Neuroimmune interactions in allergic skin diseases

Current Opinion in Allergy and Clinical Immunology

Volumn 7, Issue 5, 2007, Pages 365-373

  Cevikbas, Ferda ^a   Steinhoff, Antje ^a   Homey, Bernhard ^b   Steinhoff, Martin ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Allergy; Neuroimmunology; Neuromediator; Proteinase activated receptor

Indexed keywords

CHEMOKINE RECEPTOR; CORTICOTROPIN RELEASING FACTOR; CYTOKINE RECEPTOR; G PROTEIN COUPLED RECEPTOR; HISTAMINE; HISTAMINE H1 RECEPTOR ANTAGONIST; HISTAMINE RECEPTOR; NEUROPEPTIDE RECEPTOR; PROTEINASE ACTIVATED RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ALLERGIC REACTION; ATOPIC DERMATITIS; CELL ACTIVATION; CONTACT ALLERGY; DERMATOPHAGOIDES FARINAE; ECZEMA; ENDOTHELIUM CELL; IMMUNE RESPONSE; INFLAMMATION; LYMPHOCYTE PROLIFERATION; NEUROIMMUNOLOGY; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PRURITUS; REVIEW; SENSORY NERVE; SKIN; SKIN ALLERGY; SKIN CELL;

ALLERGENS; ANIMALS; CYTOKINES; HUMANS; HYPERSENSITIVITY; ION CHANNELS; NEUROGENIC INFLAMMATION; NEUROIMMUNOMODULATION; NEUROPEPTIDES; PERIPHERAL NERVOUS SYSTEM; SKIN; SKIN DISEASES;

EID: 34548688890     PISSN: 15284050     EISSN: 14736322     Source Type: Journal    
DOI: 10.1097/ACI.0b013e3282a644d2     Document Type: Review

References (89)

