|
|
||||||||
Physiological Reviews, Vol. 81, No. 1, January 2001, pp. 449-494
Copyright ©2001 by the American Physiological Society
Beauty Genome Sciences Inc., Skillman, New Jersey; and Department of Dermatology, University Hospital Eppendorf, University of Hamburg, Hamburg, Germany
Stenn, K. S. and
R. Paus.
Controls of Hair Follicle Cycling. Physiol. Rev. 81: 449-494, 2001.
Nearly 50 years
ago, Chase published a review of hair cycling in which he detailed hair
growth in the mouse and integrated hair biology with the biology of his
day. In this review we have used Chase as our model and tried to put
the adult hair follicle growth cycle in perspective. We have tried to
sketch the adult hair follicle cycle, as we know it today and what
needs to be known. Above all, we hope that this work will serve as an
introduction to basic biologists who are looking for a defined
biological system that illustrates many of the challenges of modern
biology: cell differentiation, epithelial-mesenchymal interactions,
stem cell biology, pattern formation, apoptosis, cell and organ growth
cycles, and pigmentation. The most important theme in studying the
cycling hair follicle is that the follicle is a regenerating system. By traversing the phases of the cycle (growth, regression, resting, shedding, then growth again), the follicle demonstrates the unusual ability to completely regenerate itself. The basis for this
regeneration rests in the unique follicular epithelial and mesenchymal
components and their interactions. Recently, some of the molecular
signals making up these interactions have been defined. They involve
gene families also found in other regenerating systems such as
fibroblast growth factor, transforming growth factor-
, Wnt pathway,
Sonic hedgehog, neurotrophins, and homeobox. For the immediate future, our challenge is to define the molecular basis for hair follicle growth
control, to regenerate a mature hair follicle in vitro from defined
populations, and to offer real solutions to our patients' problems.
This article has been cited by other articles:
![]() |
E. Fuchs and J.A. Nowak Building Epithelial Tissues from Skin Stem Cells Cold Spring Harb Symp Quant Biol, November 6, 2008; (2008) sqb.2008.73.032v1. [Abstract] [PDF] |
||||
![]() |
R. A. Joachim, B. Handjiski, S. M. Blois, E. Hagen, R. Paus, and P. C. Arck 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., November 1, 2008; 173(5): 1379 - 1388. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Semenova, H. Koegel, S. Hasse, J. E. Klatte, E. Slonimsky, D. Bilbao, R. Paus, S. Werner, and N. Rosenthal Overexpression of mIGF-1 in Keratinocytes Improves Wound Healing and Accelerates Hair Follicle Formation and Cycling in Mice Am. J. Pathol., November 1, 2008; 173(5): 1295 - 1310. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. J. Paul, N. T. George, I. Zucker, and M. P. Butler Photoperiodic and hormonal influences on fur density and regrowth in two hamster species Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2007; 293(6): R2363 - R2369. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. M.J. Peters, S. Liotiri, E. Bodo, E. Hagen, T. Biro, P. C. Arck, and R. Paus Probing the Effects of Stress Mediators on the Human Hair Follicle: Substance P Holds Central Position Am. J. Pathol., December 1, 2007; 171(6): 1872 - 1886. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Telek, T. Biro, E. Bodo, B. I. Toth, I. Borbiro, G. Kunos, and R. Paus Inhibition of human hair follicle growth by endo- and exocannabinoids FASEB J, November 1, 2007; 21(13): 3534 - 3541. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Bodo, A. Kromminga, W. Funk, M. Laugsch, U. Duske, W. Jelkmann, and R. Paus Human hair follicles are an extrarenal source and a nonhematopoietic target of erythropoietin FASEB J, October 1, 2007; 21(12): 3346 - 3354. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Bodo, D. J. Tobin, Y. Kamenisch, T. Biro, M. Berneburg, W. Funk, and R. Paus Dissecting the Impact of Chemotherapy on the Human Hair Follicle: A Pragmatic in Vitro Assay for Studying the Pathogenesis and Potential Management of Hair Follicle Dystrophy Am. J. Pathol., October 1, 2007; 171(4): 1153 - 1167. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Sainte Marie, A. Toulon, R. Paus, E. Maubec, A. Cherfa, M. Grossin, V. Descamps, M. Clemessy, J.-M. Gasc, M. Peuchmaur, et al. Targeted Skin Overexpression of the Mineralocorticoid Receptor in Mice Causes Epidermal Atrophy, Premature Skin Barrier Formation, Eye Abnormalities, and Alopecia Am. J. Pathol., September 1, 2007; 171(3): 846 - 860. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Lee, J. M. Basak, S. Demehri, and R. Kopan Bi-compartmental communication contributes to the opposite proliferative behavior of Notch1-deficient hair follicle and epidermal keratinocytes Development, August 1, 2007; 134(15): 2795 - 2806. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Wan, A. Saghatelian, L.-W. Chong, C.-L. Zhang, B. F. Cravatt, and R. M. Evans Maternal PPAR{gamma} protects nursing neonates by suppressing the production of inflammatory milk Genes & Dev., August 1, 2007; 21(15): 1895 - 1908. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Osaka, T. Takahashi, S. Murakami, A. Matsuzawa, T. Noguchi, T. Fujiwara, H. Aburatani, K. Moriyama, K. Takeda, and H. Ichijo ASK1-dependent recruitment and activation of macrophages induce hair growth in skin wounds J. Cell Biol., March 26, 2007; 176(7): 903 - 909. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Sugawara, D. Tsuruta, H. Kobayashi, K. Ikeda, S. B. Hopkinson, J. C.R. Jones, and M. Ishii Spatial and Temporal Control of Laminin-332 (5) and -511 (10) Expression During Induction of Anagen Hair Growth J. Histochem. Cytochem., January 1, 2007; 55(1): 43 - 55. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Y. Fessing, T. Y. Sharova, A. A. Sharov, R. Atoyan, and V. A. Botchkarev Involvement of the Edar Signaling in the Control of Hair Follicle Involution (Catagen) Am. J. Pathol., December 1, 2006; 169(6): 2075 - 2084. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. A. Sharov, T. Y. Sharova, A. N. Mardaryev, A. T. di Vignano, R. Atoyan, L. Weiner, S. Yang, J. L. Brissette, G. P. Dotto, and V. A. Botchkarev Bone morphogenetic protein signaling regulates the size of hair follicles and modulates the expression of cell cycle-associated genes PNAS, November 28, 2006; 103(48): 18166 - 18171. [Abstract] [Full Text] [PDF] |
||||
![]() |
A J Craven, A J Nixon, M G Ashby, C J Ormandy, K Blazek, R J Wilkins, and A J Pearson Prolactin delays hair regrowth in mice. J. Endocrinol., November 1, 2006; 191(2): 415 - 425. [Abstract] [Full Text] [PDF] |
||||
![]() |
U. Ohnemus, M. Uenalan, J. Inzunza, J.-A. Gustafsson, and R. Paus The Hair Follicle as an Estrogen Target and Source Endocr. Rev., October 1, 2006; 27(6): 677 - 706. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Okada, Y. Ishii, K. Masujin, A. Yasoshima, J. Matsuda, A. Ogura, H. Nakayama, T. Kunieda, and K. Doi The Critical Roles of Serum/Glucocorticoid-Regulated Kinase 3 (SGK3) in the Hair Follicle Morphogenesis and Homeostasis: The Allelic Difference Provides Novel Insights into Hair Follicle Biology Am. J. Pathol., April 1, 2006; 168(4): 1119 - 1133. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. M.J. Peters, S. Hendrix, G. Golz, B. F. Klapp, P. C. Arck, and R. Paus Nerve Growth Factor and its Precursor Differentially Regulate Hair Cycle Progression in Mice J. Histochem. Cytochem., March 1, 2006; 54(3): 275 - 288. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Foitzik, K. Krause, F. Conrad, M. Nakamura, W. Funk, and R. Paus 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., March 1, 2006; 168(3): 748 - 756. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. M.J. Peters, M. G. Stieglitz, C. Liezman, R. W. Overall, M. Nakamura, E. Hagen, B. F. Klapp, P. Arck, and R. Paus p75 Neurotrophin Receptor-Mediated Signaling Promotes Human Hair Follicle Regression (Catagen) Am. J. Pathol., January 1, 2006; 168(1): 221 - 234. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. M. J. Beaudoin III, J. M. Sisk, P. A. Coulombe, and C. C. Thompson Hairless triggers reactivation of hair growth by promoting Wnt signaling PNAS, October 11, 2005; 102(41): 14653 - 14658. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Yang, C. Mao, Y. Teng, W. Li, J. Zhang, X. Cheng, X. Li, X. Han, Z. Xia, H. Deng, et al. Targeted Disruption of Smad4 in Mouse Epidermis Results in Failure of Hair Follicle Cycling and Formation of Skin Tumors Cancer Res., October 1, 2005; 65(19): 8671 - 8678. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Legue and J.-F. Nicolas Hair follicle renewal: organization of stem cells in the matrix and the role of stereotyped lineages and behaviors Development, September 15, 2005; 132(18): 4143 - 4154. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Bamberger, A. Scharer, M. Antsiferova, B. Tychsen, S. Pankow, M. Muller, T. Rulicke, R. Paus, and S. Werner Activin Controls Skin Morphogenesis and Wound Repair Predominantly via Stromal Cells and in a Concentration-Dependent Manner via Keratinocytes Am. J. Pathol., September 1, 2005; 167(3): 733 - 747. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Alonso, H. Okada, H. A. Pasolli, A. Wakeham, A. I. You-Ten, T. W. Mak, and E. Fuchs Sgk3 links growth factor signaling to maintenance of progenitor cells in the hair follicle J. Cell Biol., August 15, 2005; 170(4): 559 - 570. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Mazzieri, V. Jurukovski, H. Obata, J. Sung, A. Platt, E. Annes, N. Karaman-Jurukovska, P.-E. Gleizes, and D. B. Rifkin Expression of truncated latent TGF-{beta}-binding protein modulates TGF-{beta} signaling J. Cell Sci., May 15, 2005; 118(10): 2177 - 2187. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Bodo, T. Biro, A. Telek, G. Czifra, Z. Griger, B. I. Toth, A. Mescalchin, T. Ito, A. Bettermann, L. Kovacs, et al. A Hot New Twist to Hair Biology: Involvement of Vanilloid Receptor-1 (VR1/TRPV1) Signaling in Human Hair Growth Control Am. J. Pathol., April 1, 2005; 166(4): 985 - 998. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Zcharia, D. Philp, E. Edovitsky, H. Aingorn, S. Metzger, H. K. Kleinman, I. Vlodavsky, and M. Elkin Heparanase Regulates Murine Hair Growth Am. J. Pathol., April 1, 2005; 166(4): 999 - 1008. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. E. Olson, J. Zhang, H. Taylor, D. W. Rose, and M. G. Rosenfeld Barx2 functions through distinct corepressor classes to regulate hair follicle remodeling PNAS, March 8, 2005; 102(10): 3708 - 3713. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Slominski, J. Wortsman, and D. J. Tobin The cutaneous serotoninergic/melatoninergic system: securing a place under the sun FASEB J, February 1, 2005; 19(2): 176 - 194. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. E. Hutchin, M. S.T. Kariapper, M. Grachtchouk, A. Wang, L. Wei, D. Cummings, J. Liu, L. E. Michael, A. Glick, and A. A. Dlugosz Sustained Hedgehog signaling is required for basal cell carcinoma proliferation and survival: conditional skin tumorigenesis recapitulates the hair growth cycle Genes & Dev., January 15, 2005; 19(2): 214 - 223. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. K. Lin, D. Chudova, G. W. Hatfield, P. Smyth, and B. Andersen Identification of hair cycle-associated genes from time-course gene expression profile data by using replicate variance PNAS, November 9, 2004; 101(45): 15955 - 15960. [Abstract] [Full Text] [PDF] |
