Increased platelet mitochondrial respiration after cardiac arrest and resuscitation as a potential peripheral biosignature of cerebral bioenergetic dysfunction

Journal of Bioenergetics and Biomembranes

Volumn 48, Issue 3, 2016, Pages 269-279

  Ferguson, Michael A ^a   Sutton, Robert M ^a   Karlsson, Michael ^b   Sjövall, Fredrik ^b   Becker, Lance B ^c   Berg, Robert A ^a   Margulies, Susan S ^d   Kilbaugh, Todd J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b LUND UNIVERSITY   (Sweden)

^c HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Biomarker; Brain injury; Cardiac arrest; Innate immune response; Mitochondria; Platelets

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASPHYXIA; BIOENERGY; BRAIN CORTEX; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; ELECTRON TRANSPORT; HEART ARREST; HEART VENTRICLE FIBRILLATION; HIPPOCAMPUS; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; RESUSCITATION; RETURN OF SPONTANEOUS CIRCULATION; SYSTOLIC BLOOD PRESSURE; THROMBOCYTE; ADOLESCENT; ANIMAL; BLOOD; BRAIN DISEASE; CELL RESPIRATION; CHILD; DISEASE MODEL; ENERGY METABOLISM; HUMAN; METABOLISM; MITOCHONDRION; OXYGEN CONSUMPTION; PATHOLOGY; PATHOPHYSIOLOGY; PIG; PRESCHOOL CHILD; ULTRASTRUCTURE;

ADOLESCENT; ANIMALS; BLOOD PLATELETS; BRAIN DISEASES; CELL RESPIRATION; CHILD; CHILD, PRESCHOOL; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; HEART ARREST; HUMANS; MITOCHONDRIA; OXYGEN CONSUMPTION; RESUSCITATION; SWINE;

EID: 84961589383     PISSN: 0145479X     EISSN: 15736881     Source Type: Journal    
DOI: 10.1007/s10863-016-9657-9     Document Type: Article

References (64)

