Oxidation-sensitive nociception involved in endometriosis-associated pain

Pain

Volumn 156, Issue 3, 2015, Pages 528-539

  Ray, Kristeena ^a   Fahrmann, Johannes ^a   Mitchell, Brenda ^a   Paul, Dennis ^b   King, Holly ^a   Crain, Courtney ^a   Cook, Carla ^a   Golovko, Mikhail ^c   Brose, Stephen ^c   Golovko, Svetlana ^c   Santanam, Nalini ^a  

^a MARSHALL UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

Antioxidants; Inflammation; Oxidized lipoproteins; Peritoneal fluid

Indexed keywords

12 HYDROXYICOSATETRAENOIC ACID; 15 HYDROXYICOSATETRAENOIC ACID; 15 HYDROXYPROSTAGLANDIN DEHYDROGENASE; 5 HYDROXYICOSATETRAENOIC ACID; ACETYLCYSTEINE; ALPHA TOCOPHEROL; INDOMETACIN; LIPOPROTEIN; LIPOXYGENASE; LOW DENSITY LIPOPROTEIN; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE; 8-EPI-PROSTAGLANDIN F2ALPHA; ANTIOXIDANT; NONSTEROID ANTIINFLAMMATORY AGENT; PEROXIDE; PROSTAGLANDIN F2 ALPHA; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOMETRIOSIS; ENDOMETRIUM CELL; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INDUCED HYPOTHERMIA; INFLAMMATION; LIQUID CHROMATOGRAPHY; MOUSE; NOCICEPTION; NONHUMAN; OXIDATION; PELVIS PAIN SYNDROME; PERITONEAL FLUID; PRIORITY JOURNAL; RAT; RESPONSE TIME; TANDEM MASS SPECTROMETRY; UPREGULATION; ADOLESCENT; ANALOGS AND DERIVATIVES; ANALYSIS OF VARIANCE; ANIMAL; ASCITES FLUID; BODY TEMPERATURE; COMPLICATION; DRUG EFFECTS; METABOLISM; MIDDLE AGED; PAIN MEASUREMENT; PELVIC PAIN; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME FACTOR; YOUNG ADULT;

ADOLESCENT; ADULT; ANALYSIS OF VARIANCE; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIOXIDANTS; ASCITIC FLUID; BODY TEMPERATURE; DINOPROST; DINOPROSTONE; ENDOMETRIOSIS; FEMALE; HUMANS; INDOMETHACIN; LIPOPROTEINS, LDL; LIPOXYGENASE; MICE; MIDDLE AGED; NOCICEPTION; PAIN MEASUREMENT; PELVIC PAIN; PEROXIDES; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RATS; RATS, SPRAGUE-DAWLEY; TANDEM MASS SPECTROMETRY; THIOBARBITURIC ACID REACTIVE SUBSTANCES; TIME FACTORS; VITAMIN E; YOUNG ADULT;

EID: 84964603410     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1097/01.j.pain.0000460321.72396.88     Document Type: Article

References (84)

