Role of mast cells and sensory nerves in skin inflammation

Giornale Italiano di Dermatologia e Venereologia

Volumn 145, Issue 2, 2010, Pages 195-204

  Harvima, I T ^a   Nilsson, G ^b   Naukkarinen, A ^c  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b KAROLINSKA INSTITUTE   (Sweden)

^c KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

Inflammation; Mast cells; Nerve fibers, unmyelinated; Sensory receptor cells; Skin; Stress

Indexed keywords

ALPHA INTERMEDIN; CORTICOTROPIN RELEASING FACTOR; NERVE GROWTH FACTOR; NEUROPEPTIDE; NEUROTROPHIN; TRYPTASE;

ATOPIC DERMATITIS; CYTOKINE RELEASE; HISTAMINE RELEASE; HUMAN; INFLAMMATORY CELL; MAST CELL; MENTAL STRESS; NEUROENDOCRINE SYSTEM; NEUROGENIC INFLAMMATION; NONHUMAN; NUMMULAR DERMATITIS; PERIPHERAL NERVOUS SYSTEM; PSORIASIS; PUSTULOSIS PALMOPLANTARIS; REVIEW; SENSORY NERVE CELL; SKIN DISEASE; SKIN INFLAMMATION;

EID: 77954530001     PISSN: 03920488     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (86)

