Table of Contents Author Guidelines Submit a Manuscript
BioMed Research International
Volume 2014, Article ID 686908, 12 pages
http://dx.doi.org/10.1155/2014/686908
Research Article

Alterations in the Anandamide Metabolism in the Development of Neuropathic Pain

Laboratory of Pain Pathophysiology, Department of Pain Pharmacology, Institute of Pharmacology, Polish Academy of Sciences, Smetna Street 12, 31-343 Krakow, Poland

Received 28 May 2014; Revised 4 July 2014; Accepted 6 July 2014; Published 2 September 2014

Academic Editor: Livio Luongo

Copyright © 2014 Natalia Malek et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. Z. Ali, S. N. Raja, U. Wesselmann, P. N. Fuchs, R. A. Meyer, and J. N. Campbell, “Intradermal injection of norepinephrine evokes pain in patients with sympathetically maintained pain,” Pain, vol. 88, no. 2, pp. 161–168, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. M. A. Rogawski and W. Löscher, “The neurobiology of antiepileptic drugs for the treatment of nonepileptic conditions,” Nature Medicine, vol. 10, no. 7, pp. 685–692, 2004. View at Publisher · View at Google Scholar · View at Scopus
  3. D. S. Goldberg and S. J. McGee, “Pain as a global public health priority,” BMC Public Health, vol. 11, no. 1, article 770, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. B. Costa, M. Colleoni, S. Conti et al., “Repeated treatment with the synthetic cannabinoid WIN 55,212-2 reduces both hyperalgesia and production of pronociceptive mediators in a rat model of neuropathic pain,” British Journal of Pharmacology, vol. 141, no. 1, pp. 4–8, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. B. Costa, A. E. Trovato, F. Comelli, G. Giagnoni, and M. Colleoni, “The non-psychoactive cannabis constituent cannabidiol is an orally effective therapeutic agent in rat chronic inflammatory and neuropathic pain,” European Journal of Pharmacology, vol. 556, no. 1–3, pp. 75–83, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. E. Palazzo, V. de Novellis, S. Petrosino et al., “Neuropathic pain and the endocannabinoid system in the dorsal raphe: pharmacological treatment and interactions with the serotonergic system,” European Journal of Neuroscience, vol. 24, no. 7, pp. 2011–2020, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. M. M. Ibrahim, H. Deng, A. Zvonok et al., “Activation of CB2 cannabinoid receptors by AM1241 inhibits experimental neuropathic pain: pain inhibition by receptors not present in the CNS,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 18, pp. 10529–10533, 2003. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Guindon and P. Beaulieu, “Antihyperalgesic effects of local injections of anandamide, ibuprofen, rofecoxib and their combinations in a model of neuropathic pain,” Neuropharmacology, vol. 50, no. 7, pp. 814–823, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Jayamanne, R. Greenwood, V. A. Mitchell, S. Aslan, D. Piomelli, and C. W. Vaughan, “Actions of the FAAH inhibitor URB597 in neuropathic and inflammatory chronic pain models,” British Journal of Pharmacology, vol. 147, no. 3, pp. 281–288, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Fox, A. Kesingland, C. Gentry et al., “The role of central and peripheral Cannabinoid1 receptors in the antihyperalgesic activity of cannabinoids in a model of neuropathic pain,” Pain, vol. 92, no. 1-2, pp. 91–100, 2001. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Petrosino and V. Di Marzo, “FAAH and MAGL inhibitors: therapeutic opportunities from regulating endocannabinoid levels,” Current Opinion in Investigational Drugs, vol. 11, no. 1, pp. 51–62, 2010. View at Google Scholar · View at Scopus
