Hydrogen Sulfide Donor NaHS Reduces Organ Injury in a Rat Model of Pneumococcal Pneumosepsis, Associated with Improved Bio-Energetic Status

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Aslami, Hamid ^a   Pulskens, Wilco P ^a   Kuipers, Maria T ^a   Bos, Aafkeline P ^a   van Kuilenburg, André B P ^a   Wanders, Ronald J A ^a   Roelofsen, Jeroen ^a   Roelofs, Joris J T H ^a   Kerindongo, Raphaela P ^a   Beurskens, Charlotte J P ^a   Schultz, Marcus J ^a   Kulik, Wim ^a   Weber, Nina C ^a   Juffermans, Nicole P ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ALPHA TUBULIN; HYDROGEN SULFIDE; MITOCHONDRIAL DNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN KINASE C; SODIUM HYDROSULFIDE; UNCLASSIFIED DRUG;

ACCIDENT PREVENTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BIOENERGY; BIOGENESIS; BODY TEMPERATURE; CELL DAMAGE; CELL FUNCTION; CELL VIABILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; GAS EXCHANGE; HEART RATE; HOST RESISTANCE; KIDNEY FUNCTION; KIDNEY INJURY; LIVER INJURY; LUNG INJURY; MITOCHONDRIAL RESPIRATION; NONHUMAN; ORGAN INJURY; OXIDATIVE PHOSPHORYLATION; PROTEIN EXPRESSION; RAT; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE; UPREGULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT COMPLEX I; ENERGY METABOLISM; HEART RATE; KIDNEY; LIVER; LUNG INJURY; MITOCHONDRIA; MITOCHONDRIAL TURNOVER; OXIDATION-REDUCTION; PNEUMONIA, PNEUMOCOCCAL; PROTEIN KINASE C-EPSILON; RATS; RATS, SPRAGUE-DAWLEY; SEPSIS; SULFIDES; TUBULIN; UP-REGULATION;

EID: 84878148420     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063497     Document Type: Article

References (45)