1. Namura K, Hasegawa G, Egawa M, et al. Relationship of serum brain-derived neurotrophic factor level with other markers of disease severity in patients with atopic dermatitis. Clin Immunol 2007; 122:181-186. This publication reveals the importance of neuropeptides as marker proteins for allergic skin diseases.
2. Raap U, Werfel T, Goltz C, et al. Circulating levels of brain-derived neurotrophic factor correlate with disease severity in the intrinsic type of atopic dermatitis. Allergy 2006; 61:1416-1418. The authors show a clearcut correlation between a recently described neurotrophin and disease severity.
3. Dou YC, Hagstromer L, Emtestam L, Johansson O. Increased nerve growth factor and its receptors in atopic dermatitis: an immunohistochemical study. Arch Dermatol Res 2006; 298:31-37. This study confirms previous animal and in-vitro results.
4. Toyoda M, Nakamura M, Makino T, et al. Nerve growth factor and substance P are useful plasma markers of disease activity in atopic dermatitis. Br J Dermatol 2002; 147:71-79.
5. El-Nour H, Lundeberg L, Al-Tawil R, et al. Upregulation of the axonal growth and the expression of substance P and its NK1 receptor in human allergic contact dermatitis. Immunopharmacol Immunotoxicol 2006; 28:621-631. The authors not only investigated peptide but also receptor levels in a human allergic skin disease.
6. Costa SK, Starr A, Hyslop S, et al. How important are NK1 receptors for influencing microvascular inflammation and itch in the skin? Studies using Phoneutria nigriventer venom. Vascul Pharmacol 2006; 45:209-214. First description of NK1 receptors involved in venom-induced scratching behaviour.
7. Peters EM, Raap U, Welker P, et al. Neurotrophins act as neuroendocrine regulators of skin homeostasis in health and disease. Horm Metab Res 2007; 39:110-124.
8. Yoshioka T, Hikita I, Asakawa M, et al. Spontaneous scratching behaviour in DS-Nh mice as a possible model for pruritus in atopic dermatitis. Immunology 2006; 118:293-301. This publication highlights that DS-Nh mice are suitable as an animal model for pruritus and that histamine 1 antagonist application can serve as therapeutical treatment in atopic dermatitis.
9. Tanaka A, Matsuda H. Expression of nerve growth factor in itchy skins of atopic NC/NgaTnd mice. J Vet Med Sci 2005; 67:915-919.
10. Roosterman D, Goerge T, Schneider SW, et al. Neuronal control of skin function: the skin as a neuroimmunoendocrine organ. Physiol Rev 2006; 86:1309-1379. Concise review about neuroimmune interactions in the skin.
11. Garry A, Fromy B, Blondeau N, et al. Altered acetylcholine, bradykinin and cutaneous pressure-induced vasodilation in mice lacking the TREK1 potassium channel: the endothelial link. EMBO Rep 2007; 8:354-359.
12. Steinhoff M, Brzoska T, Luger TA. Keratinocytes in epidermal immune responses. Curr Opin Allergy Clin Immunol 2001; 1:469-476.
13. Vassilatis DK, Hohmann JG, Zeng H, et al. The G protein-coupled receptor repertoires of human and mouse. Proc Natl Acad Sci USA 2003; 100: 4903-4908.
14. Turner DJ, Martin PC, Rao JN, et al. Substance P regulates migration in rat intestinal epithelial cells. Ann Surg 2007; 245:408-414.
15. Gupta S, Mehrotra S, Villalon C, et al. Effects of female sex hormones on responses to CGRP, acetylcholine, and 5-HT in rat isolated arteries. Headache 2007; 47:564-575. This study verifies the speculated hypothesis about thus far poorly understood direct interactions between the nervous and hormone system.
16. Delgado JM, Cacicedo L, Lorenzo MJ, et al. Secretions of somatostatin and VIP in cultures of fetal rat neuroblasts increased by amino acids. Life Sci 1990; 46:55-58.
17. Gonzalez-Rey E, Chorny A, Delgado M. Regulation of immune tolerance by anti-inflammatory neuropeptides. Nat Rev Immunol 2007; 7:52-63. This review sums up the recent findings of antiinflammatory neuropeptides in the immune response.
18. Fernandez-Martin A, Gonzalez-Rey E, Chorny A, et al. VIP prevents experimental multiple sclerosis by downregulating both inflammatory and autoimmune components of the disease. Ann N Y Acad Sci 2006; 1070:276-281.
