Stress, the neuroendocrine system and mast cells: current understanding of their role in psoriasis

References

• Sabat R, Philipp S, Höflich C et al. Immunopathogenesis of psoriasis. Exp. Dermatol.16(10), 779–798 (2007).
   PubMed Web of Science ®Google Scholar
• Harvima IT, Nilsson G, Suttle MM, Naukkarinen A. Is there a role for mast cells in psoriasis? Arch. Dermatol. Res.300(9), 461–478 (2008).
   PubMed Web of Science ®Google Scholar
• Basavaraj KH, Navya MA, Rashmi R. Stress and quality of life in psoriasis. Int. J. Dermatol50(7), 783–792 (2011).
   PubMed Web of Science ®Google Scholar
• Arck PC, Slominski A, Theoharides TC, Peters EMJ, Paus R. Neuroimmunology of stress: skin takes center stage. J. Invest. Dermatol.126(8), 1697–1704 (2006).
   PubMed Web of Science ®Google Scholar
• 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.278(1), 14–19 (2000).
   PubMedGoogle Scholar
• 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.69(3), 998–1006 (2006).
   PubMed Web of Science ®Google Scholar
• Church MK, Lowman MA, Rees PH, Benyon RC. Mast cells, neuropeptides and inflammation. Agents Actions27(1–2), 8–16 (1989).
   PubMedGoogle Scholar
• Baldwin AL. Mast cell activation by stress. Methods Mol. Biol.315, 349–360 (2006).
   PubMedGoogle Scholar
• Farber EM, Nickoloff BJ, Recht B, Fraki JE. Stress, symmetry, and psoriasis: possible role of neuropeptides. J. Am. Acad. Dermatol.14(2 Pt 1), 305–311 (1986).
   PubMed Web of Science ®Google Scholar
• 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.285(6), 341–346 (1993).
   PubMedGoogle Scholar
• 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.180(2), 200–205 (1996).
   PubMedGoogle Scholar
• Slominski A. On the role of the corticotropin-releasing hormone signalling system in the aetiology of inflammatory skin disorders. Br. J. Dermatol.160(2), 229–232 (2009).
   PubMedGoogle Scholar
• Zmijewski MA, Slominski AT. Emerging role of alternative splicing of CRF1 receptor in CRF signaling. Acta Biochim Pol57(1), 1–13 (2010).
   PubMed Web of Science ®Google Scholar
• O´Kane M, Murphy EP, Kirby B. The role of corticotropin-releasing hormone in immune-mediated cutaneous inflammatory diseases. Exp. Dermatol.15(3), 143–153 (2006).
   PubMedGoogle Scholar
• Kim JE, Cho DH, Kim HS et al. Expression of the corticotropin-releasing hormone–proopiomelanocortin axis in the various clinical types of psoriasis. Exp. Dermatol.16(2), 104–109 (2007).
   PubMedGoogle Scholar
• Karanikas E, Harsoulis F, Giouzepas I, Griveas I, Chrisomallis F. Neuroendocrine stimulatory tests of hypothalamus–pituitary–adrenal axis in psoriasis and correlative implications with psychopathological and immune parameters. J. Dermatol.36(1), 35–44 (2009).
   PubMed Web of Science ®Google Scholar
• Buske-Kirschbaum A, Ebrecht M, Kern S, Hellhammer DH. Endocrine stress responses in TH1-mediated chronic inflammatory skin disease (psoriasis vulgaris) – do they parallel stress-induced endocrine changes in TH2-mediated inflammatory dermatoses (atopic dermatitis)? Psychoneuroendocrinology31(4), 439–446 (2006).
   PubMed Web of Science ®Google Scholar
• Richards HL, Ray DW, Kirby B et al. Response of the hypothalamic–pituitary–adrenal axis to psychological stress in patients with psoriasis. Br. J. Dermatol.153(6), 1114–1120 (2005).
   PubMed Web of Science ®Google Scholar
• Evers AWM, Verhoeven EWM, Kraaimaat FW et al. How stress gets under the skin: cortisol and stress reactivity in psoriasis. Br. J. Dermatol.163(5), 986–991 (2010).
