Cyclooxygenase-1 or -2 - Which one mediates lipopolysaccharide-induced hypothermia?

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 2, 2009, Pages

  Steiner, Alexandre A ^a,b   Hunter, John C ^c   Phipps, Sean M ^c   Nucci, Tatiane B ^a   Oliveira, Daniela L ^a   Roberts, Jennifer L ^a   Scheck, Adrienne C ^d   Simmons, Daniel L ^c   Romanovsky, Andrej A ^a  

^a ST JOSEPH'S HOSPITAL AND MEDICAL CENTER   (United States)

^b ALBANY COLLEGE OF PHARMACY AND HEALTH SCIENCES   (United States)

^c Brigham Young University   (United States)

^d BARROW NEUROLOGICAL INSTITUTE   (United States)

Author keywords

Body temperature; Fever; Inflammation; Thermoregulation

Indexed keywords

4 [5 (4 CHLOROPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOL 1 YL]BENZENESULFONAMIDE; 5 (4 CHLOROPHENYL) 1 (4 METHOXYPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOLE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; LIPOPOLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL PRESSURE; ARTICLE; BODY TEMPERATURE; COMPARATIVE STUDY; CONTROLLED STUDY; ENVIRONMENTAL TEMPERATURE; ENZYME ANALYSIS; ENZYME INHIBITION; FEVER; HYPOTENSION; HYPOTHERMIA; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMAL STRUCTURES; ANIMALS; BLOOD PRESSURE; BODY TEMPERATURE; BODY TEMPERATURE REGULATION; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYCLOOXYGENASE INHIBITORS; DINOPROSTONE; GENE EXPRESSION; HYPOTHERMIA; LIPOPOLYSACCHARIDES; MALE; PYRAZOLES; RATS; RATS, WISTAR; SPLEEN; SULFONAMIDES; TEMPERATURE;

EID: 68049102289     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.91026.2008     Document Type: Article

References (90)

