Delineating the relationships among the formation of reactive oxygen species, cell membrane instability and innate autoimmunity in intestinal reperfusion injury

Molecular Immunology

Volumn 58, Issue 2, 2014, Pages 151-159

  Lee, Haekyung ^a   Ko, Eun Hee ^a   Lai, Mark ^a,c   Wei, Na ^a,c   Balroop, Javi ^a,d   Kashem, Zerin ^a   Zhang, Ming ^a,b  

^a SUNY Downstate Medical Center   (United States)

^b SUNY DOWNSTATE MEDICAL CENTER   (United States)

^c LONG ISLAND UNIVERSITY   (United States)

^d POLYTECHNIC UNIVERSITY   (United States)

Author keywords

Cell membrane instability; Complement; Natural IgM; Reactive oxygen species; Reperfusion injury; Trehalose

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; IMMUNOGLOBULIN M; MALONALDEHYDE; MEMBRANE LIPID; REACTIVE OXYGEN METABOLITE; TREHALOSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CELL MEMBRANE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; INTESTINE INJURY; INTESTINE ISCHEMIA; LIPID OXIDATION; LIPID PEROXIDATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPERFUSION INJURY; WILD TYPE;

ANIMALIA; MURINAE; MUS;

CELL MEMBRANE INSTABILITY; COMPLEMENT; NATURAL IGM; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; TREHALOSE;

ANIMALS; AUTOIMMUNITY; CELL MEMBRANE; DISEASE MODELS, ANIMAL; IMMUNITY, INNATE; INTESTINAL MUCOSA; ISCHEMIA; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; SUPEROXIDE DISMUTASE; TREHALOSE; VASCULAR DISEASES;

EID: 84890834442     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.11.012     Document Type: Article

References (63)