1. Aley KO, McCarter G, Levine JD. Nitric oxide signaling in pain and nociceptor sensitization in the rat. J Neurosci 1998;18:7008-14.
2. Allen C, Hopewell S, Prentice A, Gregory D. Nonsteroidal antiinflammatory drugs for pain in women with endometriosis. Cochrane Database Syst Rev 2009:2:CD004753.
3. Arrio B, Bonnefont-Rousselot D, Catudioc JD, Packer L. Electrophoretic mobility changes of oxidized human low density lipoprotein measured by laser Doppler electrophoresis. Biochem Mol Biol Int 1993;30:1101-14.
4. Augoulea A, Alexandrou A, Creatsa M, Vrachnis N, Lambrinoudaki I. Pathogenesis of endometriosis: The role of genetics, inflammation and oxidative stress. Arch Gynecol Obstet 2012;286:99-103.
5. Barcz E, Kaminski P, Marianowski L. Role of cytokines in pathogenesis of endometriosis. Med Sci Monit 2000;6:1042-6.
6. Bedaiwy MA, Falcone T. Peritoneal fluid environment in endometriosis. Clinicopathological implications. Minerva Ginecol 2003;55:333-45.
7. Brose SA, Baker AG, Golovko MY. A fast one-step extraction and UPLCMS/MS analysis for E2/D 2 series prostaglandins and isoprostanes. Lipids 2013;48:411-19.
8. Brose SA, Golovko MY. A rapid oxygen exchange on prostaglandins in plasma represents plasma esterase activity that is inhibited by diethylumbelliferyl phosphate with high affinity. Rapid Comm Mass Spectrom 2012;26:2472-6.
9. Brose SA, Golovko MY. Eicosanoid post-mortem induction in kidney tissue is prevented by microwave irradiation. Prostaglandins Leukot Essent Fatty Acids 2013;89:313-18.
10. Brose SA, Thuen BT, Golovko MY. LC/MS/MS method for analysis of E(2) series prostaglandins and isoprostanes. J Lipid Res 2011;52:850-9.
11. BuchweitzO, Staebler A,WulfingP,HauzmanE, GrebR, Kiesel L. COX-2 overexpression in peritoneal lesions is correlated with nonmenstrual chronic pelvic pain. Eur J Obstet Gynecol Reprod Biol 2006;124: 216-21.
12. Burney RO, Giudice LC. Pathogenesis and pathophysiology of endometriosis. Fertil Steril 2012;98:511-19.
13. Cameron NE, Jack AM, Cotter MA. Effect of alpha-lipoic acid on vascular responses and nociception in diabetic rats. Free Radic BiolMed 2001;31: 125-35.
14. Carvalho LF, Samadder AN, Agarwal A, Fernandes LF, Abrao MS. Oxidative stress biomarkers in patients with endometriosis: systematic review. Arch Gynecol Obstet 2012;286:1033-40.
15. Castelbaum AJ, Ying L, Somkuti SG, Sun J, Ilesanmi AO, Lessey BA. Characterization of integrin expression in a well differentiated endometrial adenocarcinomacell line (Ishikawa). JClin EndocrinolMetab 1997;82:136-42.
16. Chi CH, ShieshSC, Lin XZ. Total antioxidant capacity and malondialdehyde in acute abdominal pain. Am J Emerg Med 2002;20:79-82.
17. Chung BH, Wilkinson T, Geer JC, Segrest JP. Preparative and quantitative isolation of plasma lipoproteins: rapid, single discontinuous density gradient ultracentrifugation in a vertical rotor. J Lipid Res 1980;21: 284-91.
18. Defrere S,Gonzalez-Ramos R, Lousse JC, Colette S,DonnezO,Donnez J, Van Langendonckt A. Insights into iron and nuclear factor-kappa B (NFkappaB) involvement in chronic inflammatory processes in peritoneal endometriosis. Histol Histopathol 2011;26:1083-92.
19. Deguara CS, Pepas L, Davis C. Does minimally invasive surgery for endometriosis improve pelvic symptoms and quality of life? Curr Opin Obstet Gynecol 2012;24:241-4.
20. Dib-Hajj SD, Cummins TR, Black JA, Waxman SG. Sodium channels in normal and pathological pain. Annu Rev Neurosci 2010;33:325-47.
21. Durand T, Bultel-Ponce V, Guy A, Berger S,Mueller MJ, Galano JM. New bioactive oxylipins formed by non-enzymatic free-radical-catalyzed pathways: The phytoprostanes. Lipids 2009;44:875-88.
22. Efstathiou JA,SampsonDA, Levine Z,RohanRM, ZurakowskiD, Folkman J, D'Amato RJ, RupnickMA. Nonsteroidal antiinflammatory drugs differentially suppress endometriosis in a murine model. Fertil Steril 2005;83:171-81.