19. Hosoi J, Murphy GF, Egan CL, et al. Regulation of Langerhans cell function by nerves containing calcitonin gene-related peptide. Nature 1993; 363:159-163.
20. Kodali S, Ding W, Huang J, et al. Vasoactive intestinal peptide modulates Langerhans cell immune function. J Immunol 2004; 173:6082-6088.
21. Seiffert K, Granstein RD. Neuroendocrine regulation of skin dendritic cells. Ann N Y Acad Sci 2006; 1088:195-206.
22. Steinhoff M, Brzoska T, Luger TA. Keratinocytes in epidermal immune responses. Curr Opin Allergy Clin Immunol 2001; 1:469-476.
23. Antonelli A, Lenzi L, Nakagawara A, et al. Tumor suppressor proteins are differentially affected in human ependymoblastoma and medulloblastoma cells exposed to nerve growth factor. Cancer Invest 2007; 25:94-101.
24. Boominathan L. Some facts and thoughts: p73 as a tumor suppressor gene in the network of tumor suppressors. Mol Cancer 2007; 6:27.
25. Raap U, Kapp A. Neuroimmunological findings in allergic skin diseases. Curr Opin Allergy Clin Immunol 2005; 5:419-424.
26. Bracci-Laudiero L, Aloe L, Caroleo MC, et al. Endogenous NGF regulates CGRP expression in human monocytes, and affects HLA-DR and CD86 expression and IL-10 production. Blood 2005; 106:3507-3514.
27. Kakurai M, Monteforte R, Suto H, et al. Mast cell-derived tumor necrosis factor can promote nerve fiber elongation in the skin during contact hypersensitivity in mice. Am J Pathol 2006; 169:1713-1721.
28. Grutzkau A, Henz BM, Kirchhof L, et al. alpha-Melanocyte stimulating hormone acts as a selective inducer of secretory functions in human mast cells. Biochem Biophys Res Commun 2000; 278:14-19.
29. Hartmeyer M, Scholzen T, Becher E, et al. Human dermal microvascular endothelial cells express the melanocortin receptor type 1 and produce increased levels of IL-8 upon stimulation with alpha-melanocyte- stimulating hormone. J Immunol 1997; 159:1930-1937.
30. Maaser C, Kannengiesser K, Kucharzik T. Role of the melanocortin system in inflammation. Ann N Y Acad Sci 2006; 1072:123-134.
31. Eves P, Haycock J, Layton C, et al. Anti-inflammatory and antiinvasive effects of alpha-melanocyte-stimulating hormone in human melanoma cells. Br J Cancer 2003; 89:2004-2015.
32. Kiss M, Wlaschek M, Brenneisen P, et al. Alpha-melanocyte stimulating hormone induces collagenase/matrix metalloproteinase-1 in human dermal fibroblasts. Biol Chem Hoppe Seyler 1995; 376:425-430.
33. Szolcsanyi J. Forty years in capsaicin research for sensory pharmacology and physiology. Neuropeptides 2004; 38:377-384.
34. Steinhoff M, Vergnolle N, Young SH, et al. Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat Med 2000; 6:151-158.
35. Holzer P. Tachykinins as targets of gastroenterological pharmacotherapy. Drug News Perspect 1998; 11:394-401.
36. Caterina MJ, Leffler A, Malmberg AB, et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000; 288:306-313.
37. Walker KM, Urban L, Medhurst SJ, et al. The VR1 antagonist capsazepine reverses mechanical hyperalgesia in models of inflammatory and neuropathic pain. J Pharmacol Exp Ther 2003; 304:56-62.
38. Banvolgyi A, Palinkas L, Berki T, et al. Evidence for a novel protective role of the vanilloid TRPV1 receptor in a cutaneous contact allergic dermatitis model. J Neuroimmunol 2005; 169:86-96.
39. 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; 24:4300-4312.
40. Amadesi S, Cottrell GS, Divino L, et al. Protease-activated receptor 2 sensitizes TRPV1 by protein kinase Cepsilon- and A-dependent mechanisms in rats and mice. J Physiol 2006; 575:555-571. The paper describes a novel mechanism of receptor sensitization between two neuronal GPCRs which may have an impact during neurogenic inflammation.
41. Hwang SW, Cho H, Kwak J, et al. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci USA 2000; 97:6155-6160.
42. Hutter MM, Wick EC, Day AL, et al. Transient receptor potential vanilloid (TRPV-1) promotes neurogenic inflammation in the pancreas via activation of the neurokinin-1 receptor (NK-1R). Pancreas 2005; 30:260-265.