1. Amara U., Rittirsch D., Flierl M., Bruckner U., Klos A., Gebhard F., Lambris J.D., Huber-Lang M. Interaction between the coagulation and complement system. Advances in Experimental Medicine and Biology 2008, 632:71-79.
2. Ambrosio G., Flaherty J.T. Effects of the superoxide radical scavenger superoxide dismutase, and of the hydroxyl radical scavenger mannitol, on reperfusion injury in isolated rabbit hearts. Cardiovascular Drugs and Therapy 1992, 6:623-632.
3. Barbas J.P., Mascarenhas R.D. Cryopreservation of domestic animal sperm cells. Cell Tissue Bank 2009, 10:49-62.
4. Beattie G.M., Crowe J.H., Lopez A.D., Cirulli V., Ricordi C., Hayek A. Trehalose: a cryoprotectant that enhances recovery and preserves function of human pancreatic islets after long-term storage. Diabetes 1997, 46:519-523.
5. Brandt J.L. Mesenteric Vascular Disease 2003, The McGraw-Hill Companies, Inc., New York, (Section I.9). S.L. Friedman (Ed.).
6. Charlagorla P., Liu J., Patel M., Rushbrook J.I., Zhang M. Loss of plasma membrane integrity, complement response and formation of reactive oxygen species during early myocardial ischemia/reperfusion. Molecular Immunology 2013, 56:507-512.
7. Chen F., Nakamura T., Wada H. Development of new organ preservation solutions in Kyoto University. Yonsei Medical Journal 2004, 45:1107-1114.
8. Crowe J.H., Crowe L.M., Chapman D. Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 1984, 223:701-703.
9. Cui X.D., Gao D.Y., Fink B.F., Vasconez H.C., Pu L.L. Cryopreservation of human adipose tissues. Cryobiology 2007, 55:269-278.
10. da Costa Morato Nery D., da Silva C.G., Mariani D., Fernandes P.N., Pereira M.D., Panek A.D., Eleutherio E.C. The role of trehalose and its transporter in protection against reactive oxygen species. Biochimica et Biophysica Acta 2008, 1780:1408-1411.
11. Eberhardt M. Pathological Processes Involving Reactive Oxygen Metabolites 2001, 365-379. CRC Press LLC, Boca Raton, FL. M. Eberhardt (Ed.).
12. Eleutherio E.C., Araujo P.S., Panek A.D. Role of the trehalose carrier in dehydration resistance of Saccharomyces cerevisiae. Biochimica et Biophysica Acta 1993, 1156:263-266.
13. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biology & Medicine 1991, 11:81-128.
14. Flaherty J.T., Pitt B., Gruber J.W., Heuser R.R., Rothbaum D.A., Burwell L.R., George B.S., Kereiakes D.J., Deitchman D., Gustafson N., et al. Recombinant human superoxide dismutase (h-SOD) fails to improve recovery of ventricular function in patients undergoing coronary angioplasty for acute myocardial infarction. Circulation 1994, 89:1982-1991.
15. Fleming S.D., Egan R.P., Chai C., Girardi G., Holers V.M., Salmon J., Monestier M., Tsokos G.C. Anti-phospholipid antibodies restore mesenteric ischemia/reperfusion-induced injury in complement receptor 2/complement receptor 1-deficient mice. Journal of Immunology 2004, 173:7055-7061.
16. Fukuse T., Hirata T., Ueda M., Hitomi S., Wada H. Effects of Euro-Collins, University of Wisconsin, and new extracellular-type trehalase-containing Kyoto solutions in an ex vivo rat lung preservation model. Transplantation 1996, 62:1212-1217.
17. Gallagher K.P., Buda A.J., Pace D., Gerren R.A., Shlafer M. Failure of superoxide dismutase and catalase to alter size of infarction in conscious dogs after 3hours of occlusion followed by reperfusion. Circulation 1986, 73:1065-1076.
18. Grisham M.B., Hernandez L.A., Granger D.N. Xanthine oxidase and neutrophil infiltration in intestinal ischemia. The American Journal of Physiology 1986, 251:G567-G574.
19. Gross G.J., Farber N.E., Hardman H.F., Warltier D.C. Beneficial actions of superoxide dismutase and catalase in stunned myocardium of dogs. The American Journal of Physiology 1986, 250:H372-H377.
20. Halliwell B., Chirico S. Lipid peroxidation: its mechanism, measurement, and significance. The American Journal of Clinical Nutrition 1993, 57:715S-724S. discussion 724S-725S.
21. Hangaishi M., Nakajima H., Taguchi J., Igarashi R., Hoshino J., Kurokawa K., Kimura S., Nagai R., Ohno M. Lecithinized Cu, Zn-superoxide dismutase limits the infarct size following ischemia-reperfusion injury in rat hearts in vivo. Biochemical and Biophysical Research Communications 2001, 285:1220-1225.
22. He X., Park E.Y., Fowler A., Yarmush M.L., Toner M. Vitrification by ultra-fast cooling at a low concentration of cryoprotectants in a quartz micro-capillary: a study using murine embryonic stem cells. Cryobiology 2008, 56:223-232.
23. Herdeiro R.S., Pereira M.D., Panek A.D., Eleutherio E.C. Trehalose protects Saccharomyces cerevisiae from lipid peroxidation during oxidative stress. Biochimica et Biophysica Acta 2006, 1760:340-346.
24. Higashiyama T. Novel functions and applications of trehalose. Pure and Applied Chemistry 2002, 74:1263-1269.