   PubMedGoogle Scholar
• Schauer E, Trautinger F, Köck A et al. Proopiomelanocortin-derived peptides are synthesized and released by human keratinocytes. J. Clin. Invest.93(5), 2258–2262 (1994).
   PubMed Web of Science ®Google Scholar
• Eves PC, Haycock JW. Melanocortin signalling mechanisms. Adv. Exp. Med. Biol.681, 19–28 (2010).
   PubMedGoogle Scholar
• Vukelic S, Stojadinovic O, Pastar I et al. Cortisol synthesis in epidermis is induced by IL-1 and tissue injury. J. Biol. Chem.286(12), 10265–10275 (2011).
   PubMed Web of Science ®Google Scholar
• Slominski A, Zbytek B, Semak I, Sweatman T, Wortsman J. CRH stimulates POMC activity and corticosterone production in dermal fibroblasts. J. Neuroimmunol.162(1–2), 97–102 (2005).
   PubMed Web of Science ®Google Scholar
• Cirulle F, Alleva E. The NGF saga: from animal models of psychosocial stress to stress-related psychopathology. Front. Neuroendocrinol.30(3), 379–395 (2009).
   PubMedGoogle Scholar
• Peters EM, Liezmann C, Spatz K et al. Nerve growth factor partially recovers inflamed skin from stress-induced worsening in allergic inflammation. J. Invest. Dermatol.131(3), 735–743 (2011).
   PubMedGoogle Scholar
• Raychaudhuri SK, Raychaudhuri SP. NGF and its receptor system: a new dimension in the pathogenesis of psoriasis and psoriatic arthritis. Ann. NY Acad Sci.1173, 470–477 (2009).
   PubMed Web of Science ®Google Scholar
• Nakamura M, Toyoda M, Morohashi M. Pruritogenic mediators in psoriasis: comparative evaluation of itch-associated cutaneous factors. Br. J. Dermatol.149(4), 718–730 (2003).
   PubMed Web of Science ®Google Scholar
• Amatya B, El-Nour H, Holst M, Theodorsson E, Nordlind K. Expression of tachykinins and their receptors in plaque psoriasis with pruritus. Br. J. Dermatol.164(5), 1023–1029 (2011).
   PubMed Web of Science ®Google Scholar
• 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.49(2), 197–210 (1991).
   PubMed Web of Science ®Google Scholar
• Fischer M, Harvima IT, Carvalho RFS et al. Mast cell CD30 ligand is up-regulated in cutaneous inflammations and mediates degranulation-independent chemokine secretion. J. Clin. Invest.116(10), 2748–2756 (2006).
   PubMed Web of Science ®Google Scholar
• el-Lati SG, Dahinden CA, Church MK. Complement peptides C3a- and C5a-induced mediator release from dissociated human skin mast cells. J. Invest. Dermatol.102(5), 803–806 (1994).
   PubMedGoogle Scholar
• 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.101(6 Pt 1), 793–806 (1998).
   PubMedGoogle Scholar
• Moormann C, Artuc M, Pohl E et al. Functional characterization and expression analysis of the proteinase-activated receptor-2 in human cutaneous mast cells. J. Invest. Dermatol.126(4), 746–755 (2006).
   PubMedGoogle Scholar
• Cao J, Papadopoulou N, Kempuraj D et al. Human mast cells express corticotropin-releasing hormone (CRH) receptors and CRH leads to selective secretion of vascular endothelial growth factor. J. Immunol.174(12), 7665–7675 (2005).
   PubMed Web of Science ®Google Scholar
• Papadopoulou NG, Oleson L, Kempuraj D, Donelan J, Cetrulo CL, Theoharides TC. Regulation of corticotropin-releasing hormone receptor-2 expression in human cord blood-derived cultured mast cells. J. Mol. Endocrinol.35(3), R1–R8 (2005).
