Neurophysiological, neuroimmunological, and neuroendocrine basis of pruritus

Journal of Investigative Dermatology

Volumn 126, Issue 8, 2006, Pages 1705-1718

  Steinhoff, Martin ^a   Bienenstock, John ^b   Schmelz, Martin ^c   Maurer, Marcus ^d   Wei, Ed ^e   Bíró, Tamás ^f  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b MCMASTER UNIVERSITY   (Canada)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d HUMBOLDT UNIVERSITY   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

ANALGESIC AGENT; ANANDAMIDE; ANTIHISTAMINIC AGENT; ANTIPRURITIC AGENT; BIOGENIC AMINE; BRADYKININ ANTAGONIST; CANNABINOID; CAPSAICIN; CYCLOSPORIN A; CYTOKINE; FENTANYL; IMMUNOSUPPRESSIVE AGENT; KININ; MORPHINE; NALBUPHINE; NALFURAFINE; NALMEFENE; NALOXONE; NALTREXONE; NEUROPEPTIDE; NEUROTRANSMITTER; NEUROTROPHIN; OPIATE; OPIATE AGONIST; OPIATE ANTAGONIST; PIMECROLIMUS; PROTEINASE; PROTEINASE INHIBITOR; RECOMBINANT GAMMA INTERFERON; RECOMBINANT INTERLEUKIN 1; TACROLIMUS;

CENTRAL NERVOUS SYSTEM; CYTOKINE RELEASE; EPIDERMIS; HUMAN; INJECTION SITE IRRITATION; MEDIATOR RELEASE; NERVE ENDING; NEUROIMMUNOLOGY; NEUROPHYSIOLOGY; NEUROSECRETORY CELL; NEUROTRANSMISSION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PRURITUS; REVIEW; SKIN CELL; SPINAL CORD; SPINAL CORD NERVE CELL;

EID: 33646443548     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/sj.jid.5700231     Document Type: Article

References (73)

