Human Pathology
Volume 41, Issue 5 , Pages 632-642 , May 2010

Enkephalin, its precursor, processing enzymes, and receptor as part of a local opioid network throughout the respiratory system of lung cancer patients

  • Malgorzata Krajnik, MD

      Affiliations

    • Palliative Care Department, Collegium Medicum of the Nicolaus Copernicus University, 85-094 Bydgoszcz, Poland
    • These authors contributed equally to this work.
  • ,
  • Michael Schäfer, MD

      Affiliations

    • Department of Anesthesiology and Intensive Care Medicine, Charité-Universitaetsmedizin Berlin, Campus Virchow-Klinikum and Campus Charite Mitte, 13353 Berlin, Germany
    • These authors contributed equally to this work.
  • ,
  • Piotr Sobanski, MD

      Affiliations

    • Cardiology Department, II University Hospital in Bydgoszcz, 85-168 Poland
  • ,
  • Janusz Kowalewski, MD, PhD

      Affiliations

    • Department of Thoracic Surgery and Lung Disease, Collegium Medicum of the Nicolaus Copernicus University, 85-796 Bydgoszcz, Poland
  • ,
  • Elzbieta Bloch-Boguslawska, MD

      Affiliations

    • Department of Forensic Medicine, Collegium Medicum of the Nicolaus Copernicus University, 85-094 Bydgoszcz, Poland
  • ,
  • Zbigniew Zylicz, MD, PhD

      Affiliations

    • Dove House Hospice, Hull, HU88DH United Kingdom
  • ,
  • Shaaban A. Mousa, PhD

      Affiliations

    • Department of Anesthesiology and Intensive Care Medicine, Charité-Universitaetsmedizin Berlin, Campus Virchow-Klinikum and Campus Charite Mitte, 13353 Berlin, Germany
    • Corresponding Author InformationCorresponding author.

Received 19 May 2009 ,Accepted 14 August 2009.