1. Abercrombie ED, Jacobs BL. Single-unit response of noradrenergic neurons in the locus coeruleus of freely moving cats. II. Adaptation to chronically presented stressful stimuli. J Neurosci 7: 2844-2848, 1987.
2. Akarsu ES, Mamuk S. Escherichia coli lipopolysaccharides produce serotype-specific hypothermic response in biotelemetered rats. Am J Physiol Regul Integr Comp Physiol 292: R1846-R1850, 2007.
3. Almeida MC, Steiner AA, Branco LG, Romanovsky AA. Cold-seeking behavior as a thermoregulatory strategy in systemic inflammation. Eur J Neurosci 23: 3359-3367, 2006.
4. Almeida MC, Steiner AA, Branco LG, Romanovsky AA. Neural substrate of cold-seeking behavior in endotoxin shock. PLoS One 1: e1, 2006.
5. Aronoff DM, Neilson EG. Antipyretics: mechanisms of action and clinical use in fever suppression. Am J Med 111: 304-315, 2001.
6. Arons MM, Wheeler AP, Bernard GR, Christman BW, Russell JA, Schein R, Summer WR, Steinberg KP, Fulkerson W, Wright P, Dupont WD, Swindell BB. Effects of ibuprofen on the physiology and survival of hypothermic sepsis. Ibuprofen in Sepsis Study Group. Crit Care Med 27: 699-707, 1999.
7. Azab AN, Kaplanski J. Involvement of eicosanoids in the hypothermic response to lipopolysaccharide during endotoxemia in rats. Prostaglandins Leukot Essent Fatty Acids 70: 67-75, 2004.
8. Bjork DS, Engstrom L, Blomqvist A, Engblom D. COX-2 rather than mPGES-1 is rate-limiting for fever. In: Proceedings of the Society for Neuroscience Meeting, Washington DC: Society for Neuroscience, 2008, Program # 83.1.
9. Blanque R, Meakin C, Millet S, Gardner CR. Hypothermia as an indicator of the acute effects of lipopolysaccharides: comparison with serum levels of IL1β, IL6, and TNFα. Gen Pharmacol 27: 973-977, 1996.
10. Blatteis CM. Endotoxic fever: new concepts of its regulation suggest new approaches to its management. Pharmacol Ther 111: 194-223, 2006.
11. Bone RC, Balk RA, Cerra FB, Dellinger RP, Fein AM, Knaus WA, Schein RM, Sibbald WJ. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. The ACCP/SCCM Consensus Conference Committee American College of Chest Physicians/Society of Critical Care Medicine. Chest 101: 1644-1655, 1992.
12. Brenneis C, Maier TJ, Schmidt R, Hofacker A, Zulauf L, Jakobsson PJ, Scholich K, Geisslinger G. Inhibition of prostaglandin E2 synthesis by SC-560 is independent of cyclooxygenase 1 inhibition. FASEB J 20: 1352-1360, 2006.
13. Cao C, Matsumura K, Yamagata K, Watanabe Y. Involvement of cyclooxygenase-2 in LPS-induced fever and regulation of its mRNA by LPS in the rat brain. Am J Physiol Regul Integr Comp Physiol 272: R1712-R1725, 1997.
14. 2 synthase are markedly affected by glutathione and glutathione peroxidase(s). Biochemistry 34: 3325-3337, 1995.
15. Carnio EC, Branco LG. Participation of the nitric oxide pathway in cold-induced hypertension. Life Sci 60: 1875-1880, 1997.
16. Chandrasekharan NV, Dai H, Roos KL, Evanson NK, Tomsik J, Elton TS, Simmons DL. COX-3, a cyclooxygenase-1 variant inhibited by acetaminophen and other analgesic/antipyretic drugs: cloning, structure, and expression. Proc Natl Acad Sci USA 99: 13926-13931, 2002.
17. Clemmer TP, Fisher CJ Jr, Bone RC, Slotman GJ, Metz CA, and Thomas FO. Hypothermia in the sepsis syndrome and clinical outcome. The Methylprednisolone Severe Sepsis Study Group. Crit Care Med 20: 1395-1401, 1992.
18. De Boever S, Beyaert R, Vandemaele F, Baert K, Duchateau L, Goddeeris B, De Backer P, Croubels S. The influence of age and repeated lipopolysaccharide administration on body temperature and the concentration of interleukin-6 and IgM antibodies against lipopolysaccharide in broiler chickens. Avian Pathol 37: 39-44, 2008.
19. Derijk RH, Berkenbosch F. Hypothermia to endotoxin involves the cytokine tumor necrosis factor and the neuropeptide vasopressin in rats. Am J Physiol Regul Integr Comp Physiol 266: R9-R14, 1994.
20. Dogan MD, Ataoglu H, Akarsu ES. Effects of selective cyclooxygenase enzyme inhibitors on lipopolysaccharide-induced dual thermoregulatory changes in rats. Brain Res Bull 57: 179-185, 2002.
