Small-molecule nociceptin receptor agonist ameliorates mast cell activation and pain in sickle mice

Haematologica

Volumn 100, Issue 12, 2015, Pages 1517-1525

  Vang, Derek ^a   Paul, Jinny A ^a   Nguyen, Julia ^a   Tran, Huy ^a   Vincent, Lucile ^a   Yasuda, Dennis ^b   Zaveri, Nurulain T ^b   Gupta, Kalpna ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b Astraea Therapeutics Inc   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PROTEIN; INTERLEUKIN 6; MU OPIATE RECEPTOR; NOCICEPTIN RECEPTOR AGONIST; RANTES; TUMOR NECROSIS FACTOR ALPHA; CIS-1-METHYL-7-((4-(2,6-DICHLOROPHENYL)PIPERIDIN-1-YL)METHYL)-6,7,8,9-TETRAHYDRO-5H-BENZOCYCLOHEPTEN-5-OL; CYCLOHEPTANE DERIVATIVE; NOCICEPTIN RECEPTOR; OPIATE RECEPTOR; PIPERIDINE DERIVATIVE;

ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; HYPOXIA; INFLAMMATION; MAST CELL; MAST CELL DEGRANULATION; MECHANICAL HYPERALGESIA; MOUSE; NONHUMAN; PAIN; REOXYGENATION; SICKLE CELL ANEMIA; ANEMIA, SICKLE CELL; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; MORTALITY; PATHOLOGY; TRANSGENIC MOUSE;

ANEMIA, SICKLE CELL; ANIMALS; CYCLOHEPTANES; MAST CELLS; MICE; MICE, TRANSGENIC; PAIN; PIPERIDINES; RECEPTORS, OPIOID;

EID: 84948968056     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2015.128736     Document Type: Article

References (46)

