Distinct roles for nerve growth factor and brain-derived neurotrophic factor in controlling the rate of hair follicle morphogenesis

Journal of Investigative Dermatology

Volumn 114, Issue 2, 2000, Pages 314-320

  Botchkareva, Natalia V ^a,d   Botchkarev, Vladimir A ^a,d   Albers, Kathryn M ^b   Metz, Martin ^a   Paus, Ralf ^a,c  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEUROTROPHIN; TYROSINE KINASE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HAIR FOLLICLE; HAIR GROWTH; MORPHOGENESIS; MOUSE; NEUTROPENIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; SKIN BIOPSY; SKIN CULTURE;

EID: 0034097933     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1523-1747.2000.00864.x     Document Type: Article

References (54)

1. Albers KM, Wright DE, Davis BM: Overexpression of nerve growth factor in epidermis of transgenic mice causes hypertrophy of the peripheral nervous system. J Neurosci 14:1422-1432, 1994
2. Alpers CE, Hudkins KL, Ferguson M, Johnson RJ, Schatteman GC, Bothwell M: Nerve growth factor receptor expression in fetal, mature, and diseased human kidneys. Lab Invest 69:703-713, 1993
3. Barbacid M: The Trk family of neurotrophin receptors. J Neurobiol 25:1386-1403, 1994
4. Botchkarev V, Botchkareva N, Albers K, van der Veen C, Lewin G, Paus R: Neurotrophin-3 involvement in the regulation of hair follicle morphogenesis. J Invest Dermatol 111:279-285, 1998a
5. 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
6. Botchkarev VA, Botchkareva NV, Welker P, et al: A new role for neurotrophins: involvement of brain-derived neurocrophic factor and neurocrophin-4 in hair cycle control. FASEB J 13:395-410, 1999a
7. 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 79:557-572, 1999b
8. Botchkarev VA, Botchkareva NV, Roth W, et al: Noggin is a mesenchymally-derived stimulator of hair follicle induction. Nature Cell Biol 1:158-164, 1999c
9. Botchkareva NV, Botchkarev VA, Metz M, Silos-Santiago I, Paus R: Deletion of TrkC, high affinity neurotrophin-3 receptor, leads to the retardation of hair follicle development. J Invest Dermatol 113:425-427, 1999a
10. Botchkareva NV, Botchkarev VA, Chen L-H, Lindner G, Paus R: A role for p75 neurotrophin receptor in the control of hair follicle morphogenesis. Dev Biol 216: 135-153, 1999b
11. Bothwell M: Functional interactions of neurotrophins and neurotrophin receptors. Annu Rev Neurosci 18:223-253, 1995
12. Braun A, Appel E, Baruch R, et al: Role of nerve growth factor in a mouse model of allergic airway inflammation and asthma. Eur J Immunol 28:3240-3251, 1998
13. Bronzetti E, Ciraco E, Germana G, Vega JA: Immunocytochemical localization of neurotrophin receptor proteins in human skin. Ital J Anat Embryol 100 (Suppl.1):565-571, 1996
14. Chao MV: Neurotrophin receptors: a window into neuronal differentiation. Neuron 9:583-593, 1992
15. Chao MV: The p75 neurotrophin receptor. J Neurobiol 25:1373-1385, 1994
16. Chao M, Casaccia-Bonnefil P, Carter B, Chittka A, Kong H, Yoon SO: Neurotrophin receptors: mediators of life and death. Brain Res Rev 26:295-301, 1998
17. Crowley C, Spencer SD, Nishimura MC, et al: Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76:1001-1011, 1994
18. Di Marco E, Marchisio PC, Bondanza S, Franzi AT, De Cancedda R, Luca M: Growth-regulated synthesis and secretion of biologically active nerve growth factor by human keratinocytes. J Biol Chem 266:21718-21722, 1991
19. Di Marco E, Mathor M, Bondanza S, Cutuli N, Marchisio PC, De Cancedda R, Luca M: Nerve growth factor binds to normal human keratinocytes through high and low affinity receptors and stimulates their growth by a novel autocrine loop. J Biol Chem 268:22838-22846, 1993
20. English KB, Harper S, Stayner N, Wang ZM, Davies AM: Localization of nerve growth factor (NGF) and low-affinity NGF receptors in touch domes and quantification of NGF mRNA in keratinocytes of adult rats. J Comp Neurol 344:470-480, 1994
21. Emfors P, Merlio J-P, Persson H: Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development. Eur J Neurosci 4:1140-1158, 1992
22. Hardy MH: The secret life of the hair follicle. Trends Genet 8:55-61, 1992
23. Kaplan DR, Miller FD: Signal transduction by the neurotrophin receptors. Curr Opin Cell Biol 9:213-221, 1997
24. Kaufman MH: The Atlas of Mouse Development. London: Academic Press, 1992
25. LeMaster AM, Krimm RF, Davis BM, Noel T, Forbes ME, Johnson JE, Albers KM: Overexpression of brain-derived neurotrophic factor enhances sensory innervation and selectively increases neuron number. J Neurosci 19:5919-5931, 1999
26. Lewin GR, Barde YA: Physiology of the neurotrophins. Annu Rev Neurosci 19:289-317, 1996
