The Journal of Pain
Volume 11, Issue 7 , Pages 663-671 , July 2010

Endothelin-A Receptor Antagonism Attenuates Carcinoma-Induced Pain Through Opioids in Mice

  • Phuong N. Quang

      Affiliations

    • UCSF School of Dentistry, Oral and Craniofacial Sciences Graduate Program, University of California, San Francisco
  • ,
  • Brian L. Schmidt

      Affiliations

    • UCSF Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco
    • Department of Oral and Maxillofacial Surgery, University of California, San Francisco
    • Corresponding Author InformationAddress reprint requests to Dr Brian Schmidt, UCSF Department of Oral and Maxillofacial Surgery, Box 0440, 521 Parnassus Avenue, Clinic Sci C-525, University of California, San Francisco, San Francisco, CA 94143-0440.

Received 4 July 2009 ,Revised 10 September 2009 ,Accepted 8 October 2009.

References 

  1. Ahmed SI, Thompson J, Coulson JM, Woll PJ. Studies on the expression of endothelin, its receptor subtypes, and converting enzymes in lung cancer and in human bronchial epithelium. Am J Respir Cell Mol Biol. 2000;22:422–431
  2. Alanen K, Deng DX, Chakrabarti S. Augmented expression of endothelin-1, endothelin-3 and the endothelin-B receptor in breast carcinoma. Histopathology. 2000;36:161–167
  3. Arai H, Hori S, Aramori I, Ohkubo H, Nakanishi S. Cloning and expression of a cDNA encoding an endothelin receptor. Nature. 1990;348:730–732
  4. Asham E, Shankar A, Loizidou M, Fredericks S, Miller K, Boulos PB, et al. Increased endothelin-1 in colorectal cancer and reduction of tumour growth by ET(A) receptor antagonism. Br J Cancer. 2001;85:1759–1763
  5. Awano S, Dawson LA, Hunter AR, Turner AJ, Usmani BA. Endothelin system in oral squamous carcinoma cells: Specific siRNA targeting of ECE-1 blocks cell proliferation. Int J Cancer. 2006;118:1645–1652
  6. Bhalla S, Matwyshyn G, Gulati A. Endothelin receptor antagonists restore morphine analgesia in morphine tolerant rats. Peptides. 2003;24:553–561
  7. Bhalla S, Matwyshyn G, Gulati A. Morphine tolerance does not develop in mice treated with endothelin-A receptor antagonists. Brain Res. 2005;1064:126–135
  8. Bhalla S, Matwyshyn G, Gulati A. Potentiation of morphine analgesia by BQ123, an endothelin antagonist. Peptides. 2002;23:1837–1845
  9. Brasseur L. Review of current pharmacologic treatment of pain. Drugs. 1997;53(Suppl 2):10–17
  10. Bremnes T, Paasche JD, Mehlum A, Sandberg C, Bremnes B, Attramadal H. Regulation and intracellular trafficking pathways of the endothelin receptors. J Biol Chem. 2000;275(17):596–604
  11. Cabot PJ, Carter L, Gaiddon C, Zhang Q, Schafer M, Loeffler JP, et al. Immune cell-derived beta-endorphin: Production, release, and control of inflammatory pain in rats. J Clin Invest. 1997;100:142–148
  12. Carducci MA, Nelson JB, Bowling MK, Rogers T, Eisenberger MA, Sinibaldi V, et al. Atrasentan, an endothelin-receptor antagonist for refractory adenocarcinomas: Safety and pharmacokinetics. J Clin Oncol. 2002;20(21):71–80
  13. Chaplin JM, Morton RP. A prospective, longitudinal study of pain in head and neck cancer patients. Head Neck. 1999;21:531–537
  14. Chen X, Li M, Sun W, Bi Y, Cai M, Liang H, et al. Peroxisome proliferator-activated receptor alpha agonist-induced down-regulation of hepatic glucocorticoid receptor expression in SD rats. Biochem Biophys Res Commun. 2008;368:865–870
  15. Connelly ST, Macabeo-Ong M, Dekker N, Jordan RC, Schmidt BL. Increased nitric oxide levels and iNOS over-expression in oral squamous cell carcinoma. Oral Oncol. 2005;41:261–267
  16. Connor M, Osborne PB, Christie MJ. Mu-opioid receptor desensitization: Is morphine different?. Br J Pharmacol. 2004;143:685–696
  17. Dahlof B, Gustafsson D, Hedner T, Jern S, Hansson L. Regional haemodynamic effects of endothelin-1 in rat and man: Unexpected adverse reaction. J Hypertens. 1990;8:811–817
  18. Davar G. Endothelin-1 and metastatic cancer pain. Pain Med. 2001;2:24–27
