Inflammatory hyperalgesia induces essential bioactive lipid production in the spinal cord

Journal of Neurochemistry

Volumn 114, Issue 4, 2010, Pages 981-993

  Buczynski, Matthew W ^a   Svensson, Camilla I ^b   Dumlao, Darren S ^a   Fitzsimmons, Bethany L ^b   Shim, Jae Hang ^b,c   Scherbart, Thomas J ^a   Jacobsen, Faith E ^a   Hua, Xiao Ying ^b   Yaksh, Tony L ^b   Dennis, Edward A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California   (United States)

^c Hanyang University   (South Korea)

Author keywords

12 lipoxygenase; hepoxilin; lipidomics; nociception; prostaglandin; spinal

Indexed keywords

ANANDAMIDE; ARACHIDONATE 12 LIPOXYGENASE; CARRAGEENAN; FATTY ACID; HEPOXILIN B; ICOSANOID; KETOROLAC; LIPID; LIPOXYGENASE; MORPHINE SULFATE; NORDIHYDROGUAIARETIC ACID; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE; AUTACOID; CANNABINOID RECEPTOR AFFECTING AGENT; ETHANOLAMINE DERIVATIVE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBROSPINAL FLUID ANALYSIS; CONTROLLED STUDY; HINDLIMB; HYPERALGESIA; INFLAMMATION; LIPID METABOLISM; MALE; MASS SPECTROMETRY; NONHUMAN; PAW EDEMA; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; SIGNAL TRANSDUCTION; SPINAL CORD; SYSTEMIC THERAPY; TOUCH; ANIMAL; BIOSYNTHESIS; CEREBROSPINAL FLUID; DRUG EFFECTS; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALIA; RATTUS;

ANIMALS; ARACHIDONATE 12-LIPOXYGENASE; CANNABINOID RECEPTOR MODULATORS; EICOSANOIDS; ETHANOLAMINES; FATTY ACIDS; HYPERALGESIA; INFLAMMATION MEDIATORS; LIPIDS; MALE; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SPINAL CORD;

EID: 77954751552     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06815.x     Document Type: Article

References (56)