1. Adrie C, Laurent I, Monchi M, Cariou A, Dhainaou JF, Spaulding C (2004) Postresuscitation disease after cardiac arrest: a sepsis-like syndrome? Curr Opin Crit Care 10:208–212
2. Anabel AS, Eduardo PC, Pedro Antonio HC, Carlos SM, Juana NM, Honorio TA, Nicolas VS, Sergio Roberto AR (2014) Human platelets express toll-like receptor 3 and respond to poly I:C. Hum Immunol 75:1244–1251. doi:10.1016/j.humimm.2014.09.013
3. Andersen JN, Sathyanarayanan S, Di Bacco A, Chi A, Zhang T, Chen AH, Dolinski B, Kraus M, Roberts B, Arthur W, Klinghoffer RA, Gargano D, Li L, Feldman I, Lynch B, Rush J, Hendrickson RC, Blume-Jensen P, Paweletz CP (2010) Pathway-based identification of biomarkers for targeted therapeutics: personalized oncology with PI3K pathway inhibitors. Sci Transl Med 2:43ra55. doi:10.1126/scitranslmed.3001065
4. Armstead WM (2005) Age and cerebral circulation. Pathophysiology 12:5–15. doi:10.1016/j.pathophys.2005.01.002
5. Biasucci LM, Liuzzo G (2015) Between death and Hope after Out-Of-Hospital cardiac arrest: should We rely on biomarkers? J Am Coll Cardiol 65:2115–2117. doi:10.1016/j.jacc.2015.03.554
6. Bruserud O (2013) Bidirectional crosstalk between platelets and monocytes initiated by toll-like receptor: an important step in the early defense against fungal infections? Platelets 24:85–97. doi:10.3109/09537104.2012.678426
7. Carre JE, Orban JC, Re L, Felsmann K, Iffert W, Bauer M, Suliman HB, Piantadosi CA, Mayhew TM, Breen P, Stotz M, Singer M (2010) Survival in critical illness is associated with early activation of mitochondrial biogenesis. Am J Respir Crit Care Med 182:745–751. doi:10.1164/rccm.201003-0326OC
8. Castellheim A, Brekke OL, Espevik T, Harboe M, Mollnes TE (2009) Innate immune responses to danger signals in systemic inflammatory response syndrome and sepsis. Scand J Immunol 69:479–491. doi:10.1111/j.1365-3083.2009.02255.x
9. Chan JK, Roth J, Oppenheim JJ, Tracey KJ, Vogl T, Feldmann M, Horwood N, Nanchahal J (2012) Alarmins: awaiting a clinical response. J Clin Invest 122:2711–2719. doi:10.1172/JCI62423
10. Cherry AD, Piantadosi CA (2015) Regulation of mitochondrial biogenesis and its intersection with inflammatory responses. Antioxid Redox Signal 22:965–976. doi:10.1089/ars.2014.6200
11. Chouchani ET, Methner C, Nadtochiy SM, Logan A, Pell VR, Ding S, James AM, Cocheme HM, Reinhold J, Lilley KS, Partridge L, Fearnley IM, Robinson AJ, Hartley RC, Smith RA, Krieg T, Brookes PS, Murphy MP (2013) Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I. Nat Med 19:753–759. doi:10.1038/nm.3212
12. Chouchani ET, Pell VR, Gaude E, Aksentijevic D, Sundier SY, Robb EL, Logan A, Nadtochiy SM, Ord EN, Smith AC, Eyassu F, Shirley R, Hu CH, Dare AJ, James AM, Rogatti S, Hartley RC, Eaton S, Costa AS, Brookes PS, Davidson SM, Duchen MR, Saeb-Parsy K, Shattock MJ, Robinson AJ, Work LM, Frezza C, Krieg T, Murphy MP (2014) Ischaemic accumulation of succinate controls reperfusion injury through mitochondrial ROS. Nature 515:431–435. doi:10.1038/nature13909
13. de Lucas RD, Caputo F, Mendes de Souza K, Sigwalt AR, Ghisoni K, Lock Silveira PC, Remor AP, da Luz SD, Guglielmo LG, Latini A (2014) Increased platelet oxidative metabolism, blood oxidative stress and neopterin levels after Ultra-endurance exercise. J Sports Sci 32:22–30. doi:10.1080/02640414.2013.797098
14. de Paula Martins R, Glaser V, da Luz Scheffer D, de Paula Ferreira PM, Wannmacher CM, Farina M, de Oliveira PA, Prediger RD, Latini A (2013) Platelet oxygen consumption as a peripheral blood marker of brain energetics in a mouse model of severe neurotoxicity. J Bioenerg Biomembr 45:449–457. doi:10.1007/s10863-013-9499-7
15. Duhaime AC (2006) Large animal models of traumatic injury to the immature brain. Dev Neurosci 28:380–387. doi:10.1159/000094164
16. Durham TB, Blanco MJ (2015) Target engagement in lead generation. Bioorg Med Chem Lett 25:998–1008. doi:10.1016/j.bmcl.2014.12.076
17. Fink EL, Berger RP, Clark RS, Watson RS, Angus DC, Richichi R, Panigrahy A, Callaway CW, Bell MJ, Kochanek PM (2014) Serum biomarkers of brain injury to classify outcome after pediatric cardiac arrest*. Crit Care Med 42:664–674. doi:10.1097/01.ccm.0000435668.53188.80