1. Ballas SK, Gupta K, Adams-Graves P. Sickle cell pain: a critical reappraisal. Blood. 2012; 120(18):3647-3656.
2. Platt OS, Thorington BD, Brambilla DJ, et al. Pain in sickle cell disease. Rates and risk factors. N Engl J Med. 1991;325(1):11-16.
3. Mellbye A, Karlstad O, Skurtveit S, Borchgrevink PC, Fredheim OM. Co-morbidity in persistent opioid users with chronic non-malignant pain in Norway. Eur J Pain. 2014;18(8):1083-1093.
4. Chu LF, Angst MS, Clark D. Opioidinduced hyperalgesia in humans: molecular mechanisms and clinical considerations. Clin J Pain. 2008;24(6):479-496.
5. Degenhardt L, Whiteford HA, Ferrari AJ, et al. Global burden of disease attributable to illicit drug use and dependence: findings from the Global Burden of Disease Study 2010. Lancet. 2013;382(9904):1564-1574.
6. Wang X, Loram LC, Ramos K, et al. Morphine activates neuroinflammation in a manner parallel to endotoxin. Proc Natl Acad Sci USA. 2012;109(16):6325-6330.
7. Vincent L, Vang D, Nguyen J, et al. Mast cell activation contributes to sickle cell pathobiology and pain in mice. Blood. 2013;122(11):1853-1862.
8. Mogil JS, Pasternak GW. The molecular and behavioral pharmacology of the orphanin FQ/nociceptin peptide and receptor family. Pharmacol Rev. 2001;53(3):381-415.
9. Mollereau C, Parmentier M, Mailleux P, et al. ORL1, a novel member of the opioid receptor family. Cloning, functional expression and localization. FEBS Lett. 1994;341(1):33-38.
10. Neal CR Jr, Mansour A, Reinscheid R, Nothacker HP, Civelli O, Watson SJ Jr. Localization of orphanin FQ (nociceptin) peptide and messenger RNA in the central nervous system of the rat. J Comp Neurol. 1999;406(4):503-547.
11. Neal CR Jr, Akil H, Watson SJ Jr. Expression of orphanin FQ and the opioid receptor-like (ORL1) receptor in the developing human and rat brain. J Chem Neuroanat. 2001;22(4):219-249.
12. Khroyan TV, Polgar WE, Orduna J, et al. Differential effects of nociceptin/orphanin FQ (NOP) receptor agonists in acute versus chronic pain: studies with bifunctional NOP/mu receptor agonists in the sciatic nerve ligation chronic pain model in mice. J Pharmacol Exp Ther. 2011;339(2):687-693.
13. Toll L, Khroyan TV, Polgar W, Husbands SM, Zaveri NT. Pharmacology of mixed NOP/Mu ligands. In: Ko MC, Husbands SM, eds. Research and Development of Opioid-Related Ligands. Washington DC: American Chemical Society, 2013:369-391 (ACS Symposium Series; 1131).
14. Sukhtankar DD, Zaveri NT, Husbands SM, Ko MC. Effects of spinally administered bifunctional nociceptin/orphanin FQ peptide receptor/mu-opioid receptor ligands in mouse models of neuropathic and inflammatory pain. J Pharmacol Exp Ther. 2013; 346(1):11-22.
15. Inoue M, Kawashima T, Takeshima H, et al. In vivo pain-inhibitory role of nociceptin/orphanin FQ in spinal cord. J Pharmacol Exp Ther. 2003;305(2):495-501.
16. Kohli DR, Li Y, Khasabov SG, et al. Painrelated behaviors and neurochemical alterations in mice expressing sickle hemoglobin: modulation by cannabinoids. Blood. 2010;116(3):456-465.
17. Michaels LA, Ohene-Frempong K, Zhao H, Douglas SD. Serum levels of substance P are elevated in patients with sickle cell disease and increase further during vaso-occlusive crisis. Blood. 1998;92(9):3148-3151.
18. Helyes Z, Nemeth J, Pinter E, Szolcsanyi J. Inhibition by nociceptin of neurogenic inflammation and the release of SP and CGRP from sensory nerve terminals. Br J Pharmacol. 1997;121(4):613-615.
19. Nemeth J, Helyes Z, Oroszi G, Than M, Pinter E, Szolcsanyi J. Inhibition of nociceptin on sensory neuropeptide release and mast cell-mediated plasma extravasation in rats. Eur J Pharmacol. 1998;347(1):101-104.
20. Galli SJ, Tsai M. IgE and mast cells in allergic disease. Nat Med. 2012;18(5):693-704.
21. Abraham SN, St John AL. Mast cell-orchestrated immunity to pathogens. Nat Rev Immunol. 2010;10(6):440-452.
22. Zuo Y, Perkins NM, Tracey DJ, Geczy CL. Inflammation and hyperalgesia induced by nerve injury in the rat: a key role of mast cells. Pain. 2003;105(3):467-479.
23. Amadesi S, Nie J, Vergnolle N, et al. Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci. 2004;24(18):4300-4312.
24. Brandow AM, Stucky CL, Hillery CA, Hoffmann RG, Panepinto JA. Patients with sickle cell disease have increased sensitivity to cold and heat. Am J Hematol. 2013;88 (1):37-43.