1. Abadji V., Lin S., Taha G., Griffin G., Stevenson L. A., Pertwee R. G. Makriyannis A. (1994) (R)-methanandamide: a chiral novel anandamide possessing higher potency and metabolic stability. J. Med. Chem. 37, 1889 1893.
2. Amer R. K., Pace-Asciak C. R. Mills L. R. (2003) A lipoxygenase product, hepoxilin A(3), enhances nerve growth factor-dependent neurite regeneration post-axotomy in rat superior cervical ganglion neurons in vitro. Neuroscience 116, 935 946.
3. Argentieri D. C., Ritchie D. M., Ferro M. P., Kirchner T., Wachter M. P., Anderson D. W., Rosenthale M. E. Capetola R. J. (1994) Tepoxalin: a dual cyclooxygenase5-lipoxygenase inhibitor of arachidonic acid metabolism with potent anti-inflammatory activity and a favorable gastrointestinal profile. J. Pharmacol. Exp. Ther. 271, 1399 1408.
4. Beloeil H., Ji R. R. Berde C. B. (2006) Effects of bupivacaine and tetrodotoxin on carrageenan-induced hind paw inflammation in rats (Part 2): cytokines and p38 mitogen-activated protein kinases in dorsal root ganglia and spinal cord. Anesthesiology 105, 139 145.
5. Beloeil H., Gentili M., Benhamou D. Mazoit J. X. (2009) The effect of a peripheral block on inflammation-induced prostaglandin E2 and cyclooxygenase expression in rats. Anesth. Analg. 109, 943 950.
6. Bianchi M., Martucci C., Ferrario P., Franchi S. Sacerdote P. (2007) Increased tumor necrosis factor-alpha and prostaglandin E2 concentrations in the cerebrospinal fluid of rats with inflammatory hyperalgesia: the effects of analgesic drugs. Anesth. Analg. 104, 949 954.
7. Blaho V. A., Buczynski M. W., Brown C. R. Dennis E. A. (2009) Lipidomic analysis of dynamic eicosanoid responses during the induction and resolution of lyme arthritis. J. Biol. Chem. 284, 21598 21612.
8. Buczynski M. W., Stephens D. L., Bowers-Gentry R. C., Grkovich A., Deems R. A. Dennis E. A. (2007) TLR-4 and sustained calcium agonists synergistically produce eicosanoids independent of protein synthesis in RAW264.7 cells. J. Biol. Chem. 282, 22834 22847.
9. Buczynski M. W., Dumlao D. S. Dennis E. A. (2009) Thematic review series: proteomics. an integrated omics analysis of eicosanoid biology. J. Lipid Res. 50, 1015 1038.
10. Campos C. R., Ocheltree S. M., Hom S., Egleton R. D. Davis T. P. (2008) Nociceptive inhibition prevents inflammatory pain induced changes in the blood-brain barrier. Brain Res. 1221, 6 13.
11. Carlen P. L., Gurevich N., Wu P. H., Su W. G., Corey E. J. Pace-Asciak C. R. (1989) Actions of arachidonic acid and hepoxilin A3 on mammalian hippocampal CA1 neurons. Brain Res. 497, 171 176.
12. Chaplan S. R., Bach F. W., Pogrel J. W., Chung J. M. Yaksh T. L. (1994) Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 53, 55 63.
13. Coderre T. J., Gonzales R., Goldyne M. E., West J. Levine J. D. (1990) Noxious stimulus-induced increase in spinal prostaglandin E2 is noradrenergic terminal-dependent. Neurosci. Lett. 115, 253 258.
14. Cortes-Burgos L. A., Zweifel B. S., Settle S. L. et al. (2009) CJ-13610, an orally active inhibitor of 5-lipoxygenase is efficacious in preclinical models of pain. Eur. J. Pharmacol. 617, 59 67.
15. Deems R., Buczynski M. W., Bowers-Gentry R., Harkewicz R. Dennis E. A. (2007) Detection and quantitation of eicosanoids via high performance liquid chromatography-electrospray ionization-mass spectrometry. Methods Enzymol. 432, 59 82.
16. Deschamps J. D., Gautschi J. T., Whitman S., Johnson T. A., Gassner N. C., Crews P. Holman T. R. (2007) Discovery of platelet-type 12-human lipoxygenase selective inhibitors by high-throughput screening of structurally diverse libraries. Bioorg. Med. Chem. 15, 6900 6908.
17. Engblom D., Ek M., Saha S., Ericsson-Dahlstrand A., Jakobsson P. J. Blomqvist A. (2002) Prostaglandins as inflammatory messengers across the blood-brain barrier. J. Mol. Med. 80, 5 15.
18. Grubbs F. E. (1969) Procedures for detecting outlying observations in samples. Technometrics 11, 1.
