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

Expert Review of Clinical Immunology

Volumn 8, Issue 3, 2012, Pages 235-241

  Harvima, Ilkka T ^a   Nilsson, Gunnar ^b  

^a KUOPIO UNIVERSITY HOSPITAL   (Finland)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

hormone; mast cell; nerve; psoriasis; stress

Indexed keywords

ADRENALIN; ALPHA INTERMEDIN; CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR 1; CORTICOTROPIN RELEASING FACTOR RECEPTOR 2; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYDROCORTISONE; INTERLEUKIN 3; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; NERVE GROWTH FACTOR; NEUROKININ 1 RECEPTOR; NEUROKININ 2 RECEPTOR; NEUROKININ 3 RECEPTOR; NEUROPEPTIDE; NEUROTROPHIN; NEUROTROPHIN 3; NORADRENALIN; PROOPIOMELANOCORTIN; PROTEINASE ACTIVATED RECEPTOR 2; RANTES; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; VASOACTIVE INTESTINAL POLYPEPTIDE; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR 2;

ADRENALIN RELEASE; APOPTOSIS; CELL ACTIVATION; CELL ADHESION; CELL INTERACTION; CELL SURVIVAL; CORTICOTROPIN RELEASE; CYTOKINE PRODUCTION; EPIDERMIS; HAIR FOLLICLE; HYDROCORTISONE RELEASE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNOREACTIVITY; MAST CELL; MAST CELL DEGRANULATION; MENTAL STRESS; NEUROENDOCRINE SYSTEM; NONHUMAN; NORADRENALIN RELEASE; PROTEIN EXPRESSION; PSORIASIS; REVIEW; SENSORY NERVE; STRESS; SWEAT GLAND;

ANIMALS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INFLAMMATION MEDIATORS; MAST CELLS; MICE; NEUROSECRETORY SYSTEMS; PEPTIDE HORMONES; PITUITARY-ADRENAL SYSTEM; PSORIASIS; RATS; SENSORY RECEPTOR CELLS; SKIN; STRESS, PHYSIOLOGICAL;

EID: 84858408532     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/eci.12.1     Document Type: Review

References (74)

1. Sabat R, Philipp S, Höflich C et al. Immunopathogenesis of psoriasis. Exp. Dermatol. 16(10), 779-798 (2007).
2. 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).
3. Basavaraj KH, Navya MA, Rashmi R. Stress and quality of life in psoriasis. Int. J. Dermatol 50(7), 783-792 (2011).
4. 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).
5. 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).
6. 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).
7. Church MK, Lowman MA, Rees PH, Benyon RC. Mast cells, neuropeptides and inflammation. Agents Actions 27(1-2), 8-16 (1989).
8. Baldwin AL. Mast cell activation by stress. Methods Mol. Biol. 315, 349-360 (2006).
9. 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).
10. 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). 11 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).
11. 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).
12. Zmijewski MA, Slominski AT. Emerging role of alternative splicing of CRF1 receptor in CRF signaling. Acta Biochim Pol 57(1), 1-13 (2010).
13. ÓKane M, Murphy EP, Kirby B. The role of corticotropin-releasing hormone in immune-mediated cutaneous inflammatory diseases. Exp. Dermatol. 15(3), 143-153 (2006).
14. 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).
15. 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).
16. 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)? Psychoneuroendocrinology 31(4), 439-446 (2006).
17. 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).
18. 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).
19. 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).
20. Eves PC, Haycock JW. Melanocortin signalling mechanisms. Adv. Exp. Med. Biol. 681, 19-28 (2010).
21. 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).
22. 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).
23. Cirulle F, Alleva E. The NGF saga: from animal models of psychosocial stress to stress-related psychopathology. Front. Neuroendocrinol. 30(3), 379-395 (2009).
24. 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).
25. 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).
26. 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).
27. 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).
28. 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).
29. 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).
30. 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).
31. 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).
32. 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).
33. 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).
34. 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).
35. 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).
36. Kempuraj D, Papadopoulou NG, Lytinas M et al. Corticotropin-releasing hormone and its structurally related urocortin are synthesized and secreted by human mast cells. Endocrinology 145(1), 43-48 (2004).
37. 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 a-MSH. J. Invest. Dermatol. 126(9), 1976-1981 (2006).
38. Sarkar A, Sreenivasan Y, Manna SK. a-Melanocyte-stimulating hormone induces cell death in mast cells: involvement of NF-kB. FEBS Lett. 549(1-3), 87-93 (2003).
39. Montano JA, Pérez-Pinera P, Garcia-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).
40. 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. Blood 106(4), 1330-1336 (2005).
41. Nilsson G, Blom T, Harvima I, Kusche-Gullberg M, Nilsson K. Stem cell factor-dependent human cord blood derived mast cells express a- and β-tryptase, heparin and chondroitin sulphate. Immunology 88(2), 308-314 (1996).
42. 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 30(8), 1113-1120 (2000).
43. Welker P, Grabbe J, Gibbs B, Zuberbier T, Henz BM. Nerve growth factor-b induces mast-cell marker expression during in vitro culture of human umbilical cord blood cells. Immunology 99(3), 418-426 (2000).
44. 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).
45. 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).
46. Xiang Z, Nilsson G. IgE receptor-mediated release of nerve growth factor by mast cells. Clin. Exp. Allergy 30(10), 1379-1386 (2000).
47. di Mola FF, Friess H, Zhu ZW et al. Nerve growth factor and Trk high affinity receptor (TrkA) gene expression in inflammatory bowel disease. Gut 46(5), 670-679 (2000).
48. 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).
49. 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).
50. 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).
51. Eedy DJ, Johnston CF, Shaw C, Buchanan KD. Neuropeptides in psoriasis: an immunocytochemical and radioimmunoassay study. J. Invest. Dermatol. 96(4), 434-438 (1991).
52. Kulka M, Sheen CH, Tancowny BP, Grammer LC, Schleimer RP. Neuropeptides activate human mast cell degranulation and chemokine production. Immunology 123(3), 398-410 (2008).
53. 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).
54. 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).
55. 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).
56. 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).
57. 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).
58. 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).
59. 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).
60. Tam EK, Caughey GH. Degradation of airway neuropeptides by human lung tryptase. Am. J. Respir. Cell. Mol. Biol. 3(1), 27-32 (1990).
61. 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).
62. 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).
63. 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).
64. 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).
65. 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).
66. 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).
67. 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 243(4887), 83-85 (1989).
68. 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).
69. 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).
70. Theoharides TC, Spanos C, Pang X et al. Stress-induced intracranial mast cell degranulation: a corticotropin-releasing hormone-mediated effect. Endocrinology 136(12), 5745-5750 (1995).
71. 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).
72. 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).
73. 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).
74. 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).