||||
![]() |
U. Guha, L. Mecklenburg, P. Cowin, L. Kan, W. M. O'Guin, D. D'Vizio, R. G. Pestell, R. Paus, and J. A. Kessler Bone Morphogenetic Protein Signaling Regulates Postnatal Hair Follicle Differentiation and Cycling Am. J. Pathol., September 1, 2004; 165(3): 729 - 740. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. M. Zarach, G. M. J. Beaudoin III, P. A. Coulombe, and C. C. Thompson The co-repressor hairless has a role in epithelial cell differentiation in the skin Development, September 1, 2004; 131(17): 4189 - 4200. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. M. J. Peters, B. Handjiski, A. Kuhlmei, E. Hagen, H. Bielas, A. Braun, B. F. Klapp, R. Paus, and P. C. Arck Neurogenic Inflammation in Stress-Induced Termination of Murine Hair Growth Is Promoted by Nerve Growth Factor Am. J. Pathol., July 1, 2004; 165(1): 259 - 271. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. L. Celso, D. M. Prowse, and F. M. Watt Transient activation of {beta}-catenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours Development, April 15, 2004; 131(8): 1787 - 1799. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. ZCHARIA, S. METZGER, T. CHAJEK-SHAUL, H. AINGORN, M. ELKIN, Y. FRIEDMANN, T. WEINSTEIN, J.-P. LI, U. LINDAHL, and I. VLODAVSKY Transgenic expression of mammalian heparanase uncovers physiological functions of heparan sulfate in tissue morphogenesis, vascularization, and feeding behavior FASEB J, February 1, 2004; 18(2): 252 - 263. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Ito, N. Ito, A. Bettermann, Y. Tokura, M. Takigawa, and R. Paus Collapse and Restoration of MHC Class-I-Dependent Immune Privilege: Exploiting the Human Hair Follicle as a Model Am. J. Pathol., February 1, 2004; 164(2): 623 - 634. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Allen, M. Grachtchouk, H. Sheng, V. Grachtchouk, A. Wang, L. Wei, J. Liu, A. Ramirez, D. Metzger, P. Chambon, et al. Hedgehog Signaling Regulates Sebaceous Gland Development Am. J. Pathol., December 1, 2003; 163(6): 2173 - 2178. [Abstract] [Full Text] |
||||
![]() |
K. TAKEBE, Y. OKA, D. RADISKY, H. TSUDA, K. TOCHIGUI, S. KOSHIDA, K. KOGO, and Y. HIRAI Epimorphin acts to induce hair follicle anagen in C57BL/6 mice FASEB J, November 1, 2003; 17(14): 2037 - 2047. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. M. Braun, C. Niemann, U. B. Jensen, J. P. Sundberg, V. Silva-Vargas, and F. M. Watt Manipulation of stem cell proliferation and lineage commitment: visualisation of label-retaining cells in wholemounts of mouse epidermis Development, November 1, 2003; 130(21): 5241 - 5255. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Wong and P. A. Coulombe Loss of keratin 6 (K6) proteins reveals a function for intermediate filaments during wound repair J. Cell Biol., October 27, 2003; 163(2): 327 - 337. [Abstract] [Full Text] [PDF] |
||||
![]() |
X. Xu, S. Lyle, Y. Liu, B. Solky, and G. Cotsarelis Differential Expression of Cyclin D1 in the Human Hair Follicle Am. J. Pathol., September 1, 2003; 163(3): 969 - 978. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Suzuki, M. Hirata, and S. Kondo From the Cover: Traveling stripes on the skin of a mutant mouse PNAS, August 19, 2003; 100(17): 9680 - 9685. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. K. L. Mak and S. Y. Chan Epidermal Growth Factor as a Biologic Switch in Hair Growth Cycle J. Biol. Chem., July 3, 2003; 278(28): 26120 - 26126. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Gafter-Gvili, B. Sredni, R. Gal, U. Gafter, and Y. Kalechman Cyclosporin A-induced hair growth in mice is associated with inhibition of calcineurin-dependent activation of NFAT in follicular keratinocytes Am J Physiol Cell Physiol, June 1, 2003; 284(6): C1593 - C1603. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Van Mater, F. T. Kolligs, A. A. Dlugosz, and E. R. Fearon Transient activation of beta -catenin signaling in cutaneous keratinocytes is sufficient to trigger the active growth phase of the hair cycle in mice Genes & Dev., May 15, 2003; 17(10): 1219 - 1224. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Foitzik, K. Krause, A. J. Nixon, C. A. Ford, U. Ohnemus, A. J. Pearson, and R. Paus Prolactin and Its Receptor Are Expressed in Murine Hair Follicle Epithelium, Show Hair Cycle-Dependent Expression, and Induce Catagen Am. J. Pathol., May 1, 2003; 162(5): 1611 - 1621. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Ma, J. Liu, T. Wu, M. Plikus, T.-X. Jiang, Q. Bi, Y.-H. Liu, S. Muller-Rover, H. Peters, J. P. Sundberg, et al. `Cyclic alopecia' in Msx2 mutants: defects in hair cycling and hair shaft differentiation Development, March 2, 2003; 130(2): 379 - 389. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. A. Botchkarev Stress and the Hair Follicle: Exploring the Connections Am. J. Pathol., March 1, 2003; 162(3): 709 - 712. [Full Text] [PDF] |
||||
![]() |
P. C. Arck, B. Handjiski, E. M. J. Peters, A. S. Peter, E. Hagen, A. Fischer, B. F. Klapp, and R. Paus 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., March 1, 2003; 162(3): 803 - 814. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. A. Rogers, L. Langbein, H. Winter, C. Ehmann, S. Praetzel, and J. Schweizer Characterization of a First Domain of Human High Glycine-Tyrosine and High Sulfur Keratin-associated Protein (KAP) Genes on Chromosome 21q22.1 J. Biol. Chem., December 6, 2002; 277(50): 48993 - 49002. [Abstract] [Full Text] [PDF] |
||||
![]() |
H. Y. Chang, J.-T. Chi, S. Dudoit, C. Bondre, M. van de Rijn, D. Botstein, and P. O. Brown Diversity, topographic differentiation, and positional memory in human fibroblasts PNAS, October 1, 2002; 99(20): 12877 - 12882. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Benavides, M. F. Starost, M. Flores, I. B. Gimenez-Conti, J.-L. Guenet, and C. J. Conti Impaired Hair Follicle Morphogenesis and Cycling with Abnormal Epidermal Differentiation in nackt Mice, a Cathepsin L-Deficient Mutation Am. J. Pathol., August 1, 2002; 161(2): 693 - 703. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. J. Tobin, K. Foitzik, T. Reinheckel, L. Mecklenburg, V. A. Botchkarev, C. Peters, and R. Paus The Lysosomal Protease Cathepsin L Is an Important Regulator of Keratinocyte and Melanocyte Differentiation During Hair Follicle Morphogenesis and Cycling Am. J. Pathol., May 1, 2002; 160(5): 1807 - 1821. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. A. BOTCHKAREV, N. V. BOTCHKAREVA, M. NAKAMURA, O. HUBER, K. FUNA, R. LAUSTER, R. PAUS, and B. A. GILCHREST Noggin is required for induction of the hair follicle growth phase in postnatal skin FASEB J, October 1, 2001; 15(12): 2205 - 2214. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. A. Botchkarev, E. A. Komarova, F. Siebenhaar, N. V. Botchkareva, A. A. Sharov, P. G. Komarov, M. Maurer, A. V. Gudkov, and B. A. Gilchrest p53 Involvement in the Control of Murine Hair Follicle Regression Am. J. Pathol., June 1, 2001; 158(6): 1913 - 1919. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. A. Panteleyev, C. A. B. Jahoda, and A. M. Christiano Hair follicle predetermination J. Cell Sci., January 10, 2001; 114(19): 3419 - 3431. [Abstract] [Full Text] [PDF] |
||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH |