Mental stress in atopic dermatitis - Neuronal plasticity and the cholinergic system are affected in atopic dermatitis and in response to acute experimental mental stress in a randomized controlled pilot study

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Peters, Eva Milena Johanne ^a,b   Michenko, Anna ^a,b,c   Kupfer, Jörg ^b   Kummer, Wolfgang ^b   Wiegand, Silke ^b   Niemeier, Volker ^d   Potekaev, Nikolay ^e   Lvov, Andrey ^c   Gieler, Uwe ^b,d  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c I M SECHENOV FIRST MOSCOW STATE MEDICAL UNIVERSITY   (Russian Federation)

^d UNIVERSITY HOSPITAL GIESSEN   (Germany)

^e Moscow Scientific and Practical Center of Dermatovenereology and Cosmetology   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

BUNGAROTOXIN RECEPTOR; ENDOGENOUS NICOTINIC ACETYLCHOLINE RECEPTOR LIGAND; LY 6 UROKINASE TYPE PLASMINOGEN ACTIVATOR RECEPTOR RELATED PROTEIN; MESSENGER RNA; NERVE GROWTH FACTOR; NEUROMODULIN; NEUROPEPTIDE; PROTEIN; UNCLASSIFIED DRUG; LY ANTIGEN; NICOTINIC RECEPTOR; SLURP1 PROTEIN, HUMAN; UROKINASE;

ACUTE STRESS; ADULT; ARTICLE; ATOPIC DERMATITIS; CELL ACTIVATION; CELL CONTACT; CHOLINERGIC SYSTEM; CHRONIC INFLAMMATION; CLINICAL ARTICLE; CONTROLLED STUDY; EMOTIONAL STRESS; FEMALE; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMUNE RESPONSE; INFLAMMATORY DISEASE; LABORATORY TEST; MALE; MAST CELL; MENTAL STRESS; MORPHOMETRICS; MOUSE MODEL; NAMED INVENTORIES, QUESTIONNAIRES AND RATING SCALES; NERVE CELL PLASTICITY; NERVE FIBER; NEUROGENIC INFLAMMATION; NUCLEOTIDE SEQUENCE; PILOT STUDY; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCORAD; SKIN BIOPSY; SKIN PRURITUS; SOCIAL STRESS; TRIER SOCIAL STRESS TEST; ADOLESCENT; ANIMAL; BIOPSY; BIOSYNTHESIS; CLINICAL TRIAL; COMPLICATION; IMMUNOLOGY; INFLAMMATION; INNATE IMMUNITY; METABOLISM; MIDDLE AGED; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL;

ADOLESCENT; ADULT; ANIMALS; ANTIGENS, LY; BIOPSY; DERMATITIS, ATOPIC; HUMANS; IMMUNITY, INNATE; INFLAMMATION; MAST CELLS; MICE; MIDDLE AGED; NERVE FIBERS; NEURONAL PLASTICITY; RECEPTORS, NICOTINIC; STRESS, PSYCHOLOGICAL; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84914682306     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113552     Document Type: Article

References (41)

