Capsaicin-sensitive sensory nerves exert complex regulatory functions in the serum-transfer mouse model of autoimmune arthritis

Brain, Behavior, and Immunity

Volumn 45, Issue , 2015, Pages 50-59

  Borbély, Éva ^a,b   Botz, Bálint ^a,b   Bölcskei, Kata ^a,b   Kenyér, Tibor ^a   Kereskai, László ^a   Kiss, Tamás ^b   Szolcsányi, János ^a,b,d   Pintér, Erika ^a,b,d   Csepregi, Janka Zsófia ^c   Mócsai, Attila ^c   Helyes, Zsuzsanna ^a,b,d  

^a UNIVERSITY OF PÉCS   (Hungary)

^b UNIVERSITY OF PÉCS   (Hungary)

^c SEMMELWEIS UNIVERSITY OF MEDICINE   (Hungary)

^d PharmInVivo Ltd   (Hungary)

Author keywords

Capsaicin sensitive sensory nerves; Inflammation; Matrix metalloproteinase; Pain; Somatostatin

Indexed keywords

CAPSAICIN; COLLAGENASE 3; GELATINASE A; GELATINASE B; RESINIFERATOXIN; SOMATOSTATIN; STROMELYSIN; AGENTS ACTING ON THE PERIPHERAL NERVOUS AND NEUROMUSCULAR SYSTEMS; DITERPENE; MATRIX METALLOPROTEINASE; PEROXIDASE; REACTIVE OXYGEN METABOLITE; TRPV1 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ANIMAL MODEL; ARTICLE; BODY WEIGHT; BONE MASS; BONE STRUCTURE; CONTROLLED STUDY; DESENSITIZATION; ENZYME ACTIVITY; FEMALE; FLUORESCENCE IMAGING; HEAT SENSATION; HISTOPATHOLOGY; HYPERALGESIA; IMMUNOREACTIVITY; IN VIVO STUDY; JOINT FUNCTION; MALE; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; OSSIFICATION; PAIN SEVERITY; PAW EDEMA; PRIORITY JOURNAL; REGULATORY MECHANISM; RHEUMATOID ARTHRITIS; SENSORY NERVE; WEIGHT REDUCTION; AGONISTS; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; EDEMA; EXPERIMENTAL ARTHRITIS; HINDLIMB; HOCK; METABOLISM; PAIN RECEPTOR; PAIN THRESHOLD; PATHOLOGY; PHYSIOLOGY; RADIOGRAPHY;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; CAPSAICIN; DISEASE MODELS, ANIMAL; DITERPENES; EDEMA; HINDLIMB; HYPERALGESIA; MATRIX METALLOPROTEINASES; MICE; MICE, INBRED C57BL; NOCICEPTORS; PAIN THRESHOLD; PEROXIDASE; REACTIVE OXYGEN SPECIES; SENSORY SYSTEM AGENTS; SOMATOSTATIN; TARSUS, ANIMAL; TRPV CATION CHANNELS; X-RAY MICROTOMOGRAPHY;

EID: 84924033234     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.12.012     Document Type: Article

References (60)