  12. S. G. Kinsey, J. Z. Long, S. T. O'Neal et al., “Blockade of endocannabinoid-degrading enzymes attenuates neuropathic pain,” Journal of Pharmacology and Experimental Therapeutics, vol. 330, no. 3, pp. 902–910, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Starowicz, W. Makuch, M. Osikowicz et al., “Spinal anandamide produces analgesia in neuropathic rats: possible CB1- and TRPV1-mediated mechanisms,” Neuropharmacology, vol. 62, no. 4, pp. 1746–1755, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Starowicz and B. Przewlocka, “Modulation of neuropathic-pain-related behaviour by the spinal endocannabinoid/endovanilloid system,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 367, no. 1607, pp. 3286–3299, 2012. View at Publisher · View at Google Scholar · View at Scopus
  15. V. Di Marzo and L. De Petrocellis, “Why do cannabinoid receptors have more than one endogenous ligand?” Philosophical Transactions of the Royal Society B, vol. 367, no. 1607, pp. 3216–3228, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Sousa-Valente, A. Varga, K. Ananthan, A. Khajuria, and I. Nagy, “Anandamide in primary sensory neurons: too much of a good thing?” European Journal of Neuroscience, vol. 39, no. 3, pp. 409–418, 2014. View at Publisher · View at Google Scholar
  17. P. M. Zygmunt, J. Petersson, D. A. Andersson et al., “Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide,” Nature, vol. 400, no. 6743, pp. 452–457, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. P. Movahed, B. A. G. Jönsson, B. Birnir et al., “Endogenous unsaturated C18 N-acylethanolamines are vanilloid receptor (TRPV1) agonists,” The Journal of Biological Chemistry, vol. 280, no. 46, pp. 38496–38504, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. W. J. Martin, P. O. Coffin, E. Attias, M. Balinsky, K. Tsou, and J. M. Walker, “Anatomical basis for cannabinoid-induced antinociception as revealed by intracerebral microinjections,” Brain Research, vol. 822, no. 1-2, pp. 237–242, 1999. View at Publisher · View at Google Scholar · View at Scopus
  20. J. M. Walker, S. M. Huang, N. M. Strangman, K. Tsou, and M. C. Sañudo-Peña, “Pain modulation by release of the endogenous cannabinoid anandamide,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 21, pp. 12198–12203, 1999. View at Google Scholar
  21. A. G. Hohmann, R. L. Suplita, N. M. Bolton et al., “An endocannabinoid mechanism for stress-induced analgesia,” Nature, vol. 435, no. 7045, pp. 1108–1112, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. P. Bishay, H. Schmidt, C. Marian et al., “R-flurbiprofen reduces neuropathic pain in rodents by restoring endogenous cannabinoids,” PLoS ONE, vol. 5, no. 5, Article ID e10628, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Bishay, A. Häussler, H.-Y. Lim et al., “Anandamide deficiency and heightened neuropathic pain in aged mice,” Neuropharmacology, vol. 71, pp. 204–215, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Petrosino, E. Palazzo, V. de Novellis et al., “Changes in spinal and supraspinal endocannabinoid levels in neuropathic rats,” Neuropharmacology, vol. 52, no. 2, pp. 415–422, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. M. D. Jhaveri, D. Richardson, D. A. Kendall, D. A. Barrett, and V. Chapman, “Analgesic effects of fatty acid amide hydrolase inhibition in a rat model of neuropathic pain,” The Journal of Neuroscience, vol. 26, no. 51, pp. 13318–13327, 2006. View at Publisher · View at Google Scholar · View at Scopus
  26. M. Van Der Stelt, M. Trevisani, V. Vellani et al., “Anandamide acts as an intracellular messenger amplifying Ca2+ influx via TRPV1 channels,” The EMBO Journal, vol. 24, no. 17, pp. 3026–3037, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. G. G. Muccioli, “Endocannabinoid biosynthesis and inactivation, from simple to complex,” Drug Discovery Today, vol. 15, no. 11-12, pp. 474–483, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. V. Vellani, S. Petrosino, L. de Petrocellis et al., “Functional lipidomics. Calcium-independent activation of endocannabinoid/endovanilloid lipid signalling in sensory neurons by protein kinases C and A and thrombin,” Neuropharmacology, vol. 