Increasing 2-arachidonoyl glycerol signaling in the periphery attenuates mechanical hyperalgesia in a model of bone cancer pain

Pharmacological Research

Volumn 64, Issue 1, 2011, Pages 60-67

  Khasabova, Iryna A ^a   Chandiramani, Anisha ^b   Harding Rose, Catherine ^a   Simone, Donald A ^a   Seybold, Virginia S ^c  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

2 arachidonoyl glycerol; Cancer; Cannabinoid receptor; Endocannabinoid; Monoglycerol lipase; Pain

Indexed keywords

2 ARACHIDONOYLGLYCEROL; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; JZL 184; MORPHINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE CANCER; BONE PAIN; CANCER PAIN; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG SELECTIVITY; HYPERALGESIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION;

ANIMALS; ARACHIDONIC ACIDS; BENZODIOXOLES; BONE NEOPLASMS; CALCANEUS; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBROSARCOMA; GANGLIA, SPINAL; GLYCERIDES; HYPERALGESIA; MALE; MICE; MICE, INBRED C3H; MONOACYLGLYCEROL LIPASES; PIPERIDINES; POLYUNSATURATED ALKAMIDES; RECEPTOR, CANNABINOID, CB2; RECEPTORS, CANNABINOID; SIGNAL TRANSDUCTION; SKIN; TIBIAL NERVE;

EID: 79957687799     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2011.03.007     Document Type: Article

References (55)

