Neuroimmunological mechanism of pruritus in atopic dermatitis focused on the role of serotonin

Biomolecules and Therapeutics

Volumn 20, Issue 6, 2012, Pages 506-512

  Kim, Kwangmi ^a  

^a Dankook University   (South Korea)

Author keywords

Atopic dermatitis; Neuromediator; Pruritus; Serotonin; T cells

Indexed keywords

4 IODO 2,5 DIMETHOXYAMPHETAMINE; AMFEBUTAMONE; CYCLOSPORIN A; DOXEPIN; FENFLURAMINE; FLUOXETINE; FLUVOXAMINE; GLUCOCORTICOID; NALTREXONE; PAROXETINE; PIMECROLIMUS; RECOMBINANT INTERLEUKIN 2; SEROTONIN RECEPTOR; SEROTONIN TRANSPORTER; TACROLIMUS; TANDOSPIRONE; TRIMIPRAMINE;

ATOPIC DERMATITIS; CD3+ T LYMPHOCYTE; CELL PROLIFERATION; CLINICAL FEATURE; DENDRITIC CELL; DRUG ACTIVITY; DRUG DETERMINATION; DRUG EFFICACY; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; FIBROBLAST; HUMAN; IMMUNE SYSTEM; KERATINOCYTE; LANGERHANS CELL; MAST CELL; MELANOCYTE; NATURAL KILLER CELL; NERVOUS SYSTEM; NEUROIMMUNOLOGY; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; PRURITUS; REVIEW; SENSORY NERVE; T LYMPHOCYTE; TREATMENT RESPONSE;

EID: 84870905551     PISSN: 19769148     EISSN: 20054483     Source Type: Journal    
DOI: 10.4062/biomolther.2012.20.6.506     Document Type: Review

References (86)