55, no. 8, pp. 1274–1279, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Liu, L. Wang, J. Harvey-White et al., “A biosynthetic pathway for anandamide,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 36, pp. 13345–13350, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. J. Liu, L. Wang, J. Harvey-White et al., “Multiple pathways involved in the biosynthesis of anandamide,” Neuropharmacology, vol. 54, no. 1, pp. 1–7, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Sun, K. Tsuboi, Y. Okamoto et al., “Biosynthesis of anandamide and N-palmitoylethanolamine by sequential actions of phospholipase A2 and lysophospholipase D,” Biochemical Journal, vol. 380, part 3, pp. 749–756, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Maccarrone, M. Attinà, M. Bari, A. Cartoni, C. Ledent, and A. Finazzi-Agrò, “Anandamide degradation and N-acylethanolamines level in wild-type and CB1 cannabinoid receptor knockout mice of different ages,” Journal of Neurochemistry, vol. 78, no. 2, pp. 339–348, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. K. Starowicz, W. Makuch, M. Korostynski et al., “Full inhibition of spinal FAAH leads to TRPV1-mediated analgesic effects in neuropathic rats and possible lipoxygenase-mediated remodeling of anandamide metabolism,” PLoS ONE, vol. 8, no. 4, Article ID e60040, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. C. A. Rouzer and L. J. Marnett, “Non-redundant functions of cyclooxygenases: oxygenation of endocannabinoids,” The Journal of Biological Chemistry, vol. 283, no. 13, pp. 8065–8069, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. W. B. Veldhuis, M. van der Stelt, M. W. Wadman et al., “Neuroprotection by the endogenous cannabinoid anandamide and arvanil against in vivo excitotoxicity in the rat: role of vanilloid receptors and lipoxygenases,” Journal of Neuroscience, vol. 23, no. 10, pp. 4127–4133, 2003. View at Google Scholar · View at Scopus
  36. E. J. Rahn and A. G. Hohmann, “Cannabinoids as pharmacotherapies for neuropathic pain: from the bench to the bedside,” Neurotherapeutics, vol. 6, no. 4, pp. 713–737, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. D. R. Sagar, S. Kelly, P. J. Millns, C. T. O'Shaughnessey, D. A. Kendall, and V. Chapman, “Inhibitory effects of CB1 and CB2 receptor agonists on responses of DRG neurons and dorsal horn neurons in neuropathic rats,” European Journal of Neuroscience, vol. 22, no. 2, pp. 371–379, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Guasti, D. Richardson, M. Jhaveri et al., “Minocycline treatment inhibits microglial activation and alters spinal levels of endocannabinoids in a rat model of neuropathic pain,” Molecular Pain, vol. 5, article 35, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. I. A. Khasabova, S. G. Khasabov, C. Harding-Rose et al., “A decrease in anandamide signaling contributes to the maintenance of cutaneous mechanical hyperalgesia in a model of bone cancer pain,” The Journal of Neuroscience, vol. 28, no. 44, pp. 11141–11152, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. B. N. Okine, L. M. Norris, S. Woodhams et al., “Lack of effect of chronic pre-treatment with the FAAH inhibitor URB597 on inflammatory pain behaviour: evidence for plastic changes in the endocannabinoid system,” British Journal of Pharmacology, vol. 167, no. 3, pp. 627–640, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Leung, A. Saghatelian, G. M. Simon, and B. F. Cravatt, “Inactivation of N-Acyl phosphatidylethanolamine phospholipase D reveals multiple mechanisms for the biosynthesis of endocannabinoids,” Biochemistry, vol. 45, no. 15, pp. 4720–4726, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. G. M. Simon and B. F. Cravatt, “Characterization of mice lacking candidate N-acyl ethanolamine biosynthetic enzymes provides evidence for multiple pathways that contribute to endocannabinoid production in vivo,” Molecular BioSystems, vol. 6, no. 8, pp. 1411–1418, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Varga, A. Jenes, T. H. Marczylo et al., “Anandamide produced by Ca(2+)-insensitive enzymes induces excitation in primary sensory neurons,” Pflügers Archiv, vol. 466, no. 7, pp. 1421–1435, 2013. View at Google Scholar