  19. Davar G, Hans G, Fareed MU, Sinnott C, Strichartz G. Behavioral signs of acute pain produced by application of endothelin-1 to rat sciatic nerve. Neuroreport. 1998;9:2279–2283
  20. Denning GM, Ackermann LW, Barna TJ, Armstrong JG, Stoll LL, Weintraub NL, et al. Proenkephalin expression and enkephalin release are widely observed in non-neuronal tissues. Peptides. 2008;29:83–92
  21. Eisenstein TK, Rogers TJ, Meissler JJ, Adler MW, Hilburger ME. Morphine depresses macrophage numbers and function in mouse spleens. Adv Exp Med Biol. 1998;437:33–41
  22. Ferreira SH, Romitelli M, de Nucci G. Endothelin-1 participation in overt and inflammatory pain. J Cardiovasc Pharmacol. 1989;13(Suppl 5):S220–S222
  23. Franco-Cereceda A, Rydh M, Lou YP, Dalsgaard CJ, Lundberg JM. Endothelin as a putative sensory neuropeptide in the guinea-pig: Different properties in comparison with calcitonin gene-related peptide. Regul Pept. 1991;32:253–265
  24. Fujita M, Andoh T, Saiki I, Kuraishi Y. Involvement of endothelin and ET(A) endothelin receptor in mechanical allodynia in mice given orthotopic melanoma inoculation. J Pharmacol Sci. 2008;106:257–263
  25. Gokin AP, Fareed MU, Pan HL, Hans G, Strichartz GR, Davar G. Local injection of endothelin-1 produces pain-like behavior and excitation of nociceptors in rats. J Neurosci. 2001;21:5358–5366
  26. Grant K, Loizidou M, Taylor I. Endothelin-1: A multifunctional molecule in cancer. Br J Cancer. 2003;88:163–166
  27. Gulati A, Bhalla S, Matwyshyn G. A novel combination of opiates and endothelin antagonists to manage pain without any tolerance development. J Cardiovasc Pharmacol. 2004;44(Suppl 1):S129–S131
  28. Hamamoto DT, Khasabov SG, Cain DM, Simone DA. Tumor-evoked sensitization of C nociceptors: A role for endothelin. J Neurophysiol. 2008;100:2300–2311
  29. Harada N, Himeno A, Shigematsu K, Sumikawa K, Niwa M. Endothelin-1 binding to endothelin receptors in the rat anterior pituitary gland: Possible formation of an ETA-ETB receptor heterodimer. Cell Mol Neurobiol. 2002;22:207–226
  30. Hybbinette S, Bostrom M, Lindberg K. Enzymatic dissociation of keratinocytes from human skin biopsies for in vitro cell propagation. Exp Dermatol. 1999;8:30–38
  31. Ihara M, Noguchi K, Saeki T, Fukuroda T, Tsuchida S, Kimura S, et al. Biological profiles of highly potent novel endothelin antagonists selective for the ETA receptor. Life Sci. 1992;50:247–255
  32. Inoue A, Yanagisawa M, Kimura S, Kasuya Y, Miyauchi T, Goto K, et al. The human endothelin family: Three structurally and pharmacologically distinct isopeptides predicted by three separate genes. Proc Natl Acad Sci U S A. 1989;86:2863–2867
  33. Khodorova A, Montmayeur JP, Strichartz G. Endothelin receptors and pain. J Pain. 2009;10:4–28
  34. Khodorova A, Navarro B, Jouaville LS, Murphy JE, Rice FL, Mazurkiewicz JE, et al. Endothelin-B receptor activation triggers an endogenous analgesic cascade at sites of peripheral injury. Nat Med. 2003;9:1055–1061
  35. Kloog Y, Sokolovsky M. Similarities in mode and sites of action of sarafotoxins and endothelins. Trends Pharmacol Sci. 1989;10:212–214
  36. Kurbel S, Kurbel B, Kovacic D, Sulava D, Krajina Z, Dmitrovic B, et al. Endothelin-secreting tumors and the idea of the pseudoectopic hormone secretion in tumors. Med Hypotheses. 1999;52:329–333
  37. Law PY, Loh HH. Regulation of opioid receptor activities. J Pharmacol Exp Ther. 1999;289:607–624
  38. Machelska H, Stein C. Pain control by immune-derived opioids. Clin Exp Pharmacol Physiol. 2000;27:533–536
  39. Mao J, Price DD, Lu J, Keniston L, Mayer DJ. Two distinctive antinociceptive systems in rats with pathological pain. Neurosci Lett. 2000;280:13–16
  40. Mao J, Price DD, Mayer DJ. Experimental mononeuropathy reduces the antinociceptive effects of morphine: Implications for common intracellular mechanisms involved in morphine tolerance and neuropathic pain. Pain. 1995;61:353–364
  41. Melzig MF, Nylander I, Vlaskovska M, Terenius L. Beta-endorphin stimulates proliferation of small cell lung carcinoma cells in vitro via nonopioid binding sites. Exp Cell Res. 1995;219:471–476