18. Fuentes E, Rojas A, Palomo I (2014) Role of multiligand/RAGE axis in platelet activation. Thromb Res 133:308–314. doi:10.1016/j.thromres.2013.11.007
19. Genova ML, Lenaz G (2014) Functional role of mitochondrial respiratory supercomplexes. Biochim Biophys Acta 1837:427–443. doi:10.1016/j.bbabio.2013.11.002
20. Girotra S, Spertus JA, Li Y, Berg RA, Nadkarni VM, Chan PS, American Heart Association get with the guidelines-resuscitation I (2013) Survival trends in pediatric in-hospital cardiac arrests: an analysis from Get with the Guidelines-Resuscitation. Circ Cardiovasc Qual Outcomes 6:42–49. doi:10.1161/CIRCOUTCOMES.112.967968
21. Goldberger ZD, Chan PS, Berg RA, Kronick SL, Cooke CR, Lu M, Banerjee M, Hayward RA, Krumholz HM, Nallamothu BK, American Heart Association Get With The Guidelines-Resuscitation I (2012) Duration of resuscitation efforts and survival after in-hospital cardiac arrest: an observational study. Lancet 380:1473–1481. doi:10.1016/S0140-6736(12)60862-9
22. Grundler K, Angstwurm M, Hilge R, Baumann P, Annecke T, Crispin A, Sohn HY, Massberg S, Kraemer BF (2014) Platelet mitochondrial membrane depolarization reflects disease severity in patients with sepsis and correlates with clinical outcome. Crit Care 18:R31. doi:10.1186/cc13724
23. Han F, Da T, Riobo NA, Becker LB (2008) Early mitochondrial dysfunction in electron transfer activity and reactive oxygen species generation after cardiac arrest. Critical Care Medicine 36:S447–S453
24. Harker LA, Roskos LK, Marzec UM, Carter RA, Cherry JK, Sundell B, Cheung EN, Terry D, Sheridan W (2000) Effects of megakaryocyte growth and development factor on platelet production, platelet life span, and platelet function in healthy human volunteers. Blood 95:2514–2522
25. Hopper RK, Carroll S, Aponte AM, Johnson DT, French S, Shen RF, Witzmann FA, Harris RA, Balaban RS (2006) Mitochondrial matrix phosphoproteome: effect of extra mitochondrial calcium. Biochemistry 45:2524–2536. doi:10.1021/bi052475e
26. Hsu CH, Li J, Cinousis MJ, Sheak KR, Gaieski DF, Abella BS, Leary M (2014) Cerebral performance category at hospital discharge predicts long-term survival of cardiac arrest survivors receiving targeted temperature management*. Crit Care Med 42:2575–2581. doi:10.1097/CCM.0000000000000547
27. Huttemann M, Lee I, Samavati L, Yu H, Doan JW (2007) Regulation of mitochondrial oxidative phosphorylation through cell signaling. Biochim Biophys Acta 1773:1701–1720
28. Huttemann M, Lee I, Pecinova A, Pecina P, Przyklenk K, Doan JW (2008) Regulation of oxidative phosphorylation, the mitochondrial membrane potential, and their role in human disease. J Bioenerg Biomembr 40:445–456. doi:10.1007/s10863-008-9169-3
29. Japiassu AM, Santiago AP, d’Avila JC, Garcia-Souza LF, Galina A, Castro Faria-Neto HC, Bozza FA, Oliveira MF (2011) Bioenergetic failure of human peripheral blood monocytes in patients with septic shock is mediated by reduced F1Fo adenosine-5′-triphosphate synthase activity. Crit Care Med 39:1056–1063. doi:10.1097/CCM.0b013e31820eda5c
30. Jeger V, Djafarzadeh S, Jakob SM, Takala J (2013) Mitochondrial function in sepsis. Eur J Clin Invest 43:532–542. doi:10.1111/eci.12069
31. Kalvegren H, Skoglund C, Helldahl C, Lerm M, Grenegard M, Bengtsson T (2010) Toll-like receptor 2 stimulation of platelets is mediated by purinergic P2X1-dependent Ca2+ mobilisation, cyclooxygenase and purinergic P2Y1 and P2Y12 receptor activation. Thromb Haemost 103:398–407. doi:10.1160/TH09-07-0442
32. Kilbaugh TJ, Karlsson M, Byro M, Bebee A, Ralston J, Sullivan S, Duhaime AC, Hansson MJ, Elmer E, Margulies SS (2015a) Mitochondrial bioenergetic alterations after focal traumatic brain injury in the immature brain. Exp Neurol 271:136–144. doi:10.1016/j.expneurol.2015.05.009
33. Kilbaugh TJ, Sutton RM, Karlsson M, Hansson MJ, Naim MY, Morgan RW, Bratinov G, Lampe JW, Nadkarni VM, Becker LB, Margulies SS, Berg RA (2015b) Persistently Altered Brain Mitochondrial Bioenergetics after apparently Successful Resuscitation from Cardiac Arrest. J Am Heart Assoc 4:–e002232. doi:10.1161/JAHA.115.002232