1. Coleman RE. Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin Cancer Res 2006;12:6243s-9s.
2. Cherny NI, Portenoy RK. Cancer pain management. Current strategy. Cancer 1993;72:3393-415.
3. Clapper JR, Moreno-Sanz G, Russo R, Guijarro A, Vacondio F, Duranti A, et al. Anandamide suppresses pain initiation through a peripheral endocannabinoid mechanism. Nat Neurosci 2010;13:1265-70.
4. Guindon J, Beaulieu P. The role of the endogenous cannabinoid system in peripheral analgesia. Curr Mol Pharmacol 2009;2:134-9.
5. Sagar DR,GawAG, Okine BN,WoodhamsSG,WongA, Kendall DA, et al. Dynamic regulation of the endocannabinoid system: implications for analgesia. Mol Pain 2009;8:5-59.
6. Bisogno T, Howell F, Williams G,Minassi A, Cascio MG, Ligresti A, et al. Cloning of the first sn1-DAG lipases points to the spatial and temporal regulation of endocannabinoid signaling in the brain. J Cell Biol 2003;163:463-8. (Pubitemid 37429860)
7. Dinh TP, Carpenter D, Leslie FM, Freund TF, Katona I, Sensi SL, et al. Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci USA 2002;99:10819-24.
8. Stella N, Schweitzer P, Piomelli D. A second endogenous cannabinoid that modulates long-term potentiation. Nature 1997;388:773-8. (Pubitemid 27375156)
9. Blankman JL, Simon GM, Cravatt BF. A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem Biol 2007;14:1347-56. (Pubitemid 350257008)
10. Marrs WR, Blankman JL, Horne EA, Thomazeau A, Lin YH, Coy J, et al. The serine hydrolase ABHD6 controls the accumulation and efficacy of 2-AG at cannabinoid receptors. Nat Neurosci 2010;13:951-7.
11. Maione S,DePetrocellis L, de Novellis V, Moriello AS, Petrosino S, Palazzo E, et al. Analgesic actions of N-arachidonoyl-serotonin, a fatty acid amide hydrolase inhibitor with antagonistic activity at vanilloid TRPV1 receptors. Br J Pharmacol 2007;150:766-81. (Pubitemid 46440215)
12. Sugiura T, Kishimoto S, Oka S, Gokoh M. Biochemistry, pharmacology and physiology of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand. Prog Lipid Res 2006;45:405-46.
13. Guindon J, Desroches J, Beaulieu P. The antinociceptive effects of intraplantar injections of 2-arachidonoyl glycerol are mediated by cannabinoid CB2 receptors. Br J Pharmacol 2007;150:693-701. (Pubitemid 46440208)
14. Mecs L, Tuboly G, Toth K, Nagy E, Nyari T, Benedek G, et al. Peripheral antinociceptive effect of 2-arachidonoyl-glycerol and its interaction with endomorphin-1 in arthritic rat ankle joints. Clin Exp Pharmacol Physiol 2010;37:544-50.
15. Desroches J, Guindon J, Lambert C, Beaulieu P. Modulation of the antinociceptive effects of 2-arachidonoyl glycerol by peripherally administered FAAH and MGL inhibitors in a neuropathic pain model. Br J Pharmacol 2008;155:913-24.
16. Hohmann AG, Suplita RL, Bolton NM, Neely MH, Fegley D, Mangieri R, et al. An endocannabinoid mechanism for stress-induced analgesia. Nature 2005;435:1108-12. (Pubitemid 40910518)
17. King AR, Duranti A, Tontini A, Rivara S, Rosengarth A, Clapper JR, et al. URB602 inhibits monoacylglycerol lipase and selectively blocks 2-arachidonoylglycerol degradation in intact brain slices. Chem Biol 2007;14:1357-65. (Pubitemid 350257009)
18. Vandevoorde S, Jonsson KO, Labar G, Persson E, Lambert DM, Fowler CJ. Lack of selectivity of URB602 for 2-oleoylglycerol compared to anandamide hydrolysis in vitro. Br J Pharmacol 2007;150:186-91. (Pubitemid 46160608)
19. Long JZ, Li W, Booker L, Burston JJ, Kinsey SG, Schlosburg JE, et al. Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat Chem Biol 2009;5:37-44.
20. Schlosburg JE, Blankman JL, Long JZ, Nomura DK, Pan B, Kinsey SG, et al. Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system. Nat Neurosci 2010;13:1113-9.
21. Wacnik PW, Eikmeier LJ, Ruggles TR, Ramnaraine ML, Walcheck BK, Beitz AJ, et al. Functional interactions between tumor and peripheral nerve: morphology, algogen identification, and behavioral characterization of a new murine model of cancer pain. J Neurosci 2001;21:9355-66. (Pubitemid 33096879)
22. El Mouedden M, Meert TF. Evaluation of pain-related behavior, bone destruction and effectiveness of fentanyl, sufentanil, and morphine in amurine model of cancer pain. Pharmacol Biochem Behav 2005;82:109-19. (Pubitemid 41423493)
23. Hamamoto DT, Giridharagopalan S, Simone DA. Acute and chronic administration of the cannabinoid receptor agonist CP 55,940 attenuates tumor-evoked hyperalgesia. Eur J Pharmacol 2007;558:73-87. (Pubitemid 46328873)
24. Kehl LJ, Hamamoto DT, Wacnik PW, Croft DL, Norsted BD, Wilcox GL, et al. A cannabinoid agonist differentially attenuates deep tissue hyperalgesia in animal models of cancer and inflammatory muscle pain. Pain 2003;103:175-86. (Pubitemid 36579097)
25. Potenzieri C, Harding-Rose C, Simone DA. The cannabinoid receptor agonist, WIN 55, 212-2, attenuates tumor-evoked hyperalgesia through peripheral mechanisms. Brain Res 2008;1215:69-75.
26. Khasabova IA, Khasabov SG, Harding-Rose C, Coicou LG, Seybold BA, Lindberg AE, et al. A decrease in anandamide signaling contributes to the maintenance of cutaneous mechanical hyperalgesia in a model of bone cancer pain. J Neurosci 2008;28:11141-52.
27. Backonja MM, Stacey B. Neuropathic pain symptoms relative to overall pain rating. J Pain 2004;5:491-7. (Pubitemid 39535205)
28. Lan R, Gatley J, Lu Q, Fan P, Fernando SR, Volkow ND, et al. Design and synthesis of the CB1 selective cannabinoid antagonist AM281: a potential human SPECT ligand. AAPS Pharm Sci 1999;1:E4.
29. Ross RA, Brockie HC, Stevenson LA, Murphy VL, Templeton F, Makriyannis A, et al. Agonist-inverse agonist characterization at CB1 and CB2 cannabinoid receptors of L759633, L759656, and AM630. Br J Pharmacol 1999;126:665-72. (Pubitemid 29087845)
