Cutaneous denervation of psoriasiform mouse skin improves acanthosis and inflammation in a sensory neuropeptide-dependent manner

Journal of Investigative Dermatology

Volumn 131, Issue 7, 2011, Pages 1530-1538

  Ostrowski, Stephen M ^a   Belkadi, Abdelmadjid ^a   Loyd, Candace M ^a   Diaconu, Doina ^a   Ward, Nicole L ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 [1 IMINO 2 (2 METHOXYPHENYL)ETHYL] 7,7 DIPHENYLPERHYDROISOINDOL 4 ONE; 5 AMINOVALERYLSUBSTANCE P [7-11][9 PROLINE 10 (N METHYLLEUCINE)]; CALCITONIN GENE RELATED PEPTIDE; CALCITONIN GENE RELATED PEPTIDE RECEPTOR ANTAGONIST; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 6; MESSENGER RNA; SOMATOMEDIN C RECEPTOR; SOMATOSTATIN; SUBSTANCE P; VASCULOTROPIN; VASOACTIVE INTESTINAL POLYPEPTIDE;

ACANTHOSIS; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; DENDRITIC CELL; DENERVATION; LYMPHOCYTE; MOUSE; NERVE INJURY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSORIASIS; REMISSION; SIGNAL TRANSDUCTION; SKIN INFLAMMATION; SPINAL GANGLION;

EID: 79958783026     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2011.60     Document Type: Article

References (54)