1. Alarcón G.S. Methotrexate use in rheumatoid arthritis. A Clinician's perspective. Immunopharmacology 2000, 47:259-271.
2. Almási R., Pethö G., Bölcskei K., Szolcsányi J. Effect of resiniferatoxin on the noxious heat threshold temperature in the rat: a novel heat allodynia model sensitive to analgesics. Br. J. Pharmacol. 2003, 139:49-58.
3. Anichini M., Cesaretti S., Lepori M., Maddali Bongi S., Maresca M., Zoppi M. Substance P in the serum of patients with rheumatoid arthritis. Rev. Rhum. Engl. Ed. 1997, 64:18-21.
4. Arnhold J., Flemmig J. Human myeloperoxidase in innate and acquired immunity. Arch. Biochem. Biophys. 2010, 500:92-106. 10.1016/j.abb.2010.04.008.
5. Bevaart L., Vervoordeldonk M.J., Tak P.P. Evaluation of therapeutic targets in animal models of arthritis: how does it relate to rheumatoid arthritis?. Arthritis Rheum. 2010, 62:2192-2205.
6. Bíró T., Maurer M., Modarres S., Lewin N.E., Brodie C., Acs G., Paus R., Blumberg P.M. Characterization of functional vanilloid receptors expressed by mast cells. Blood 1998, 91:1332-1340.
7. Boettger M.K., Weber K., Gajda M., Bräuer R., Schaible H.G. Spinally applied ketamine or morphine attenuate peripheral inflammation and hyperalgesia in acute and chronic phases of experimental arthritis. Brain Behav. Immun. 2010, 24:474-485. 10.1016/j.bbi.2009.12.002.
8. Bölcskei K., Tékus V., Dézsi L., Szolcsányi J., Petho G. Antinociceptive desensitizing actions of TRPV1 receptor agonists capsaicin, resiniferatoxin and N-oleoyldopamine as measured by determination of the noxious heat and cold thresholds in the rat. Eur. J. Pain 2010, 14:480-486.
9. Botz B., Bölcskei K., Kereskai L., Kovács M., Németh T., Szigeti K., Horváth I., Máthé D., Kovács N., Hashimoto H., Reglodi D., Szolcsányi J., Pintér E., Mócsai A., Helyes Z. Differential regulatory role of pituitary adenylate-cyclase activating polypeptide in the serum-transfer-induced arthritis model. Arthritis Rheumatol. 2014, 66:2739-2750. 10.1002/art.38772.
10. Brito R., Sheth S., Mukherjea D., Rybak L.P., Ramkumar V. TRPV1: a potential drug target for treating various diseases. Cells 2014, 3:517-545.
11. Cai A., Hutchison E., Hudson J., Kawashima Y., Komori N., Singh A., Brush R.S., Anderson R.E., Sonntag W.E., Matsumoto H., Griffin T.M. Metabolic enrichment of omega-3 polyunsaturated fatty acids does not reduce the onset of idiopathic knee osteoarthritis in mice. Osteoarthritis Cartilage 2014, 22:1301-1309. 10.1016/j.joca.2014.06.033.
12. Cavanaugh D.J., Lee H., Lo L., Shields S.D., Zylka M.J., Basbaum A.I., Anderson D.J. Distinct subsets of unmyelinated primary sensory fibers mediate behavioural responses to noxious thermal and mechanical stimuli. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:9075-9080. 10.1073/pnas.0901507106.
13. Chen W.T., Tung C.H., Weissleder R. Imaging reactive oxygen species in arthritis. Mol. Imag. 2004, 3:159-162.
14. Christianson C.A., Corr M., Firestein G.S., Mobargha A., Yaksh T.L., Svensson C.I. Characterization of the acute and persistent pain state present in K/BxN serum transfer arthritis. Pain 2010, 151:394-403.
15. Czikora Á., Rutkai I., Pásztor E.T., Szalai A., Pórszász R., Boczán J., Édes I., Papp Z., Tóth A. Different desensitization patterns for sensory and vascular TRPV1 populations in the rat: expression, localization and functional consequences. PLoS ONE 2013, 8:e78184. 10.1371/journal.pone.0078184.
16. Danigo A., Magy L., Richard L., Sturtz F., Funalot B., Demiot C. A reversible functional sensory neuropathy model. Neurosci. Lett. 2014, 571:39-44.
17. Denko C.W., Malemud C.J. The serum growth hormone to somatostatin ratio is skewed upward in rheumatoid arthritis patients. Front. Biosci. 2004, 9:1660-1664.
18. Edwards R.R., Wasan A.D., Bingham C.O., Bathon J., Haythornthwaite J.A., Smith M.T., Page G.G. Enhanced reactivity to pain in patients with rheumatoid arthritis. Arthritis Res. Ther. 2009, 11:R61. 10.1186/ar2684.
19. Elekes K., Helyes Z., Németh J., Sándor K., Pozsgai G., Kereskai L., Börzsei R., Pintér E., Szabó A., Szolcsányi J. Role of capsaicin-sensitive afferents and sensory neuropeptides in endotoxin-induced airway inflammation and consequent bronchial hyperreactivity in the mouse. Regul. Pept. 2007, 141:44-54.
20. Fernandes E.S., Russell F.A., Spina D., McDougall J.J., Graepel R., Gentry C., Staniland A.A., Mountford D.M., Keeble J.E., Malcangio M., Bevan S., Brain S.D. A distinct role for transient receptor potential ankyrin 1, in addition to transient receptor potential vanilloid 1, in tumor necrosis factor α-induced inflammatory hyperalgesia and Freund's complete adjuvant-induced monarthritis. Arthritis Rheum. 2011, 63:819-829. 10.1002/art.30150.
21. Fioravanti A., Govoni M., La Montagna G., Perpignano G., Tirri G., Trotta F., Bogliolo A., Ciocci A., Mauceri M.T., Marcolongo R. Somatostatin 14 and joint inflammation: evidence for intraarticular efficacy of prolonged administration in rheumatoid arthritis. Drugs Exp. Clin. Res. 1995, 21:97-103.
22. Fukushima A., Boyle D.L., Corr M., Firestein G.S. Kinetic analysis of synovial signalling and gene expression in animal models of arthritis. Ann. Rheum. Dis. 2010, 69:918-923.
23. Gross S., Gammon S.T., Moss B.L., Rauch D., Harding J., Heinecke J.W., Ratner L., Piwnica-Worms D. Bioluminescence imaging of myeloperoxidase activity in vivo. Nat. Med. 2009, 15:455-461.
24. Helyes Z., Szabó A., Németh J., Jakab B., Pintér E., Bánvölgyi A., Kereskai L., Kéri G., Szolcsányi J. Antiinflammatory and analgesic effect of somatostatin released from capsaicin-sensitive sensory nerve terminals in Freund's adjuvant-induced chronic arthritis model of the rat. Arthritis Rheum. 2004, 50:1677-1685.
25. Hickman-Brecks C.L., Racz J.L., Meyer D.M., LaBranche T.P., Allen P.M. Th17 cells can provide B cell help in autoantibody induced arthritis. J. Autoimmun. 2011, 36:65-75.
26. Hulse R.P., Beazley-Long N., Hua J., Kennedy H., Prager J., Bevan H., Qiu Y., Fernandes E.S., Gammons M.V., Ballmer-Hofer K., Gittenberger de Groot A.C., Churchill A.J., Harper S.J., Brain S.D., Bates D.O., Donaldson L.F. Regulation of alternative VEGF-A mRNA splicing is a therapeutic target for analgesia. Neurobiol. Dis. 2014, 71C:245-259. 10.1016/j.nbd.2014.08.012.
27. Imhof A.K., Glück L., Gajda M., Lupp A., Bräuer R., Schaible H.G., Schulz S. Differential antiinflammatory and antinociceptive effects of the somatostatin analogs octreotide and pasireotide in a mouse model of immune-mediated arthritis. Arthritis Rheum. 2011, 63:2352-2362.
28. Jones G., Halbert J., Crotty M., Shanahan E.M., Batterham M., Ahern M. The effect of treatment on radiological progression in rheumatoid arthritis: a systematic review of randomized placebo-controlled trials. Rheumatology (Oxford) 2003, 42:6-13.
29. Kelly S., Chapman R.J., Woodhams S., Sagar D.R., Turner J., Burston J.J., Bullock C., Paton K., Huang J., Wong A., McWilliams D.F., Okine B.N., Barrett D.A., Hathway G.J., Walsh D.A., Chapman V. Increased function of pronociceptive TRPV1 at the level of the joint in a rat model of osteoarthritis pain. Ann. Rheum. Dis 2013, 10.1136/annrheumdis-2013-203413.
30. Konttinen Y.T., Tiainen V.M., Gomez-Barrena E., Hukkanen M., Salo J. Innervation of the joint and role of neuropeptides. Ann. N. Y. Acad. Sci. 2006, 1069:149-154.
31. Korganow A.S., Ji H., Mangialaio S., Duchatelle V., Pelanda R., Martin T., Degott C., Kikutani H., Rajewsky K., Pasquali J.L., Benoist C., Mathis D. From systemic T cell self-reactivity to organ-specific autoimmune disease via immunoglobulins. Immunity 1999, 10:451-461.
32. Kourilovitch M., Galarza-Maldonado C., Ortiz-Prado E. Diagnosis and classification of rheumatoid arthritis. J. Autoimmun. 2014, 48-49:26-30.
33. Kouskoff V., Korganow A.S., Duchatelle V., Degott C., Benoist C., Mathis D. Organ-specific disease provoked by systemic autoimmunity. Cell 1996, 87:811-822.
34. Kun J., Helyes Z., Perkecz A., Bán Á., Polgár B., Szolcsányi J., Pintér E. Effect of surgical and chemical sensory denervation on non-neural expression of the transient receptor potential vanilloid 1 (TRPV1) receptors in the rat. J. Mol. Neurosci. 2012, 48:795-803.
35. Larsson J., Ekblom A., Henriksson K., Lundeberg T., Theodorsson E. Concentration of substance P, neurokinin A, calcitonin generelated peptide, neuropeptide Y and vasoactive intestinal polypeptide in synovial fluid from knee joints in patients suffering from rheumatoid arthritis. Scand. J. Rheumatol. 1991, 20:326-335.
36. Leffler A.S., Kosek E., Lerndal T., Nordmark B., Hansson P. Somatosensory perception and function of diffuse noxious inhibitory controls (DNIC) in patients suffering from rheumatoid arthritis. Eur. J. Pain 2002, 6:161-176.
37. Levine J.D., Khasar S.G., Green P.G. Neurogenic inflammation and arthritis. Ann. N. Y. Acad. Sci. 2006, 1069:155-167.
38. Maggi C.A. Tachykinins and calcitonin gene-related peptide (CGRP) as cotransmitters released from peripheral endings of sensory nerves. Prog. Neurobiol. 1995, 45:1-98.
39. Meinel T., Pongratz G., Rauch L., Straub R.H. Neuronal α1/2-adrenergic stimulation of IFN-γ, IL-6, and CXCL-1 in murine spleen in late experimental arthritis. Brain Behav. Immun. 2013, 33:80-89. 10.1016/j.bbi.2013.06.003.
40. Mishra S.K., Hoon M.A. Ablation of TrpV1 neurons reveals their selective role in thermal pain sensation. Mol. Cell. Neurosci. 2010, 43:157-163.
41. Németh J., Helyes Z., Görcs T., Gardi J., Pintér E., Szolcsányi J. Development of somatostatin radioimmunoassay for the measurement of plasma and tissue contents of hormone. Acta Physiol. Hung. 1996, 84:313-315.
42. Németh T., Futosi K., Hably C., Brouns M.R., Jakob S.M., Kovács M., Kertész Z., Walzog B., Settleman J., Mócsai A. Neutrophil functions and autoimmune arthritis in the absence of p190RhoGAP: generation and analysis of a novel null mutation in mice. J. Immunol. 2010, 185:3064-3075.
43. Paran D., Elkayam O., Mayo A., Paran H., Amit M., Yaron M., Caspi D. A pilot study of a long acting somatostatin analogue for the treatment of refractory rheumatoid arthritis. Ann. Rheum. Dis. 2001, 60:888-891.
44. Pintér E., Helyes Z., Szolcsányi J. Inhibitory effect of somatostatin on inflammation and nociception. Pharmacol. Ther. 2006, 112:440-456.