21. Dogan MD, Ataoglu H, Akarsu ES. Nimesulide and diclofenac inhibit lipopolysaccharide-induced hypothermia and tumour necrosis factor-α elevation in rats. Fundam Clin Pharmacol 16: 303-309, 2002.
22. Donhoffer S. Homeothermia of the Brain (Cerebral Blood Flow, Metabolic Rate, and Brain Temperature in the Cold: the Possible Role of Neuroglia). Budapest, Hungary: Akadémiai Kiadó, 1980.
23. Engblom D, Saha S, Engstrom L, Westman M, Audoly LP, Jakobsson PJ, Blomqvist A. Microsomal prostaglandin E synthase-1 is the central switch during immune-induced pyresis. Nat Neurosci 6: 1137-1138, 2003.
24. Feleder C, Li Z, Perlik V, Evans A, Blatteis CM. The spleen modulates the febrile response of guinea pigs to LPS. Am J Physiol Regul Integr Comp Physiol 284: R1466-R1476, 2003.
25. Feleder C, Perlik V, Tang Y, Blatteis CM. Putative antihyperpyretic factor induced by LPS in spleen of guinea pigs. Am J Physiol Regul Integr Comp Physiol 289: R680-R687, 2005.
26. Forman HJ, Torres M. Redox signaling in macrophages. Mol Aspects Med 22: 189-216, 2001.
27. 2. Eur J Pharmacol 608: 28-31, 2009.
28. Gordon CJ, Yang Y. Contribution of spontaneous motor activity to the 24-hour control of body temperature in male and female rats. J Therm Biol 22: 59-68, 1997.
29. 2-α and COX-1 with the Golgi apparatus of A549 human lung epithelial cells. J Cell Sci 116: 2303-2310, 2003.
30. 2 biosynthesis in mice spinal cord. Neuropharmacology 50: 165-173, 2006.
31. Gross GJ, Moore J. Effect of COX-1/COX-2 inhibition versus selective COX-2 inhibition on coronary vasodilator responses to arachidonic acid and acetylcholine. Pharmacology 71: 135-142, 2004.
32. Hashimoto K, Suemaru S, Takao T, Sugawara M, Makino S, Ota Z. Corticotropin-releasing hormone and pituitary-adrenocortical responses in chronically stressed rats. Regul Pept 23: 117-126, 1988.
33. Hocherl K, Dreher F, Kurtz A, Bucher M. Cyclooxygenase-2 inhibition attenuates lipopolysaccharide-induced cardiovascular failure. Hypertension 40: 947-953, 2002.
34. 2-synthesizing enzymes in fever: differential transcriptional regulation. Am J Physiol Regul Integr Comp Physiol 283: R1104-R1117, 2002.
35. 2 as a mediator of fever: synthesis and catabolism. Front Biosci 9: 1977-1993, 2004.
36. 2 in lipopolysaccharide fever. Am J Physiol Regul Integr Comp Physiol 284: R698-R706, 2003.
37. 2 synthases. Biochem J 359: 507-516, 2001.
38. Juttler E, Inta I, Eigler V, Herrmann O, Maegele I, Maser-Gluth C, Schwaninger M. Neuronal NF-κB influences thermoregulation and survival in a sepsis model. J Neuroimmunol 189: 41-49, 2007.
39. Kim SJ, Jeong HJ, Choi IY, Lee KM, Park RK, Hong SH, Kim HM. Cyclooxygenase-2 inhibitor SC-236 [4-[5-(4-chlorophenyl)-3-(trifluoromethyl)-1- pyrazol-1-l] benzenesulfonamide] suppresses nuclear factor-κB activation and phosphorylation of p38 mitogen-activated protein kinase, extracellular signal-regulated kinase, and c-Jun N-terminal kinase in human mast cell line cells. J Pharmacol Exp Ther 314: 27-34, 2005.
40. Kis B, Snipes A, Bari F, Busija DW. Regional distribution of cyclooxygenase-3 mRNA in the rat central nervous system. Brain Res Mol Brain Res 126: 78-80, 2004.
41. Kis B, Snipes JA, Isse T, Nagy K, Busija DW. Putative cyclooxygenase-3 expression in rat brain cells. J Cereb Blood Flow Metab 23: 1287-1292, 2003.
42. Kluger MJ. Fever: role of pyrogens and cryogens. Physiol Rev 71: 93-127, 1991.
43. Kluger MJ, Ringler DH, Anver MR. Fever and survival. Science 188: 166-168, 1975.
44. 2 have little effect on rabbit sleep. Physiol Behav 51: 481-485, 1992.
45. Kulmacz RJ, Wang LH. Comparison of hydroperoxide initiator requirements for the cyclooxygenase activities of prostaglandin H synthase-1 and -2. J Biol Chem 270: 24019-24023, 1995.
46. Lang CH, Bagby GJ, Spitzer JJ. Glucose kinetics and body temperature after lethal and nonlethal doses of endotoxin. Am J Physiol Regul Integr Comp Physiol 248: R471-R478, 1985.