43. Stander S, Moormann C, Schumacher M, et al. Expression of vanilloid receptor subtype 1 in cutaneous sensory nerve fibers, mast cells, and epithelial cells of appendage structures. Exp Dermatol 2004; 13:129-139.
44. Southall MD, Li T, Gharibova LS, et al. Activation of epidermal vanilloid receptor-1 induces release of proinflammatory mediators in human keratinocytes. J Pharmacol Exp Ther 2003; 304:217-222.
45. Bodo E, Kovacs I, Telek A, et al. Vanilloid receptor-1 (VR1) is widely expressed on various epithelial and mesenchymal cell types of human skin. J Invest Dermatol 2004; 123:410-413.
46. Inoue K, Koizumi S, Fuziwara S, et al. Functional vanilloid receptors in cultured normal human epidermal keratinocytes. Biochem Biophys Res Commun 2002; 291:124-129.
47. Bodo E, Biro T, Telek A, et al. A hot new twist to hair biology: involvement of vanilloid receptor-1 (VR1/TRPV1) signaling in human hair growth control. Am J Pathol 2005; 166:985-998.
48. Xue Q, Jong B, Chen T, Schumacher MA. Transcription of rat TRPV1 utilizes a dual promoter system that is positively regulated by nerve growth factor. J Neurochem 2007; 101:212-222. First description of regulatory mechanisms on transcription level.
49. Takaoka A, Arai I, Sugimoto M, et al. Expression of IL-31 gene transcripts in NC/Nga mice with atopic dermatitis. Eur J Pharmacol 2005; 516:180-181.
50. •]) that IL-31 is critically involved in inflammation and itch in humans.
51. DillonSR, Sprecher C,Hammond A, et al. Interleukin 31, a cytokine produced by activated T cells, induces dermatitis in mice. Nat Immunol 2004; 5:752-760.
52. Bilsborough J, Leung DY, Maurer M, et al. IL-31 is associated with cutaneous lymphocyte antigen-positive skin homing T cells in patients with atopic dermatitis. J Allergy Clin Immunol 2006; 117:418-425.
53. Kanda N, Shimizu T, Tada Y, Watanabe S. IL-18 enhances IFN-gamma-induced production of CXCL9, CXCL10, and CXCL11 in human keratinocytes. Eur J Immunol 2007; 37:338-350.
54. Vergnolle N, Ferazzini M, D'Andrea MR, et al. Proteinase-activated receptors: novel signals for peripheral nerves. Trends Neurosci 2003; 26:496-500.
55. Hollenberg MD. Proteinase-mediated signaling: proteinase-activated receptors (PARs) and much more. Life Sci 2003; 74:237-246.
56. Hollenberg MD, Compton SJ. International Union of Pharmacology. XXVIII: Proteinase-activated receptors. Pharmacol Rev 2002; 54:203-217.
57. Shpacovitch V, Seeliger S, Huber-Lang M, Balkow S. Agonists of proteinase-activated receptor-2 affect transendothelial migration and apoptosis of human neutrophils in vitro. Exp Dermatol (in press).
58. Steinhoff M, Neisius U, Ikoma A, et al. Proteinase-activated receptor-2 mediates itch: a novel pathway for pruritus in human skin. J Neurosci 2003; 23:6176-6180.
59. Shimada SG, Shimada KA, Collins JG. Scratching behavior in mice induced by the proteinase-activated receptor-2 agonist, SLIGRL-NH2. Eur J Pharmacol 2006; 20:281-283.
60. 2 in itch.
61. Hachem JP, Houben E, Crumrine D, et al. Serine protease signaling of epidermal permeability barrier homeostasis. J Invest Dermatol 2006; 126:2074-2086.
62. Dunford PJ, Williams KN, Desai PJ, et al. Histamine H4 receptor antagonists are superior to traditional antihistamines in the attenuation of experimental pruritus. J Allergy Clin Immunol 2007; 119:176-183. The authors suggest that H4R antagonists are able of attenuating pruritic diseases when H1R antagonists are not effective.
63. Heyer G, Koppert W, Martus P, Handwerker HO. Histamine and cutaneous nociception: histamine-induced responses in patients with atopic eczema, psoriasis and urticaria. Acta Derm Venereol 1998; 78:123-126.
64. Heyer GR, Hornstein OP. Recent studies of cutaneous nociception in atopic and nonatopic subjects. J Dermatol 1999; 26:77-86.
65. Ohmura T, Hayashi T, Satoh Y, et al. Involvement of substance P in scratching behaviour in an atopic dermatitis model. Eur J Pharmacol 2004; 491:191-194.
66. Yokote R, Yagi H, Furukawa F, Takigawa M. Regulation of peripheral blood mononuclear cell responses to Dermatophagoides farinae by substance P in patients with atopic dermatitis. Arch Dermatol Res 1998; 290:191-197.