25. Isowa N., Hitomi S., Wada H. Trehalose-containing solutions enhance preservation of cultured endothelial cells. The Annals of Thoracic Surgery 1996, 61:542-545.
26. Jones S.P., Hoffmeyer M.R., Sharp B.R., Ho Y.S., Lefer D.J. Role of intracellular antioxidant enzymes after in vivo myocardial ischemia and reperfusion. American Journal of Physiology. Heart and Circulatory Physiology 2003, 284:H277-H282.
27. Kanamasa K., Ishida N., Ishikawa K. Protective effect of PEG-SOD against early coronary reperfusion injury assessed in reperfused and non-reperfused ischaemic areas of the same heart. Acta Cardiologica 2001, 56:181-186.
28. Klein H.H., Pich S., Lindert S., Buchwald A., Nebendahl K., Kreuzer H. Intracoronary superoxide dismutase for the treatment of "reperfusion injury", a blind randomized placebo-controlled trial in ischemic, reperfused porcine hearts. Basic Research in Cardiology 1988, 83:141-148.
29. Kolkman J., Geelkerken R. Splanchnic Ischemia 2005, 2021-2029. Elsevier Sauders, Amsterdam, Netherlands. M.P. Fink (Ed.).
30. Kurose I., Wolf R.E., Grisham M.B., Granger D.N. Hypercholesterolemia enhances oxidant production in mesenteric venules exposed to ischemia/reperfusion. Arteriosclerosis, Thrombosis, and Vascular Biology 1998, 18:1583-1588.
31. Lee H., Green D.J., Lai L., Hou Y.J., Jensenius J.C., Liu D., Cheong C., Park C.G., Zhang M. Early complement factors in the local tissue immunocomplex generated during intestinal ischemia/reperfusion injury. Molecular Immunology 2010, 47:972-981.
32. Lee H.T., Kim M., Kim J.Y., Brown K.M., Ham A., D'Agati V.D., Mori-Akiyama Y. Critical role of interleukin-17A in murine intestinal ischemia-reperfusion injury. American Journal of Physiology. Gastrointestinal and Liver Physiology 2013, 304:G12-G25.
33. Li C., Jackson R.M. Reactive species mechanisms of cellular hypoxia-reoxygenation injury. American Journal of Physiology. Cell Physiology 2002, 282:C227-C241.
34. Matsuda M., Fujiwara H., Kawamura A., Ishida M., Takemura G., Kida M., Uegaito T., Fujiwara Y., Fujiwara T., Kawai C. Failure to reduce infarct size by intracoronary infusion of recombinant human superoxide dismutase at reperfusion in the porcine heart: immunohistochemical and histological analysis. Journal of Molecular and Cellular Cardiology 1991, 23:1287-1296.
35. Minutoli L., Altavilla D., Bitto A., Polito F., Bellocco E., Lagana G., Giuliani D., Fiumara T., Magazu S., Ruggeri P., Guarini S., Squadrito F. The disaccharide trehalose inhibits proinflammatory phenotype activation in macrophages and prevents mortality in experimental septic shock. Shock 2007, 27:91-96.
36. Moore R.M., Muir W.W., Granger D.N. Mechanisms of gastrointestinal ischemia-reperfusion injury and potential therapeutic interventions: a review and its implications in the horse. Journal of Veterinary Internal Medicine 1995, 9:115-132.
37. Murohara Y., Yui Y., Hattori R., Kawai C. Effects of superoxide dismutase on reperfusion arrhythmias and left ventricular function in patients undergoing thrombolysis for anterior wall acute myocardial infarction. American Journal of Cardiology 1991, 67:765-767.
38. Nejima J., Knight D.R., Fallon J.T., Uemura N., Manders W.T., Canfield D.R., Cohen M.V., Vatner S.F. Superoxide dismutase reduces reperfusion arrhythmias but fails to salvage regional function or myocardium at risk in conscious dogs. Circulation 1989, 79:143-153.
39. Newman Y.M., Ring S.G., Colaco C. The role of trehalose and other carbohydrates in biopreservation. Biotechnology & Genetic Engineering Reviews 1993, 11:263-294.
40. Nishikawa Y., Yamamoto S., Ataka K., Nakamura K. The effect of superoxide dismutase and catalase on myocardial reperfusion injury in the isolated rat heart. The Japanese Journal of Surgery 1991, 21:423-432.
41. Oku T., Nakamura S. Estimation of intestinal trehalase activity from a laxative threshold of trehalose and lactulose on healthy female subjects. European Journal of Clinical Nutrition 2000, 54:783-788.
42. Ooiwa H., Stanley A., Felaneous-Bylund A.C., Wilborn W., Downey J.M. Superoxide dismutase conjugated to polyethylene glycol fails to limit myocardial infarct size after 30min ischemia followed by 72h of reperfusion in the rabbit. Journal of Molecular and Cellular Cardiology 1991, 23:119-125.
43. Opal S.M., Esmon C.T. Bench-to-bedside review: functional relationships between coagulation and the innate immune response and their respective roles in the pathogenesis of sepsis. Critical Care 2003, 7:23-38.
44. Otani H., Umemoto M., Kagawa K., Nakamura Y., Omoto K., Tanaka K., Sato T., Nonoyama A., Kagawa T. Protection against oxygen-induced reperfusion injury of the isolated canine heart by superoxide dismutase and catalase. The Journal of Surgical Research 1986, 41:126-133.