23. Furuya K, Murakami M, Makimura N, Matsuda H, Ikou K, Saito K, Kawakami Y, Shibazaki T, Fukui U, Mizumoto Y, Tokuoka S, Nagata I, Kikuchi Y. Immunological and endocrinological studies on lymphocyte subpopulation and medical treatment for infertility in patients with endometriosis. Mol Cell Endocrinol 2003;202:195-9.
24. Golovko MY, Murphy EJ. An improved LC-MS/MS procedure for brain prostanoid analysis using brain fixation with head-focused microwave irradiation and liquid-liquid extraction. J Lipid Res 2008;49:893-902.
25. Goteri G, Lucarini G, Pieramici T, Filosa A, Pugnaloni A,Montik N, Biagini G, Tranquilli AL, Fabris G, Ciavattini A, Lo Muzio L. Endothelial cell survivin is involved in the growth of ovarian endometriotic cysts. Anticancer Res 2005; 25:4313-18.
26. Gould HJ III, England JD, Soignier RD, Nolan P, Minor LD, Liu ZP, Levinson SR, Paul D. Ibuprofen blocks changes in Na v 1.7 and 1.8 sodium channels associated with complete Freund's adjuvant-induced inflammation in rat. J Pain 2004;5:270-80.
27. Haley TJ, McCormick WG. Pharmacological effects produced by intracerebral injection of drugs in the conscious mouse. Br J Pharmacol Chemother 1957;12:12-15.
28. Hargreaves K, Dubner R, Brown F, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. PAIN 1988;32:77-88.
29. Kashanian M, Lakeh MM, Ghasemi A, Noori S. Evaluation of the effect of vitamin E on pelvic pain reduction in women suffering from primary dysmenorrhea. J Reprod Med 2013;58:34-8.
30. Koga K, Osuga Y, Takemura Y, Takamura M, Taketani Y. Recurrence of endometrioma after laparoscopic excision and its prevention by medical management. Front Biosci (Elite Ed) 2013;5:676-83.
31. Koga K,Osuga Y, Tsutsumi O,Okagaki R,MomoedaM, Yano T, Fujiwara T, Takai Y, Kugu K, Morita Y, Taketani Y. Increased concentrations of soluble tumour necrosis factor receptor (sTNFR) I and II in peritoneal fluid from women with endometriosis. Mol Hum Reprod 2000;6:929-33.
32. Komiyama SI, Aoki D, Katsuki Y, Nozawa S. Proliferative activity of early ovarian clear cell adenocarcinoma depends on association with endometriosis. Eur J Obstet Gynecol Reprod Biol 2006;127:130-36.
33. Kozak W, Fraifeld V. Non-prostaglandin eicosanoids in fever and anapyrexia. Front Biosci 2004;9:3339-55.
34. KyamaCM,MihalyiA, SimsaP, FalconerH, Fulop V,Mwenda JM, PeeraerK, Tomassetti C, Meuleman C, D'Hooghe TM. Role of cytokines in the endometrial-peritoneal cross-talk and development of endometriosis. Front Biosci (Elite Ed) 2009;1:444-54.
35. Lessey BA, Ilesanmi AO, Castelbaum AJ, Yuan L, Somkuti SG, Chwalisz K, Satyaswaroop PG. Characterization of the functional progesterone receptor in an endometrial adenocarcinoma cell line (Ishikawa): progesterone-induced expression of the alpha1 integrin. J Steroid Biochem Mol Biol 1996;59:31-9.
36. Lousse JC, Defrere S, Colette S, Van Langendonckt A, Donnez J. Expression of eicosanoid biosynthetic and catabolic enzymes in peritoneal endometriosis. Hum Reprod 2010;25:734-41.
37. Lousse JC, Van Langendonckt A, Defrere S, Ramos RG, Colette S, Donnez J. Peritoneal endometriosis is an inflammatory disease. Front Biosci (Elite Ed) 2012;4:23-40.
38. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biological, Chemistry 1951;193: 265-75.
39. Machado DE, Berardo PT, Landgraf RG, Fernandes PD, Palmero C, Alves LM, Abrao MS, Nasciutti LE. A selective cyclooxygenase-2 inhibitor suppresses the growth of endometriosis with an antiangiogenic effect in a rat model. Fertil Steril 2010;93:2674-9.
40. Matsuzaki S. DNA microarray analysis in endometriosis for development of more effective targeted therapies. Front Biosci (Elite Ed) 2011;3: 1139-53.
41. Matsuzaki S, Canis M, Pouly JL, Botchorishvili R, Dechelotte PJ,Mage G. Both GnRH agonist and continuous oral progestin treatments reduce the expression of the tyrosine kinase receptor B and mu-opioid receptor in deep infiltrating endometriosis. Hum Reprod 2007;22:124-8.