   PubMedGoogle Scholar
• Crompton R, Clifton VL, Bisits AT, Read MA, Smith R, Wright IM. Corticotropin-releasing hormone causes vasodilation in human skin via mast cell-dependent pathway. J. Clin. Endocrinol. Metab.88(11), 5427–5432 (2003).
   PubMedGoogle Scholar
• Kempuraj D, Papadopoulou NG, Lytinas M et al. Corticotropin-releasing hormone and its structurally related urocortin are synthesized and secreted by human mast cells. Endocrinology145(1), 43–48 (2004).
   PubMed Web of Science ®Google Scholar
• Artuc M, Böhm M, Grützkau A et al. Human mast cells in the neurohormonal network: expression of POMC, detection of precursor proteases, and evidence for IgE-dependent secretion of α-MSH. J. Invest. Dermatol.126(9), 1976–1981 (2006).
   PubMedGoogle Scholar
• Sarkar A, Sreenivasan Y, Manna SK. α-Melanocyte-stimulating hormone induces cell death in mast cells: involvement of NF-κB. FEBS Lett.549(1–3), 87–93 (2003).
   PubMedGoogle Scholar
• 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.73(5), 513–529 (2010).
   PubMed Web of Science ®Google Scholar
• Möller C, Alfredsson J, Engström M 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. Blood106(4), 1330–1336 (2005).
   PubMed Web of Science ®Google Scholar
• 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. Immunology88(2), 308–314 (1996).
   PubMed Web of Science ®Google Scholar
• 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. Allergy30(8), 1113–1120 (2000).
   PubMedGoogle Scholar
• 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. Immunology99(3), 418–426 (2000).
   PubMedGoogle Scholar
• Lorentz A, Hoppe J, Worthmann H et al. Neurotrophin-3, but not nerve growth factor, promotes survival of human intestinal mast cells. Neurogastroenterol. Motil.19(4), 301–308 (2007).
   PubMedGoogle Scholar
• 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.27(9), 2295–2301 (1997).
   PubMed Web of Science ®Google Scholar
• Xiang Z, Nilsson G. IgE receptor-mediated release of nerve growth factor by mast cells. Clin. Exp. Allergy30(10), 1379–1386 (2000).
   PubMed Web of Science ®Google Scholar
• di Mola FF, Friess H, Zhu ZW et al. Nerve growth factor and Trk high affinity receptor (TrkA) gene expression in inflammatory bowel disease. Gut46(5), 670–679 (2000).
   PubMedGoogle Scholar
• Groneberg DA, Serowka F, Peckenschneider N et al. Gene expression and regulation of nerve growth factor in atopic dermatitis mast cells and the human mast cell line-1. J. Neuroimmunol.161(1–2), 87–92 (2005).
   PubMed Web of Science ®Google Scholar
• 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.)76(3), 205–209 (1996).
   PubMedGoogle Scholar
• Naukkarinen A, Nickoloff BJ, Farber EM. Quantification of cutaneous sensory nerves and their substance P content in psoriasis. J. Invest. Dermatol.92(1), 126–129 (1989).
   PubMed Web of Science ®Google Scholar
• Eedy DJ, Johnston CF, Shaw C, Buchanan KD. Neuropeptides in psoriasis: an immunocytochemical and radioimmunoassay study. J. Invest. Dermatol.96(4), 434–438 (1991).
   PubMed Web of Science ®Google Scholar
• Kulka M, Sheen CH, Tancowny BP, Grammer LC, Schleimer RP. Neuropeptides activate human mast cell degranulation and chemokine production. Immunology123(3), 398–410 (2008).
   PubMed Web of Science ®Google Scholar
• Saarinen JV, Harvima RJ, Naukkarinen A, Horsmanheimo M, Harvima IT. Release of histamine and leukotriene C4 in immediate allergic wheal reaction as measured with the microdialysis technique. Arch. Dermatol. Res.292(7), 333–340 (2000).
   PubMedGoogle Scholar
• Schmelz M, Luz O, Averbeck B, Bickel A. Plasma extravasation and neuropeptide release in human skin as measured by intradermal microdialysis. Neurosci. Lett.230(2), 117–120 (1997).
