resuscitation. J Trauma. 2006;61(1):82-89.
5. Desborough JP. The stress response to trauma and surgery. Br J Anaesth. 2000;85(1):109-117.
6. Weekers F, Giulietti AP, Michalaki M, Coopmans W, van Herck E, Mathieu C, van den Berghe G. Metabolic, endocrine, and immune effects of stress hyperglycemia in a rabbit model of prolonged critical illness. Endocrinology. 2003;144(12):5329-5338.
7. Sauaia A, Moore EE, Johnson JL, Chin TL, Banerjee A, Sperry JL, Maier RV, Burlew CC. Temporal trends of postinjurymultiple-organ failure: still resource intensive, morbid, and lethal. J Trauma Acute Care Surg. 2014;76(3): 582-592, discussion 592-593.
8. Chouchani ET, Pell VR, Gaude E, Aksentijevic D, Sundier SY, Robb EL, Logan A, Nadtochiy SM, Ord EN, Smith AC, et al. Ischaemic accumulation of succinate controls reperfusion injury throughmitochondrial ROS. Nature. 2014;515(7527):431-435.
9. Chinopoulos C. Which way does the citric acid cycle turn during hypoxia?. The critical role of a-ketoglutarate dehydrogenase complex. J Neurosci Res. 2013;91(8):1030-1043.
10. Kaplan LJ, Cheung NH, Maerz L, Lui F, Schuster K, Luckianow G, Davis K. A physicochemical approach to acid-base balance in critically ill trauma patients minimizes errors and reduces inappropriate plasma volume expansion. J Trauma. 2009;66(4):1045-1051.
11. Kaplan LJ, Kellum JA. Initial pH, base deficit, lactate, anion gap, strong ion difference, and strong ion gap predict outcome from major vascular injury. Crit Care Med. 2004;32(5):1120-1124.
12. Kaplan LJ, Kellum JA. Comparison of acid-base models for prediction of hospital mortality after trauma. Shock. 2008;29(6):662-666.
13. Martin M, Murray J, Berne T, Demetriades D, Belzberg H. Diagnosis of acidbase derangements andmortality prediction in the trauma intensive care unit: the physiochemical approach. J Trauma. 2005;58(2):238-243.
14. Sen S, Wiktor A, Berndtson A, Greenhalgh D, Palmieri T. Strong ion gap is associated with mortality in pediatric burn injuries. J Burn Care Res. 2014; 35(4):337-341.
15. D?Alessandro A, Moore HB, Moore EE, Wither M, Nemkov T, Gonzalez E, Slaughter A, Fragoso M, Hansen KC, Silliman CC, Banerjee A. Early hemorrhage triggers metabolic responses that build up during prolonged shock. Am J Physiol Regul Integr Comp Physiol. 2015;8(12):R1034-R1044.
16. Peltz ED, D?Alessandro A, Moore EE, Chin T, Silliman CC, Sauaia A, Hansen KC, Banerjee A. Pathologic metabolism: an exploratory study of the plasma metabolome of critical injury. J Trauma Acute Care Surg. 2015;78(4):742-751.
17. D?Alessandro A, Slaughter AL, Peltz ED, Moore EE, Silliman CC, Wither M, Nemkov T, Bacon AW, Fragoso M, Banerjee A, Hansen KC. Trauma/ hemorrhagic shock instigates aberrant metabolic flux through glycolytic pathways, as revealed by preliminary (13)C-glucose labeling metabolomics. J Transl Med. 2015;13:253.
18. Aguiar CJ, Rocha-Franco JA, Sousa PA, Santos AK, Ladeira M, Rocha-Resende C, Ladeira LO, Resende RR, Botoni FA, Barrouin Melo M, et al. Succinate causes pathological cardiomyocyte hypertrophy through GPR91 activation. Cell Commun Signal. 2014;12:78.
19. de Castro Fonseca M, Aguiar CJ, da Rocha Franco JA, Gingold RN, Leite MF. GPR91: expanding the frontiers of Krebs cycle intermediates. Cell Commun Signal. 2016;14:3.
20. Ariza AC, Deen PM, Robben JH. The succinate receptor as a novel therapeutic target for oxidative and metabolic stress-related conditions. Front Endocrinol (Lausanne). 2012;3:22.
21. Tannahill GM, Curtis AM, Adamik J, Palsson-McDermott EM, McGettrick AF, Goel G, Frezza C, Bernard NJ, Kelly B, Foley NH, et al. Succinate is an inflammatory signal that induces IL-1b through HIF-1a. Nature. 2013; 496(7444):238-242.