1. Harvima IT, Nilsson G, Suttle M-M, Naukkarinen A. Is there a role for mast cells in psoriasis? Arch Dermatol Res 2008;300:461-78.
2. TC types of human mast cells by immunohistochemistry using new monoclonal anti-tryptase and anti-chymase antibodies. J Histochem Cytochem 1989;37:1509-15.
3. Weidner N, Austen KF. Heterogeneity of mast cells at multiple body sites: fluorescent determination of avidin binding and immunofluorescent determination of chymase, tryptase, and carboxypeptidase content. Path Res Pract 1993;189:156-62.
4. Kivinen PK, Nilsson G, Naukkarinen A, Harvima IT. Mast cell survival and apoptosis in organ-cultured human skin. Exp Dermatol 2003;12:53-60.
5. Dvorak AM, Kissell S. Granule changes of human skin mast cells characteristic of piecemeal degranulation and associated with recovery during wound healing in situ. J Leukoc Biol 1991;49:197-210.
6. Skokos D, Goubran Botros H, Demeure C, Morin J, Peronet R, Birkenmeier G et al. Mast cell-derived exosomes induce phenotypic and functional maturation of dendritic cells and elicit specific immune responses in vivo. J Immunol 2003;170:3037-45.
7. Cao J, Cetrulo CL, Theoharides TC. Corticotropin-releasing hormone induces vascular endothelial growth factor release from human mast cells via the cAMP/protein kinase A/p38 mitogen-activated protein kinase pathway. Mol Pharmacol 2006;69:998-1006.
8. Fischer M, Harvima IT, Carvalho RFS, Möller C, Naukkarinen A, Enblad G et al. Mast cell CD30 ligand is up-regulated in cutaneous inflammations and mediates degranulation-independent chemokine secretion. J Clin Invest 2006;116:2748-56. (Pubitemid 44511638)
9. Zhao W, Kepley CL, Morel PA, Okumoto LM, Fukuoka Y, Schwartz LB. FcγRIIa, not FcγRIIb, is constitutively and functionally expressed on skin-derived human mast cells. J Immunol 2006;177:694-701.
10. Okayama Y, Kirshenbaum AS, Metcalfe DD. Expression of a functional high-affinity IgG receptor, FcγRI, on human mast cells: up-regulation by IFN-γ. J Immunol 2000;164:4332-9.
11. Dawicki W, Marshall JS. New and emerging roles for mast cells in host defence. Curr Opin Immunol 2007;19:31-8.
12. el-Lati SG, Dahinden CA, Church MK. Complement peptides C3a- and C5a-induced mediator release from dissociated human skin mast cells. J Invest Dermatol 1994;102:803-6.
13. Dvorak AM, Costa JJ, Monahan-Earley RA, Fox P, Galli SJ. Ultrastructural analysis of human skin biopsy specimens from patients receiving recombinant human stem cell factor subcutaneous injection of rhSCF induces mast cell degranulation and granulocyte recruitment at the injection site. J Allergy Clin Immunol 1998;101:793-806. (Pubitemid 28293188)
14. van Overveld FJ, Jorens PG, Rampart M, de Backer W, Vermeire PA. Tumour necrosis factor stimulates human skin mast cells to release of histamine and tryptase. Clin Exp Allergy 1991;21:711-4.
15. Moormann C, Artuc M, Pohl E, Varga G, Buddenkotte J, Vergnolle N et al. Functional characterization and expression analysis of the proteinase-activated receptor-2 in human cutaneous mast cells. J Invest Dermatol 2006;126:746-55.
16. Grützkau A, Henz BM, Kirchhof L, Luger T, Artuc M. α-Melanocyte stimulating hormone acts as a selective inducer of secretory functions in human mast cells. Biochem Biophys Res Commun 2000;278:14-9.
17. Church MK, Lowman MA, Rees PH, Benyon RC. Mast cells, neuropeptides and inflammation. Agents Actions 1989;27:8-16.
18. Montano JA, Pérez-Pinera P, García-Suárez O, Cobo J, Vega JA. Development and neuronal dependence of cutaneous sensory nerve formations: lessons from neurotrophins. Microsc Res Tech 2009 [Epub ahead of print].
19. Naukkarinen A, Harvima IT, Aalto M-L, Harvima RJ, Horsmanheimo M. Quantitative analysis of contact sites between mast cells and sensory nerves in cutaneous psoriasis and lichen planus based on a histochemical double staining technique. Arch Dermatol Res 1991;283:433-7.
20. Huttunen M, Harvima IT, Ackermann L, Harvima RJ, Naukkarinen A, Horsmanheimo M. Neuropeptide-and capsaicin-induced histamine release in skin monitored with the microdialysis technique. Acta Derm Venereol (Stockh) 1996;76:205-9.
21. Tausk F, Undem B. Exogenous but not endogenous substance P releases histamine from isolated human skin fragments. Neuropeptides 1995;29:351-5. (Pubitemid 26025807)