45. Pintér E., Pozsgai G., Hajna Z., Helyes Z., Szolcsányi J. Neuropeptide receptors as potential drug targets in the treatment of inflammatory conditions. Br. J. Clin. Pharmacol. 2014, 77:5-20.
46. Pongratz G., Straub R.H. The B cell, arthritis, and the sympathetic nervous system. Brain Behav. Immun. 2010, 24:186-192. 10.1016/j.bbi.2009.07.002.
47. Riol-Blanco L., Ordovas-Montanes J., Perro M., Naval E., Thiriot A., Alvarez D., Paust S., Wood J.N., von Andrian U.H. Nociceptive sensory neurons drive interleukin-23-mediated psoriasiform skin inflammation. Nature 2014, 510:157-161.
48. Rossi F., Bellini G., Luongo L., Torella M., Mancusi S., De Petrocellis L., Petrosino S., Siniscalco D., Orlando P., Scafuro M., Colacurci N., Perrotta S., Nobili B., Di Marzo V., Maione S. The endovanilloid/endocannabinoid system: a new potential target for osteoporosis therapy. Bone 2011, 48:997-1007. 10.1016/j.bone.2011.01.001.
49. Schett G., Gravallese E. Bone erosion in rheumatoid arthritis: mechanisms, diagnosis and treatment. Nat. Rev. Rheumatol. 2012, 8:656-664.
50. Sousa-Valente J., Andreou A.P., Urban L., Nagy I. Transient receptor potential ion channels in primary sensory neurons as targets for novel analgesics. Br. J. Pharmacol. 2014, 171:2508-2527.
51. Stangenberg L., Burzyn D., Binstadt B.A., Weissleder R., Mahmood U., Benoist C., Mathis D. Denervation protects limbs from inflammatory arthritis via an impact on the microvasculature. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:11419-11424.
52. Szabó Á., Helyes Z., Sándor K., Bite A., Pintér E., Németh J., Bánvölgyi A., Bölcskei K., Elekes K., Szolcsányi J. Role of TRPV1 receptors in adjuvant-induced chronic arthritis: in vivo study using gene-deficient mice. J. Pharmacol. Exp. Ther. 2005, 314:111-119.
53. Szolcsanyi J. Capsaicin-sensitive sensory nerve terminals with local and systemic efferent functions: facts and scopes of an unorthodox neuroregulatory mechanism. Prog. Brain Res. 1996, 113:343-359.
54. Szolcsanyi J., Szallasi A., Szallasi Z., Joo F., Blumberg P.M. Resiniferatoxin: an ultrapotent selective modulator of capsaicin-sensitive primary afferent neurons. J. Pharmacol. Exp. Ther. 1990, 255:923-928.
55. Takeba Y., Suzuki N., Takeno M., Asai T., Tsuboi S., Hoshino T., Sakane T. Modulation of synovial cell function by somatostatin in patients with rheumatoid arthritis. Arthritis Rheum. 1997, 40:2128-2138.
56. Tauber S., Paulsen K., Wolf S., Synwoldt P., Pahl A., Schneider-Stock R., Ullrich O. Regulation of MMP-9 by a WIN-binding site in the monocyte-macrophage system independent from cannabinoid receptors. PLoS ONE 2012, 7:e48272.
57. Vanderschueren D., Laurent M.R., Claessens F., Gielen E., Lagerquist M.K., Vandenput L., Börjesson A.E., Ohlsson C. Sex steroid actions in male bone. Endocr. Rev. 2014, 9. er20141024.
58. Wang W., Jian Z., Guo J., Ning X. Increased levels of serum myeloperoxidase in patients with active rheumatoid arthritis. Life Sci. 2014, S0024-3205(14):761-769. 10.1016/j.lfs.2014.09.012.
59. Yoo S., Lim J.Y., Hwang S.W. Sensory TRP channel interactions with endogenous lipids and their biological outcomes. Molecules 2014, 19:4708-4744.
60. Zhang X., Lan N., Bach P., Nordstokke D., Yu W., Ellis L., Meadows G.G., Weinberg J. Prenatal alcohol exposure alters the course and severity of adjuvant-induced arthritis in female rats. Brain Behav. Immun. 2012, 26:439-450. 10.1016/j.bbi.2011.11.005.