22. Högberg C, Gidlöf O, Tan C, Svensson S, Nilsson-Öhman J, Erlinge D, Olde B. Succinate independently stimulates full platelet activation via cAMP and phosphoinositide 3-kinase-b signaling. J Thromb Haemost. 2011;9(2):361-372.
23. Lukyanova LD, Kirova YI. Mitochondria-controlled signaling mechanisms of brain protection in hypoxia. Front Neurosci. 2015;9:320.
24. D?Alessandro A, Nemkov T, Hansen KC, Szczepiorkowski ZM, Dumont LJ. Red blood cell storage in additive solution-7 preserves energy and redox metabolism: a metabolomics approach. Transfusion. 2015;55(12):2955-2966.
25. Clasquin MF, Melamud E, Rabinowitz JD. LC-MS data processing with MAVEN: a metabolomic analysis and visualization engine. In: Baxevanis AD, et al., ed. Current Protocols in Bioinformatics. 2012;Chapter 14:Unit14, 1.
26. D?Alessandro A, Amelio I, Berkers CR, Antonov A, Vousden KH, Melino G, Zolla L. Metabolic effect of TAp63a: enhanced glycolysis and pentose phosphate pathway, resulting in increased antioxidant defense. Oncotarget. 2014;5(17):7722-7733.
27. Moore EE, Moore FA, Franciose RJ, Kim FJ, Biffl WL, Banerjee A. The postischemic gut serves as a priming bed for circulating neutrophils that provoke multiple organ failure. J Trauma. 1994;37(6):881-887.
28. Stringham JR, Moore EE, Gamboni F, Harr JN, Fragoso M, Chin TL, Carr CE, Silliman CC, Banerjee A. Mesenteric lymph diversion abrogates 5-lipoxygenase activation in the kidney following trauma and hemorrhagic shock. J Trauma Acute Care Surg. 2014;76(5):1214-1221.
29. Rutherford EJ, Morris JA Jr, Reed GW, Hall KS. Base deficit stratifies mortality and determines therapy. J Trauma. 1992;33(3):417-423.
30. Cohen MJ, Serkova NJ, Wiener-Kronish J, Pittet JF, Niemann CU. 1H-NMRbased metabolic signatures of clinical outcomes in trauma patients-beyond lactate and base deficit. J Trauma. 2010;69(1):31-40.
31. Krebs HA. The citric acid cycle: a reply to the criticisms of F. L. Breusch and of J. Thomas. Biochem J. 1940;34(3):460-463.
32. Chouchani ET, Pell VR, James AM, Work LM, Saeb-Parsy K, Frezza C, Krieg T, Murphy MP. A unifying mechanism for mitochondrial superoxide production during ischemia-reperfusion injury. Cell Metab. 2016;23(2): 254-263.
33. Moore EE, Moore FA, Harken AH, Johnson JL, Ciesla D, Banerjee A. The two-event construct of postinjury multiple organ failure. Shock. 2005; 24(Suppl 1):71-74.
34. Yi J, Slaughter A, Kotter CV, Moore EE, Hauser CJ, Itagaki K, Wohlauer M, Frank DN, Silliman C, Banerjee A, Peltz E. A " clean case " of systemic injury: mesenteric lymph after hemorrhagic shock elicits a sterile inflammatory response. Shock. 2015;44(4):336-340.
35. Garcia-Morales LJ, Chen NY, Weng T, Luo F, Davies J, Philip K, Volcik KA, Melicoff E, Amione-Guerra J, Bunge RR, et al. Altered hypoxicadenosine axis and metabolism in Group III pulmonary hypertension. Am J Respir Cell Mol Biol. 2016;54(4):574-583.
36. Yang L, Yu D, Fan HH, Feng Y, Hu L, Zhang WY, Zhou K, Mo XM. Triggering the succinate receptor GPR91 enhances pressure overload-induced right ventricular hypertrophy. Int J Clin Exp Pathol. 2014;7(9): 5415-5428.
37. van der Worp HB, Howells DW, Sena ES, Porritt MJ, Rewell S, O?Collins V, Macleod MR. Can animal models of disease reliably inform human studies?. PLoS Med. 2010;7(3):e1000245.
38. Perel P, Roberts I, Sena E, Wheble P, Briscoe C, Sandercock P, Macleod M, Mignini LE, Jayaram P, Khan KS. Comparison of treatment effects between animal experiments and clinical trials: systematic review. BMJ. 2007; 334(7586):197.
39. Tompkins RG. Genomics of injury: the Glue Grant experience. J Trauma Acute Care Surg. 2015;78(4):671-686.