References 

  1. Philippe D, Dubuquoy L, Groux H, et al. Anti-inflammatory properties of the μ opioid receptor support its use in the treatment of colon inflammation. J Clin Invest. 2003;111:1329–1338
  2. Sharp BM, McKean DJ, McAllen K, Shahabi NA. Signaling through delta opioid receptors on murine splenic T cells and stably transfected Jurkat cells. Ann N Y Acad Sci. 1998;840:420–424
  3. Slominski A, Wortsman J. Self-regulated endocrine systems in the skin. Minerva Endocrinol. 2003;28:135–143
  4. Wang L, Tiniakov RL, Yeates DB. Peripheral opioidergic regulation of the tracheobronchial mucociliary transport system. J Appl Physiol. 2003;94:2375–2383
  5. Ramnarine SI, Liu YC, Rogers DF. Neuroregulation of mucus secretion by opioid receptors and K(ATP) and BK(Ca) channels in ferret trachea in vitro. Br J Pharmacol. 1998;123:1631–1638
  6. Belvisi MG, Stretton CD, Verleden GM, Ledingham SJ, Yacoub MH, Barnes PJ. Inhibition of cholinergic neurotransmission in human airways by opioids. J Appl Physiol. 1992;72:1096–1100
  7. Jennings AL, Davies AN, Higgins JP, Broadley K. Opioids for the palliation of breathlessness in terminal illness. Cochrane Database Syst Rev. 2001;CD002066
  8. Bruera E, Sala R, Spruyt O, Palmer JL, Zhang T, Willey J. Nebulized versus subcutaneous morphine for patients with cancer dyspnea: a preliminary study. J Pain Symptom Manage. 2005;29:613–618
  9. Coyne PJ, Viswanathan R, Smith TJ. Nebulized fentanyl citrate improves patients' perception of breathing, respiratory rate, and oxygen saturation in dyspnea. J Pain Symptom Manage. 2002;23:157–160
  10. Mousa SA, Shakibaei M, Sitte N, Schäfer M, Stein C. Subcellular pathways of beta-endorphin synthesis, processing, and release from immunocytes in inflammatory pain. Endocrinology. 2004;145:1331–1341
  11. Maneckjee R, Minna JD. Opioid and nicotine receptors affect growth regulation of human lung cancer cell lines. Proc Natl Acad Sci U S A. 1990;87:3294–3298
  12. Roth KA, Barchas JD. Small cell carcinoma cell lines contain opioid peptides and receptors. Cancer. 1986;57:769–773
  13. Cabot PJ, Dodd PR, Cramond T, Smith MT. Characterization of non-conventional opioid binding sites in rat and human lung. Eur J Pharmacol. 1994;268:247–255
  14. Wittert G, Hope P, Pyle D. Tissue distribution of opioid receptors gene expression in the rat. Biochem Biophys Res Commun. 1996;218:877–881
  15. Peinado JR, Li H, Johanning K, Lindberg I. Cleavage of recombinant proenkephalin and blockade mutants by prohormone convertases 1 and 2: an in vitro specificity study. J Neurochem. 2003;87:868–878
  16. Loh YP, Maldonado A, Zhang C, Tam WH, Cawley N. Mechanism of sorting proopiomelanocortin and proenkephalin to the regulated secretory pathway of neuroendocrine cells. Ann N Y Acad Sci. 2002;97:416–425
  17. Mousa SA, Cheppudira BP, Shaqura M, Fischer O, Hofmann J, Hellweg R, et al. Nerve growth factor governs the enhanced ability of opioids to suppress inflammatory pain. Brain. 2007;130:502–513
  18. Haworth R, Woodfine J, McCawley S, Pilling AM, Lewis DJ, Williams TC. Pulmonary neuroendocrine cell hyperplasia: identification, diagnostic criteria and incidence in untreated ageing rats of different strains. Toxicol Pathol. 2007;35:735–740
  19. Cutz E, Perrin DG, Pan J, Haas EA, Krous HF. Pulmonary neuroendocrine cells and neuroepithelial bodies in sudden infant death syndrome: potential markers of airway chemoreceptor dysfunction. Pediatr Dev Pathol. 2007;10:106–116
  20. Tang J, Chow J, Hang AZ, Yang HYT, Costa E. Met3-enkephalin-Arg6-Phe7 and its receptor in lung. Life Sci. 1983;32:2371–2377
  21. Kew D, Kilpatrick DL. Widespread organ expression of the rat proenkephalin gene during early postnatal development. Mol Endocrinol. 1990;4:337–340
  22. Lansac G, Dong W, Dubois CM, et al. Lipopolysaccharide mediated regulation of neuroendocrine associated proprotein convertases and neuropeptide precursor processing in the rat spleen. J Neuroimmunol. 2006;171:57–71
  23. Sacerdote P. Effects of in vitro and in vivo opioids on the production of IL-12 and IL-10 by murine macrophages. Ann N Y Acad Sci. 2003;992:129–140
  24. Husted TL, Govindaswami M, Oeltgen PR, Rudich SM, Lentsch AB. A delta2-opioid agonist inhibits p38 MAPK and suppresses activation of murine macrophages. J Surg Res. 2005;128:45–49
  25. Bidlack JM, Khimich M, Parkhill AL, Sumagin S, Sun B, Tipton CM. Opioid receptors and signaling on cells from the immune system. J Neuroimmune Pharmacol. 2006;1:260–269
  26. Brar BK, Lowry PJ. The differential processing of proenkephalin A in mouse and human breast tumor cell lines. J Endocrinol. 1999;161:475–484
  27. North WG, Du J. Key peptide processing enzymes are expressed by a variant form of small-cell carcinoma of the lung. Peptides. 1998;19:1743–1747
  28. Rounseville MP, Davis TP. Prohormone convertase and autocrine growth factor mPNAs are coexpressed in small cell lung carcinoma. J Mol Endocrinol. 2000;25:121–128
  29. Campa MJ, Schreiber G, Bepler G, et al. Characterization of delta opioid receptors in lung cancer using a novel nonpeptidic ligand. Cancer Res. 1996;56:1695–1701
  30. Scholar EM, Violi L, Hexum TD. The antimetastatic activity of enkephalin-like peptides. Cancer Lett. 1987;35:133–138
  31. Zagon IS, Rahn KA, McLaughlin PJ. Opioids and migration, chemotaxis, invasion, and adhesion of human cancer cells. Neuropeptides. 2007;41:441–452
  32. Cadet P, Rasmussen M, Zhu W, Tonnesen E, Mantione KJ, Stefano GB. Endogenous morphinergic signaling and tumor growth. Front Biosci. 2004;9:3176–3186
  33. Wine J. Parasympathetic control of airway submucosal glands: central reflexes and the airway intrinsic nervous system. Auton Neurosci. 2007;133:35–54
  34. Nagaki M, Ishihara H, Shimura S, Sasaki T, Takishima T, Shirato K. Tachykinins induce a [Ca2+]i rise in the acinar cells of feline tracheal submucosal gland. Respir Physiol. 1994;98:111–120
  35. Adriaensen D, Brouns I, Pintelon I, De Proost I, Timmermans JP. Evidence for a role of neuroepithelial bodies as complex airway sensors: comparison with smooth muscle-associated airway receptors. J Appl Physiol. 2006;101:960–970

PII: S0046-8177(09)00362-1

doi: 10.1016/j.humpath.2009.08.025

Human Pathology
Volume 41, Issue 5 , Pages 632-642 , May 2010