34. Krysko DV, Agostinis P, Krysko O, Garg AD, Bachert C, Lambrecht BN, Vandenabeele P (2011) Emerging role of damage-associated molecular patterns derived from mitochondria in inflammation. Trends Immunol 32:157–164. doi:10.1016/j.it.2011.01.005
35. Kurtz P, Claassen J, Schmidt JM, Helbok R, Hanafy KA, Presciutti M, Lantigua H, Connolly ES, Lee K, Badjatia N, Mayer SA (2013) Reduced brain/serum glucose ratios predict cerebral metabolic distress and mortality after severe brain Injury. Neurocrit Care 19:311–319. doi:10.1007/s12028-013-9919-x
36. Lin CS, Sharpley MS, Fan W, Waymire KG, Sadun AA, Carelli V, Ross-Cisneros FN, Baciu P, Sung E, McManus MJ, Pan BX, Gil DW, Macgregor GR, Wallace DC (2012) Mouse mtDNA mutant model of Leber hereditary optic neuropathy. Proc Natl Acad Sci U S A 109:20065–20070. doi:10.1073/pnas.1217113109
37. Maugeri N, Campana L, Gavina M, Covino C, De Metrio M, Panciroli C, Maiuri L, Maseri A, D’Angelo A, Bianchi ME, Rovere-Querini P, Manfredi AA (2014) Activated platelets present high mobility group box 1 to neutrophils, inducing autophagy and promoting the extrusion of neutrophil extracellular traps. J Thromb Haemost 12:2074–2088. doi:10.1111/jth.12710
38. Mayr VD, Dunser MW, Greil V, Jochberger S, Luckner G, Ulmer H, Friesenecker BE, Takala J, Hasibeder WR (2006) Causes of death and determinants of outcome in critically ill patients. Crit Care 10:R154. doi:10.1186/cc5086
39. McKenna MC (2011) Glutamate dehydrogenase in brain mitochondria: do lipid modifications and transient metabolon formation influence enzyme activity? Neurochem Int 59:525–533. doi:10.1016/j.neuint.2011.07.003
40. Meaney PA, Nadkarni VM, Kern KB, Indik JH, Halperin HR, Berg RA (2010) Rhythms and outcomes of adult in-hospital cardiac arrest. Crit Care Med 38:101–108. doi:10.1097/CCM.0b013e3181b43282
41. Merchant RM, Yang L, Becker LB, Berg RA, Nadkarni V, Nichol G, Carr BG, Mitra N, Bradley SM, Abella BS, Groeneveld PW, American Heart Association get with the guidelines-resuscitation I (2011) Incidence of treated cardiac arrest in hospitalized patients in the United States. Crit Care Med 39:2401–2406. doi:10.1097/CCM.0b013e3182257459
42. Missios S, Harris BT, Dodge CP, Simoni MK, Costine BA, Lee YL, Quebada PB, Hillier SC, Adams LB, Duhaime AC (2009) Scaled cortical impact in immature swine: effect of age and gender on lesion volume. J Neurotrauma 26:1943–1951. doi:10.1089/neu.2009-0956
43. Neumar RW, Nolan JP, Adrie C, Aibiki M, Berg RA, Bottiger BW, Callaway C, Clark RS, Geocadin RG, Jauch EC, Kern KB, Laurent I, Longstreth WT Jr, Merchant RM, Morley P, Morrison LJ, Nadkarni V, Peberdy MA, Rivers EP, Rodriguez-Nunez A, Sellke FW, Spaulding C, Sunde K, Vanden Hoek T (2008) Post-cardiac arrest syndrome: epidemiology, pathophysiology, treatment, and prognostication. A consensus statement from the International Liaison Committee on Resuscitation (American Heart Association, Australian and New Zealand Council on Resuscitation, European Resuscitation Council, Heart and Stroke Foundation of Canada, InterAmerican Heart Foundation, Resuscitation Council of Asia, and the Resuscitation Council of Southern Africa); the American Heart Association Emergency Cardiovascular Care Committee; the Council on Cardiovascular Surgery and Anesthesia; the Council on Cardiopulmonary, Perioperative, and Critical Care; the Council on Clinical Cardiology; and the Stroke Council. Circulation 118:2452–2483. doi:10.1161/CIRCULATIONAHA.108.190652
44. Neurauter A, Nysaether J, Kramer-Johansen J, Eilevstjonn J, Paal P, Myklebust H, Wenzel V, Lindner KH, Schmolz W, Pytte M, Steen PA, Strohmenger HU (2009) Comparison of mechanical characteristics of the human and porcine chest during cardiopulmonary resuscitation. Resuscitation 80:463–469. doi:10.1016/j.resuscitation.2008.12.014
45. O’Neill LA (2014) Biochemistry: succinate strikes. Nature 515:350–351. doi:10.1038/nature13941
46. Park JS, Gamboni-Robertson F, He Q, Svetkauskaite D, Kim JY, Strassheim D, Sohn JW, Yamada S, Maruyama I, Banerjee A, Ishizaka A, Abraham E (2006) High mobility group box 1 protein interacts with multiple toll-like receptors. Am J Physiol Cell Physiol 290:C917–C924. doi:10.1152/ajpcell.00401.2005