   PubMed Web of Science ®Google Scholar
• Schmelz M, Schmidt R, Bickel A, Handwerker HO, Torebjörk HE. Specific C-receptors for itch in human skin. J. Neurosci.17(20), 8003–8008 (1997).
   PubMed Web of Science ®Google Scholar
• Steinhoff M, Vergnolle N, Young SH et al. Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat. Med.6(2), 151–158 (2000).
   PubMed Web of Science ®Google Scholar
• Steinhoff M, Neisius U, Ikoma A et al. Proteinase-activated receptor-2 mediates itch: a novel pathway for pruritus in human skin. J. Neurosci.23(15), 6176–6180 (2003).
   PubMed Web of Science ®Google Scholar
• 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.19(2), 117–122 (2010).
   PubMedGoogle Scholar
• 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.248(3), 947–951 (1989).
   PubMedGoogle Scholar
• Tam EK, Caughey GH. Degradation of airway neuropeptides by human lung tryptase. Am. J. Respir. Cell. Mol. Biol.3(1), 27–32 (1990).
   PubMed Web of Science ®Google Scholar
• Walls AF, Brain SD, Desai A et al. Human mast cell tryptase attenuates the vasodilator activity of calcitonin gene-related peptide. Biochem. Pharmacol.43(6), 1243–1248 (1992).
   PubMed Web of Science ®Google Scholar
• 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.244(1), 133–137 (1988).
   PubMed Web of Science ®Google Scholar
• Harvima IT, Naukkarinen A, Paukkonen K et al. Mast cell tryptase and chymase in developing and mature psoriatic lesions. Arch. Dermatol. Res.285(4), 184–192 (1993).
   PubMedGoogle Scholar
• 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.)79(2), 98–104 (1999).
   PubMed Web of Science ®Google Scholar
• 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.283(7), 433–437 (1991).
   PubMedGoogle Scholar
• Harvima IT, Viinamäki H, Naukkarinen A et al. Association of cutaneous mast cells and sensory nerves with psychic stress in psoriasis. Psychother. Psychosom.60(3–4), 168–176 (1993).
   PubMed Web of Science ®Google Scholar
• MacQueen G, Marshall J, Perdue M, Siegel S, Bienenstock J. Pavlovian conditioning of rat mucosal mast cells to secrete rat mast cell protease II. Science243(4887), 83–85 (1989).
   PubMed Web of Science ®Google Scholar
• Gauci M, Husband AJ, Saxarra H, King MG. Pavlovian conditioning of nasal tryptase release in human subjects with allergic rhinitis. Physiol. Behav.55(5), 823–825 (1994).
   PubMedGoogle Scholar
• Kimata H. Enhancement of allergic skin wheal responses in patients with atopic eczema/dermatitis syndrome by playing video games or by a frequently ringing mobile phone. Eur. J. Clin. Invest.33(6), 513–517 (2003).
   PubMed Web of Science ®Google Scholar
• Theoharides TC, Spanos C, Pang X et al. Stress-induced intracranial mast cell degranulation: a corticotropin-releasing hormone-mediated effect. Endocrinology136(12), 5745–5750 (1995).
   PubMed Web of Science ®Google Scholar
• Esposito P, Chandler N, Kandere K et al. Corticotropin-releasing hormone and brain mast cells regulate blood–brain-barrier permeability induced by acute stress. J. Pharmacol. Exp. Ther.303(3), 1061–1066 (2002).
   PubMed Web of Science ®Google Scholar
• 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.13(3), 225–239 (1999).
   PubMed Web of Science ®Google Scholar
• 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.19(3), 252–262 (2005).
   PubMed Web of Science ®Google Scholar
• Pavlovic S, Daniltchenko M, Tobin DJ et al. Further exploring the brain–skin connection: stress worsens dermatitis via substance P-dependent neurogenic inflammation in mice. J. Invest. Dermatol.128(2), 434–446 (2008).
   PubMed Web of Science ®Google Scholar