1. Amadesi S, Nie J, Vergnolle N, Cottrell GS, Grady EF, Trevisani M et al. (2004) Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci 24:4300-12
2. Andoh T, Kuraishi Y (2003) Nitric oxide enhances substance P-induced itch-associated responses in mice. Br J Pharmacol 138:202-8
3. Andoh T, Yageta Y, Takeshima H, Kuraishi Y (2004) Intradermal nociceptin elicits itch-associated responses through leukotriene B(4) in mice. J Invest Dermatol 123:196-201
4. Andrew D, Craig AD (2001) Spinothalamic lamina I neurons selectively sensitive to histamine: a central neural pathway for itch. Nat Neurosci 4:72-7
5. Ashida Y, Denda M, Hirao T (2001) Histamine H1 and H2 receptor antagonists accelerate skin barrier repair and prevent epidermal hyperplasia induced by barrier disruption in a dry environment. J Invest Dermatol 116:261-5
6. Behrendt HJ, Germann T, Gillen C, Hatt H, Jostock R (2004) Characterization of the mouse cold-menthol receptor TRPM8 and vanilloid receptor type-1 VR1 using a fluorometric imaging plate reader (FLIPR) assay. Br J Pharmacol 141:737-45
7. Bienenstock J, Tomioka M, Matsuda H, Stead RH, Quinonez G, Simon GT et al. (1987) The role of mast cells in inflammatory processes: evidence for nerve/mast cell interactions. Int Arch Allergy Appl Immunol 82:238-43
8. Bigliardi-Qi M, Lipp B, Sumanovski LT, Buechner SA, Bigliardi PL (2005) Changes of epidermal mu-opiate receptor expression and nerve endings in chronic atopic dermatitis. Dermatology 210:91-9
9. Biro T, Acs G, Acs P, Modarres S, Blumberg PM (1997) Recent advances in understanding of vanilloid receptors: a therapeutic target for treatment of pain and inflammation in skin. J Investig Dermatol Symp Proc 2:56-60
10. Biro T, Ko MC, Bromm B, Wei ET, Bigliardi P, Siebenhaar F et al. (2005) How best to fight that nasty itch - from new insights into the neuroimmunological, neuroendocrine, and neurophysiological bases of pruritus to novel therapeutic approaches. Exp Dermatol 14:225-40
11. Blunk JA, Schmelz M, Zeck S, Skov P, Likar R, Koppert W (2004) Opioid-induced mast cell activation and vascular responses is not mediated by mu-opioid receptors: an in vivo microdialysis study in human skin. Anesth Analg 98:364-70
12. Bodo E, Biro T, Telek A, Czifra G, Griger Z, Toth BI et al. (2005) A hot new twist to hair biology: involvement of vanilloid receptor-1 (VR1/TRPV1) signaling in human hair growth control. Am J Pathol 166:985-98
13. Brain SD, Grant AD (2004) Vascular actions of calcitonin gene-related peptide and adrenomedullin. Physiol Rev 84:903-34
14. Brain SD, Williams TJ (1988) Neuropharmacology of peptides in skin. Semin Dermatol 7:278-83
15. Buddenkotte J, Stroh C, Engels IH, Moormann C, Shpacovitch VM, Seeliger S et al. (2005) Agonists of proteinase-activated receptor-2 stimulate upregulation of intercellular cell adhesion molecule-1 in primary human keratinocytes via activation of NF-kappa B. J Invest Dermatol 124:38-45
16. Cao J, Papadopoulou N, Kempuraj D, Boucher WS, Sugimoto K, Cetrulo CL et al. (2005) Human mast cells express corticotropin-releasing hormone (CRH) receptors and CRH leads to selective secretion of vascular endothelial growth factor. J Immunol 174:7665-75
17. Caterina MJ, Julius D (2001) The vanilloid receptor: a molecular gateway to the pain pathway. Annu Rev Neurosci 24:487-517
18. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-24
19. Darsow U, Drzezga A, Frisch M, Munz F, Weilke F, Bartenstein P et al. (2000) Processing of histamine-induced itch in the human cerebral cortex: a correlation analysis with dermal reactions. J Invest Dermatol 115:1029-33
20. Dillon SR, Sprecher C, Hammond A, Bilsborough J, Rosenfeld-Franklin M, Presnell SR et al. (2004) Interleukin 31, a cytokine produced by activated T cells, induces dermatitis in mice. Nat Immunol 5:752-60
21. 2O positron emission tomography studies. Pain 92:295-305
22. Grewe M, Vogelsang K, Ruzicka T, Stege H, Krutmann J (2000) Neurotrophin-4 production by human epidermal keratinocytes: increased expression in atopic dermatitis. J Invest Dermatol 114:1108-12
23. Groneberg DA, Serowka F, Peckenschneider N, Artuc M, Grutzkau A, Fischer A et al. (2005) Gene expression and regulation of nerve growth factor in atopic dermatitis mast cells and the human mast cell line-1. J Neuroimmunol 161:87-92