47. Paweletz CP, Andersen JN, Pollock R, Nagashima K, Hayashi ML, Yu SU, Guo H, Bobkova EV, Xu Z, Northrup A, Blume-Jensen P, Hendrickson RC, Chi A (2011) Identification of direct target engagement biomarkers for kinase-targeted therapeutics. PLoS One 6:e26459. doi:10.1371/journal.pone.0026459
48. Pesta D, Gnaiger E (2012) High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle. Methods Mol Biol 810:25–58. doi:10.1007/978-1-61779-382-0_3
49. Ramzan R, Staniek K, Kadenbach B, Vogt S (2010) Mitochondrial respiration and membrane potential are regulated by the allosteric ATP-inhibition of cytochrome c oxidase. Biochim Biophys Acta 1797:1672–1680. doi:10.1016/j.bbabio.2010.06.005
50. Robertson CL, Soane L, Siegel ZT, Fiskum G (2006) The potential role of mitochondria in pediatric traumatic brain Injury. Dev Neurosci 28:432–446. doi:10.1159/000094169
51. Rouhiainen A, Imai S, Rauvala H, Parkkinen J (2000) Occurrence of amphoterin (HMG1) as an endogenous protein of human platelets that is exported to the cell surface upon platelet activation. Thromb Haemost 84:1087–1094
52. Santilli F, Vazzana N, Iodice P, Lattanzio S, Liani R, Bellomo RG, Lessiani G, Perego F, Saggini R, Davi G (2013) Effects of high-amount-high-intensity exercise on in vivo platelet activation: modulation by lipid peroxidation and AGE/RAGE axis. Thromb Haemost 110:1232–1240. doi:10.1160/TH13-04-0295
53. Scolletta S, Donadello K, Santonocito C, Franchi F, Taccone FS (2012) Biomarkers as predictors of outcome after cardiac arrest. Expert Rev Clin Pharmacol 5:687–699. doi:10.1586/ecp.12.64
54. Shiraki R, Inoue N, Kawasaki S, Takei A, Kadotani M, Ohnishi Y, Ejiri J, Kobayashi S, Hirata K, Kawashima S, Yokoyama M (2004) Expression of Toll-like receptors on human platelets. Thromb Res 113:379–385. doi:10.1016/j.thromres.2004.03.023
55. Sjovall F, Morota S, Hansson MJ, Friberg H, Gnaiger E, Elmer E (2010) Temporal increase of platelet mitochondrial respiration is negatively associated with clinical outcome in patients with sepsis. Crit Care 14:R214. doi:10.1186/cc9337
56. Sjovall F, Ehinger JK, Marelsson SE, Morota S, Frostner EA, Uchino H, Lundgren J, Arnbjornsson E, Hansson MJ, Fellman V, Elmer E (2013a) Mitochondrial respiration in human viable platelets–methodology and influence of gender, age and storage. Mitochondrion 13:7–14. doi:10.1016/j.mito.2012.11.001
57. Sjovall F, Morota S, Persson J, Hansson MJ, Elmer E (2013b) Patients with sepsis exhibit increased mitochondrial respiratory capacity in peripheral blood immune cells. Crit Care 17:R152. doi:10.1186/cc12831
58. Soustiel JF, Larisch S (2010) Mitochondrial damage: a target for new therapeutic horizons. Neurotherapeutics 7:13–21. doi:10.1016/j.nurt.2009.11.001
59. Sutton RM, Friess SH, Naim MY, Lampe JW, Bratinov G, Weiland TR 3rd, Garuccio M, Nadkarni VM, Becker LB, Berg RA (2014) Patient-centric blood pressure-targeted cardiopulmonary resuscitation improves survival from cardiac arrest. Am J Respir Crit Care Med 190:1255–1262. doi:10.1164/rccm.201407-1343OC
60. Tasker RC (2009) Validating serologic biomarkers of brain injury for cardiac arrest research. Pediatr Crit Care Med 10:529–530. doi:10.1097/PCC.0b013e3181a0e102
61. Weiss SL, Haymond S, Ralay Ranaivo H, Wang D, De Jesus VR, Chace DH, Wainwright MS (2012) Evaluation of asymmetric dimethylarginine, arginine, and carnitine metabolism in pediatric sepsis. Pediatr Crit Care Med 13:e210–e218. doi:10.1097/PCC.0b013e318238b5cd
62. Yamakawa K, Ogura H, Koh T, Ogawa Y, Matsumoto N, Kuwagata Y, Shimazu T (2013) Platelet mitochondrial membrane potential correlates with severity in patients with systemic inflammatory response syndrome. J Trauma Acute Care Surg 74:411–417 discussion 418. doi:10.1097/TA.0b013e31827a34cf
63. Zhang Q, Itagaki K, Hauser CJ (2010) Mitochondrial DNA is released by shock and activates neutrophils via p38 map kinase. Shock 34:55–59. doi:10.1097/SHK.0b013e3181cd8c08
64. Zharikov S, Shiva S (2013) Platelet mitochondrial function: from regulation of thrombosis to biomarker of disease. Biochem Soc Trans 41:118–123. doi:10.1042/BST20120327