19. Guay J., Bateman K., Gordon R., Mancini J. Riendeau D. (2004) Carrageenan-induced paw edema in rat elicits a predominant prostaglandin E2 (PGE2) response in the central nervous system associated with the induction of microsomal PGE2 synthase-1. J. Biol. Chem. 279, 24866 24872.
20. Hamberg M. Samuelsson B. (1971) On the metabolism of prostaglandins E 1 and E 2 in man. J. Biol. Chem. 246, 6713 6721.
21. Handley D. A., Cervoni P., McCray J. E. McCullough J. R. (1998) Preclinical enantioselective pharmacology of (R)- and (S)-ketorolac. J. Clin. Pharmacol. 38, 25S 35S.
22. Honore P., Buritova J. Besson J. M. (1996) The effects of morphine on carrageenin-induced spinal c-Fos expression are completely blocked by beta-funaltrexamine, a selective mu-opioid receptor antagonist. Brain Res. 732, 242 246.
23. Huber J. D., Campos C. R., Mark K. S. Davis T. P. (2006) Alterations in blood-brain barrier ICAM-1 expression and brain microglial activation after lambda-carrageenan-induced inflammatory pain. Am. J. Physiol. Heart. Circ. Physiol. 290, H732 H740.
24. Ibuki T., Matsumura K., Yamazaki Y., Nozaki T., Tanaka Y. Kobayashi S. (2003) Cyclooxygenase-2 is induced in the endothelial cells throughout the central nervous system during carrageenan-induced hind paw inflammation; its possible role in hyperalgesia. J. Neurochem. 86, 318 328.
25. Inceoglu B., Jinks S. L., Schmelzer K. R., Waite T., Kim I. H. Hammock B. D. (2006) Inhibition of soluble epoxide hydrolase reduces LPS-induced thermal hyperalgesia and mechanical allodynia in a rat model of inflammatory pain. Life Sci. 79, 2311 2319.
26. Inceoglu B., Jinks S. L., Ulu A. et al. (2008) Soluble epoxide hydrolase and epoxyeicosatrienoic acids modulate two distinct analgesic pathways. Proc. Natl Acad. Sci. USA 105, 18901 18906.
27. Jett M. F., Ramesha C. S., Brown C. D. et al. (1999) Characterization of the analgesic and anti-inflammatory activities of ketorolac and its enantiomers in the rat. J. Pharmacol. Exp. Ther. 288, 1288 1297.
28. Kenyon V., Chorny I., Carvajal W. J., Holman T. R. Jacobson M. P. (2006) Novel human lipoxygenase inhibitors discovered using virtual screening with homology models. J. Med. Chem. 49, 1356 1363.
29. Kim J. A., Gu J. L., Natarajan R., Berliner J. A. Nadler J. L. (1995) A leukocyte type of 12-lipoxygenase is expressed in human vascular and mononuclear cells. Evidence for upregulation by angiotensin II. Arterioscler. Thromb. Vasc. Biol. 15, 942 948.
30. van Leyen K., Arai K., Jin G., Kenyon V., Gerstner B., Rosenberg P. A., Holman T. R. Lo E. H. (2008) Novel lipoxygenase inhibitors as neuroprotective reagents. J. Neurosci. Res. 86, 904 909.
31. Liu Y., Zhang Y., Schmelzer K. et al. (2005) The antiinflammatory effect of laminar flow: the role of PPARgamma, epoxyeicosatrienoic acids, and soluble epoxide hydrolase. Proc. Natl Acad. Sci. USA 102, 16747 16752.
32. Loram L. C., Fuller A., Fick L. G., Cartmell T., Poole S. Mitchell D. (2007) Cytokine profiles during carrageenan-induced inflammatory hyperalgesia in rat muscle and hind paw. J. Pain 8, 127 136.
33. Lucas K. K., Svensson C. I., Hua X. Y., Yaksh T. L. Dennis E. A. (2005) Spinal phospholipase A2 in inflammatory hyperalgesia: role of group IVA cPLA2. Br. J. Pharmacol. 144, 940 952.
34. Malmberg A. B., Hamberger A. Hedner T. (1995) Effects of prostaglandin E2 and capsaicin on behavior and cerebrospinal fluid amino acid concentrations of unanesthetized rats: a microdialysis study. J. Neurochem. 65, 2185 2193.
35. Nie D., Tang K., Diglio C. Honn K. V. (2000) Eicosanoid regulation of angiogenesis: role of endothelial arachidonate 12-lipoxygenase. Blood 95, 2304 2311.
36. Oka Y., Ibuki T., Matsumura K., Namba M., Yamazaki Y., Poole S., Tanaka Y. Kobayashi S. (2007) Interleukin-6 is a candidate molecule that transmits inflammatory information to the CNS. Neuroscience 145, 530 538.
37. Pham-Marcou T. A., Beloeil H., Sun X., Gentili M., Yaici D., Benoit G., Benhamou D. Mazoit J. X. (2008) Antinociceptive effect of resveratrol in carrageenan-evoked hyperalgesia in rats: prolonged effect related to COX-2 expression impairment. Pain 140, 274 283.