22. Naukkarinen A, Nickoloff BJ, Farber EM. Quantification of cutaneous sensory nerves and their substance P content in psoriasis. J Invest Dermatol 1989;92:126-9. (Pubitemid 19027707)
23. Eedy DJ, Johnston CF, Shaw C, Buchanan KD. Neuropeptides in psoriasis: an immunocytochemical and radioimmunoassay study. J Invest Dermatol 1991;96:434-8.
24. Okayama Y, Ono Y, Nakazawa T, Church MK, Mori M. Human skin mast cells produce TNF-α by substance P. Int Arch Allergy Immunol 1998;117(Suppl):48-51.
25. Kulka M, Sheen CH, Tancowny BP, Grammer LC, Schleimer RP Neuropeptides activate human mast cell degranulation and chemokine production. Immunology 2007;123:398-410.
26. Takei Y, Laskey R. Interpreting crosstalk between TNF-α and NGF: potential implications for disease. Trends Mol Med 2008;14:381-8.
27. Chang S-E, Han S-S, Jung H-J, Choi J-H. Neuropeptides and their receptors in psoriatic skin in relation to pruritus. Br J Dermatol 2007;156:1272-7.
28. Nakamura M, Toyoda M, Morohashi M. Pruritogenic mediators in psoriasis: comparative evaluation of itch-associated cutaneous factors. Br J Dermatol 2003;149:718-30.
29. Möller C, Alfredsson J, Engström M, Wootz H, Xiang Z, Lennartsson J et al. Stem cell factor promotes mast cell survival via inactivation of FOXO3a-mediated transcriptional induction and MEK-regulated phosphorylation of the proapoptotic protein Bim. Blood 2005;106:1330-6.
30. Nilsson G, Blom T, Harvima I, Kusche-Gullberg M, Nilsson K. Stem cell factor-dependent human cord blood derived mast cells express α-and β-tryptase, heparin and chondroitin sulphate. Immunology 1996;88:308-14.
31. Kanbe N, Kurosawa M, Miyachi Y, Kanbe M, Saitoh H, Matsuda H. Nerve growth factor prevents apoptosis of cord blood-derived human cultured mast cells synergistically with stem cell factor. Clin Exp Allergy 2000;30:1113-20.
32. Welker P, Grabbe J, Gibbs B, Zuberbier T, Henz BM. Nerve growth factor-β induces mast-cell marker expression during in vitro culture of human umbilical cord blood cells. Immunology 2000;99:418-26.
33. Lorentz A, Hoppe J, Worthmann H, Gebhardt T, Hesse U, Bienenstock J et al. Neurotrophin-3, but not nerve growth factor, promotes survival of human intestinal mast cells. Neurogastroenterol Motil 2007;19:301-8.
34. Nilsson G, Forsberg-Nilsson K, Xiang Z, Hallböök F, Nilsson K, Metcalfe DD. Human mast cells express functional TrkA and are a source of nerve growth factor. Eur J Immunol 1997;27:2295-301.
35. Xiang Z, Nilsson G. IgE receptor-mediated release of nerve growth factor by mast cells. Clin Exp Allergy 2000;30:1379-86.
36. di Mola FF, Friess H, Zhu ZW, Koliopanos A, Bley T, Di Sebastiano P et al. Nerve growth factor and Trk high affinity receptor (TrkA) gene expression in inflammatory bowel disease. Gut 2000;46:670-9.
37. Wu X, Myers AC, Goldstone AC, Togias A, Sanico AM. Localization of nerve growth factor and its receptors in the human nasal mucosa. J Allergy Clin Immunol 2006;118:428-33. (Pubitemid 44142716)
38. Skaper SD, Pollock M, Facci L. Mast cells differentially express and release active high molecular weight neurotrophins. Brain Res Mol Brain Res 2001;97:177-85.
39. Hermes B, Zuberbier T, Haas N, Henz BM. Decreased cutaneous expression of stem cell factor and of the p75NGF receptor in urticaria. Br J Dermatol 2003;148:411-7.
40. Groneberg DA, Serowka F, Peckenschneider N, Artuc M, Grützkau A, Fischer A et al. Gene expression and regulation of nerve growth factor in atopic dermatitis mast cells and the human mast cell line-1. J Neuroimmunol 2005;161:87-92.
41. Luger TA, Brzoska T. Alpha-MSH related peptides: a new class of anti-inflammatory and immunomodulating drugs. Ann Rheum Dis 2007;66(Suppl3): iii52-5.
42. Ständer S, Moormann C, Schumacher M, Buddenkotte J, Artuc M, Shpacovitch V et al. Expression of vanilloid receptor subtype 1 in cutaneous sensory nerve fibers, mast cells, and epithelial cells of appendage structures. Exp Dermatol 2004;13:129-39.
43. Saarinen JV, Harvima RJ, Naukkarinen A, Horsmanheimo M, Harvima JT. Release of histamine and leukotriene C4 in immediate allergic wheal reaction as measured with the microdialysis technique. Arch Dermatol Res 2000;292:333-40. (Pubitemid 30449934)