  44. K. R. Kozak, J. J. Prusakiewicz, and L. J. Marnett, “Oxidative metabolism of endocannabinoids by COX-2,” Current Pharmaceutical Design, vol. 10, no. 6, pp. 659–667, 2004. View at Publisher · View at Google Scholar · View at Scopus
  45. M. D. Jhaveri, D. Richardson, I. Robinson et al., “Inhibition of fatty acid amide hydrolase and cyclooxygenase-2 increases levels of endocannabinoid related molecules and produces analgesia via peroxisome proliferator-activated receptor-alpha in a model of inflammatory pain,” Neuropharmacology, vol. 55, no. 1, pp. 85–93, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. B. Costa, F. Comelli, I. Bettoni, M. Colleoni, and G. Giagnoni, “The endogenous fatty acid amide, palmitoylethanolamide, has anti-allodynic and anti-hyperalgesic effects in a murine model of neuropathic pain: involvement of CB1, TRPV1 and PPARγ receptors and neurotrophic factors,” Pain, vol. 139, no. 3, pp. 541–550, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Kelly, R. J. Chapman, S. Woodhams et al., “Increased function of pronociceptive TRPV1 at the level of the joint in a rat model of osteoarthritis pain,” Annals of the Rheumatic Diseases, 2013. View at Publisher · View at Google Scholar
  48. M. Yu, D. Ives, and C. S. Ramesha, “Synthesis of prostaglandin E2 ethanolamide from anandamide by cyclooxygenase-2,” The Journal of Biological Chemistry, vol. 272, no. 34, pp. 21181–21186, 1997. View at Publisher · View at Google Scholar · View at Scopus
  49. D. K. Nomura, B. E. Morrison, J. L. Blankman et al., “Endocannabinoid hydrolysis generates brain prostaglandins that promote neuroinflammation,” Science, vol. 334, no. 6057, pp. 809–813, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Ligresti, J. Martos, J. Wang et al., “Prostamide F(2) α receptor antagonism combined with inhibition of FAAH may block the pro-inflammatory mediators formed following selective FAAH inhibition,” British Journal of Pharmacology, vol. 171, no. 6, pp. 1408–1419, 2014. View at Google Scholar
  51. M. van der Stelt, J. A. van Kuik, M. Bari et al., “Oxygenated metabolites of anandamide and 2-arachidonoylglycerol: conformational analysis and interaction with cannabinoid receptors, membrane transporter, and fatty acid amide hydrolase,” Journal of Medicinal Chemistry, vol. 45, no. 17, pp. 3709–3720, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. R. G. Pertwee, “Cannabinoid receptors and pain,” Progress in Neurobiology, vol. 63, no. 5, pp. 569–611, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. D. Bridges, K. Ahmad, and A. S. C. Rice, “The synthetic cannabinoid WIN55,212-2 attenuates hyperalgesia and allodynia in a rat model of neuropathic pain,” British Journal of Pharmacology, vol. 133, no. 4, pp. 586–594, 2001. View at Publisher · View at Google Scholar · View at Scopus
  54. A. F. Paszcuk, R. C. Dutra, K. A. B. S. da Silva, N. L. M. Quintão, M. M. Campos, and J. B. Calixto, “Cannabinoid agonists inhibit neuropathic pain induced by brachial plexus avulsion in mice by affecting glial cells and MAP kinases,” PLoS ONE, vol. 6, no. 9, Article ID e24034, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Furuse, T. Kawamata, J. Yamamoto et al., “Reduction of bone cancer pain by activation of spinal cannabinoid receptor 1 and its expression in the superficial dorsal horn of the spinal cord in a murine model of bone cancer pain,” Anesthesiology, vol. 111, no. 1, pp. 173–186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  56. J. Guindon, Y. Lai, S. M. Takacs, H. B. Bradshaw, and A. G. Hohmann, “Alterations in endocannabinoid tone following chemotherapy-induced