38. Popp L., Haussler A., Olliges A., Nusing R., Narumiya S., Geisslinger G. Tegeder I. (2009) Comparison of nociceptive behavior in prostaglandin E, F, D, prostacyclin and thromboxane receptor knockout mice. Eur. J. Pain 13, 691 703.
39. Pulichino A. M., Rowland S., Wu T., Clark P., Xu D., Mathieu M. C., Riendeau D. Audoly L. P. (2006) Prostacyclin antagonism reduces pain and inflammation in rodent models of hyperalgesia and chronic arthritis. J. Pharmacol. Exp. Ther. 319, 1043 1050.
40. Quehenberger O., Armando A., Dumlao D., Stephens D. L. Dennis E. A. (2008) Lipidomics analysis of essential fatty acids in macrophages. Prostaglandins Leukot. Essent. Fatty Acids 79, 123 129.
41. Richardson J. D., Aanonsen L. Hargreaves K. M. (1998) Antihyperalgesic effects of spinal cannabinoids. Eur. J. Pharmacol. 345, 145 153.
42. Shi L., Smolders I., Umbrain V., Lauwers M. H., Sarre S., Michotte Y., Zizi M. Camu F. (2006) Peripheral inflammation modifies the effect of intrathecal IL-1beta on spinal PGE2 production mainly through cyclooxygenase-2 activity. A spinal microdialysis study in freely moving rats. Pain 120, 307 314.
43. Shin J., Cho H., Hwang S. W. et al. (2002) Bradykinin-12-lipoxygenase-VR1 signaling pathway for inflammatory hyperalgesia. Proc. Natl Acad. Sci. USA 99, 10150 10155.
44. Singh V. P., Patil C. S. Kulkarni S. K. (2005) Differential effect of zileuton, a 5-lipoxygenase inhibitor, against nociceptive paradigms in mice and rats. Pharmacol. Biochem. Behav. 81, 433 439.
45. Svensson C. I. Yaksh T. L. (2002) The spinal phospholipase- cyclooxygenase-prostanoid cascade in nociceptive processing. Annu. Rev. Pharmacol. Toxicol. 42, 553 583.
46. Svensson C. I., Hua X. Y., Protter A. A., Powell H. C. Yaksh T. L. (2003a) Spinal p38 MAP kinase is necessary for NMDA-induced spinal PGE(2) release and thermal hyperalgesia. Neuroreport 14, 1153 1157.
47. Svensson C. I., Marsala M., Westerlund A. et al. (2003b) Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing. J. Neurochem. 86, 1534 1544.
48. Svensson C. I., Hua X. Y., Powell H. C., Lai J., Porreca F. Yaksh T. L. (2005a) Prostaglandin E2 release evoked by intrathecal dynorphin is dependent on spinal p38 mitogen activated protein kinase. Neuropeptides 39, 485 494.
49. Svensson C. I., Lucas K. K., Hua X. Y., Powell H. C., Dennis E. A. Yaksh T. L. (2005b) Spinal phospholipase A2 in inflammatory hyperalgesia: role of the small, secretory phospholipase A2. Neuroscience 133, 543 553.
50. Telleria-Diaz A., Ebersberger A., Vasquez E., Schache F., Kahlenbach J. Schaible H. G. (2008) Different effects of spinally applied prostaglandin D(2) on responses of dorsal horn neurons with knee input in normal rats and in rats with acute knee inflammation. Neuroscience 156, 184 192.
51. Trang T., McNaull B., Quirion R. Jhamandas K. (2004) Involvement of spinal lipoxygenase metabolites in hyperalgesia and opioid tolerance. Eur. J. Pharmacol. 491, 21 30.
52. Tuboly G., Kekesi G., Nagy E., Benedek G. Horvath G. (2009) The antinociceptive interaction of anandamide and adenosine at the spinal level. Pharmacol. Biochem. Behav. 91, 374 379.
53. Yang L. C., Marsala M. Yaksh T. L. (1996a) Characterization of time course of spinal amino acids, citrulline and PGE2 release after carrageenankaolin-induced knee joint inflammation: a chronic microdialysis study. Pain 67, 345 354.
54. Yang L. C., Marsala M. Yaksh T. L. (1996b) Effect of spinal kainic acid receptor activation on spinal amino acid and prostaglandin E2 release in rat. Neuroscience 75, 453 461.
55. Yoo S., Han S., Park Y. S., Lee J. H., Oh U. Hwang S. W. (2009) Lipoxygenase inhibitors suppressed carrageenan-induced Fos-expression and inflammatory pain responses in the rat. Mol. Cells 27, 417 422.
56. Zarini S., Gijon M. A., Folco G. Murphy R. C. (2006) Effect of arachidonic acid reacylation on leukotriene biosynthesis in human neutrophils stimulated with granulocyte-macrophage colony-stimulating factor and formyl-methionyl-leucyl-phenylalanine. J. Biol. Chem. 281, 10134 10142.