1. Arck PC, Handjiski B, Peters EM et al. (2003) Stress inhibits hair growth in mice by induction of premature catagen development and deleterious perifollicular inflammatory events via neuropeptide substance P-depen-dent pathways. Am J Pathol 162:803-14 (Pubitemid 36237489)
2. Arck PC, Slominski A, Theoharides TC et al. (2006) Neuroimmunology of stress: skin takes center stage. J Invest Dermatol 126:1697-704 (Pubitemid 44086503)
3. Casasco A, Marchetti C, Calligaro A et al. (1990) Immunocytochemical labelling of Merkel cells of human oral mucosa by means of antibodies to protein gene product 9.5. Bull Group Int Rech Sci Stomatol Odontol 33:61-4
4. Chamian F, Lowes MA, Lin SL et al. (2005) Alefacept reduces infiltrating T cells, activated dendritic cells, and inflammatory genes in psoriasis vulgaris. Proc Natl Acad Sci USA 102:2075-80 (Pubitemid 40262014)
5. Chiang HY, Huang IT, Chen WP et al. (1998) Regional difference in epidermal thinning after skin denervation. Exp Neurol 154:137-45
6. Costa R, Marotta DM, Manjavachi MN et al. (2008) Evidence for the role of neurogenic inflammation components in trypsin-elicited scratching behaviour in mice. Br J Pharmacol 154:1094-103 (Pubitemid 351915068)
7. Costa SK, Yshii LM, Poston RN et al. (2006) Pivotal role of endogenous tachykinins and the NK1 receptor in mediating leukocyte accumulation, in the absence of oedema formation, in response to TNFalpha in the cutaneous microvasculature. J Neuroimmunol 171:99-109 (Pubitemid 41832281)
8. Dewing SB (1971) Remission of psoriasis associated with cutaneous nerve section. Arch Dermatol 104:220-1
9. Ding W, Wagner JA, Granstein RD (2007) CGRP, PACAP, and VIP modulate Langerhans cell function by inhibiting NF-kappaB activation. J Invest Dermatol 127:2357-67 (Pubitemid 47619742)
10. Farber EM, Lanigan SW, Boer J (1990) The role of cutaneous sensory nerves in the maintenance of psoriasis. Int J Dermatol 29:418-20 (Pubitemid 20252108)
11. Farber EM, Nickoloff BJ, Recht B et al. (1986) Stress, symmetry, and psoriasis: possible role of neuropeptides. J Am Acad Dermatol 14:305-11
12. Fuller RW, Conradson TB, Dixon CM et al. (1987) Sensory neuropeptide effects in human skin. Br J Pharmacol 92:781-8 (Pubitemid 18014927)
13. Gottlieb AB, Chamian F, Masud S et al. (2005) TNF inhibition rapidly down-regulates multiple proinflammatory pathways in psoriasis plaques. J Immunol 175:2721-9 (Pubitemid 41113889)
14. Goyarts E, Matsui M, Mammone T et al. (2008) Norepinephrine modulates human dendritic cell activation by altering cytokine release. Exp Dermatol 17:188-96 (Pubitemid 351233863)
15. Griffiths CE, Strober BE, van de Kerkhof P et al. (2010) Comparison of ustekinumab and etanercept for moderate-to-severe psoriasis. N Engl J Med 362:118-28
16. Gudjonsson JE, Johnston A, Dyson M et al. (2007) Mouse models of psoriasis. J Invest Dermatol 127:1292-308 (Pubitemid 46763003)
17. Hosoi J, Murphy GF, Egan CL et al. (1993) Regulation of Langerhans cell function by nerves containing calcitonin gene-related peptide. Nature 363:159-63 (Pubitemid 23147013)
18. Hsieh ST, Lin WM (1999) Modulation of keratinocyte proliferation by skin innervation. J Invest Dermatol 113:579-86
19. Huang IT, Lin WM, Shun CT et al. (1999) Influence of cutaneous nerves on keratinocyte proliferation and epidermal thickness in mice. Neu-roscience 94:965-73
20. Joachim RA, Handjiski B, Blois SM et al. (2008) Stress-induced neurogenic inflammation in murine skin skews dendritic cells towards maturation and migration: key role of intercellular adhesion molecule-1/leukocyte function-associated antigen interactions. Am J Pathol 173:1379-88
21. Joachim RA, Kuhlmei A, Dinh QT et al. (2007) Neuronal plasticity of the "brain-skin connection": stress-triggered up-regulation of neuropeptides in dorsal root ganglia and skin via nerve growth factor-dependent pathways. J Mol Med 85:1369-78 (Pubitemid 350234092)
22. Joseph T, Kurian J, Warwick DJ et al. (2005) Unilateral remission of psoriasis following traumatic nerve palsy. Br J Dermatol 152:185-6
23. Kinnman E (1987) Collateral sprouting of sensory axons in the hairy skin of the trunk: a morphological study in adult rats. Brain Res 414:385-9 (Pubitemid 17091965)
24. Lee E, Trepicchio WL, Oestreicher JL et al. (2004) Increased expression of interleukin 23 p19 and p40 in lesional skin of patients with psoriasis vulgaris. J Exp Med 199:125-30 (Pubitemid 38076484)
25. Legat FJ, Jaiani LT, Wolf P et al. (2004) The role of calcitonin gene-related peptide in cutaneous immunosuppression induced by repeated subinflammatory ultraviolet irradiation exposure. Exp Dermatol 13:242-50 (Pubitemid 38618080)
26. Lowes MA, Chamian F, Abello MV et al. (2005) Increase in TNF-alpha and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc Natl Acad Sci USA 102:19057-62 (Pubitemid 43049565)