1. Andrew, D. and Craig, A. D. (2001) Spinothalamic lamina I neurons selectively sensitive to histamine: a central neural pathway for itch. Nat. Neurosci. 4, 72-77.
2. Aune, T. M., McGrath, K. M., Sarr, T., Bombara, M. P. and Kelley, K. A. (1993) Expression of 5HT1a receptors on activated human T cells. Regulation of cyclic AMP levels and T cell proliferation by 5-hydroxytryptamine. J. Immunol. 151, 1175-1183.
3. Aune, T. M., Golden, H. W. and McGrath, K. M. (1994) Inhibitors of se rotonin synthesis and antagonists of serotonin 1A receptors inhibit T lymphocyte function in vitro and cell-mediated immunity in vivo. J. Immunol. 153, 489-498.
4. Bilsborough, J., Leung, D. Y., Maurer, M., Howell, M., Boguniewicz, M., Yao, L., Storey, H., LeCiel, C., Harder, B. and Gross, J. A. (2006) IL-31 is associated with cutaneous lymphocyte antigen-positive skin homing T cells in patients with atopic dermatitis. J. Allergy Clin. Immunol. 117, 418-425.
5. Buske-Kirschbaum, A., Geiben, A. and Hellhammer, D. (2001) Psy chobiological aspects of atopic dermatitis: an overview. Psychother. Psychosom. 70, 6-16.
6. Cevikbas, F., Steinhoff, A., Homey, B. and Steinhoff M. (2007) Neuro immune interactions in allergic skin diseases. Curr. Opin. Allergy Clin. Immunol. 7, 365-373.
7. Cevikbas, F., Steinhoff, M. and Ikoma, A. (2011) Role of spinal neu rotransmitter receptors in itch: new insights into therapies and drug development. CNS Neurosci. Ther. 17, 742-749
8. Connor, T. J., Kelly, J. P. and Leonard, B. E. (2000) An assessment of the acute effects of serotonin releasers methylenedioxymethamphetamine, methylenedioxyamphetamine and fenfluramine on immunity in rats. Immunopharmacology 46, 223-235.
9. Cowden, J. M., Zhang, M., Dunford, P. J. and Thurmond, R. L. (2010) The histamine H4 receptor mediates inflammation and pruritus in Th2-dependent dermal inflammation. J. Invest. Dermatol. 130, 1023-1033.
10. Darsow, U., Scharein, E., Bromm, B. and Ring, J. (1997) Skin testing of the pruritogenic activity of histamine and cytokines (interleukinand tumour necrosis factor-alpha) at the dermal-epidermal junction. Br. J. Dermatol. 137, 415-417.
11. de Mel, S., Nordlind, K., Holst, M., Frohm-Nilsson, M. and Lonne Rahm, S. B. (2012) Polymorphisms in the serotonin transporter gene of patients with atopic dermatitis-association with personality traits related to high level of anxiety. Immunopharmacol. Immunotoxicol. 34, 534-538.
12. Diehn, F. and Tefferi, A. (2001) Pruritus in polycythaemia vera: preva lence, laboratory correlates and management. Br. J. Haematol. 115, 619-621.
13. Dijkstra, D., Leurs, R., Chazot, P., Shenton, F. C., Stark, H. and Wer fel, T. and Gutzmer, R. (2007) Histamine downregulates monocyte CCL2 production through the histamine H4 receptor. J. Allergy Clin. Immunol. 120, 300-307.
14. Drake, L. A. and Millikan, L. E. (1995) The antipruritic effect of 5% doxepin cream in patients with eczematous dermatitis. Doxepin Study Goup. Arch. Dermatol. 131, 1403-1408.
15. Dunford, P. J., Williams, K. N., Desai, P. J., Karlsson, L., McQueen, D. and Thurmond, R. L. (2007) Histamine H4 receptor antagonists are superior to traditional antihistamines in the attenuation of experimental pruritus. J. Allergy Clin. Immunol. 119, 176-183.
16. Edgar V. A., Sterin-Borda, L., Cremaschi, G. A. and Genaro, A. M. (1999) Role of protein kinase C and cAMP in fluoxetine effects on human T-cell proliferation. Eur. J. Pharmacol. 372, 65-73.
17. El-Nour, H., Lundeberg, L., Abdel-Magid, N., Lonne-Rahm, S. B., Azmitia, E. C. and Nordlind, K. (2007) Serotonergic mechanisms in human allergic contact dermatitis. Acta Derm. Venereol. 87, 390-396.
18. Elenkov, I. J. (2004) Glucocorticoids and the Th1/Th2 balance. Ann. N. Y. Acad. Sci. 1024, 138-146.
19. Faraj, B. A., Olkowski, Z. L. and Jackson, R. T. (1994) Expression of a high-affinity serotonin transporter in human lymphocytes. Int. J. Immunopharmacol. 16, 561-567.
20. Frank, M. G., Hendricks, S. E., Johnson, D. R., Wieseler, J. L. and Burke, W. J. (1999) Antidepressants augment natural killer cell activity: in vivo and in vitro. Neuropsychobiology. 39, 18-24.