42. Matsuzaki S,Canis M, Vaurs-Barriere C,Boespflug-Tanguy O,Dastugue B, Mage G. DNA microarray analysis of gene expression in eutopic endometrium from patients with deep endometriosis using laser capture microdissection. Fertil Steril 2005;84(suppl 2):1180-90.
43. Milingos S, Protopapas A, Kallipolitis G, Drakakis P, Loutradis D, Liapi A, Antsaklis A. Endometriosis in patients with chronic pelvic pain: is staging predictive of the efficacy of laparoscopic surgery in pain relief? Gynecol Obstet Invest 2006;62:48-54.
44. Monroy M, Kuluz JW, He D, Dietrich WD, Schleien CL. Role of nitric oxide in the cerebrovascular and thermoregulatory response to interleukin-1 beta. Am J Physiol Heart Circ Physiol 2001;280:H1448-1453.
45. Morimoto A, Long NC, Nakamori T, Murakami N. The effect of prostaglandin E2 on the body temperature of restrained rats. Physiol Behav 1991;50:249-53.
46. Murphy AA, Santanam N, Morales AJ, Parthasarathy S. Lysophosphatidyl choline, a chemotactic factor for monocytes/T-lymphocytes is elevated in endometriosis. J Clin Endocrinol Metab 1998;83: 2110-13.
47. Murphy AA, Santanam N, Parthasarathy S. Endometriosis: A disease of oxidative stress? Semin Reprod Endocrinol 1998;16:263-73.
48. Oka T. Prostaglandin E2 as a mediator of fever: The role of prostaglandin E (EP) receptors. Front Biosci 2004;9:3046-57.
49. Ozgocmen S, Ozyurt H, Sogut S, Akyol O. Current concepts in the pathophysiology of fibromyalgia: The potential role of oxidative stress and nitric oxide. Rheumatol Int 2006;26:585-97.
50. Parazzini F, Vigano P, Candiani M, Fedele L. Diet and endometriosis risk: A literature review. Reprod Biomed Online 2013;26:323-36.
51. Parthasarathy S, Auge N, Santanam N. Implications of lag time concept in the oxidation of LDL. Free Radic Res 1998;28:583-91.
52. Parthasarathy S, Raghavamenon A, Garelnabi MO, Santanam N. Oxidized low-density lipoprotein. Methods Mol Biol 2010;610:403-17.
53. Parthasarathy S, Santanam N, Auge N. Oxidized low-density lipoprotein, a two-faced Janus in coronary artery disease? Biochem Pharmacol 1998; 56:279-84.
54. Parthasarathy S, Santanam N, Ramachandran S, Meilhac O. Potential role of oxidized lipids and lipoproteins in antioxidant defense. Free Radic Res 2000;33:197-215.
55. Patwardhan AM, Akopian AN, Ruparel NB, Diogenes A, Weintraub ST, Uhlson C, Murphy RC, Hargreaves KM. Heat generates oxidized linoleic acid metabolites that activate TRPV1 and produce pain in rodents. J Clin Invest 2010;120:1617-26.
56. Petho G, Reeh PW. Sensory and signaling mechanisms of bradykinin, eicosanoids, platelet-activating factor, and nitric oxide in peripheral nociceptors. Physiol Rev 2012;92:1699-775.
57. Pittaluga E, Costa G, Krasnowska E, Brunelli R, Lundeberg T, PorporaMG, Santucci D, Parasassi T. More than antioxidant: N-acetyl-L-cysteine in a murine model of endometriosis. Fertil Steril 2010;94:2905-08.
58. Polak G, Barczynski B, Kwasniewski W, Bednarek W, Wertel I, Derewianka-Polak M, Kotarski J. Low-density lipoproteins oxidation and endometriosis. Mediators Inflamm 2013;2013:624540.
59. Polak G, Wertel I, Barczynski B, Kwasniewski W, BednarekW, Kotarski J. Increased levels of oxidative stress markers in the peritoneal fluid of women with endometriosis. Eur J Obstet Gynecol Reprod Biol 2013;168: 187-90.
60. Porpora MG, Brunelli R, Costa G, Imperiale L, Krasnowska EK, Lundeberg T, Nofroni I, Piccioni MG, Pittaluga E, Ticino A, Parasassi T. A promise in the treatment of endometriosis: an observational cohort study on ovarian endometrioma reduction by N-acetylcysteine. Evid Based Complementary Alternative Med 2013;2013:240702.
61. Practice Committee of the American Society for Reproductive M. Treatment of pelvic pain associated with endometriosis: A committee opinion. Fertil Steril 2014;101:927-35.
62. Proudfoot JM, Beilin LJ, Croft KD. PGF2-isoprostanes formed during copper-induced oxidation of low-density lipoproteins are the prostaglandins that cross-react with PGE2 antibodies. Biochem Biophys Res Commun 1995;206:455-61.