30. Khasabova IA, Gielissen J, Chandiramani A, Harding-Rose C,AbuOdehD, Simone DA, et al. CB1 and CB2 receptor agonists promote analgesia through synergy in a murine model of tumor pain. Behav Pharm, in press.
31. Calignano A, La Rana G, Giuffrida A, Piomelli D. Control of pain initiation by endogenous cannabinoids. Nature 1998;394:277-81. (Pubitemid 28335039)
32. Beaulieu P, Bisogno T, Punwar S, Farquhar-Smith WP, Ambrosino G, Di Marzo V, et al. Role of the endogenous cannabinoid system in the formalin test of persistent pain in the rat. Eur J Pharmacol 2000;396:85-92. (Pubitemid 30265563)
33. Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin CE, Brenner GJ, et al. Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptor. Nat Neurosci 2007;10:870-9. (Pubitemid 47013432)
34. van den Beuken-van Everdingen MH, de Rijke JM, Kessels AG, Schouten HC, van Kleef M, Patijn J. High prevalence of pain in patients with cancer in a large population-based study in The Netherlands. Pain 2007;132:312-20. (Pubitemid 350051568)
35. Sugiura T, Kondo S, Sukagawa A, Nakane S, Shinoda A, Itoh K, et al. 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 1995;215:89-97.
36. Kinsey SG, Long JZ, Cravatt BF, Lichtman AH. Fatty acid amide hydrolase and monoacylglycerol lipase inhibitors produce anti-allodynic effects in mice through distinct cannabinoid receptor mechanisms. J Pain 2010;11:1420-8.
37. Honore P, Rogers SD, Schwei MJ, Salak-Johnson JL, Luger NM, Sabino MC, et al. Murine models of inflammatory, neuropathic and cancer pain each generates a unique set of neurochemical changes in the spinal cord and sensory neurons. Neuroscience 2000;98:585-98. (Pubitemid 30408178)
38. Khasabova IA, Stucky CL, Harding-Rose C, Eikmeier L, Beitz AJ, Coicou LG, et al. Chemical interactions between fibrosarcoma cancer cells and sensory neurons contribute to cancer pain. J Neurosci 2007;27:10289-98. (Pubitemid 47450473)
39. Chizhmakov I, Mamenko N, Volkova T, Khasabova I, Simone DA, Krishtal O. P2X receptors in sensory neurons co-cultured with cancer cells exhibit a decrease in opioid sensitivity. Eur J Neurosci 2009;29:76-86.
40. Schweizerhof M, Stösser S, Kurejova M, Njoo C, Gangadharan V, Agarwal N, et al. Hematopoietic colony-stimulating factors mediate tumor-nerve interactions and bone cancer pain. Nat Med 2009;15:802-7.
41. Oka S, Wakui J, Ikeda S, Yanagimoto S, Kishimoto S, Gokoh M, et al. Involvement of the cannabinoid CB2 receptor and its endogenous ligand 2-arachidonoylglycerol in oxazolone-induced contact dermatitis in mice. J Immunol 2006;177:8796-805. (Pubitemid 44893846)
42. Moody JS, Kozak KR, Ji C, Marnett LJ. Selective oxygenation of the endocannabinoid 2-arachidonylglycerol by leukocyte-type 12-lipoxygenase. Biochemistry 2001;40:861-6.
43. Kozak KR, Gupta RA, Moody JS, Ji C, Boeglin WE, DuBois RN, et al. 15-Lipoxygenase metabolism of 2-arachidonylglycerol. Generation of a peroxisome proliferator-activated receptor alpha agonist. J Biol Chem 2002;277:23278-86. (Pubitemid 34952156)
44. NomuraDK, Long JZ, Niessen S, Hoover HS,NgSW, Cravatt BF. Monoacylglycerol lipase regulates a fatty acid network that promotes cancer pathogenesis. Cell 2010;140:49-61.
45. Kinsey SG, Long JZ, O'Neal ST, Abdullah RA, Poklis JL, Boger DL, et al. Blockade of endocannabinoid-degrading enzymes attenuates neuropathic pain. J Pharmacol Exp Ther 2009;330:902-10.
46. Spradley JM, Guindon J, Hohmann AG. Inhibitors of monoacylglycerol lipase, fatty-acid amide hydrolase and endocannabinoid transport differentially suppress capsaicin-induced behavioral sensitization through peripheral endocannabinoid mechanisms. Pharmacol Res 2010;62:249-58.
47. Casanova ML, Blázquez C, Martínez-Palacio J, Villanueva C, Fernández-Aceñero MJ, Huffman JW, et al. Inhibition of skin tumor growth and angiogenesis in vivo by activation of cannabinoid receptors. J Clin Invest 2003;111:43-50. (Pubitemid 36134847)
48. Ibrahim MM, Porreca F, Lai J, Albrecht PJ, Rice FL, Khodorova A, et al. CB2 cannabinoid receptor activation produces antinociception by stimulating peripheral release of endogenous opioids. Proc Natl Acad Sci USA 2005;102:3093-8. (Pubitemid 40299921)
49. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993;365:61-5. (Pubitemid 23305569)
50. Klein TW, Newton C, Larsen K, Lu L, Perkins I, Nong L, et al. The cannabinoid system and immune modulation. J Leukoc Biol 2003;74:486-96. (Pubitemid 38040375)
51. Anand U, Otto WR, Sanchez-Herrera D, Facer P, Yiangou Y, Korchev Y, et al. Cannabinoid receptor CB2 localisation and agonist-mediated inhibition of capsaicin responses in human sensory neurons. Pain 2008;138:667-80.
52. Wotherspoon G, Fox A, McIntyre P, Colley S, Bevan S, Winter J. Peripheral nerve injury induces cannabinoid receptor 2 protein expression in rat sensory neurons. Neuroscience 2005;135:235-45. (Pubitemid 41219752)
53. Cain DM,Wacnik PW, Turner M, Wendelschafer-Crabb G, Kennedy WR,Wilcox GL, et al. Functional interactions between tumor and peripheral nerve: changes in excitability and morphology of primary afferent fibers in a murine model of cancer pain. J Neurosci 2001;21:9367-76. (Pubitemid 33096880)
54. Fujita M, Andoh T, Sasaki A, Saiki I, Kuraishi Y. Involvement of peripheral adenosine 5′-triphosphate and P2X purinoceptor in pain-related behavior produced by orthotopic melanoma inoculation in mice. Eur J Neurosci 2010;31:1629-36.
55. Gilchrist LS, Cain DM, Harding-Rose C, Kov AN, Wendelschafer-Crabb G, Kennedy WR, et al. Re-organization of P2X3 receptor localization on epidermal nerve fibers in a murine model of cancer pain. Brain Res 2005;1044:197-205. (Pubitemid 40693452)