45. Patel B.S., Jeroudi M.O., O'Neill P.G., Roberts R., Bolli R. Effect of human recombinant superoxide dismutase on canine myocardial infarction. The American Journal of Physiology 1990, 258:H369-H380.
46. Pope M.R., Hoffman S.M., Tomlinson S., Fleming S.D. Complement regulates TLR4-mediated inflammatory responses during intestinal ischemia reperfusion. Molecular Immunology 2010, 48:356-364.
47. Przyklenk K., Kloner R.A. "Reperfusion injury" by oxygen-derived free radicals? Effect of superoxide dismutase plus catalase, given at the time of reperfusion, on myocardial infarct size, contractile function, coronary microvasculature, and regional myocardial blood flow. Circulation Research 1989, 64:86-96.
48. Qin X., Dong W., Sharpe S.M., Sheth S.U., Palange D.C., Rider T., Jandacek R., Tso P., Deitch E.A. Role of lipase-generated free fatty acids in converting mesenteric lymph from a noncytotoxic to a cytotoxic fluid. American Journal of Physiology. Gastrointestinal and Liver Physiology 2012, 303:G969-G978.
49. Richard V.J., Murry C.E., Jennings R.B., Reimer K.A. Therapy to reduce free radicals during early reperfusion does not limit the size of myocardial infarcts caused by 90minutes of ischemia in dogs. Circulation 1988, 78:473-480.
50. Russell J., Epstein C.J., Grisham M.B., Alexander J.S., Yeh K.Y., Granger D.N. Regulation of E-selectin expression in postischemic intestinal microvasculature. American Journal of Physiology. Gastrointestinal and Liver Physiology 2000, 278:G878-G885.
51. Satpathy G.R., Torok Z., Bali R., Dwyre D.M., Little E., Walker N.J., Tablin F., Crowe J.H., Tsvetkova N.M. Loading red blood cells with trehalose: a step towards biostabilization. Cryobiology 2004, 49:123-136.
52. Testa L., Van Gaal W.J., Bhindi R., Biondi-Zoccai G.G., Abbate A., Agostoni P., Porto I., Andreotti F., Crea F., Banning A.P. Pexelizumab in ischemic heart disease: a systematic review and meta-analysis on 15,196 patients. The Journal of Thoracic and Cardiovascular Surgery 2008, 136:884-893.
53. Toledo-Pereyra L.H., Lopez-Neblina F., Toledo A.H. Reactive oxygen species and molecular biology of ischemia/reperfusion. Annals of Transplantation 2004, 9:81-83.
54. Uraizee A., Reimer K.A., Murry C.E., Jennings R.B. Failure of superoxide dismutase to limit size of myocardial infarction after 40minutes of ischemia and 4 days of reperfusion in dogs. Circulation 1987, 75:1237-1248.
55. Wang P., Chen H., Qin H., Sankarapandi S., Becher M.W., Wong P.C., Zweier J.L. Overexpression of human copper, zinc-superoxide dismutase (SOD1) prevents postischemic injury. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:4556-4560.
56. Watanabe B.I., Premaratne S., Limm W., Mugiishi M.M., McNamara J.J. High- and low-dose superoxide dismutase plus catalase does not reduce myocardial infarct size in a subhuman primate model. American Heart Journal 1993, 126:840-846.
57. Watanabe T., Kobata A., Tanigawa T., Nadatani Y., Yamagami H., Watanabe K., Tominaga K., Fujiwara Y., Takeuchi K., Arakawa T. Activation of the MyD88 signaling pathway inhibits ischemia-reperfusion injury in the small intestine. American Journal of Physiology. Gastrointestinal and Liver Physiology 2012, 303:G324-G334.
58. Watts J.A., Kline J.A. Bench to bedside: the role of mitochondrial medicine in the pathogenesis and treatment of cellular injury. Academic Emergency Medicine 2003, 10:985-997.
59. Yokomise H., Inui K., Wada H., Ueda M., Hitomi S. Long-term cryopreservation can prevent rejection of canine tracheal allografts with preservation of graft viability. The Journal of Thoracic and Cardiovascular Surgery 1996, 111:930-934.
60. Zhang G.X., Kimura S., Murao K., Obata K., Matsuyoshi H., Takaki M. Inhibition of cytochrome c release by 10-N-nonyl acridine orange, a cardiolipin-specific dye, during myocardial ischemia-reperfusion in the rat. American Journal of Physiology. Heart and Circulatory Physiology 2010, 298:H433-H439.
61. Zhang M., Alicot E.M., Chiu I., Li J., Verna N., Vorup-Jensen T., Kessler B., Shimaoka M., Chan R., Friend D., Mahmood U., Weissleder R., Moore F.D., Carroll M.C. Identification of the target self-antigens in reperfusion injury. The Journal of Experimental Medicine 2006, 203:141-152.
62. Zhang M., Austen W.G., Chiu I., Alicot E.M., Hung R., Ma M., Verna N., Xu M., Hechtman H.B., Moore F.D., Carroll M.C. Identification of a specific self-reactive IgM antibody that initiates intestinal ischemia/reperfusion injury. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:3886-3891.
63. Zhang M., Carroll M.C. Natural antibody mediated innate autoimmune response. Molecular Immunology 2007, 44:103-110.