24. Hagermark O (1974) Studies on experimental itch induced by kallikrein and bradykinin. Acta Dermatol Venereol 54:397-400
25. Haüstein UF (1990) Adrenergic urticaria and adrenergic pruritus. Acta Dermatol Venerol 70:82-4
26. Hayashi I, Majima M (1999) Reduction of sodium deoxycholic acid-induced scratching behaviour by bradykinin B2 receptor antagonists. Br J Pharmacol 126:197-204
27. Hayashi K, Sato H, Kaise T, Ohmori K, Ishii A, Sano J et al. (2001) Roles of mast cells and sensory nerves in cutaneous vascular hyperpermeability and scratching behavior induced by poly-L-arginine in rats. Eur J Pharmacol 425:219-27
28. Heyer G, Groene D, Martus P (2002) Efficacy of naltrexone on acetylcholine-induced allokinesis in atopic eczema. Exp Dermatol 11:448-55
29. Hossen MA, Sugimoto Y, Kayasuga R, Kamei C (2003) Involvement of histamine H3 receptors in scratching behaviour in mast cell-deficient mice. Br J Dermatol 149:17-22
30. Hundley SL, Yosipovitch G (2004) Mirtazapine for reducing nocturnal itch in patients with chronic pruritus: a pilot study. J Am Acad Derm 50:889-91
31. Ibrahim MM, Porreca F, Lai J, Albrecht PJ, Rice FL, Khodorova A et al. (2005) CB2 cannabinoid receptor activation produces antinociception by stimulating peripheral release of endogenous opioids. Proc Natl Acad Sci USA 102:3093-8
32. Ikoma A, Handwerker H, Miyachi Y, Schmelz M (2005) Electrically evoked itch in humans. Pain 113:148-54
33. Inagaki N, Igeta K, Kim JF, Nagao M, Shiraishi N, Nakamura N et al. (2002) Involvement of unique mechanisms in the induction of scratching behavior in BALB/c mice by compound 48/80. Eur J Pharmacol 448:175-83
34. Inoue K, Denda M, Tozaki H, Fujishita K, Koizumi S, Inoue K (2005) Characterization of multiple P2X receptors in cultured normal human epidermal keratinocytes. J Invest Dermatol 124:756-63
35. Janiszewski J, Bienenstock J, Blennerhassett MC (1994) Picomolar doses of substance P trigger electrical responses in mast cells without degranulation. Am J Physiol 267:C138-45
36. Kamei J, Nagase H (2001) Norbinaltorphimine, a selective kappa-opioid receptor antagonist, induces an itch-associated response in mice. Eur J Pharmacol 418:141-5
37. Kanda N, Koike S, Watanabe S (2005) Prostaglandin E2 enhances neurotrophin-4 production via EP3 receptor in human keratinocytes. J Pharmacol Exp Ther 315:796-804
38. Kanda N, Watanabe S (2003) Histamine enhances the production of nerve growth factor in human keratinocytes. J Invest Dermatol 121:570-7
39. Katugampola R, Church MK, Clough GF (2000) The neurogenic vasodilator response to endothelin-1: a study in human skin in vivo. Exp Physiol 85:839-46
40. Kennedy WR, Wendelschafer-Crabb G, Brelje TC (1994) Innervation and vasculature of human sweat glands: an immunohistochemistry-laser scanning confocal fluorescence microscopy study. J Neurosci 14:6825-33
41. Lazar J, Szabo T, Marincsak R, Kovacs L, Blumberg PM, Biro T (2004) Sensitization of recombinant vanilloid receptor-1 by various neurotrophic factors. Life Sci 75:153-63
42. Lytinas M, Kempuraj D, Huang M, Boucher W, Esposito P, Theoharides TC (2003) Acute stress results in skin corticotropin-releasing hormone secretion, mast cell activation and vascular permeability, an effect mimicked by intradermal corticotropin-releasing hormone and inhibited by histamine-1 receptor antagonists. Int Arch Allergy Immunol 130:224-31
43. Maurer BA (2002) Big thinking. Nature 415:489-91
44. Metze D, Reimann S, Beissert S, Luger T (1999) Efficacy and safety of naltrexone, an oral opiate receptor antagonist, in the treatment of pruritus in internal and dermatological diseases. J Am Acad Dermatol 41:533-9
45. Miyamoto T, Nojima H, Shinkado T, Nakahashi T, Kuraishi Y (2002) Itch-associated response induced by experimental dry skin in mice. Jpn J Pharmacol 88:285-92
46. Mochizuki H, Tashiro M, Kano M, Sakurada Y, Itoh M, Yanai K (2003) Imaging of central itch modulation in the human brain using positron emission tomography. Pain 105:339-46
47. Moqrich A, Hwang SW, Earley TJ, Petrus MJ, Murray AN, Spencer KS et al. (2005) Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307:1468-72
48. Nojima H, Cuellar JM, Simons CT, Carstens MI, Carstens E (2004) Spinal c-fos expression associated with spontaneous biting in a mouse model of dry skin pruritus. Neurosci Lett 361:79-82