21. Gonzaléz-Rey, E., Chorny, A. and Delgado, M. (2007) Regulation of immune tolerance by anti-inflammatory neuropeptides. Nat. Rev. Immunol. 7, 52-63.
22. Gonzalez, E., Sanguino, R. M. and Franco, M. A. (2006). Bupropion in atopic dermatitis. Pharmacopsychiatry 39, 229.
23. Gordon, J. and Barnes, N. M. (2003) Lymphocytes transport serotonin and dopamine: agony or ecstasy? Trends Immunol. 24, 438-443.
24. Greaves, M. W. and Khalifa, N. (2004) Itch: more than skin deep. Int. Arch. Allergy Immunol. 135, 166-172.
25. Gutzmer, R., Mommert, S., Gschwandtner, M., Zwingmann, K., Stark, H. and Werfel, T. (2009) The histamine H4 receptor is functionally expressed on Th2 cells. J. Allergy Clin. Immunol. 123, 619-625.
26. Handwerker, H. O. and Schmelz, M. (2009) Pain: itch without pain-a labeled line for itch sensation? Nat. Rev. Neurol. 5, 640-641.
27. Hanifin, J. M., Ling, M. R., Langley, R., Breneman, D. and Rafal, E. (2001) Tacrolimus ointment for the treatment of atopic dermatitis in adult patients: part I, efficacy. J. Am. Acad. Dermatol. 44, S28-S38.
28. Hennino, A., Jean-Decoster, C., Giordano-Labadie, F., Debeer, S., Vanbervliet, B., Rozières, A., Schmitt, A. M. and Nicolas, J. F. (2011) CD8+ T cells are recruited early to allergen exposure sites in atopy patch test reactions in human atopic dermatitis. J. Allergy Clin. Immunol. 127, 1064-1067.
29. Heyer, G. R. and Hornstein, O. P. (1999). Recent studies of cutaneous nociception in atopic and non-atopic subjects. J. Dermatol. 26, 77-86.
30. Hoare, C., Li Wan Po, A. and Williams, H. (2000) Systematic review of treatments for atopic eczema. Health Technol. Assess. 4, 1-191.
31. Jameson, J., Ugarte, K., Chen, N., Yachi, P., Fuchs, E., Boismenu, R. and Havran, W. L. (2002) A role for skin gammadelta T cells in wound repair. Science 296, 747-749.
32. Järvikallio, A., Harvima, I. T. and Naukkarinen, A. (2003) Mast cells, nerves and neuropeptides in atopic dermatitis and nummular eczema. Arch. Dermatol. Res. 295, 2-7.
33. Kawana, S., Kato, Y. and Omi, T. (2010) Efficacy of a 5-HT1a receptor agonist in atopic dermatitis. Clin. Exp. Dermatol. 35, 835-840.
34. Klein, P. A. and Clark, R. A. (1999) An evidence-based review of the efficacy of antihistamines in relieving pruritus in atopic dermatitis. Arch. Dermatol. 135, 1522-1525.
35. Koblenzer, C. S. (1999) Itching and the atopic skin. J. Allergy Clin. Immunol. 104, S109-S113.
36. Kroeze, W. K., Kristiansen, K. and Roth, B. L. (2002) Molecular biology of serotonin receptors structure and function at the molecular level. Curr. Top. Med. Chem. 2, 507-528.
37. Lee, C. H. (2010) Progress of pruritus research in atopic dermatitis. Biomol. Ther. 18, 246-256.
38. Lee, H. J., Park, M. K., Kim, S. Y., Park Choo H. Y., Lee, A. Y. and Lee, C. H. (2011) Serotonin induces melanogenesis via serotonin receptor 2A. Br. J. Dermatol. 165, 1344-1348.
39. Leung, D. Y. and Bieber, T. (2003) Atopic dermatitis. Lancet 361, 151-160.
40. Leung, D. M., Boguniewicz, M., Howell, M. D., Nomura, I. and Hamid, Q. A. (2004) New insights into atopic dermatitis. J. Clin. Invest. 113, 651-657.
41. Lonne-Rahm, S. B., Rickberg, H., El-Nour, H., Mårin, P., Azmitia, E. C. and Nordlind, K. (2008) Neuroimmune mechanisms in patients with atopic dermatitis during chronic stress. J. Eur. Acad. Dermatol. Venereol. 22, 11-18.
42. Luger, T. A. (2002) Neuromediators a crucial component of the skin immune system. J. Dermatol. Sci. 30, 87-93.
43. Luger, T., Van Leent, E. J., Graeber, M., Hedgecock, S., Thurston, M., Kandra, A., Berth-Jones, J., Bjerke, J., Christophers, E., Knop, J., Knulst, A. C., Morren, M., Morris, A., Reitamo, S., Roed-Petersen, J., Schoepf, E., Thestrup-Pedersen, K., Van Der Valk, P. G. and Bos, J. D. (2001) SDZ ASM 981: an emerging safe and effective treatment for atopic dermatitis. Br. J. Dermatol. 144, 788-794.
44. Meredith, E. J., Chamba, A., Holder, M. J., Barnes, N. M. and Gordon, J. (2005) Close encounters of the monoamine kind: immune cells betray their nervous disposition. Immunology 115, 289-295.