63. Ray KL, Mitchell BL, Santanam N. Power over pain: A brief review of current and novel interventions for endometriosis-associated pain. J Endometriosis Pelvic Pain Disord 2014;6:doi: 10.5301/je.5000199.
64. Rokyta R, Holecek V, Pekarkova I, Krejcova J, Racek J, Trefil L, Yamamotova A. Free radicals after painful stimulation are influenced by antioxidants and analgesics. Neuro Endocrinol Lett 2003;24:304-9.
65. Romanovsky AA, Simons CT, Szekely M, Kulchitsky VA. The vagus nerve in the thermoregulatory response to systemic inflammation. Am J Physiol 1997;273:R407-413.
66. Sacco K, Portelli M, Pollacco J, Schembri-Wismayer P, Calleja-Agius J. The role of prostaglandin E2 in endometriosis. Gynecol Endocrinol 2012; 28:134-8.
67. Santanam N, Kavtaradze N, Murphy A, Dominguez C, Parthasarathy S. Antioxidant supplementation reduces endometriosis-related pelvic pain in humans. Transl Res 2013;161:189-95.
68. Santanam N, Murphy AA, Parthasarathy S. Macrophages, oxidation, and endometriosis. Ann N Y Acad Sci 2002;955:183-98; Discussion 119-200, 396-406.
69. Santanam N, Song M, Rong R, Murphy AA, Parthasarathy S. Atherosclerosis, oxidation and endometriosis. Free Radic Res 2002;36: 1315-21.
70. Shahed AR, Shoskes DA. Oxidative stress in prostatic fluid of patients with chronic pelvic pain syndrome: correlation with gram positive bacterial growth and treatment response. J Androl 2000;21:669-75.
71. Sinzinger H, Lupattelli G, Chehne F, Oguogho A, Furberg CD. Isoprostane 8-epi-PGF2alpha is frequently increased in patients with muscle pain and/or CK-elevation after HMG-Co-enzyme-A-reductase inhibitor therapy. J Clin Pharm Ther 2001;26:303-10.
72. Smith HS. Arachidonic acid pathways in nociception. J Support Oncol 2006;4:277-87.
73. Stratton P, Berkley KJ. Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications. Hum Reprod Update 2011;17:327-46.
74. Stratton P, Sinaii N, Segars J, Koziol D, Wesley R, Zimmer C, Winkel C, Nieman LK. Return of chronic pelvic pain from endometriosis after raloxifene treatment: A randomized controlled trial. Obstet Gynecol 2008; 111:88-96.
75. Streuli I, de Ziegler D, Santulli P, Marcellin L, Borghese B, Batteux F, Chapron C. An update on the pharmacological management of endometriosis. Expert Opin Pharmacother 2013;14:291-305.
76. SugiharaK,Kobayashi Y,Suzuki A, Tamura N,Motamedchaboki K, HuangCT, Akama TO, Pecotte J, Frost P, Bauer C, Jimenez JB Jr, Nakayama J, Aoki D, Fukuda MN. Development of pro-apoptotic peptides as potential therapy for peritoneal endometriosis. Nat Commun 2014;5:4478.
77. Taylor RN, Hummelshoj L, Stratton P, Vercellini P. Pain and endometriosis: Etiology, impact, and therapeutics. Middle East Fertil Soc J 2012;17:221-5.
78. Trabert B, Peters U, De Roos AJ, Scholes D, Holt VL. Diet and risk of endometriosis in a population-based case-control study. Br J Nutr 2011; 105:459-67.
79. Turgut A, Ozler A, Goruk NY, Tunc SY, Evliyaoglu O, Gul T. Copper, ceruloplasmin and oxidative stress in patients with advanced-stage endometriosis. Eur Rev Med Pharmacol Sci 2013;17:1472-8.
80. Vardeh D, Wang D, Costigan M, Lazarus M, Saper CB, Woolf CJ, Fitzgerald GA, Samad TA. COX2 in CNS neural cells mediates mechanical inflammatory pain hypersensitivity in mice. J Clin Invest 2009;119:287-94.
81. Wang ZQ, Porreca F, Cuzzocrea S, Galen K, Lightfoot R, Masini E, Muscoli C, Mollace V, Ndengele M, Ischiropoulos H, Salvemini D. A newly identified role for superoxide in inflammatory pain. J Pharmacol Exp Ther 2004;309:869-78.
82. Wu MH, Lu CW, Chuang PC, Tsai SJ. Prostaglandin E2: The master of endometriosis? Exp Biol Med (Maywood) 2010;235:668-77.
83. Yagi K. Simple assay for the level of total lipid peroxides in serum or plasma. Methods Mol Biol 1998;108:101-6.
84. Zeilhofer HU. Prostanoids in nociception and pain. Biochem Pharmacol 2007;73:165-74.