1. Dhabhar FS (2013) Psychological stress and immunoprotection versus immunopathology in the skin. Clinics in dermatology 31: 18-30.
2. Buske-Kirschbaum A, Ebrecht M, Hellhammer DH (2010) Blunted HPA axis responsiveness to stress in atopic patients is associated with the acuity and severeness of allergic inflammation. Brain Behav Immun 24: 1347-1353.
3. Cevikbas F, Steinhoff A, Homey B, Steinhoff M (2007) Neuroimmune interactions in allergic skin diseases. Current opinion in allergy and clinical immunology 7: 365-373.
4. Lonne-Rahm SB, Rickberg H, El-Nour H, Marin P, Azmitia EC, et al. (2008) Neuroimmune mechanisms in patients with atopic dermatitis during chronic stress. J Eur Acad Dermatol Venereol 22: 11-18.
5. Pavlovic S, Liezmann C, Blois SM, Joachim R, Kruse J, et al. (2011) Substance P is a key mediator of stress-induced protection from allergic sensitization via modified antigen presentation. J Immunol 186: 848-855.
6. Peters EM, Liezmann C, Klapp BF, Kruse J (2012) The neuroimmune connection interferes with tissue regeneration and chronic inflammatory disease in the skin. Ann N Y Acad Sci 1262: 118-126.
7. Schut C, Weik U, Tews N, Gieler U, Deinzer R, et al. (2013) Psychophysiological effects of stress management in patients with atopic dermatitis: a randomized controlled trial. Acta Derm Venereol 93: 57-61.
8. Segerstrom SC, Miller GE (2004) Psychological stress and the human immune system: a meta-analytic study of 30 years of inquiry. Psychological bulletin 130: 601-630.
9. Singh LK, Pang X, Alexacos N, Letourneau R, Theoharides TC (1999) 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: 225-239.
10. Steinhoff M, Stander S, Seeliger S, Ansel JC, Schmelz M, et al. (2003) Modern aspects of cutaneous neurogenic inflammation. Archives of dermatology 139: 1479-1488.
11. Harvima IT, Nilsson G, Naukkarinen A (2010) Role of mast cells and sensory nerves in skin inflammation. G Ital Dermatol Venereol 145: 195-204.
12. Theoharides TC, Alysandratos KD, Angelidou A, Delivanis DA, Sismanopoulos N, et al. (2012) Mast cells and inflammation. Biochim Biophys Acta 1822: 21-33.
13. Pavlovic S, Daniltchenko M, Tobin DJ, Hagen E, Hunt SP, et al. (2008) Further exploring the brain-skin connection: stress worsens dermatitis via substance P-dependent neurogenic inflammation in mice. J Invest Dermatol 128: 434-446.
14. Peters EM, Liezmann C, Spatz K, Daniltchenko M, Joachim R, et al. (2011) Nerve growth factor partially recovers inflamed skin from stress-induced worsening in allergic inflammation. J Invest Dermatol 131: 735-743.
15. Spradley JM, Davoodi A, Carstens MI, Carstens E (2012) Effects of acute stressors on itch- and painrelated behaviors in rats. Pain 153: 1890-1897.
16. Grando SA (2008) Basic and clinical aspects of non-neuronal acetylcholine: biological and clinical significance of non-canonical ligands of epithelial nicotinic acetylcholine receptors. J Pharmacol Sci 106: 174-179.
17. Grando SA, Pittelkow MR, Schallreuter KU (2006) Adrenergic and cholinergic control in the biology of epidermis: physiological and clinical significance. J Invest Dermatol 126: 1948-1965.
18. Kindt F, Wiegand S, Niemeier V, Kupfer J, Loser C, et al. (2008) Reduced expression of nicotinic alpha subunits 3, 7, 9 and 10 in lesional and nonlesional atopic dermatitis skin but enhanced expression of alpha subunits 3 and 5 in mast cells. Br J Dermatol 159: 847-857.
19. Mishra NC, Rir-Sima-Ah J, Langley RJ, Singh SP, Pena-Philippides JC, et al. (2008) Nicotine primarily suppresses lung Th2 but not goblet cell and muscle cell responses to allergens. J Immunol 180: 7655-7663.
20. Sinkus ML, Wamboldt MZ, Barton A, Fingerlin TE, Laudenslager ML, et al. (2011) The alpha7 nicotinic acetylcholine receptor and the acute stress response: maternal genotype determines offspring phenotype. Physiol Behav 104: 321-326.
