Probing the effects of stress mediators on the human hair follicle: Substance P holds central position

American Journal of Pathology

Volumn 171, Issue 6, 2007, Pages 1872-1886

  Peters, Eva M J ^a   Liotiri, Sofia ^b   Bodó, Eniko ^b   Hagen, Evelin ^a   Bíró, Tamás ^c   Arck, Petra C ^a   Paus, Ralf ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^c UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 MICROGLOBULIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NERVE GROWTH FACTOR; NERVE GROWTH FACTOR RECEPTOR; NEUROTROPHIN RECEPTOR P75; PROTEIN TYROSINE KINASE A; PROTEINASE; SUBSTANCE P;

ALOPECIA AREATA; ARTICLE; CELLULAR STRESS RESPONSE; CONNECTIVE TISSUE; CONTROLLED STUDY; DISEASE EXACERBATION; DOWN REGULATION; HAIR ANALYSIS; HAIR FOLLICLE; HAIR GROWTH; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; MAST CELL DEGRANULATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

EID: 38349078214     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2007.061206     Document Type: Article

References (92)

1. York J, Nicholson T, Minors P, Duncan DF: Stressful life events and loss of hair among adult women, a case-control study. Psychol Rep 1998, 82:1044-1046
2. Paus R: Stress, hair growth control and the neuro-endocrine immune connection. Allergo J 2000, 9411-9420
3. Hadshiew IM, Foitzik K, Arck PC, Paus R: Burden of hair loss: stress and the underestimated psychosocial impact of telogen effluvium and androgenetic alopecia. J Invest Dermatol 2004, 123:455-457
4. Peters EM, Arck PC, Paus R: Hair growth inhibition by psychoemotional stress: a mouse model for neural mechanisms in hair growth control. Exp Dermatol 2006, 15:1-13
5. Arck PC, Handjiski B, Hagen E, Joachim R, Klapp BF, Paus R: Indications for a 'brain-hair follicle axis (BHA)': inhibition of keratinocyte proliferation and up-regulation of keratinocyte apoptosis in telogen hair follicles by stress and substance P. FASEB J 2001, 15:2536-2538
6. Peters EM, Handjiski B, Kuhlmei A, Hagen E, Bielas H, Braun A, Klapp BF, Paus R, Arck PC: Neurogenic inflammation in stress-induced termination of murine hair growth is promoted by nerve growth factor. Am J Pathol 2004, 165:259-271
7. Arck PC, Handjiski B, Kuhlmei A, Peters EM, Knackstedt M, Peter A, Hunt SP, Klapp BF, Paus R: Mast cell deficient and neurokinin-1 receptor knockout mice are protected from stress-induced hair growth inhibition. J Mol Med 2005, 83:386-396
8. Paus R, Peters EM, Eichmuller S, Botchkarev VA: Neural mechanisms of hair growth control. J Invest Dermatol Symp Proc 1997, 2:61-68
9. Arck PC, Handjiski B, Peters EMJ, Peter AS, Hagen E, Fischer A, Klapp BF, Paus R: Stress inhibits hair growth in mice by induction of premature catagen development and deleterious perifollicular inflammatory events via neuropeptide substance P-dependent pathways. Am J Pathol 2003, 162:803-814
10. Botchkarev VA: Neurotrophins and their role in pathogenesis of alopecia areata. J Invest Dermatol Symp Proc 2003, 8:195-198
11. Toyoda M, Morohashi M: New aspects in acne inflammation. Dermatology 2003, 206:17-23
12. Peters EM, Kuhlmei A, Tobin DJ, Muller-Rover S, Klapp BF, Arck PC: Stress exposure modulates peptidergic innervation and degranulates mast cells in murine skin. Brain Behav Immun 2005, 19:252-262
13. 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, 13:225-239
14. Katayama I, Bae SJ, Hamasaki Y, Igawa K, Miyazaki Y, Yokozeki H, Nishioka K: Stress response, tachykinin, and cutaneous inflammation. J Invest Dermatol Symp Proc 2001, 6:81-86