45. Metz, M., Grundmann, S. and Ständer, S. (2011) Pruritus: an overview of current concepts. Veterinary. Dermatology 22, 121-131.
46. Mommert, S., Gschwandtner, M., Gutzmer, R. and Werfel, T. (2011) The role of the histamine H4 receptor in atopic dermatitis. Curr. Allergy Asthma Rep. 11, 21-28.
47. Morren, M. A., Przybilla, B., Bamelis, M., Heykants, B., Reynaers, A. and Degreef, H. (1994) Atopic dermatitis: triggering factors. J. Am. Acad. Dermatol. 31, 467-473.
48. Mössner, R. and Lesch, K. P. (1998) Role of serotonin in the immune system and in neuroimmune interactions. Brain. Behav. Immun. 12, 249-271.
49. Nakano, T., Andoh, T., Lee, J. B. and Kuraishi, Y. (2008) Different dorsal horn neurons responding to histamine and allergic itch stimuli. Neuroreport 19, 723-726.
50. Novak, N. and Leung, D. Y. (2011) Advances in atopic dermatitis. Curr. Opin. Immunol. 23, 778-783.
51. Pastar, Z., Lipozencic, J. and Ljubojevic S. (2005) Etiopathogenesis of atopic dermatitis an overview. Acta Dermatovenerol. Croat. 13, 54-62.
52. Paus, R., Schmelz, M., Bíró, T. and Steinhoff, M. (2006) Frontiers in pruritus research: scratching the brain for more effective itch therapy. J. Clin. Invest. 116, 1174-1186.
53. Pellegrino, T. C. and Bayer, B. M. (2000) Specific serotonin reuptake inhibitor-induced decreases in lymphocyte activity require endogenous serotonin release. Neuroimmunomodulation 8, 179-187
54. Pellegrino, T. C. and Bayer, B. M. (2002) Role of central 5-HT (2) receptors in fluoxetine-induced decreases in T lymphocyte activity. Brain Behav. Immun. 16, 87-103.
55. Roosterman, D., Goerge, T., Schneider, S.W., Bunnett, N. W. and Steinhoff, M. (2006) Neuronal control of skin function: the skin as a neuroimmunoendocrine organ. Physiol. Rev. 86, 1309-1379.
56. Rudd, M. L., Nicolas, A. N., Brown, B. L., Fischer-Stenger, K. and Stewart, J. K. (2005) Peritoneal macrophages express the serotonin transporter. J. Neuroimmunol. 159, 113-118.
57. Rukwied, R., Lischetzki, G., McGlone, F., Heyer, G. and Schmelz, M. (2000) Mast cell mediators other than histamine induce pruritus in atopic dermatitis patients: a dermal microdialysis study. Br. J. Dermatol. 142, 1114-1120.
58. Savin, J. A., Paterson, W. D., Adam, K. and Oswald, I. (1979) Effects of trimeprazine and trimipramine on nocturnal scratching in patients with atopic eczema. Arch. Dermatol.115, 313-315.
59. Schmelz, M. (2001) A neural pathway for itch. Nat. Neurosci. 4, 9-10
60. Schmelz, M., Hilliges, M., Schmidt, R., Ørstavik, K., Vahlquist, C., Weidner, C., Handwerker, H. O. and Torebjörk, H. E. (2003) Active "itch fibers" in chronic pruritus. Neurology 61, 564-566.
61. Seuwen, K. and Pouysségur, J. (1990) Serotonin as a growth factor. Biochem. Pharmacol. 39, 985-990.
62. Sharp, L. L., Jameson, J. M., Witherden, D. A., Komori, H. K. and Havran, W. L. (2005) Dendritic epidermal T-cell activation. Crit. Rev. Immunol. 25, 1-18.
63. Shimoda, T., Liang, Z., Suzuki, H. and Kawana, S. (2010) Inhibitory effects of antipsychotic and anxiolytic agents on stress induced degranulation of mouse dermal mast cells. Clin. Exp. Dermatol. 35, 531-536.
64. Slominski, A., Pisarchik, A., Zbytek, B., Tobin, D. J., Kauser, S. and Wortsman, J. (2003) Functional activity of serotoninergic and melatoninergic systems expressed in the skin. J. Cell. Physiol. 196, 144-153.
65. Slominski, A., Wortsman, J. and Tobin, D. J. (2005) The cutaneous serotonergic/melatonergic system: securing a place under the sun. FASEB J. 19, 176-194.
66. Sonkoly, E., Muller, A., Lauerma, A. I., Pivarcsi, A., Soto, H., Kemeny, L., Alenius, H., Dieu-Nosjean, M. C., Meller, S., Rieker, J., Steinhoff, M., Hoffmann, T. K., Ruzicka, T., Zlotnik, A. and Homey, B. (2006) IL-31: A new link between T cells and pruritus in atopic skin inflammation. J. Allergy Clin. Immunol. 117, 411-417.
67. Ständer, S., Gunzer, M., Metze, D., Luger, T. and Steinhoff, M. (2002) Localization of mu-opioid receptor 1A on sensory nerve fibers in human skin. Regul. Pept. 110, 75-83.