21. Chernyavsky AI, Kalantari-Dehaghi M, Phillips C, Marchenko S, Grando SA (2012) Novel cholinergic peptides SLURP-1 and -2 regulate epithelialization of cutaneous and oral wounds. Wound Repair Regen 20: 103-113.
22. Kawashima K, Fujii T, Moriwaki Y, Misawa H, Horiguchi K (2012) Reconciling neuronally and nonneuronally derived acetylcholine in the regulation of immune function. Ann N Y Acad Sci 1261: 7-17.
23. Hanifin JM (1989) Recognizing and managing clinical problems in atopic dermatitis. Allergy Proc 10: 397-402.
24. Kirschbaum C, Pirke KM, Hellhammer DH (1993) The 'Trier Social Stress Test'-a tool for investigating psychobiological stress responses in a laboratory setting. Neuropsychobiology 28: 76-81.
25. Peters EM, Liotiri S, Bodo E, Hagen E, Biro T, et al. (2007) Probing the effects of stress mediators on the human hair follicle: substance P holds central position. Am J Pathol 171: 1872-1886.
26. Hendrix S, Picker B, Liezmann C, Peters EM (2008) Skin and hair follicle innervation in experimental models: a guide for the exact and reproducible evaluation of neuronal plasticity. Exp Dermatol 17: 214-227.
27. Dou YC, Hagstromer L, Emtestam L, Johansson O (2006) Increased nerve growth factor and its receptors in atopic dermatitis: an immunohistochemical study. Arch Dermatol Res 298: 31-37.
28. Joachim RA, Kuhlmei A, Dinh QT, Handjiski B, Fischer T, 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: 1369-1378.
29. Howe CL, Mobley WC (2005) Long-distance retrograde neurotrophic signaling. Curr Opin Neurobiol 15: 40-48.
30. Lips KS, Luhrmann A, Tschernig T, Stoeger T, Alessandrini F, et al. (2007) Down-regulation of the non-neuronal acetylcholine synthesis and release machinery in acute allergic airway inflammation of rat and mouse. Life Sci 80: 2263-2269.
31. Chimienti F, Hogg RC, Plantard L, Lehmann C, Brakch N, et al. (2003) Identification of SLURP-1 as an epidermal neuromodulator explains the clinical phenotype of Mal de Meleda. Human molecular genetics 12: 3017-3024.
32. Chernyavsky AI, Arredondo J, Galitovskiy V, Qian J, Grando SA (2010) Upregulation of nuclear factor-kappaB expression by SLURP-1 is mediated by alpha7-nicotinic acetylcholine receptor and involves both ionic events and activation of protein kinases. Am J Physiol Cell Physiol 299: C903-911.
33. Chernyavsky AI, Arredondo J, Skok M, Grando SA (2010) Auto/paracrine control of inflammatory cytokines by acetylcholine in macrophage-like U937 cells through nicotinic receptors. Int Immunopharmacol 10: 308-315.
34. Narumoto O, Niikura Y, Ishii S, Morihara H, Okashiro S, et al. (2013) Effect of secreted lymphocyte antigen-6/urokinase-type plasminogen activator receptor-related peptide-1 (SLURP-1) on airway epithelial cells. Biochemical and biophysical research communications 438: 175-179.
35. Matoso A, Mukkada VA, Lu S, Monahan R, Cleveland K, et al. (2013) Expression microarray analysis identifies novel epithelial-derived protein markers in eosinophilic esophagitis. Mod Pathol 26: 665-676.
36. Swamynathan S, Buela KA, Kinchington P, Lathrop KL, Misawa H, et al. (2012) Klf4 regulates the expression of Slurp1, which functions as an immunomodulatory peptide in the mouse cornea. Invest Ophthalmol Vis Sci 53: 8433-8446.
37. Misery L (2004) Nicotine effects on skin: are they positive or negative? Exp Dermatol 13: 665-670.
38. Hendrix S, Peters EM (2007) Neuronal plasticity and neuroregeneration in the skin - The role of inflammation. J Neuroimmunol 184: 113-126.
39. Rohleder N (2012) Acute and chronic stress induced changes in sensitivity of peripheral inflammatory pathways to the signals of multiple stress systems -2011 Curt Richter Award Winner. Psychoneuroendocrinology 37: 307-316.
40. Ofek K, Soreq H (2013) Cholinergic involvement and manipulation approaches in multiple system disorders. Chem Biol Interact 203: 113-119.
41. Giovanoli S, Engler H, Engler A, Richetto J, Voget M, et al. (2013) Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice. Science 339: 1095-1099.