25. Cain DM, Vang D, Simone DA, Hebbel RP, Gupta K. Mouse models for studying pain in sickle disease: effects of strain, age, and acuteness. Br J Haematol. 2012;156(4):535-544.
26. Zaveri NT, Jiang F, Olsen Cris M, et al. A novel series of piperidin-4-yl-1,3-dihydroindol-2-ones as agonist and antagonist ligands at the nociceptin receptor. J Med Chem. 2004;47 2973-2976.
27. Paszty C, Brion CM, Manci E, et al. Transgenic knockout mice with exclusively human sickle hemoglobin and sickle cell disease. Science. 1997;278(5339):876-878.
28. Hillery CA, Kerstein PC, Vilceanu D, et al. Transient receptor potential vanilloid 1 mediates pain in mice with severe sickle cell disease. Blood. 2011;118(12):3376-3383.
29. Cataldo G, Rajput S, Gupta K, Simone DA. Sensitization of nociceptive spinal neurons contributes to pain in a transgenic model of sickle cell disease. Pain. 2015;156(4):722-730.
30. Belcher JD, Bryant CJ, Nguyen J, et al. Transgenic sickle mice have vascular inflammation. Blood. 2003;101(10):3953-3959.
31. Barlocco D, Cignarella G, Giardina G, Grugni M, and Ronzoni S, Inventors. (2006) inventors; GaxoSmithKline S.p.A., assignee. Benzosuberonylpiperidine compounds as analgesics. U.S. Patent 7,115,633. 2006 Oct 3.
32. Darbari DS, Ballas SK, Clauw DJ. Thinking beyond sickling to better understand pain in sickle cell disease. Eur J Haematol. 2014; 93(2):89-95.
33. Podlesnik CA, Ko MC, Winger G, Wichmann J, Prinssen EP, Woods JH. The effects of nociceptin/orphanin FQ receptor agonist Ro 64-6198 and diazepam on antinociception and remifentanil selfadministration in rhesus monkeys. Psychopharmacology. 2011;213(1):53-60.
34. Toll L, Khroyan TV, Polgar WE, Jiang F, Olsen C, Zaveri NT. Comparison of the anti-nociceptive and anti-rewarding profiles of novel bifunctional nociceptin/orphanin FQ receptor (NOPr)-Mu opioid receptor (MOPr) ligands: implications for therapeutic applications. J Pharmacol Exp Ther. 2009;331(3):954-964.
35. Lin AP, Ko MC. The therapeutic potential of nociceptin/orphanin FQ receptor agonists as analgesics without abuse liability. ACS Chem Neurosci. 2013;4(2):214-224.
36. Dautzenberg FM, Wichmann J, Higelin J, et al. Pharmacological characterization of the novel nonpeptide orphanin FQ/nociceptin receptor agonist Ro 64-6198: rapid and reversible desensitization of the ORL1 receptor in vitro and lack of tolerance in vivo. J Pharmacol Exp Ther. 2001;298(2): 812-819.
37. Varty GB, Hyde LA, Hodgson RA, et al. Characterization of the nociceptin receptor (ORL-1) agonist, Ro64-6198, in tests of anxiety across multiple species. Psychopharmacology (Berl). 2005;182(1): 132-143.
38. Varty GB, Lu SX, Morgan CA, et al. The anxiolytic-like effects of the novel, orally active nociceptin opioid receptor agonist 8-[bis(2-methylphenyl)methyl]-3-phenyl-8-azabicyclo[3.2.1]octan-3-ol (SCH 221510). J Pharmacol Exp Ther. 2008;326(2):672-682.
39. Jenck F, Wichmann J, Dautzenberg FM, et al. A synthetic agonist at the orphanin FQ/nociceptin receptor ORL1: anxiolytic profile in the rat. Proc Natl Acad Sci USA. 2000;97(9):4938-4943.
40. Sogutlu A, Levenson JL, McClish DK, Rosef SD, Smith WR. Somatic symptom burden in adults with sickle cell disease predicts pain, depression, anxiety, health care utilization, and quality of life: the PiSCES project. Psychosomatics. 2011;52(3):272-279.
41. Khroyan TV, Zaveri NT, Polgar WE, et al. SR 16435 [1-(1-(bicyclo[3.3.1]nonan-9-yl)piperidin-4-yl)indolin-2-one], a novel mixed nociceptin/orphanin FQ/mu-opioid receptor partial agonist: analgesic and rewarding properties in mice. J Pharmacol Exp Ther. 2007;320(2):934-943.
42. Oliveira SM, Silva CR, Ferreira J. Critical role of protease-activated receptor 2 activation by mast cell tryptase in the development of postoperative pain. Anesthesiology. 2013;118(3): 679-690.
43. Hesselink JM. New targets in pain, non-neuronal cells, and the role of palmitoylethanolamide. Open Pain J. 2012;5:12-23.
44. Levy D, Kainz V, Burstein R, Strassman AM. Mast cell degranulation distinctly activates trigemino-cervical and lumbosacral pain pathways and elicits widespread tactile pain hypersensitivity. Brain Behav Immun. 2012;26(2):311-317.
45. Ren K, Dubner R. Interactions between the immune and nervous systems in pain. Nat Med. 2010;16(11):1267-1276.
46. Grandi D, Massi M, Guerrini R, Calo G, Morini G. Role of nociceptin/orphanin FQ receptors in the decrease of mucosal mast cells caused by acute stress in the rat colon. Life Sci. 2011;89(19-20):735-740.