67. Liu JY, Hu JH, Zhu QG, et al. Effect of matrine on the expression of substance P receptor and inflammatory cytokines production in human skin keratinocytes and fibroblasts. Int Immunopharmacol 2007; 7:816-823.
68. Amano H, Negishi I, Akiyama H, Ishikawa O. Psychological stress can trigger atopic dermatitis in NC/Nga mice: an inhibitory effect of corticotropin-releasing factor. Neuropsychopharmacology (2007). This paper describes a novel mechanism of the therapeutical approach.
69. Bigliardi-Qi M, Lipp B, Sumanovski LT, et al. Changes of epidermal mu-opiate receptor expression and nerve endings in chronic atopic dermatitis. Dermatology 2005; 210:91-99.
70. Bigliardi-Qi M, Gaveriaux-Ruff C, Pfaltz K, et al. Deletion of mu- and kappa-opioid receptors in mice changes epidermal hypertrophy, density of peripheral nerve endings, and itch behavior. J Invest Dermatol 2007; 127:1479-1488.
71. Grewe M, Vogelsang K, Ruzicka T, et al. Neurotrophin-4 production by human epidermal keratinocytes: increased expression in atopic dermatitis. J Invest Dermatol 2000; 114:1108-1112.
72. Raap U, Kapp A. Neuroimmunological findings in allergic skin diseases. Curr Opin Allergy Clin Immunol 2005; 5:419-424.
73. Bae SJ, Lee JB, Takenaka M, et al. Topical glucocorticoid augments scratching behaviour in dinitrofluorobenzene-sensitized mice by the induction of substance P. Exp Dermatol 2004; 13:780-785.
74. Scholzen TE, Steinhoff M, Sindrilaru A, et al. Cutaneous allergic contact dermatitis responses are diminished in mice deficient in neurokinin 1 receptors and augmented by neurokinin 2 receptor blockage. FASEB J 2004; 18:1007-1009.
75. Niizeki H, Kurimoto I, Streilein JW. A substance P agonist acts as an adjuvant to promote hapten-specific skin immunity. J Invest Dermatol 1999; 112:437-442.
76. Ansel JC, Brown JR, Payan DG, Brown MA. Substance P selectively activates TNF-alpha gene expression in murine mast cells. J Immunol 1993; 150:4478-4485.
77. Niizeki H, Alard P, Streilein JW. Calcitonin gene-related peptide is necessary for ultraviolet B-impaired induction of contact hypersensitivity. J Immunol 1997; 159:5183-5186.
78. Elliott JC, Picker MJ, Nelson CJ, et al. Sex differences in opioid-induced enhancement of contact hypersensitivity. J Invest Dermatol 2003; 121:1053-1059.
79. Elliott JC, Wagner AF, Lysle DT. Neurokinin 1 receptor signaling mediates sex differences in mu and kappa opioid-induced enhancement of contact hypersensitivity. J Neuroimmunol 2006; 181:100-105. Verifies findings of Ref. [78], and presents novel insights into receptor-receptor interactions in allergic diseases.
80. Nelson DA, Bost KL. Quantification of hemokinin-1 peptide production and secretion from mouse B cells. Cell Immunol 2005; 237:115-122.
81. Morteau O, Lu B, Gerard C, Gerard NP. Hemokinin 1 is a full agonist at the substance P receptor. Nat Immunol 2001; 2:1088.
82. Zhang Y, Lu L, Furlonger C, et al. Hemokinin is a hematopoietic-specific tachykinin that regulates B lymphopoiesis. Nat Immunol 2000; 1:392-397.
83. Homey B, Steinhoff M, Ruzicka T, Leung DY. Cytokines and chemokines orchestrate atopic skin inflammation. J Allergy Clin Immunol 2006; 118:178-189.
84. Steinhoff M, Steinhoff A, Homey B, et al. Role of vasculature in atopic dermatitis. J Allergy Clin Immunol 2006; 118:190-197.
85. Steinhoff M, Bienenstock J, Schmelz M, et al. Neurophysiological, neuroimmunological, and neuroendocrine basis of pruritus. J Invest Dermatol 2006; 126:1705-1718.
86. Luger TA, Brzoska T, Scholzen TE, et al. The role of alpha-MSH as a modulator of cutaneous inflammation. Ann N Y Acad Sci 2000; 917:232-238.
87. Grassberger M, Steinhoff M, Schneider D, Luger TA. Pimecrolimus: an anti-inflammatory drug targeting the skin. Exp Dermatol 2004; 13:721-730.
88. Sugata Y, Okano M, Fujiwara T, et al. Histamine H4 receptor agonists have more activities than H4 agonism in antigen-specific human T-cell responses. Immunology 2007; 121:266-275.
89. Gutzmer R, Diestel C, Mommert S, et al. Histamine H4 receptor stimulation suppresses IL-12p70 production and mediates chemotaxis in human monocyte-derived dendritic cells. J Immunol 2005; 174:5224-5232.