27. Niizeki H, Kurimoto I, Streilein JW (1999) A substance p agonist acts as an adjuvant to promote hapten-specific skin immunity. J Invest Dermatol 112:437-42 (Pubitemid 29171932)
28. Papp KA, Langley RG, Lebwohl M et al. (2008) Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 52-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 2). The Lancet 371:1675-84 (Pubitemid 351671884)
29. Pavlovic S, Daniltchenko M, Tobin DJ et al. (2008) Further exploring the brain-skin connection: stress worsens dermatitis via substance P-dependent neurogenic inflammation in mice. J Invest Dermatol 128:434-46
30. Perlman HH (1972) Remission of psoriasis vulgaris from the use of nerve-blocking agents. Arch Dermatol 105:128-9
31. Peters EM, Kuhlmei A, Tobin DJ et al. (2005) Stress exposure modulates peptidergic innervation and degranulates mast cells in murine skin. Brain Behav Immun 19:252-62 (Pubitemid 40431540)
32. Peters EM, Liotiri S, Bodo E et al. (2007) Probing the effects of stress mediators on the human hair follicle: substance P holds central position. Am J Pathol 171:1872-86
33. Raychaudhuri SP, Jiang WY, Raychaudhuri SK (2008) Revisiting the Koebner phenomenon: role of NGF and its receptor system in the pathogenesis of psoriasis. Am J Pathol 172:961-71 (Pubitemid 351519993)
34. Raychaudhuri SP, Raychaudhuri SK (2004) Role of NGF and neurogenic inflammation in the pathogenesis of psoriasis. Prog Brain Res 146:433-7 (Pubitemid 37541398)
35. Raychaudhuri SP, Sanyal M, Weltman H et al. (2004) K252a, a High-Affinity Nerve Growth Factor Receptor Blocker, Improves Psoriasis: An In Vivo Study Using the Severe Combined Immunodeficient Mouse-Human Skin Model. J Invest Dermatol 122:812-9 (Pubitemid 38471352)
36. Saint-Mezard P, Chavagnac C, Bosset S et al. (2003) Psychological stress exerts an adjuvant effect on skin dendritic cell functions in vivo. J Immunol 171:4073-80 (Pubitemid 37238682)
37. Saraceno R, Kleyn CE, Terenghi G et al. (2006) The role of neuropeptides in psoriasis. Br J Dermatol 155:876-82 (Pubitemid 44564493)
38. Seiffert K, Hosoi J, Torii H et al. (2002) Catecholamines inhibit the antigen-presenting capability of epidermal Langerhans cells. J Immunol 168:6128-35 (Pubitemid 34620030)
39. Seike M, Ikeda M, Morimoto A et al. (2002) Increased synthesis of calcitonin gene-related peptide stimulates keratinocyte proliferation in murine UVB-irradiated skin. J Dermatol Sci 28:135-43 (Pubitemid 34155342)
40. Seville RH (1977) Psoriasis and stress. Br J Dermatol 97:297-302 (Pubitemid 8208173)
41. Siebenhaar F, Magerl M, Peters EM et al. (2008) Mast cell-driven skin inflammation is impaired in the absence of sensory nerves. J Allergy Clin Immunol 121:955-61
42. Stankovic N, Johansson O, Hildebrand C (1999) Increased occurrence of PGP 9.5-immunoreactive epidermal Langerhans cells in rat plantar skin after sciatic nerve injury. Cell Tissue Res 298:255-60 (Pubitemid 29512077)
43. Stratigos AJ, Katoulis AK, Stavrianeas NG (1998) Spontaneous clearing of psoriasis after stroke. J Am Acad Dermatol 38:768-70 (Pubitemid 28213726)
44. Swindell WR, Johnston A, Carbajal S et al. (2011) Genome-wide expression profiling of five mouse models identifies similarities and differences with human psoriasis. Plos One (in press)
45. Talme T, Liu Z, Sundqvist KG (2008) The neuropeptide calcitonin gene-related peptide (CGRP) stimulates T cell migration into collagen matrices. J Neuroimmunol 196:60-6
46. Tanaka T, Danno K, Ikai K et al. (1988) Effects of substance P and substance K on the growth of cultured keratinocytes. J Invest Dermatol 90:399-401 (Pubitemid 18079788)
47. Torii H, Tamaki K, Granstein RD (1988) The effect of neuropeptides/ hormones on Langerhans cells. J Dermatol Sci 20:21-8
48. van der Fits L, Mourits S, Voerman JS et al. (2009) Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J Immunol 182:5836-45
49. Ward NL, Hatala DA, Wolfram JA et al. (2011) Cutaneous manipulation of vascular growth factors leads to alterations in immunocytes, blood vessels and nerves: Evidence for a cutaneous neurovascular unit. J Dermatol Sci 61:14-22
50. Ward NL, Loyd CM, Wolfram JA et al. (2010) Depletion of antigen presenting cells by clodronate liposomes reverses the psoriatic skin phenotype in KC-Tie2 mice. Br J Dermatol; e-pub ahead of print 11 November 2010
51. Wolfram JA, Diaconu D, Hatala DA et al. (2009) Keratinocyte but not endothelial cell specific overexpression of Tie2 leads to the development of psoriasis. Am J Pathol 174:1443-58
52. Yu XJ, Li CY, Xu YH et al. (2009) Calcitonin gene-related peptide increases proliferation of human HaCaT keratinocytes by activation of MAP kinases. Cell Biol Int 33:1144-8
53. Zaba LC, Cardinale I, Gilleaudeau P et al. (2007) Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. J Exp Med 204:3183-94
54. Zheng Y, Danilenko DM, Valdez P et al. (2007) Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445:648-51 (Pubitemid 46232884)