peripheral neuropathy: effects of endocannabinoid deactivation inhibitors targeting fatty-acid amide hydrolase and monoacylglycerol lipase in comparison to reference analgesics following cisplatin treatment,” Pharmacological Research, vol. 67, no. 1, pp. 94–109, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. N. Agarwal, P. Pacher, I. Tegeder et al., “Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors,” Nature Neuroscience, vol. 10, no. 7, pp. 870–879, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Zhang, C. Hoffert, H. K. Vu, T. Groblewski, S. Ahmad, and D. O'Donnell, “Induction of CB2 receptor expression in the rat spinal cord of neuropathic but not inflammatory chronic pain models,” European Journal of Neuroscience, vol. 17, no. 12, pp. 2750–2754, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. I. Racz, X. Nadal, J. Alferink et al., “Crucial role of CB2 cannabinoid receptor in the regulation of central immune responses during neuropathic pain,” Journal of Neuroscience, vol. 28, no. 46, pp. 12125–12135, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Beltramo, N. Bernardini, R. Bertorelli et al., “CB2 receptor-mediated antihyperalgesia: possible direct involvement of neural mechanisms,” European Journal of Neuroscience, vol. 23, no. 6, pp. 1530–1538, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Romero-Sandoval, N. Nutile-Mcmenemy, and J. A. Deleo, “Spinal microglial and perivascular cell cannabinoid receptor type 2 activation reduces behavioral hypersensitivity without tolerance after peripheral nerve injury,” Anesthesiology, vol. 108, no. 4, pp. 722–734, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. E. J. Rahn, A. M. Zvonok, G. A. Thakur, A. D. Khanolkar, A. Makriyannis, and A. G. Hohmann, “Selective activation of cannabinoid CB2 receptors suppresses neuropathic nociception induced by treatment with the chemotherapeutic agent paclitaxel in rats,” The Journal of Pharmacology and Experimental Therapeutics, vol. 327, no. 2, pp. 584–591, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. E. J. Rahn, A. Makriyannis, and A. G. Hohmann, “Activation of cannabinoid CB 1 and CB 2 receptors suppresses neuropathic nociception evoked by the chemotherapeutic agent vincristine in rats,” The British Journal of Pharmacology, vol. 152, no. 5, pp. 765–777, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. Z. Winter, A. Buhala, F. Ötvös et al., “Functionally important amino acid residues in the transient receptor potential vanilloid 1 (TRPV1) ion channel—an overview of the current mutational data,” Molecular Pain, vol. 9, no. 1, article 30, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Zimmermann, “Ethical guidelines for investigations of experimental pain in conscious animals,” Pain, vol. 16, no. 2, pp. 109–110, 1983. View at Publisher · View at Google Scholar · View at Scopus
  66. M. Osikowicz, J. Mika, W. Makuch, and B. Przewlocka, “Glutamate receptor ligands attenuate allodynia and hyperalgesia and potentiate morphine effects in a mouse model of neuropathic pain,” Pain, vol. 139, no. 1, pp. 117–126, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. S. J. R. Elmes, M. D. Jhaveri, D. Smart, D. A. Kendall, and V. Chapman, “Cannabinoid CB2 receptor activation inhibits mechanically evoked responses of wide dynamic range dorsal horn neurons in naïve rats and in rat models of inflammatory and neuropathic pain,” European Journal of Neuroscience, vol. 20, no. 9, pp. 2311–2320, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. G. J. Bennett and Y. K. Xie, “A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man,” Pain, vol. 33, no. 1, pp. 87–107, 1988. View at Publisher · View at Google Scholar · View at Scopus
  69. P. Chomczynski and N. Sacchi, “Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction,” Analytical Biochemistry, vol. 162, no. 1, pp. 156–159, 1987. View at Google Scholar · View at Scopus