27. Li L, Paus R, Slominski A, Hoffman R: Skin histoculture assay for studying the hair cycle. In Vitro Cell Dev Biol 28:695-698, 1992
28. Liang Y, Marcusson J, Johansson O: Light and electron microscopic immunohistochemical observations of p75 nerve growth factor receptor-immunoreactive dermal nerves in prurigo nodularis. Arch Dermatol Res 291:14-21, 1999
29. Lindner G, Botchkarev VA, Botchkareva NV, Ling G, Paus R: Analysis of apoptosis during hair follicle regression (catagen). Am J Pathol 151:1601-1617, 1997
30. Luukko K, Moshnyakov M, Sainio K, Saarma M, Sariola H, Thesleff I: Expression of neurotrophin receptors during rat tooth development is developmentally regulated, independent of innervation, and suggests functions in the regulation of morphogenesis and innervation. Dev Dynam 206:87-99, 1996
31. Meakin SO, Shooter EM: The nerve growth factor family of receptors. Trends Neurosci 15:323-331, 1992
32. Mearow KM, Kril Y, Diamond J: Increased NGF mRNA expression in denervated rat skin. Neuroreport 4:351-354, 1993
33. Müller-Röver S, Paus R. Topobiology of hair follicle: adhesion molecules as morphoregulatory signals during hair follicle morphogenesis. In: Chuong C (ed.). Molecular Biology of Epithelial Appendages Morphogenesis. Austin, TX: Landes Bioscience, 1998, pp 283-314
34. Oro AE, Scott MP: Splitting hairs: dissecting roles of signaling systems in epidermal development. cell 96:575-578, 1998
35. Paus R, Cotsarelis G: The biology of hair follicles. N Engl J Med 341:491-497, 1999
36. Paus R, Lüftl M, Czametzki BM: Nerve growth factor modulates keratinocyte proliferation in murine skin organ culture. Br J Dermatol 130:174-180, 1994a
37. Paus R, Handjiski B, Czarnetzki BM, Eichmüller S: A murine model for inducing and manipulating hair follicle regression (catagen): effects of dexamethasone and cyclosporin A. J Invest Dermatol 103:143-147, 1994b
38. Paus R, Peters EMJ, Eichmüller S, Botchkarev VA: Neural mechanisms of hair growth control. J Invest Dermatol Symp Proc 2:61-68, 1997
39. Paus R, Müller-Röver S, van der Veen C, et al. A comprehensive guide for the recognition and classification of distinct types of hair follicle morphogenesis. J Invest Dermatol 113:523-532, 1999
40. Philpott M, Paus R. Principles of hair follicle morphogenesis. In: Chuong C (ed.). Molecular Biology of Epithelial Appendages Morphogenesis. Austin,TX: Landes Bioscience, 1998, pp 75-110
41. Pincelli C, Yaar M: Nerve growth factor: its significance in cutaneous biology. J Invest Dermatol Symp Proc The 2:31-36, 1997
42. Pincelli C, Sevignani C, Manfredini R, et al: Expression and function of nerve growth factor and nerve growth factor receptor on cultured keratinocytes. J Invest Dermatol 103:13-18, 1994
43. Pincelli C, Haake AR, Benassi L, et al: Autocrine nerve growth factor protects human keratinocytes from apoptosis through its high affinity receptor (Trk): a role for Bcl-2. J Invest Dermatol 109:757-764, 1997
44. Polakowska RR, Piacentini M, Bartlett R, Goldsmith LA, Haake AR: Apoptosis in human skin development: morphogenesis, periderm, and stem cells. Dev Dyn 199:176-188, 1994
45. Rice FL, Albers KM, Davis BM, et al: Differential dependency of unmyelinated and Aδ epidermal and upper dermal innervation on neurotrophins, trk receptors and p75 LNGFR. Dev Biol 198:57-81, 1998
46. Sariola H, Saarma M, Sainio K, et al. Dependence of kidney morphogenesis on the expression of nerve growth factor receptor. Science 254:571-573, 1991
47. Shibayama E, Koizumi H: Cellular localization of the Trk neurotrophin receptor family in human non-neuronal tissues. Am J Pathol 148:1807-1818, 1996
48. Srivastava D, Olson EN: Neurotrophin 3 knocks heart off Trk. Nature Med 2:1069-1071, 1996
49. 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
50. Vassar R, Fuchs E: Transgenic mice provide new insights into the role of TGF-α during epidermal development and differentiation. Genes Dev 5:714-727, 1991
51. Vielkind U, Sebzda MK, Gibson IR, Hardy MH: Dynamics of Merkel cell patterns in developing hair follicles in the dorsal skin of mice, demonstrated by a monoclonal antibody to mouse keratin 8. Acta Anat 152:95-109, 1995
52. Wheeler E, Bothwell M: Spatiotemporal patterns of expression of NGF and the low-affinity NGF receptor in rat embryos suggest functional role in tissue morphogenesis and myogenesis. J Neurosci 12:930-945, 1992
53. Wheeler EF, Gong H, Grimes R, Benoit D, Vazquez L: p75ntr and Trk receptors are expressed in reciprocal patterns in a wide variety of non-neural tissues during rat embryonic development, indicating independent receptor functions. J Comp Neurol 391:407-428, 1998
54. Yaar M: Neurotrophins in skin. In: Sieber-Blum M (ed.). Neurotrophins and the Neural Crest. Boca Raton: CRC Press, 1999, pp 117-140