Control of human hair growth by neurotrophins: Brain-derived neurotrophic factor inhibits hair shaft elongation, induces catagen, and stimulates follicular transforming growth factor β2 expression

Journal of Investigative Dermatology

Volumn 124, Issue 4, 2005, Pages 675-685

  Peters, Eva M J ^a   Hansen, Marit G ^b   Overall, Rupert W ^a,b   Nakamura, Motonobu ^b,c   Pertile, Paolo ^d   Klapp, Burghard F ^a   Arck, Petra C ^a   Paus, Ralf ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c KYOTO UNIVERSITY   (Japan)

^d Cutech Srl   (Italy)

Author keywords

Brain derived neurotrophic factor; Hair cycle; Human; Neurotrophin; Tumor growth factor 2; Tyrosinekinase B

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; NEUROTROPHIN; NEUTRALIZING ANTIBODY; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; BINDING AFFINITY; CELL CULTURE; CELL PROLIFERATION; CONTROLLED STUDY; DERMIS; DRUG TARGETING; EPITHELIUM; FIBROBLAST; HAIR; HAIR FOLLICLE; HAIR GROWTH; HUMAN; HUMAN TISSUE; KERATINOCYTE; MESENCHYME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCALP; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 16844380619     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0022-202X.2005.23648.x     Document Type: Article

References (69)