44. Schmelz M, Michael K, Weidner C, Schmidt R, Torebjörk HE, Handwerker HO. Which nerve fibers mediate the axon reflex flare in human skin. Neuroreport 2000;11:645-8. (Pubitemid 30120491)
45. Schmelz M, Luz O, Averbeck B, Bickel A. Plasma extravasation and neuropeptide release in human skin as measured by intradermal microdialysis. Neurosci Lett 1997;230:117-20. (Pubitemid 27312397)
46. Pipkorn U, Andersson M. Topical dermal anaesthesia inhibits the flare but not the weal response to allergen and histamine in the skin-prick test. Clin Allergy 1987;17:307-11.
47. Willis EF, Clough GF, Church MK. Investigation into the mechanisms by which nedocromil sodium, frusemide and bumetanide inhibit the histamine-induced itch and flare response in human skin in vivo. Clin Exp Allergy 2004;34:450-5.
48. Schmelz M, Schmidt R, Bickel A, Handwerker HO, Torebjörk HE. Specific C-receptors for itch in human skin. J Neurosci 1997;17:8003-8.
49. Han S-K, Mancino V, Simon MI. Phospholipase Cβ3 mediates the scratching response activated by the histamine H1 receptor on C-fiber nociceptive neurons. Neuron 2006;52:691-703.
50. Vieira Dos Santos R, Magert M, Zuberbier T, Church MK, Escribano L, Maurer M. Topical sodium cromoglicate relieves allergen- and histamine-induced dermal pruritus. Br J Dermatol 2009 [E-pub ahead of print].
51. Ishiuji Y, Coghill RC, Patel TS, Dawn A, Fountain J, Oshiro Y et al. Repetitive scratching and noxious heat do not inhibit histamine-induced itch in atopic dermatitis. Br J Dermatol 2008;158:78-83.
52. Steinhoff M, Vergnolle N, Young SH, Tognetto M, Amadesi S, Ennes HS et al. Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat Med 2000;6:151-8.
53. Steinhoff M, Neisius U, Ikoma A, Fartasch M, Heyer G, Skov PS et al. Proteinase-activated receptor-2 mediates itch: a novel pathway for pruritus in human skin. J Neurosci 2003;23:6176-80.
54. Amadesi S, Nie J, Vergnolle N, Cottrell G, Grady EF, Trevisani M et al. Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. J Neurosci 2004;24:4300-12.
55. Carvalho RFS, Nilsson G, Harvima IT. Increased mast cell expression of PAR-2 in skin inflammatory diseases and release of IL-8 upon PAR-2 activation. Exp Dermatol 2010;19:117-22.
56. Franconi GM, Graf PD, Lazarus SC, Nadel JA, Caughey GH. Mast cell tryptase and chymase reverse airway smooth muscle relaxation induced by vasoactive intestinal peptide in the Ferret J Pharmacol Exp Ther 1989;248:947-51.
57. Tam EK, Caughey GH. Degradation of airway neuropeptides by human lung tryptase. Am J Respir Cell Mol Biol 1990;3:27-32.
58. Walls AF, Brain SD, Desai A, Jose PJ, Hawkings E, Church MK et al. Human mast cell tryptase attenuates the vasodilator activity of calcitonin gene-related peptide. Biochem Pharmacol 1992;43:1243-8.
59. Gruber BL, Marchese MJ, Suzuki K, Schwartz LB, Okada Y, Nagase H et al. Synovial procollagenase activation by human mast cell tryptase: dependence upon matrix metalloproteinase 3 activation. J Clin Invest 1989;84:1657-62.
60. Teahan J, Harrison R, Izquierdo M, Stein RL. Substrate specificity of human fibroblast stromelysin. Hydrolysis of substance P and its analogues. Biochemistry 1989;28:8497-501.
61. Caughey GH, Leidig F, Viro NF, Nadel JA. Substance P and vasoactive intestinal peptide degradation by mast cell tryptase and chymase. J Pharmacol Exp Ther 1988;244:133-7.
62. 5-enkephalin. Peptides 1991;12:995-1000.
63. Harvima IT, Naukkarinen A, Paukkonen K, Harvima RJ, Aalto M-L, Schwartz LB et al. Mast cell tryptase and chymase in developing and mature psoriatic lesions. Arch Dermatol Res 1993;285:184-92. (Pubitemid 23210101)
64. Diaconu N-C, Kaminska R, Naukkarinen A, Harvima RJ, Harvima IT. The increase in tryptase- and chymase-positive mast cells is associated with partial inactivation of chymase and increase in protease inhibitors in basal cell carcinoma. J Eur Acad Dermatol Venereol 2007;21:908-15.
65. Schechter NM, Sprows JL, Schoenberger OL, Lazarus GS, Cooperman BS, Rubin H. Reaction of human skin chymotrypsin-like proteinase chymase with plasma proteinase inhibitors. J Biol Chem 1989;264:21308-15. (Pubitemid 20017952)
66. Walter M, Sutton RM, Schechter NM. Highly efficient inhibition of human chymase by α(2)-macroglobulin. Arch Biochem Biophys 1999;368:276-84.