47. Leach M, Hamilton LC, Olbrich A, Wray GM, Thiemermann C. Effects of inhibitors of the activity of cyclo-oxygenase-2 on the hypotension and multiple organ dysfunction caused by endotoxin: a comparison with dexamethasone. Br J Pharmacol 124: 586-592, 1998.
48. Levy MM, Fink MP, Marshall JC, Abraham E, Angus D, Cook D, Cohen J, Opal SM, Vincent JL, Ramsay G. 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med 31: 1250-1256, 2003.
49. -/- mice. Brain Res 825: 86-94, 1999.
50. 2 is phosphorylated and activated by MAP kinase. Cell 72: 269-278, 1993.
51. Lu G, Tsai AL, Van Wart HE, Kulmacz RJ. Comparison of the peroxidase reaction kinetics of prostaglandin H synthase-1 and -2. J Biol Chem 274: 16,162-16,167, 1999.
52. Martin SM, Malkinson TJ, Veale WL, Pittman QJ. Fever in pregnant, parturient, and lactating rats. Am J Physiol Regul Integr Comp Physiol 268: R919-R923, 1995.
53. Masferrer JL, Koki A, Seibert K. COX2 inhibitors. A new class of antiangiogenic agents. Ann NY Acad Sci 889: 84-86, 1999.
54. Masferrer JL, Leahy KM, Koki AT, Zweifel BS, Settle SL, Woerner BM, Edwards DA, Flickinger AG, Moore RJ, Seibert K. Antiangiogenic and antitumor activities of cyclooxygenase-2 inhibitors. Cancer Res 60: 1306-1311, 2000.
55. Matsumura K, Kobayashi S. Signaling the brain in inflammation: the role of endothelial cells. Front Biosci 9: 2819-2826, 2004.
56. Melia KR, Ryabinin AE, Schroeder R, Bloom FE, Wilson MC. Induction and habituation of immediate early gene expression in rat brain by acute and repeated restraint stress. J Neurosci 14: 5929-5938, 1994.
57. Milton AS, Wendlandt S. Effects on body temperature of prostaglandins of the A, E, and F series on injection into the third ventricle of unanaesthetized cats and rabbits. J Physiol 218: 325-336, 1971.
58. 2-biosynthetic pathway. Prog Lipid Res 43: 3-35, 2004.
59. 2 generation in immature mouse mast cells. J Biol Chem 270: 3239-3246, 1995.
60. 2 synthase that acts in concert with cyclooxygenase-2. J Biol Chem 275: 32,783-32,792, 2000.
61. 2, cyclooxygenases, and terminal prostanoid synthases in different phases of prostanoid biosynthesis in rat peritoneal macrophages. J Immunol 160: 2974-2982, 1998.
62. Ohashi K, Saigusa T. Sympathetic nervous responses during cytokine-induced fever in conscious rabbits. Pflügers Arch 433: 691-698, 1997.
63. Ohshima H, Tatemichi M, Sawa T. Chemical basis of inflammation-induced carcinogenesis. Arch Biochem Biophys 417: 3-11, 2003.
64. Papanek PE, Wood CE, Fregly MJ. Role of the sympathetic nervous system in cold-induced hypertension in rats. J Appl Physiol 71: 300-306, 1991.
65. Penning TD, Talley JJ, Bertenshaw SR, Carter JS, Collins PW, Docter S, Graneto MJ, Lee LF, Malecha JW, Miyashiro JM, Rogers RS, Rogier DJ, Yu SS, AndersonGd Burton EG, Cogburn JN, Gregory SA, Koboldt CM, Perkins WE, Seibert K, Veenhuizen AW, Zhang YY, Isakson PC. Synthesis and biological evaluation of the 1,5-diarylpyrazole class of cyclooxygenase-2 inhibitors: identification of 4-[5-(4-methylphenyl)-3-(trifluoromethyl)-1H-pyrazol-1-yl]benze nesulfonamide (SC-58635, celecoxib). J Med Chem 40: 1347-1365, 1997.
66. Romanovsky AA, Almeida MC, Aronoff DM, Ivanov AI, Konsman JP, Steiner AA, Turek VF. Fever and hypothermia in systemic inflammation: recent discoveries and revisions. Front Biosci 10: 2193-2216, 2005.
67. Romanovsky AA, Ivanov AI, Shimansky YP. Ambient temperature for experiments in rats: a new method for determining the zone of thermal neutrality. J Appl Physiol 92: 2667-2679, 2002.
68. Romanovsky AA, Kulchitsky VA, Akulich NV, Koulchitsky SV, Simons CT, Sessler DI, Gourine VN. First and second phases of biphasic fever: two sequential stages of the sickness syndrome? Am J Physiol Regul Integr Comp Physiol 271: R244-R253, 1996.
69. Romanovsky AA, Kulchitsky VA, Simons CT, Sugimoto N. Methodology of fever research: why are polyphasic fevers often thought to be biphasic? Am J Physiol Regul Integr Comp Physiol 275: R332-R338, 1998.