1. Alleva E, Santucci D: Psychosocial versus "physical" stress situations in rodents and humans: Role of neurotrophins. Physiol Behav 73:313-320, 2001
2. Amendt C, Mann A, Schirmacher P, Blessing M: Resistance of keratinocytes to TGFbeta-mediated growth restriction and apoptosis induction accelerates re-epithelialization in skin wounds. J Cell Sci 115:2189-2198, 2002
3. Asaumi K, Nakanishi T, Asahara H, Inoue H, Takigawa M: Expression of neurotrophins and their receptors (TRK) during fracture healing. Bone 26:625-633, 2000
4. Barde YA, Edgar D, Thoenen H: Purification of a new neurotrophic factor from mammalian brain. EMBO J 1:549-553, 1982
5. Barker PA: p75NTR: A study in contrasts. Cell Death Differ 5:346-356, 1998
6. Barouch R, Appel E, Kazimirsky G, Braun A, Renz H, Brodie C: Differential regulation of neurotrophin expression by mitogens and neurotransmitters in mouse lymphocytes. J Neuroimmunol 103:112-121, 2000
7. Bayas A, Kruse N, Moriabadi NF, et al: Modulation of cytokine mRNA expression by brain-derived neurotrophic factor and nerve growth factor in human immune cells. Neurosci Lett 335:155-158, 2003
8. Bergman E, Ulfhake B, Fundin BT: Regulation of NGF-family ligands and receptors in adulthood and senescence: Correlation to degenerative and regenerative changes in cutaneous innervation. Eur J Neurosci 12:2694-2706, 2000
9. Botchkareva NV, Botchkarev VA, Albers KM, Metz M, Paus R: Distinct roles for nerve growth factor and brain-derived neurotrophic factor in controlling the rate of hair follicle morphogenesis. J Invest Dermatol 114:314-320, 2000
10. Botchkareva NV, Botchkarev VA, Metz M, Silos-Santiago I, Paus R: Retardation of hair follicle development by the deletion of TrkC, high-affinity neurotrophin-3 receptor. J Invest Dermatol 113:425-427, 1999
11. Botchkarev V, Botchkareva N, Welker R et al: A new role for neurotrophins: Involvement of brain-derived neurotrophic factor and neurotrophin-4 in hair cycle control. FASEB J 13:395-410, 1999a
12. Botchkarev VA, Botchkareva NV, Albers KM, Chen LH, Welker P1 Paus R: A role for p75 neurotrophin receptor in the control of apoptosis-driven hair follicle regression. FASEB J 14:1931-1942, 2000
13. Botchkarev VA, Botchkarev NV, Albers KM, van der Veen C, Lewin GR, Paus R: Neurotrophin-3 involvement in the regulation of hair follicle morphogenesis. J Invest Dermatol 111:279-285, 1998a
14. Botchkarev VA, Botchkareva NV, Lommatzsch M, et al: BDNF overexpression induces differential increases among subsets of sympathetic innervation in murine back skin. Eur J Neurosci 10:3276-3283, 1998b
15. Botchkarev VA, Eichmüller S, Johansson O, Paus R: Hair cycle-dependent plasticity of skin and hair follicle innervation in normal murine skin. J Comp Neurol 386:379-395, 1997
16. Botchkarev VA, Metz M, Botchkareva NV, et al: Brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4 act as "eliotrophins" in murine skin. Lab Invest 79:557-572, 1999b
17. Botchkarev VA, Peters EM, Botchkareva NV, Maurer M, Paus R: Hair cycle-dependent changes in adrenergic skin innervation, and hair growth modulation by adrenergic drugs. J Invest Dermatol 113:878-887, 1999c
18. Botchkarev VA, Welker P, Albers KM, et al: A new role for neurotrophin-3: Involvement in the regulation of hair follicle regression (catagen). Am J Pathol 153:785-799, 1998c
19. Cheifetz S, Hernandez H, Laiho M, ten Dijke P, Iwata KK, Massague J: Distinct transforming growth factor-beta (TGF-beta) receptor subsets as determinants of cellular responsiveness to three TGF-beta isoforms. J Biol Chem 265:20533-20538, 1990
20. dos Santos AA, Medina SV, Sholl-Franco A, de Araujo EG: PMA decreases the proliferation of retinal cells in vitro: The involvement of acetylcholine and BDNF. Neurochem Int 42:73-80, 2003
21. Ernfors P: Local and target-derived actions of neurotrophins during peripheral nervous system development. Cell Mol Life Sci 58:1036-1044, 2001
22. Farinas I, Cano-Jaimez M, Bellmunt E, Soriano M: Regulation of neurogenesis by neurotrophins in developing spinal sensory ganglia. Brain Res Bull 57:809-816, 2002
23. Foitzik K, Lindner G, Müller-Röver S, et al: Control of murine hair follicle regression (catagen) by TGF-beta1 in vivo. FASEB J 14:752-760, 2000
24. Foitzik K, Paus R, Doetschman T, Dotto GP: The TGF-beta2 isoform is both a required and sufficient inducer of murine hair follicle morphogenesis. Dev Biol 212:278-289, 1999
25. Hannestad J, Germana A, Catania S, Laura R, Ciriaco E, Vega JA: Neurotrophins and their receptors in the pigeon caecal tonsil. An immunohistochemical study. Vet Immunol Immunopathol 61:359-367, 1998
26. Hashimoto K: Regulation of keratinocyte function by growth factors. J Dermatol Sci 24:46-350, 2000
27. Hibino T, Nishiyama T: Role of TGF-beta2 in the human hair cycle. J Dermatol Sci 35:9-18, 2004
28. Inui S, Fukuzato Y, Nakajima T, Yoshikawa K, Itami S: Androgen-inducible TGF-beta1 from balding dermal papilla cells inhibits epithelial cell growth: A clue to understand paradoxical effects of androgen on human hair growth. FASEB J 16:1967-1969, 2002
29. Jordan-Sciutto KL, Murray Fenner BA, Wiley CA, Achim CL: Response of cell cycle proteins to neurotrophic factor and chemokine stimulation in human neuroglia. Exp Neurol 167:205-214, 2001
30. Kligman AM: The human hair cycle. J Invest Dermatol 33:307-316, 1959
31. Lambiase A, Manni L, Bonini S, Rama P, Micera A, Aloe L: Nerve growth factor promotes corneal healing: Structural, biochemical, and molecular analyses of rat and human corneas. Invest Ophthalmol Vis Sci 41:1063-1069, 2000
32. Lindner G, Botchkarev VA, Botchkareva NV, Ling G, van der Veen C, Paus R: Analysis of apoptosis during hair follicle regression (catagen). Am J Pathol 151:1601-1617, 1997
33. Lommatzsch M, Braun A, Mannsfeldt A, et al: Abundant production of brain-derived neurotrophic factor by adult visceral epithelia. Implications for paracrine and target-derived neurotrophic functions. Am J Pathol 155:1183-1193, 1999
34. Lopez-Sanchez N, Frade JM: Control of the cell cycle by neurotrophins: Lessons from the p75 neurotrophin receptor. Histol Histopathol 17:1227-1237, 2002
35. Lyall F, Simpson H, Bulmer JN, Barber A, Robson SC: Transforming growth factor-beta expression in human placenta and placental bed in third trimester normal pregnancy, preeclampsia, and fetal growth restriction. Am J Pathol 159:1827-1838, 2001
36. Marshall L, Born J: Brain-immune interactions in sleep. Int Rev Neurobiol 52:93-131, 2002
37. Maurer M, Handjiski B, Paus R: Hair growth modulation by topical immunophilin ligands: Induction of anagen, inhibition of massive catagen development, and relative protection from chemotherapy-induced alopecia. Am J Pathol 150:1433-1441, 1997
38. Mecklenburg L, Tobin DJ, Müller-Röver S, et al: Active hair growth (anagen) is associated with angiogenesis. J Invest Dermatol 114:909-916, 2000
39. Metsis M: Genes for neurotrophic factors and their receptors: Structure and regulation. Cell Mol Life Sci 58:1014-1020, 2001
40. Miknyoczki SJ, Lang D, Huang L, Klein-Szanto AJ, Dionne CA, Ruggeri BA: Neurotrophins and Trk receptors in human pancreatic ductal adenocarcinoma: Expression patterns and effects on in vitro invasive behavior. Int J Cancer 81:417-427, 1999
41. Min BM, Woo KM, Lee G, Park NH: Terminal differentiation of normal human oral keratinocytes is associated with enhanced cellular TGF-beta and phospholipase C-gamma 1 levels and apoptotic cell death. Exp Cell Res 249:377-385, 1999
42. Moalem G, Gdalyahu A, Shani Y, et al: Production of neurotrophins by activated T cells: Implications for neuroprotective autoimmunity. J Autoimmun 15:331-345, 2000
43. Müller-Röver S, Handjiski B, van der Veen C, et al: A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 117:3-15, 2001
44. Panteleyev AA, Jahoda CA, Christiano AM: Hair follicle predetermination. J Cell Sci 114:3419-3431, 2001
45. Paus R, Christoph T, Müller-Röver S: Immunology of the hair follicle: A short journey into terra incognita. J Investig Dermatol Symp Proc 4:226-234, 1999a
46. Paus R, Cotsarelis G: The biology of hair follicles. N Eng J Med 341:491-497, 1999
47. Paus R, Handjiski B, Eichmüller S, Czarnetzki BM: Chemotherapy-induced alopecia in mice. Induction by cyclophosphamide, inhibition by cyclosporine A, and modulation by dexamethasone. Am J Pathol 144:719-734, 1994a
48. Paus R, Luftl M, Czarnetzki BM: Nerve growth factor modulates keratinocyte proliferation in murine skin organ culture. Br J Dermatol 130:174-180, 1994b
49. Paus R, Müller-Röver S, Botchkarev VA: Chronobiology ol the hair follicle: Hunting the "hair cycle clock". J Invest Dermatol Symp Proc 4:338-345, 1999b
50. 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 116:236-245, 2001
51. Peters EM, Maurer M, Botchkarev VA, Gordon DS, Paus R: Hair growth-modulation by adrenergic drugs. Exp Dermatol 8:274-281, 1999
52. Peters EMJ, Botchkarev VA, Paus R: Neurotrophins act as regulators of hair follicle morphogenesis and cycling. In: Van ND (eds). Hair Science and Technology. Tournai, Belgium: Skinterface, 2003
53. Philpott M: In vitro maintenance of isolated hair follicles: Current status and future development. Exp Dermatol 8:317-319, 1999
54. 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 7:55-372, 1994
55. Pincelli C, Yaar M: Nerve growth factor: Its significance in cutaneous biology. J Investig Dermatol Symp Proc 2:31-36, 1997
56. Renz H: The role of neurotrophins in bronchial asthma. Eur J Pharmacol 429:231-237, 2001
57. Roberts AB, Anzano MA, Wakefield LM, Roche NS, Stern DF, Sporn MB: Type beta transforming growth factor: A bifunctional regulator of cellular growth. Proc Natl Acad Sci USA 82:119-123, 1985
58. Roux PP, Barker PA: Neurotrophin signaling through the p75 neurotrophin receptor. Prog Neurobiol 67:203-233, 2002
59. Shibayama E, Koizumi H: Cellular localization of the Trk neurotrophin receptor family in human non-neuronal tissues. Am J Pathol 148:1807-1818, 1996
60. Sieber-Blum M: Growth factor synergism and antagonism in early neural crest development. Biochem Cell Biol 76:1039-1050, 1998
61. Soma T, Ogo M, Suzuki J, Takahashi T, Hibino T: Analysis of apoptotic cell death in human hair follicles in vivo and in vitro. J Invest Dermatol 111:948-954, 1998
62. Soma T, Tsuji Y, Hibino T: Involvement of transforming growth factor-beta2 in catagen induction during the human hair cycle. J Invest Dermatol 118:993-997, 2002
63. Stenn KS, Paus R: Controls of hair follicle cycling. Physiol Rev 81:449-494, 2001
64. Tobin DJ, Hagen E, Botchkarev VA, Paus R: Do hair bulb melanocytes undergo apoptosis during hair follicle regression (catagen)? J Invest Dermatol 111:941-947, 1998
65. Tron VA, Coughlin MD, Jang DE, Stanisz J, Sauder DN: Expression and modulation of nerve growth factor in murine keratinocytes (PAM 212). J Clin Invest 85:1085-1089, 1990
66. Tsuji Y, Denda S, Soma T, Raftery L, Momoi T, Hibino T: A potential suppressor of TGF-beta delays catagen progression in hair follicles. J Investig Dermatol Symp Proc 8:65-68, 2003
67. Wellmer A, Misra VP, Sharief MK, Kopelman PG, Anand P: A double-blind placebo-controlled clinical trial of recombinant human brain-derived neurotrophic factor (rhBDNF) in diabetic polyneuropathy. J Peripher Nerv System 6:204-210, 2001
68. Yaar M, Eller MS, DiBenedetto P, et al: The trk family of receptors mediates nerve growth factor and neurotrophin-3 effects in melanocytes. J Clin Invest 94:1550-1562, 1994
69. You L, Kruse FE, Volcker HE: Neurotrophic factors in the human cornea. Invest Ophthalmol Vis Sci 41:692-702, 2000