  42. Mercadante S. Malignant bone pain: Pathophysiology and treatment. Pain. 1997;69(1-2):1–18
  43. Mercadante S, Arcuri E. Breakthrough pain in cancer patients: Pathophysiology and treatment. Cancer Treat Rev. 1998;24:425–432
  44. Nagahama M, Funasaka Y, Fernandez-Frez ML, Ohashi A, Chakraborty AK, Ueda M, et al. Immunoreactivity of alpha-melanocyte-stimulating hormone, adrenocorticotrophic hormone and beta-endorphin in cutaneous malignant melanoma and benign melanocytic naevi. Br J Dermatol. 1998;138:981–985
  45. Nakamizo M, Pawankar R, Ohkubo K. Presence of endothelin-1 in human salivary glands and tumors. Nippon Ika Daigaku Zasshi. 1998;65:471–477
  46. Neves SR, Ram PT, Iyengar R. G protein pathways. Science. 2002;296:1636–1639
  47. Omar RA, el Tabbakh GH. Immunoreactive beta-endorphin in ovarian sex cord-stromal tumors. Arch Pathol Lab Med. 1987;111:436–439
  48. Ossipov MH, Lai J, Malan TP, Porreca F. Spinal and supraspinal mechanisms of neuropathic pain. Ann N Y Acad Sci. 2000;909:12–24
  49. Pan HL, Wu ZZ, Zhou HY, Chen SR, Zhang HM, Li DP. Modulation of pain transmission by G-protein-coupled receptors. Pharmacol Ther. 2008;117:141–161
  50. Peters CM, Lindsay TH, Pomonis JD, Luger NM, Ghilardi JR, Sevcik MA, et al. Endothelin and the tumorigenic component of bone cancer pain. Neuroscience. 2004;126:1043–1052
  51. Pickering V, Jay Gupta R, Quang P, Jordan RC, Schmidt BL. Effect of peripheral endothelin-1 concentration on carcinoma-induced pain in mice. Eur J Pain. 2008;12:293–300
  52. Portenoy RK, Lesage P. Management of cancer pain. Lancet. 1999;353:1695–1700
  53. Quang PN, Schmidt BL. Endothelin receptor-mediated attenuation of carcinoma-induced nociception is opioid-depedent in mice. J Pain. 2009;10(4 Suppl 1):A189
  54. Rittner HL, Brack A, Machelska H, Mousa SA, Bauer M, Schafer M, et al. Opioid peptide-expressing leukocytes: Identification, recruitment, and simultaneously increasing inhibition of inflammatory pain. Anesthesiology. 2001;95:500–508
  55. Rubanyi GM, Polokoff MA. Endothelins: Molecular biology, biochemistry, pharmacology, physiology, and pathophysiology. Pharmacol Rev. 1994;46:325–415
  56. Sabino MA, Luger NM, Mach DB, Rogers SD, Schwei MJ, Mantyh PW. Different tumors in bone each give rise to a distinct pattern of skeletal destruction, bone cancer-related pain behaviors and neurochemical changes in the central nervous system. Int J Cancer. 2003;104:550–558
  57. Schauer E, Trautinger F, Kock A, Schwarz A, Bhardwaj R, Simon M, et al. Proopiomelanocortin-derived peptides are synthesized and released by human keratinocytes. J Clin Invest. 1994;93:2258–2262
  58. Schmidt BL, Pickering V, Liu S, Quang P, Dolan J, Connelly ST, et al. Peripheral endothelin A receptor antagonism attenuates carcinoma-induced pain. Eur J Pain. 2007;11:406–414
  59. Shedd DP, Carl A, Shedd C. Problems of terminal head and neck cancer patients. Head Neck Surg. 1980;2:476–482
  60. Sokolovsky M, Shraga-Levine Z, Galron R. Ligand-specific stimulation/inhibition of cAMP formation by a novel endothelin receptor subtype. Biochemistry. 1994;33:11417–11419
  61. Tyndall JD, Pfeiffer B, Abbenante G, Fairlie DP. Over one hundred peptide-activated G protein-coupled receptors recognize ligands with turn structure. Chem Rev. 2005;105:793–826
  62. Yanagisawa M, Kurihara H, Kimura S, Tomobe Y, Kobayashi M, Mitsui Y, et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature. 1988;332:411–415
  63. Yuyama H, Koakutsu A, Fujiyasu N, Tanahashi M, Fujimori A, Sato S, et al. Effects of selective endothelin ET(A) receptor antagonists on endothelin-1-induced potentiation of cancer pain. Eur J Pharmacol. 2004;492:177–182
  64. Zhou QL, Strichartz G, Davar G. Endothelin-1 activates ET(A) receptors to increase intracellular calcium in model sensory neurons. Neuroreport. 2001;12:3853–3857

 Supported by NIH/NIDCR R21 DE018561.

PII: S1526-5900(09)00811-6

doi: 10.1016/j.jpain.2009.10.011

The Journal of Pain
Volume 11, Issue 7 , Pages 663-671 , July 2010