15. Black PH: Stress and the inflammatory response: a review of neurogenic inflammation. Brain Behav Immun 2002, 16:622-653
16. Kimata H: Enhancement of allergic skin wheal responses and in vitro allergen-specific IgE production by computer-induced stress in patients with atopic dermatitis. Brain Behav Immun 2003, 17:134-138
17. Scholzen T, Armstrong CA, Bunnett NW, Luger TA, Olerud JE, Ansel JC: Neuropeptides in the skin: interactions between the neuroendocrine and the skin immune systems. Exp Dermatol 1998, 7:81-96
18. Lang UE, Anders D, Danker-Hopfe H, Hellweg R: Measurement of nerve growth factor serum concentration in a psychologically stressful situation in men. Stress 2004, 7:39-42
19. Alleva E, Santucci D: Psychosocial versus "physical" stress situations in rodents and humans: role of neurotrophins. Physiol Behav 2001, 73:313-320
20. Botchkarev VA, Yaar M, Peters EM, Raychaudhuri SP, Botchkareva NV, Marconi A, Raychaudhuri SK, Paus R, Pincelli C: Neurotrophins in skin biology and pathology. J Invest Dermatol 2006, 126:1719-1727
21. Peters EM, Stieglitz MG, Liezman C, Overall RW, Nakamura M, Hagen E, Klapp BF, Arck P, Paus R: p75 neurotrophin receptor-mediated signaling promotes human hair follicle regression (catagen). Am J Pathol 2006, 168:221-234
22. Hendrix S, Handjiski B, Peters EM, Paus R: A guide to assessing damage response pathways of the hair follicle: lessons from cyclophosphamide-induced alopecia in mice. J Invest Dermatol 2005, 125:42-51
23. Paus R, Slominski A, Czarnetzki BM: Is alopecia areata an autoimmune-response against melanogenesis-related proteins, exposed by abnormal MHC class I expression in the anagen hair bulb? Yale J Biol Med 1993, 66:541-554
24. Paus R, Ito N, Takigawa M, Ito T: The hair follicle and immune privilege. J Invest Dermatol Symp Proc 2003, 8:188-194
25. Ito T, Ito N, Bettermann A, Tokura Y, Takigawa M, Paus R: Collapse and restoration of MHC class-I-dependent immune privilege: exploiting the human hair follicle as a model. Am J Pathol 2004, 164:623-634
26. Gilhar A, Kalish RS: Alopecia areata: a tissue specific autoimmune disease of the hair follicle. Autoimmun Rev 2006, 5:64-69
27. Hordinsky MK, Kennedy W, Wendelschafer-Crabb G, Lewis S: Structure and function of cutaneous nerves in alopecia areata. J Invest Dermatol 1995, 104.28S-29S
28. Hordinsky MK, Ericson ME: Relationship between follicular nerve supply and alopecia. Dermatol Clin 1996, 14:651-660
29. Hordinsky MK: Alopecia areatia: pathophysiology and latest developments. J Cutan Med Surg 1999, 3:S28-S30
30. Hordinsky M, Ericson M: Nerves, neuropeptides, and the human anagen hair follicle. J Deut Dermatol Gesell 2004, 6:506
31. Siebenhaar F, Sharov AA, Peters EMJ, Sharova TY, Syska W, Mardariev A, Freyschmidt-Paul P, Sundberg J, Maurer M, Botchkarev VA: Substance P as immunomodulatory neuropeptide in a mouse model autoimmune hair loss (alopecia areata). J Invest Dermatol 2007, 127:1489-1497
32. Levite M: Neuropeptides, by direct interaction with T cells, induce cytokine secretion and break the commitment to a distinct T helper phenotype. Proc Natl Acad Sci USA 1998, 95:12544-12549
33. Kang H, Byun DG, Kim JW: Effects of substance P and vasoactive intestinal peptide on interferon-gamma and interleukin-4 production in severe atopic dermatitis. Ann Allergy Asthma Immunol 2000, 85:227-232
34. Buske-Kirschbaum A, Gierens A, Hollig H, Hellhammer DH: Stress-induced immunomodulation is altered in patients with atopic dermatitis. J Neuroimmunol 2002, 129:161-167
35. Buske-Kirschbaum A, Kern S, Ebrecht M, Hellhammer DH: Altered distribution of leukocyte subsets and cytokine production in response to acute psychosocial stress in patients with psoriasis vulgaris. Brain Behav Immun 2007, 21:92-99
36. Philpott M: In vitro maintenance of isolated hair follicles: current status and future development. Exp Dermatol 1999, 8:317-319
37. Ito N, Ito T, Paus R: The human hair follicle has established a fully functional peripheral equivalent of the hypothamalic-pituitary-adrenal-axis (HPA). Exp Dermatol 2005, 14:158
38. Philpott MP, Westgate GE, Kealey T: An in vitro model for the study of human hair growth. Ann NY Acad Sci 1991, 642:148-164
39. Philpott MP, Sanders D, Westgate GE, Kealey T: Human hair growth in vitro: a model for the study of hair follicle biology. J Dermatol Sci 1994, 7:S55-S72
40. Haegerstrand A, Jonzon B, Dalsgaard CJ, Nilsson J: Vasoactive intestinal polypeptide stimulates cell proliferation and adenylate cyclase activity of cultured human keratinocytes. Proc Natl Acad Sci USA 1989, 86:5993-5996
41. Takahashi K, Nakanishi S, Imamura S: Direct effects of cutaneous neuropeptides on adenylyl cyclase activity and proliferation in a keratinocyte cell line: stimulation of cyclic AMP formation by CGRP and VIP/PHM, and inhibition by NPY through G protein-coupled receptors. J Invest Dermatol 1993, 101:646-651
42. Paus R, Heinzelmann T, Robicsek S, Czarnetzki BM, Maurer M: Substance P stimulates murine epidermal keratinocyte proliferation and dermal mast cell degranulation in situ. Arch Dermatol Res 1995, 287:500-502
43. Peters EM, Botchkarev VA, Botchkareva NV, Tobin DJ, Paus R: Hair-cycle-associated remodeling of the peptidergic innervation of murine skin, and hair growth modulation by neuropeptides. J Invest Dermatol 2001, 116:236-245
44. Müller-Röver S, Handjiski B, van der Veen C, Eichmüller S, Foitzik K, McKay IA, Stenn KS, Paus R: A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 2001, 117:3-15
45. Peters EM, Hansen MG, Overall RW, Nakamura M, Pertile P, Klapp BF, Arck PC, Paus R: Control of human hair growth by neurotrophins: brain-derived neurotrophic factor inhibits hair shaft elongation, induces catagen, and stimulates follicular transforming growth factor beta2 expression. J Invest Dermatol 2005, 124:675-685
46. Foitzik K, Krause K, Conrad F, Nakamura M, Funk W, Paus R: Human scalp hair follicles are both a target and a source of prolactin, which serves as an autocrine and/or paracrine promoter of apoptosis-driven hair follicle regression. Am J Pathol 2006, 168:748-756
47. Maurer M, Paus R, Czarnetzki BM: Mast cells as modulators of hair follicle cycling. Exp Dermatol 1995, 4:266-271
48. Ito T, Ito N, Saathoff M, Bettermann A, Takigawa M, Paus R: Interferon-gamma is a potent inducer of catagen-like changes in cultured human anagen hair follicles. Br J Dermatol 2005, 152:623-631
49. Botchkareva NV, Khlgatian M, Longley BJ, Botchkarev VA, Gilchrest BA: SCF/c-kit signaling is required for cyclic regeneration of the hair pigmentation unit. FASEB J 2001, 15:645-658
50. Peters EM, Tobin DJ, Botchkareva N, Maurer M, Paus R: Migration of melanoblasts into the developing murine hair follicle is accompanied by transient c-Kit expression. J Histochem Cytochem 2002, 50:751-766
51. Gurish MF, Boyce JA: Mast cells: ontogeny, homing, and recruitment of a unique innate effector cell. J Allergy Clin Immunol 2006, 117:1285-1291
52. Botchkarev VA, Botchkareva NV, Peters EM, Paus R: Epithelial growth control by neurotrophins: leads and lessons from the hair follicle. Prog Brain Res 2004, 146:493-513
53. Christoph T, Muller-Rover S, Audring H, Tobin DJ, Hermes B, Cotsarelis G, Ruckert R, Paus R: The human hair follicle immune system: cellular composition and immune privilege. Br J Dermatol 2000, 142:862-873
54. Gupta MA, Gupta AK, Watteel GN: Stress and alopecia areata: a psychodermatologic study. Acta Derm Venereol 1997, 77:296-298
55. Maurer M, Fischer E, Handjiski B, von Stebut E, Algermissen B, Bavandi A, Paus R: Activated skin mast cells are involved in murine hair follicle regression (catagen). Lab Invest 1997, 77:319-332
56. Liu JY, Hu JH, Zhu QG, Li FQ, Sun HJ: Substance P receptor expression in human skin keratinocytes and fibroblasts. Br J Dermatol 2006, 155:657-662
57. Tanaka T, Danno K, Ikai K, Imamura S: Effects of substance P and substance K on the growth of cultured keratinocytes. J Invest Dermatol 1988, 90:399-401
58. Paus R, Heinzelmann T, Robicsek S, Czarnetzki BM, Maurer M: Substance P stimulates murine epidermal keratinocyte proliferation and dermal mast cell degranulation in situ. Arch Dermatol Res 1995, 287:500-502
59. Botchkarev VA, Metz M, Botchkareva NV, Welker P, Lommatzsch M, Renz H, Paus R: Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4 act as "epitheliotrophins" in murine skin. Lab Invest 1999, 79:557-572
60. Stenn KS, Paus R: Controls of hair follicle cycling. Physiol Rev 2001, 81:449-494
61. Paus R, Foitzik K: In search of the "hair cycle clock": a guided tour. Differentiation 2004, 72:489-511
62. Pincelli C, Fantini F, Romualdi P, Sevignani C, Lesa G, Benassi L, Giannetti A: Substance P is diminished and vasoactive intestinal peptide is augmented in psoriatic lesions and these peptides exert disparate effects on the proliferation of cultured human keratinocytes. J Invest Dermatol 1992, 98:421-427
63. McGovern UB, Jones KT, Sharpe GR: Intracellular calcium as a second messenger following growth stimulation of human keratinocytes. Br J Dermatol 1995, 132:892-896
64. Kozakiewicz M, Godlewski A: Modulation of the mitotic activity and population of the mast cells in the oral mucosa by substance P. Cell Mol Biol Lett 2003, 8:727-734
65. Ansel JC, Brown JR, Payan DG, Brown MA: Substance P selectively activates TNF-alpha gene expression in murine mast cells. J Immunol 1993, 150:4478-4485
66. Hoffmann R, Eicheler W, Huth A, Wenzel E, Happle R: Cytokines and growth factors influence hair growth in vitro. Possible implications for the pathogenesis and treatment of alopecia areata. Arch Dermatol Res 1996, 288:153-156
67. Blasing H, Hendrix S, Paus R: Pro-inflammatory cytokines upregulate the skin immunoreactivity for NGF. NT-3, NT-4 and their receptor, p75NTR in vivo: a preliminary report. Arch Dermatol Res 2005, 296:580-584
68. Tong X, Coulombe PA: Keratin 17 modulates hair follicle cycling in a TNFalpha-dependent fashion. Genes Dev 2006, 20:1353-1364
69. Scholzen TE, Luger TA: Neutral endopeptidase and angiotensin-converting enzyme - key enzymes terminating the action of neuroendocrine mediators. Exp Dermatol 2004, 4:22-26
70. Gurish MF, Boyce JA: Mast cell growth, differentiation, and death. Clin Rev Allergy Immunol 2002, 22:107-118
71. Norozian F, Kashyap M, Ramirez CD, Patel N, Kepley CL, Barnstein BO, Ryan JJ: TGFbeta1 induces mast cell apoptosis. Exp Hematol 2006, 34:579-587
72. Peters EM, Maurer M, Botchkarev VA, Jensen K, Welker P, Scott GA, Paus R: Kit is expressed by epithelial cells in vivo. J Invest Dermatol 2003, 121:976-984
73. Foitzik K, Lindner G, Mueller-Roever S, Maurer M, Botchkareva N, Botchkarev V, Handjiski B, Metz M, Hibino T, Soma T, Dotto GP, Paus R: Control of murine hair follicle regression (catagen) by TGF-beta1 in vivo. FASEB J 2000, 14:752-760
74. Maurer M, Galli SJ: Lack of significant skin inflammation during elimination by apoptosis of large numbers of mouse cutaneous mast cells after cessation of treatment with stem cell factor. Lab Invest 2004, 84:1593-1602
75. Mann-Chandler MN, Kashyap M, Wright HV, Norozian F, Barnstein BO, Gingras S, Parganas E, Ryan JJ: IFN-gamma induces apoptosis in developing mast cells. J Immunol 2005, 175:3000-3005
76. Paus R, Heinzelmann T, Schultz KD, Furkert J, Fechner K, Czarnetzki BM: Hair growth induction by substance P. Lab Invest 1994, 71:134-140
77. Botchkarev VA, Botchkareva NV, Albers KM, Chen LH, Welker P, Paus R: A role for p75 neurotrophin receptor in the control of apoptosis-driven hair follicle regression. FASEB J 2000, 14:1931-1942
78. Peters EM, Hendrix S, Golz G, Klapp BF, Arck PC, Paus R: Nerve growth factor and its precursor differentially regulate hair cycle progression in mice. J Histochem Cytochem 2005, 11:11
79. Tal M, Liberman R: Local injection of nerve growth factor (NGF) triggers degranulation of mast cells in rat paw. Neurosci Lett 1997, 221:129-132
80. Welker P, Grabbe J, Grutzkau A, Henz BM: Effects of nerve growth factor (NGF) and other fibroblast-derived growth factors on immature human mast cells (HMC-1). Immunology 1998, 94:310-317
81. Stempelj M, Ferjan I: Signaling pathway in nerve growth factor induced histamine release from rat mast cells. Inflamm Res 2005, 54:344-349
82. Tometten M, Klapp BF, Joachim R, Fest S, Zenclussen AC, Peters EM, Hertwig K, Arck PC: Nerve growth factor and its functional receptor TrkA are up-regulated in murine decidual tissue of stress-triggered and substance P-mediated abortion. Am J Reprod Immunol 2004, 51:86-93
83. Arck PC, Slominski A, Theoharides TC, Peters EM, Paus R: Neuroimmunology of stress: skin takes center stage. J Invest Dermatol 2006, 126:1697-1704
84. Paus R, Nickoloff BJ, Ito T: A 'hairy' privilege. Trends Immunol 2005, 26:32-40
85. Rückert R, Lindner G, Bulfone-Paus S, Paus R: High-dose proinflammatory cytokines induce apoptosis of hair bulb keratinocytes in vivo. Br J Dermatol 2000, 143:1036-1039
86. Sternberg EM: Neuroendocrine regulation of autoimmune/inflammatory disease. J Endocrinol 2001, 169:429-435
87. Elenkov IJ, Chrousos GP: Stress hormones, proinflammatory and antiinflammatory cytokines, and autoimmunity. Ann NY Acad Sci 2002, 966:290-303
88. Frieri M: Neuroimmunology and inflammation: implications for therapy of allergic and autoimmune diseases. Ann Allergy Asthma Immunol 2003, 90:34-40
89. Paus R, Theoharides TC, Arck PC: Neuroimmunoendocrine circuitry of the 'brain-skin connection'. Trends Immunol 2006, 27:32-39
90. Burbach GJ, Kim KH, Zivony AS, Kim A, Aranda J, Wright S, Naik SM, Caughman SW, Ansel JC, Armstrong CA: The neurosensory tachykinins substance P and neurokinin A directly induce keratinocyte nerve growth factor. J Invest Dermatol 2001, 117:1075-1082
91. Dallos A, Kiss M, Polyanka H, Dobozy A, Kemeny L, Husz S: Effects of the neuropeptides substance P, calcitonin gene-related peptide, vasoactive intestinal polypeptide and galanin on the production of nerve growth factor and inflammatory cytokines in cultured human keratinocytes. Neuropeptides 2006, 40:251-263
92. Zhou Z, Kawana S, Aoki E, Katayama M, Nagano M, Suzuki H: Dynamic changes in nerve growth factor and substance P in the murine hair cycle induced by depilation. J Dermatol 2006, 33: 833-841