49. Ny A, Egelrud T (2004) Epidermal hyperproliferation and decreased skin barrier function in mice overexpressing stratum corneum chymotryptic enzyme. Acta Dermatol Venereol 84:18-22
50. Onigbogi O, Ajayi AA, Ukponmwan OE (2000) Mechanisms of chloroquine-induced body-scratching behavior in rats: evidence of involvement of endogenous opioid peptides. Pharmacol Biochem Behav 65:333-7
51. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM et al. (2002a) A TRP channel that senses cold stimuli and menthol. Cell 108:705-15
52. Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC et al. (2002b) A heat-sensitive TRP channel expressed in keratinocytes. Science 296:2046-9
53. Raap U, Goltz C, Deneka N, Bruder M, Renz H, Kapp A et al. (2005) Brain-derived neurotrophic factor is increased in atopic dermatitis and modulates eosinophil functions compared with that seen in nonatopic subjects. J Allergy Clin Immunol 115:1268-75
54. Schmelz M, Michael K, Weidner C, Schmidt R, Torebjork HE, Handwerker HO (2000a) Which nerve fibers mediate the axon reflex flare in human skin? Neuroreport 11:645-8
55. Schmelz M, Schmid R, Handwerker HO, Torebjork HE (2000b) Encoding of burning pain from capsaicin-treated human skin in two categories of unmyelinated nerve fibres. Brain 123:560-71
56. Schmelz M, Schmidt R, Weidner C, Hilliges M, Torebjork HE, Handwerker HO (2003) Chemical response pattern of different classes of C-nociceptors to pruritogens and algogens. J Neurophysiol 89:2441-8
57. Schmidt R, Schmelz M, Ringkamp M, Handwerker HO, Torebjork HE (1997) Innervation territories of mechanically activated C nociceptor units in human skin. J Neurophysiol 78:2641-8
58. Sonkoly E, Muller A, Lauerma AI, Pivarcsi A, Soto H, Kemeny L et al. (2006) IL-31: A new link between T cells and pruritus in atopic skin inflammation. J Allergy Clin Immunol 117:411-7
59. Ständer S, Moormann C, Schumacher M, Buddenkotte J, Artuc M, Shpacovitch V et al. (2004) Expression of vanilloid receptor subtype 1 in cutaneous sensory nerve fibers, mast cells, and epithelial cells of appendage structures. Exp Dermatol 13:129-39
60. Ständer S, Schmelz M, Metze D, Luger T, Rukwied R (2005) Distribution of cannabinoid receptor 1 (CB1) and 2 (CB2) on sensory nerve fibers and adnexal structures in human skin. J Dermatol Sci 38:177-88
61. Ständer S, Steinhoff M (2002) Pathophysiology of pruritus in atopic dermatitis: an overview. Exp Dermatol 11:12-24
62. Ständer S, Steinhoff M, Schmelz M, Weisshaar E, Metze D, Luger T (2003) Neurophysiology of pruritus: cutaneous elicitation of itch. Arch Dermatol 139:1463-70
63. Steinhoff M, Buddenkotte J, Shpacovitch V, Rattenholl A, Moormann C, Vergnolle N et al. (2005) Proteinase-activated receptors: transducers of proteinase-mediated signaling in inflammation and immune response. Endocr Rev 26:1-43
64. Steinhoff M, Neisius U, Ikoma A, Fartasch M, Heyer C, Skov PS et al. (2003a) Proteinase-activated receptor-2 mediates itch: a novel pathway for pruritus in human skin. J Neurosci 23:6176-80
65. Steinhoff M, Stander S, Seeliger S, Ansel JC, Schmelz M, Luger T (2003b) Modern aspects of cutaneous neurogenic inflammation. Arch Dermatol 139:1479-88
66. Steinhoff M, Vergnolle N, Young SH, Tognetto M, Amadesi S, Ennes HS et al. (2000) Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat Med 6:151-8
67. Stokes AJ, Shimoda LM, Koblan-Huberson M, Adra CN, Turner H (2004) A TRPV2-PKA signaling module for transduction of physical stimuli in mast cells. J Exp Med 200:137-47
68. Thomsen JS, Sonne M, Benfeldt E, Jensen SB, Serup J, Menne T (2002) Experimental itch in sodium lauryl sulphate-inflamed and normal skin in humans: a randomized, double-blind, placebo-controlled study of histamine and other inducers of itch. Br J Dermatol 146:792-800
69. Vergnolle N, Ferazzini M, D'Andrea MR, Buddenkotte J, Steinhoff M (2003) Proteinase-activated receptors: novel signals for peripheral nerves. Trends Neurosci 26:496-500
70. Watanabe H, Vriens J, Prenen J, Droogmans C, Voets T, Nilius B (2003) Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424:434-8
71. Wei ET, Seid DA (1983) AG-3-5: a chemical producing sensations of cold. J Pharm Pharmacol 35:110-2
72. Yosipovitch G, Greaves MW, Schmelz M (2003) Itch. Lancet 361:690-4
73. Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D et al. (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112:293-301