68. Ständer, S., Weisshaar, E. and Luger, T. A. (2008) Neurophysiologi cal and neurochemical basis of modern pruritus treatment. Exp. Dermatol. 17, 161-169.
69. Ständer, S., Böckenholt, B., Schürmeyer-Horst, F., Weishaupt, C., Heuft, G., Luger, T. A. and Schneider, G. (2009) Treatment of chronic pruritus with the selective serotonin re-uptake inhibitors paroxetine and fluvoxamine: results of an open-labelled, two-arm proof-of concept study. Acta Derm. Venereol. 89, 45-51
70. Steinhoff, M., Bienenstock, J., Schmelz, M., Maurer, M., Wei, E. and Bíró, T. (2006) Neurophysiological, neuroimmunological, and neu roendocrine basis of pruritus. J. Invest. Dermatol. 126, 1705-1718.
71. Straub, R. H. (2004) Complexity of the bi-directional neuroimmune junction in the spleen. Trends Pharmacol. Sci. 25, 640-646.
72. Strid, J., Tigelaar, R. E. and Hayday, A. C. (2009) Skin immune surveillance by T cells--a new order? Semin. Immunol. 21, 110-120.
73. Sugimoto, Y., Iba, Y., Nakamura, Y., Kayasuga, R. and Kamei C. (2004) Pruritus-associated response mediated by cutaneous histamine H3 receptors. Clin. Exp. Allergy 34, 456-459.
74. Tobin, D., Nabarro, G., Baart de la Faille, H., van Vloten, W. A., van der Putte, S. C. and Schuurman, H. J. (1992) Increased number of immunoreactive nerve fibers in atopic dermatitis. J. Allergy Clin. Immunol. 90, 613-622.
75. Turner, D. J., Martin, P. C., Rao, J. N., Greenspon, J., Zou, T., Bass, B. L., Wang, J. Y. and Strauch, E. D. (2007) Substance P regulates migration in rat intestinal epithelial cells. Ann. Surg. 245, 408-414.
76. Urashima, R. and Mihara, M. (1998) Cutaneous nerves in atopic dermatitis. A histological, immunohistochemical and electron microscopic study. Virchows. Arch. 432, 363-370.
77. Wahlgren, C. F., Scheynius, A. and Hägemark, O. (1990) Antipruritic effect of oral cyclosporin A in atopic dermatitis. Acta. Derm. Venereol. 70, 323-329.
78. Wahlgren, C. F. (1992) Pathophysiology of itching in urticaria and atop ic dermatitis. Allergy 47, 65-75.
79. Wahlgren, C. F., Tengvall, Linder, M., Hägemark, O. and Scheynius, A. (1995) Itch and inflammation induced by intradermally injected interleukin-2 in atopic dermatitis patients and healthy subjects. Arch. Dermatol. Res. 287, 572-580.
80. Weidinger, S., Gieger, C., Rodriguez, E., Baurecht, H., Mempel, M., Klopp, N., Gohlke, H., Waqenpfeil, S., Ollert, M., Ring, J., Behrendt, H., Heinrich, J., Novak, N., Bieber, T., Krämer, U., Berdel, D., von Berg, A., Bauer, C. P., Herbarth, O., Koletzko, S., Prokisch, H., Mehta, D., Meitinger, T., Depner, M., von Mutius, E., Liang, L., Moffatt, M., Cookson, W., Kabesch, M., Wichmann, H. E. and Illig, T. (2008) Genome-wide scan on total serum IgE levels identifies FCER1A as novel susceptibility locus. PLoS. Genet. 4, e1000166.
81. Weisshaar, E., Ziethen, B. and Gollnick, H. (1997) Can a serotonin type 3 (5-HT3) receptor antagonist reduce experimentally-induced itch? Inflamm. Res. 46, 412-416
82. Witherden, D. A., Verdino, P., Rieder, S. E., Garijo, O., Mills, R. E., Teyton, L., Fischer, W. H., Wilson, I. A. and Havran, W. L. (2010) The junctional adhesion molecule JAML is a costimulatory receptor for epithelial gammadelta T cell activation. Science 329, 1205-1210.
83. Yamaguchi, T., Nagasawa, T., Satoh, M. and Kuraishi, Y. (1999) Itchassociated response induced by intradermal serotonin through 5-HT2 receptors in mice. Neurosci. Res. 35, 77-83.
84. Yaris, E., Kesim, M., Kadioglu, M., Kalyoncu, N. I., Ulku, C. and Ozyavuz, R. (2003) The effects of paroxetine on rat isolated vas deferens. Pharmacol. Res. 48, 335-345.
85. Yosipovitch, G., Szolar, C., Hui, X. Y. and Maibach, H. (1996) High potency topical corticosteroid rapidly decreases histamine-induced itch but not thermal sensation and pain in human beings. J. Am. Acad. Dermatol. 35, 118-120.
86. Zylicz, Z., Krajnik, M., Sorge, A. A. and Costantini, M. (2003) Paroxetine in the treatment of severe non-dermatological pruritus: a randomized, controlled trial. J. Pain. Symptom Manage. 26, 1105-1112.