1. Torres A, Rello J (2010) Update in community-acquired and nosocomial pneumonia 2009. Am J Respir Crit Care Med 181: 782-787. 181/8/782 [pii]; doi:10.1164/rccm.201001-0030UP.
2. Abraham E, Singer M, (2007) Mechanisms of sepsis-induced organ dysfunction. Crit Care Med 35: 2408-2416.
3. Dombrovskiy VY, Martin AA, Sunderram J, Paz HL, (2007) Rapid increase in hospitalization and mortality rates for severe sepsis in the United States: a trend analysis from 1993 to 2003. Crit Care Med 35: 1244-1250 doi:10.1097/01.CCM.0000261890.41311.E9.
4. Suliman HB, Welty-Wolf KE, Carraway M, Tatro L, Piantadosi CA (2004) Lipopolysaccharide induces oxidative cardiac mitochondrial damage and biogenesis. Cardiovasc Res 64: 279-288. S0008-6363(04)00307-4 [pii]; doi:10.1016/j.cardiores.2004.07.005.
5. Brealey D, Brand M, Hargreaves I, Heales S, Land J, et al. (2002) Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 360: 219-223.
6. Tappy L, Chiolero R (2007) Substrate utilization in sepsis and multiple organ failure. Crit Care Med 35: S531-S534. 00003246-200709001-00016 [pii]. doi:10.1097/01.CCM.0000278062.28122.A4.
7. Van den Berghe G, Wouters P, Weekers F, Verwaest C, Bruyninckx F, et al. (2001) Intensive insulin therapy in the critically ill patients. N Engl J Med 345: 1359-1367 doi:10.1056/NEJMoa011300.
8. Goeters C, Wenn A, Mertes N, Wempe C, Van AH, et al. (2002) Parenteral L-alanyl-L-glutamine improves 6-month outcome in critically ill patients. Crit Care Med 30: 2032-2037 doi:10.1097/01.CCM.0000025908.95498.A3.
9. Vanhorebeek I, De Vos R, Mesotten D, Wouters PJ, De Wolf-Peeters C, et al. (2005) Protection of hepatocyte mitochondrial ultrastructure and function by strict blood glucose control with insulin in critically ill patients. Lancet 365: 53-59. S0140-6736(04)17665-4 [pii]; doi:10.1016/S0140-6736(04)17665-4.
10. Liang H, Ward WF (2006) PGC-1alpha: a key regulator of energy metabolism. Adv Physiol Educ 30: 145-151. 30/4/145 [pii]; doi:10.1152/advan.00052.2006.
11. Carre M, Andre N, Carles G, Borghi H, Brichese L, et al. (2002) Tubulin is an inherent component of mitochondrial membranes that interacts with the voltage-dependent anion channel. J Biol Chem 277: 33664-33669. M203834200 [pii]. doi:10.1074/jbc.M203834200.
12. Rostovtseva TK, Sheldon KL, Hassanzadeh E, Monge C, Saks V, et al. (2008) Tubulin binding blocks mitochondrial voltage-dependent anion channel and regulates respiration. Proc Natl Acad Sci U S A 105: 18746-18751. 0806303105 [pii]; doi:10.1073/pnas.0806303105.
13. Elrod JW, Calvert JW, Morrison J, Doeller JE, Kraus DW, et al. (2007) Hydrogen sulfide attenuates myocardial ischemia-reperfusion injury by preservation of mitochondrial function. Proc Natl Acad Sci U S A 104: 15560-15565.
14. Baumgart K, Wagner F, Groger M, Weber S, Barth E, et al. (2010) Cardiac and metabolic effects of hypothermia and inhaled hydrogen sulfide in anesthetized and ventilated mice. Crit Care Med 38: 588-595.
15. Fu M, Zhang W, Wu L, Yang G, Li H, et al. (2012) Hydrogen sulfide (H2S) metabolism in mitochondria and its regulatory role in energy production. Proc Natl Acad Sci U S A 109: 2943-2948. 1115634109 [pii]; doi:10.1073/pnas.1115634109.
16. Szabo C, (2007) Hydrogen sulphide and its therapeutic potential. Nat Rev Drug Discov 6: 917-935.
17. Blackstone E, Morrison M, Roth MB, (2005) H2S induces a suspended animation-like state in mice. Science 308: 518.
18. Aslami H, Heinen A, Roelofs JJ, Zuurbier CJ, Schultz MJ, et al. (2010) Suspended animation inducer hydrogen sulfide is protective in an in vivo model of ventilator-induced lung injury. Intensive Care Med 36: 1946-1952 doi:10.1007/s00134-010-2022-2.
19. Spiller F, Orrico MI, Nascimento DC, Czaikoski PG, Souto FO, et al. (2010) Hydrogen sulfide improves neutrophil migration and survival in sepsis via K+ATP channel activation. Am J Respir Crit Care Med 182: 360-368. 200907-1145OC [pii]; doi:10.1164/rccm.200907-1145OC.
20. Wolthuis EK, Vlaar AP, Choi G, Roelofs JJ, Juffermans NP, et al. (2009) Mechanical ventilation using non-injurious ventilation settings causes lung injury in the absence of pre-existing lung injury in healthy mice. Crit Care 13: R1.
21. Bierau J, van Gennip AH, Helleman J, van Kuilenburg AB (2001) The cytostatic- and differentiation-inducing effects of cyclopentenyl cytosine on neuroblastoma cell lines. Biochem Pharmacol 62: 1099-1105. S0006-2952(01)00756-0 [pii].
22. Esechie A, Kiss L, Olah G, Horvath EM, Hawkins H, et al. (2008) Protective effect of hydrogen sulfide in a murine model of acute lung injury induced by combined burn and smoke inhalation. Clin Sci (Lond) 115: 91-97.
23. Yang KY, Liu KT, Chen YC, Chen CS, Lee YC, et al. (2011) Plasma soluble vascular endothelial growth factor receptor-1 levels predict outcomes of pneumonia-related septic shock patients: a prospective observational study. Crit Care 15: R11. cc9412 [pii]; doi:10.1186/cc9412.