70. Romanovsky AA, Shido O, Sakurada S, Sugimoto N, Nagasaka T. Endotoxin shock: thermoregulatory mechanisms. Am J Physiol Regul Integr Comp Physiol 270: R693-R703, 1996.
71. Romanovsky AA, Simons CT, Kulchitsky VA. "Biphasic" fevers often consist of more than two phases. Am J Physiol Regul Integr Comp Physiol 275: R323-R331, 1998.
72. Romanovsky AA, Szekely M. Fever and hypothermia: two adaptive thermoregulatory responses to systemic inflammation. Med Hypotheses 50: 219-226, 1998.
73. Rudaya AY, Steiner AA, Robbins JR, Dragic AS, Romanovsky AA. Thermoregulatory responses to lipopolysaccharide in the mouse: dependence on the dose and ambient temperature. Am J Physiol Regul Integr Comp Physiol 289: R1244-R1252, 2005.
74. Saha S, Engstrom L, Mackerlova L, Jakobsson PJ, Blomqvist A. Impaired febrile responses to immune challenge in mice deficient in microsomal prostaglandin E synthase-1. Am J Physiol Regul Integr Comp Physiol 288: R1100-R1107, 2005.
75. Saia RS, Carnio EC. Thermoregulatory role of inducible nitric oxide synthase in lipopolysaccharide-induced hypothermia. Life Sci 79: 1473-1478, 2006.
76. Smith CJ, Zhang Y, Koboldt CM, Muhammad J, Zweifel BS, Shaffer A, Talley JJ, Masferrer JL, Seibert K, Isakson PC. Pharmacological analysis of cyclooxygenase-1 in inflammation. Proc Natl Acad Sci USA 95: 13,313-13,318, 1998.
77. Snipes JA, Kis B, Shelness GS, Hewett JA, Busija DW. Cloning and characterization of cyclooxygenase-1b (putative cyclooxygenase-3) in rat. J Pharmacol Exp Ther 313: 668-676, 2005.
78. Stamp JA, Herbert J. Multiple immediate-early gene expression during physiological and endocrine adaptation to repeated stress. Neuroscience 94: 1313-1322, 1999.
79. Steiner AA, Chakravarty S, Robbins JR, Dragic AS, Pan J, Herkenham M, Romanovsky AA. Thermoregulatory responses of rats to conventional preparations of lipopolysaccharide are caused by lipopolysaccharide per se - not by lipoprotein contaminants. Am J Physiol Regul Integr Comp Physiol 289: R348-R352, 2005.
80. Steiner AA, Ivanov AI, Serrats J, Hosokawa H, Phayre AN, Robbins JR, Roberts JL, Kobayashi S, Matsumura K, Sawchenko PE, Romanovsky AA. Cellular and molecular bases of the initiation of fever. PLoS Biol 4: e284, 2006.
81. Steiner AA, Li S, Llanos QJ, Blatteis CM. Differential inhibition by nimesulide of the early and late phases of intravenous- and intracerebro-ventricular-LPS-induced fever in guinea pigs. Neuroimmunomodulation 9: 263-275, 2001.
82. Steiner AA, Romanovsky AA. Leptin: at the crossroads of energy balance and systemic inflammation. Prog Lipid Res 46: 89-107, 2007.
83. Steiner AA, Rudaya AY, Robbins JR, Dragic AS, Langenbach R, Romanovsky AA. Expanding the febrigenic role of cyclooxygenase-2 to the previously overlooked responses. Am J Physiol Regul Integr Comp Physiol 289: R1253-R1257, 2005.
84. Szekely M, Romanovsky AA. Pyretic and antipyretic signals within and without fever: a possible interplay. Med Hypotheses 50: 213-218, 1998.
85. Ueno N, Takegoshi Y, Kamei D, Kudo I, Murakami M. Coupling between cyclooxygenases and terminal prostanoid synthases. Biochem Biophys Res Commun 338: 70-76, 2005.
86. 2 in the hypothermia of rats caused by bacterial lipopolysaccharide. Proc Natl Acad Sci USA 79: 6093-6097, 1982.
87. Vayssettes-Courchay C, Bouysset F, Verbeuren TJ. Involvement of COX and NOS induction in the sympatho-activation during sepsis. Auton Neurosci 98: 33-36, 2002.
88. Weinberg JR, Wright DJ, Guz A. Interleukin-1 and tumour necrosis factor cause hypotension in the conscious rabbit. Clin Sci (Lond) 75: 251-255, 1988.
89. Yang Y, Gordon CJ. Ambient temperature limits and stability of temperature regulation in telemetered male and female rats. J Therm Biol 21: 353-363, 1996.
90. Zhang YH, Lu J, Elmquist JK, Saper CB. Specific roles of cyclooxygenase-1 and cyclooxygenase-2 in lipopolysaccharide-induced fever and Fos expression in rat brain. J Comp Neurol 463: 3-12, 2003.