67. Harvima IT, Haapanen L, Ackermann L, Naukkarinen A, Harvima RJ, Horsmanheimo M. Decreased chymase activity is associated with increased levels of protease inhibitors in mast cells of psoriatic lesions. Acta Derm Venereol (Stockh) 1999;79:98-104. (Pubitemid 29185301)
68. Lee M-G, Dong X, Liu Q, Patel KN, Choi OH, Vonakis B et al. Agonists of the Mas-related gene (Mrgs) orphan receptors as novel mediators of mast cell-sensory nerve interactions. J Immunol 2008;180:2251-5.
69. Naukkarinen A, Harvima I, Paukkonen K, Aalto M-L, Horsmanheimo M. Immunohistochemical analysis of sensory nerves and neuropeptides, and their contacts with mast cells in developing and mature psoriatic lesions. Arch Dermatol Res 1993;285:341-6. (Pubitemid 23265515)
70. Naukkarinen A, Järvikallio A, Lakkakorpi J, Harvima IT, Harvima RJ, Horsmanheimo M. Quantitative histochemical analysis of mast cells and sensory nerves in psoriatic skin. J Pathol 1996;180:200-5. (Pubitemid 26370188)
71. Järvikallio A, Harvima IT, Naukkarinen A. Mast cells, nerves and neuropeptides in atopic dermatitis and nummular eczema. Arch Dermatol Res 2003;295:2-7. (Pubitemid 36578014)
72. Siebenhaar F, Magert M, Peters EMJ, Hendrix S, Metz M, Maurer M. Mast cell-driven skin inflammation is impaired in the absence of sensory nerves. J Allergy Clin Immunol 2008;121:955-61.
73. Sugiura H, Maeda T, Uehara M. Mast cell invasion of peripheral nerve in skin lesions of atopic dermatitis. Acta Derm Venereol Suppl (Stockh) 1992;176:74-6.
74. Hagforsen E, Nordlind K, Michaëlson G. Skin nerve fibres and their contacts with mast cells in patients with palmoplanar pustulosis. Arch Dermatol Res 2000;292:269-74. (Pubitemid 30386435)
75. Ito A, Hagiyama M, Oonuma J. Nerve-mast cell and smooth muscle-mast cell interaction mediated by cell adhesion molecule-1, CADM1. J Smooth Muscle Res 2008;44:83-93.
76. Arck PC, Slominski A, Theoharides TC, Peters EMJ, Paus R. Neuroimmunology of stress: skin takes center stage. J Invest Dermatol 2006;126:1697-704. (Pubitemid 44086503)
77. MacQueen G, Marshall J, Perdue M, Siegel S, Bienenstock J. Pavlovian conditioning of rat mucosal mast cells to secrete rat mast cell protease II. Science 1989;243:83-5. (Pubitemid 19027929)
78. Gauci M, Husband AJ, Saxarra H, King MG. Pavlovian conditioning of nasal tryptase release in human subjects with allergic rhinitis. Physiol Behav 1994;55:823-5. (Pubitemid 24133795)
79. Theoharides TC, Spanos C, Pang X, Alferes L, Ligris K, Letourneau R et al. Stress-induced intracranial mast cell degranulation: a corticotropin- releasing hormone-mediated effect. Endocrinology 1995;136:5745-50.
80. Singh LK, Pang X, Alexacos N, Letourneau R, Theoharides TC. Acute immobilization stress triggers skin mast cell degranulation via corticotropin releasing hormone, neurotensin, and substance P: a link to neurogenic skin disorders. Brain Behav Immun 1999;13:225-39. (Pubitemid 29450200)
81. Peters EMJ, Kuhlmei A, Tobin DJ, Müller-Röver S, Klapp BF, Arck PC. Stress exposure modulates peptidergic innervation and degranulates mast cells in murine skin. Brain Behav Immun 2005;19:252-62. (Pubitemid 40431540)
82. Pavlovic S, Daniltchenko M, Tobin DJ, Hagen E, Hunt SP, Klapp BF et al. Further exploring the brain-skin connection: stress worsens dermatitis via substance P-dependent neurogenic inflammation in mice. J Invest Dermatol 2008;128:434-46.
83. Harvima RJ, Viinamäki H, Harvima IT, Naukkarinen A, Savolainen L, Aalto M-L et al. Association of psychic stress with clinical severity and symptoms of psoriatic patients. Acta Derm Venereol (Stockh) 1996;76:467-71.
84. Harvima IT, Viinamäki H, Naukkarinen A, Paukkonen K, Neittaanmäki H, Harvima RJ et al. Association of cutaneous mast cells and sensory nerves with psychic stress in psoriasis. Psychother Psychosom 1993;60:168-76.
85. Remröd C, Lonne-Rahm S, Nordlind K. Study of substance P and its receptor neurokinin-1 in psoriasis and their relation to chronic stress and pruritus. Arch Dermatol Res 2007;299:85-91.
86. Lonne-Rahm S, Berg M, Mårin P, Nordlind K. Atopic dermatitis, stinging, and effects of chronic stress: a pathocausal study. J Am Acad Dermatol 2004;51:899-905.