24. Akram AR, Singanayagam A, Choudhury G, Mandal P, Chalmers JD, et al. (2010) Incidence and prognostic implications of acute kidney injury on admission in patients with community-acquired pneumonia. Chest 138: 825-832. chest.09-3071 [pii]; doi:10.1378/chest.09-3071.
25. Gellerich FN, Trumbeckaite S, Hertel K, Zierz S, Muller-Werdan U, et al. (1999) Impaired energy metabolism in hearts of septic baboons: diminished activities of Complex I and Complex II of the mitochondrial respiratory chain. Shock 11: 336-341.
26. Brealey D, Karyampudi S, Jacques TS, Novelli M, Stidwill R, et al. (2004) Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure. Am J Physiol Regul Integr Comp Physiol 286: R491-R497.
27. Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R (2003) Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta 329: 23-38. S0009898103000032 [pii].
28. Baines CP, Song CX, Zheng YT, Wang GW, Zhang J, et al. (2003) Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 92: 873-880. 01.RES.0000069215.36389.8D [pii]. doi:10.1161/01.RES.0000069215.36389.8D.
29. Lemasters JJ, Holmuhamedov E (2006) Voltage-dependent anion channel (VDAC) as mitochondrial governator-thinking outside the box. Biochim Biophys Acta 1762: 181-190. S0925-4439(05)00152-3 [pii]; doi:10.1016/j.bbadis.2005.10.006.
30. Agudo-Lopez A, Miguel BG, Fernandez I, Martinez AM (2011) Role of protein kinase C and mitochondrial permeability transition pore in the neuroprotective effect of ceramide in ischemia-induced cell death. FEBS Lett 585: 99-103. S0014-5793(10)00911-7 [pii]; doi:10.1016/j.febslet.2010.11.015.
31. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, et al. (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 464: 104-107. nature08780 [pii]; doi:10.1038/nature08780.
32. Lancel S, Hassoun SM, Favory R, Decoster B, Motterlini R, et al. (2009) Carbon monoxide rescues mice from lethal sepsis by supporting mitochondrial energetic metabolism and activating mitochondrial biogenesis. J Pharmacol Exp Ther 329: 641-648. jpet.108.148049 [pii]; doi:10.1124/jpet.108.148049.
33. Nisoli E, Clementi E, Paolucci C, Cozzi V, Tonello C, et al. (2003) Mitochondrial biogenesis in mammals: the role of endogenous nitric oxide. Science 299: 896-899. 299/5608/896 [pii]. doi:10.1126/science.1079368.
34. Kamps M, Bisschops LA, van der Hoeven JG, Hoedemaekers CW (2011) Hypothermia does not increase the risk of infection: a case control study. Crit Care 15: R48. cc10012 [pii]; doi:10.1186/cc10012.
35. Mongardon N, Perbet S, Lemiale V, Dumas F, Poupet H, et al. (2011) Infectious complications in out-of-hospital cardiac arrest patients in the therapeutic hypothermia era. Crit Care Med. doi:10.1097/CCM.0b013e3182120b56.
36. Fries M, Stoppe C, Brucken D, Rossaint R, Kuhlen R (2009) Influence of mild therapeutic hypothermia on the inflammatory response after successful resuscitation from cardiac arrest. J Crit Care 24: 453-457. S0883-9441(08)00235-9 [pii]; doi:10.1016/j.jcrc.2008.10.012.
37. Lim CM, Kim EK, Koh Y, Kim WS, Kim DS, et al. (2004) Hypothermia inhibits cytokine release of alveolar macrophage and activation of nuclear factor kappaB in endotoxemic lung. Intensive Care Med 30: 1638-1644 doi:10.1007/s00134-004-2336-z.
38. Chu SJ, Perng WC, Hung CM, Chang DM, Lin SH, et al. (2005) Effects of various body temperatures after lipopolysaccharide-induced lung injury in rats. Chest 128: 327-336.
39. Lim CM, Kim MS, Ahn JJ, Kim MJ, Kwon Y, et al. (2003) Hypothermia protects against endotoxin-induced acute lung injury in rats. Intensive Care Med 29: 453-459.
40. Weinrauch V, Safar P, Tisherman S, Kuboyama K, Radovsky A, (1992) Beneficial effect of mild hypothermia and detrimental effect of deep hypothermia after cardiac arrest in dogs. Stroke 23: 1454-1462.
41. Fairchild KD, Singh IS, Patel S, Drysdale BE, Viscardi RM, et al. (2004) Hypothermia prolongs activation of NF-kappaB and augments generation of inflammatory cytokines. Am J Physiol Cell Physiol 287: C422-C431. 00507.2003 [pii]. doi:10.1152/ajpcell.00507.2003.
42. Polderman KH, (2009) Mechanisms of action, physiological effects, and complications of hypothermia. Crit Care Med 37: S186-S202.
43. Faller S, Ryter SW, Choi AM, Loop T, Schmidt R, et al. (2010) Inhaled hydrogen sulfide protects against ventilator-induced lung injury. Anesthesiology 113: 104-115. 00000542-201007000-00018 [pii]. doi:10.1097/ALN.0b013e3181de7107.
44. Wagner F, Wagner K, Weber S, Stahl B, Knoferl MW, et al. (2010) Inflammatory Effects of Hypothermia and Inhaled H2S During Resuscitated, Hyperdynamic Murine Septic Shock. Shock. doi:10.1097/SHK.0b013e3181ffff0e.
45. Bracht H, Scheuerle A, Groger M, Hauser B, Matallo J, et al. (2012) Effects of intravenous sulfide during resuscitated porcine hemorrhagic shock*. Crit Care Med 40: 2157-2167. 00003246-201207000-00020 [pii]. doi:10.1097/CCM.0b013e31824e6b30.