Resting no more: Re-defining telogen, the maintenance stage of the hair growth cycle

Biological Reviews

Volumn 90, Issue 4, 2015, Pages 1179-1196

  Geyfman, Mikhail ^a   Plikus, Maksim V ^b   Treffeisen, Elsa ^c   Andersen, Bogi ^a   Paus, Ralf ^d,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e INST OF REPRO MED OF THE UNIV   (Germany)

Author keywords

Energy; Gene expression; Hair growth cycle; Hair regeneration; Telogen

Indexed keywords

ANIMAL; GROWTH, DEVELOPMENT AND AGING; HAIR; HAIR FOLLICLE; PHYSIOLOGY;

ANIMALS; HAIR; HAIR FOLLICLE;

EID: 84943400078     PISSN: 14647931     EISSN: 1469185X     Source Type: Journal    
DOI: 10.1111/brv.12151     Document Type: Article

References (206)

1. Adachi, K. (1973). The matabolism and control mechanism of human hair follicles. Current Problems in Dermatology 5, 37-78.
2. Adly, M. A., Assaf, H. A. & Hussein, M. R. A. (2009). Expression pattern of p75 neurotrophin receptor protein in human scalp skin and hair follicles: hair cycle-dependent expression. Journal of the American Academy of Dermatology 60, 99-109.
3. Adly, M. A., Assaf, H. A. & Hussein, M. R. A. (2010). Expression of Ras homologous B protein in the human scalp skin and hair follicles: hair follicle cycle stages-associated changes. Journal of Cutaneous Pathology 37, 751-757.
4. Allain, D. & Rougeot, J. (1980). Induction of autumn moult in mink (Mustela vison Peale and Beauvois) with melatonin. Reproduction Nutrition Development 20, 197-201.
5. Al-Nuaimi, Y., Baier, G., Watson, R. E. B., Chuong, C. M. & Paus, R. (2010). The cycling hair follicle as an ideal systems biology research model. Experimental Dermatology 19, 707-713.
6. Al-Nuaimi, Y., Goodfellow, M., Paus, R. & Baier, G. (2012). A prototypic mathematical model of the human hair cycle. Journal of Theoretical Biology 310, 143-159.
7. Al-Nuaimi, Y., Hardman, J. A., Haslam, I. S., Biro, T., Toth, B. I., Farjo, N., Farjo, B., Philpott, M., Watson, R., Grimaldi, B., Kloepper, J. E. & Paus, R. (2014). A meeting of two chronobiological systems: period1 and BMAL1 modulate the human hair cycle. Journal of Investigative Dermatology 134, 610-619.
8. Alonso, L. & Fuchs, E. (2006). The hair cycle. Journal of Cell Science 119, 391-393.
9. Ansell, D. M., Kloepper, J. E., Thomason, H. A., Paus, R. & Hardman, M. J. (2011). Exploring the "hair growth-wound healing connection": anagen phase promotes wound re-epithelialization. The Journal of Investigative Dermatology 131, 518-528.
10. Aoki, E., Shibasaki, T. & Kawana, S. (2003). Intermittent foot shock stress prolongs the telogen stage in the hair cycle of mice. Experimental Dermatology 12, 371-377.
11. Arck, P. C., Handjiski, B., Hagen, E., Joachim, R., Klapp, B. F. & Paus, R. (2001). 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 Journal 15, 2536-2538.
12. Argyris, T. S. & Argyris, B. F. (1962). Factors affecting stimulation of hair growth during wound healing. Anatomical Record 142, 139-145.
13. Argyris, T. S. & Trimble, M. E. (1964). On mechanism of hair growth stimulation in wound healing. Developmental Biology 9, 230-254.
14. Baker, R. E. & Murray, P. J. (2012). Understanding hair follicle cycling: a systems approach. Current Opinion in Genetics & Development 22, 607-612.
15. Barman, J. M., Pecoraro, V., Astore, I. & Ferrer, J. (1967). First stage in natural history of human scalp hair cycle. Journal of Investigative Dermatology 48, 138-142.
16. Bernard, B. A. (2012). The human hair follicle, a bistable organ? Experimental Dermatology 21, 401-403.
17. Blanco, S., Kurowski, A., Nichols, J., Watt, F. M., Benitah, S. A. & Frye, M. (2011). The RNA-methyltransferase Misu (NSun2) poises epidermal stem cells to differentiate. PLoS Genetics 7, e1002403.
18. Blanpain, C. & Fuchs, E. (2006). Epidermal stem cells of the skin. Annual Review of Cell and Developmental Biology 22, 339-373.
19. Blume-Peytavi, U., Atkin, S., Gieler, U. & Grimalt, R. (2012). Skin academy: hair, skin, hormones and menopause - current status/knowledge on the management of hair disorders in menopausal women. European Journal of Dermatology 22, 310-318.
20. Botchkarev, V. A. & Kishimoto, J. (2003). Molecular control of epithelial-mesenchymal interactions during hair follicle cycling. Journal of Investigative Dermatology Symposium Proceedings 8, 46-55.
21. Breitkopf, T., Leung, G., Yu, M., Wang, E. & McElwee, K. J. (2013). The basic science of hair biology what are the causal mechanisms for the disordered hair follicle? Dermatologic Clinics 31, 1-19.
22. Brownell, I., Guevara, E., Bai, C. B., Loomis, C. A. & Joyner, A. L. (2011). Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 8, 552-565.
23. Bullough, W. S. (1973). Epidermal chalone mechanism. National Cancer Institute Monographs 38, 99-107.
24. Bullough, W. S. & Laurence, E. B. (1968). Epidermal chalone and mitotic control in Vx2 epidermal tumour. Nature 220, 134-135.
25. Bullough, W. S., Laurence, E. B. & Hewett, C. L. (1964). Epidermal chalone - preliminary attempt at isolation. Experimental Cell Research 36, 192-200.
26. Chanda, S., Robinette, C. L., Couse, J. F. & Smart, R. C. (2000). 17beta-estradiol and ICI-182780 regulate the hair follicle cycle in mice through an estrogen receptor-alpha pathway. American Journal of Physiology. Endocrinology and Metabolism 278, 202-210.
27. Chase, H. B. (1954). Growth of the hair. Physiological Reviews 34, 113-126.
28. Chase, H. B. & Eaton, G. J. (1959). The growth of hair follicles in waves. Annals of the New York Academy of Sciences 83, 365-368.
29. Chase, H. B. & Montagna, W. (1951). Relation of hair proliferation to damage induced in the mouse skin. Proceedings of the Society for Experimental Biology and Medicine 76, 35-37.
30. Chase, H. B., Montagna, W. & Malone, J. D. (1953). Changes in the skin in relation to the hair growth cycle. Anatomical Record 116, 75-81.
31. Chen, J., Kelz, M. B., Zeng, G., Steffen, C., Shockett, P. E., Terwilliger, G., Schatz, D. G. & Nestler, E. J. (2002). Inducible, reversible hair loss in transgenic mice. Transgenic Research 11, 241-247.
32. Chuong, C. M., Nickoloff, B. J., Elias, P. M., Goldsmith, L. A., Macher, E., Maderson, P. A., Sundberg, J. P., Tagami, H., Plonka, P. M., Thestrup-Pederson, K., Bernard, B. A., Schroder, J. M., Dotto, P., Chang, C. M., Williams, M. L., Feingold, K. R., King, L. E., Kligman, A. M., Rees, J. L. & Christophers, E. (2002). What is the 'true' function of skin? Experimental Dermatology 11, 159-187.
33. Cotsarelis, G. (2006). Epithelial stem cells: a folliculocentric view. Journal of Investigative Dermatology 126, 1459-1468.
34. Cotsarelis, G., Sun, T. T. & Lavker, R. M. (1990). Label-retaining cells reside in the bulge area of pilosebaceous unit - Implications for follicular stem-cells, hair cycle, and skin carcinogenesis. Cell 61, 1329-1337.
35. Couchman, J. R. (1993). Hair follicle proteoglycans. The Journal of Investigative Dermatology 101, 60-64.
36. Craven, A. J., Ormandy, C. J., Robertson, F. G., Wilkins, R. J., Kelly, P. A., Nixon, A. J. & Pearson, A. J. (2001). Prolactin signaling influences the timing mechanism of the hair follicle: analysis of hair growth cycles in prolactin receptor knockout mice. Endocrinology 142, 2533-2539.
37. Davis, B. K. (1962). Mechanism of hair-growth. Nature 193, 1304-1305.
38. Dawber, R. P. R. (ed.) (1997). Diseases of the Hair and Scalp. Third Edition (Oxford, UK). Blackwell.
39. Donati, G., Proserpio, V., Lichtenberger, B. M., Natsuga, K., Sinclair, R., Fujiwara, H. & Watt, F. M. (2014). Epidermal Wnt/β-catenin signaling regulates adipocyte differentiation via secretion of adipogenic factors. Proceedings of the National Academy of Sciences of the United States of America 111, E1501-1509.
40. Dicks, P., Russel, A. J. & Lincoln, G. A. (1994). The role of prolactin in the reactivation of hair follicles in relation to moulting in cashmere goats. Journal of Endocrinology 143, 441-448.
41. Driskell, R., Jahoda, C. A. B., Chuong, C.-M., Watt, F. & Horsley, V. (2014). Defining dermal adipose tissue. Experimental Dermatology 23, 629-631.
42. Dry, F. W. (1926). The coat of the mouse (Mus. musculus). Journal of Genetics 16, 287-340.
43. Ebling, F. J. (1988). The hair cycle and its regulation. Clinical Dermatology 6, 67-73.
44. Ebling, F. J. & Johnson, E. (1961). Systemic influence on activity of hair follicles in skin homografts. Journal of Embryology and Experimental Morphology 9, 285-293.
45. Enshell-Seijffers, D., Lindon, C., Kashiwagi, M. & Morgan, B. A. (2010). Beta-catenin activity in the dermal papilla regulates morphogenesis and regeneration of hair. Developmental Cell 18, 633-642.
46. Festa, E., Fretz, J., Berry, R., Schmidt, B., Rodeheffer, M., Horowitz, M. & Horsley, V. (2011). Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 146, 761-771.
47. Foitzik, K., Krause, K., Conrad, F., Nakamura, M., Funk, W. & Paus, R. (2006). 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. American Journal of Pathology 168, 748-756.
48. Foitzik, K., Krause, K., Nixon, A. J., Ford, C. A., Ohnemus, U., Pearson, A. J. & Paus, R. (2003). Prolactin and its receptor are expressed in murine hair follicle epithelium, show hair cycle-dependent expression, and induce catagen. American Journal of Pathology 162, 1611-1621.
49. Gandarillas, A., Davies, D. & Blanchard, J. M. (2000). Normal and c-Myc-promoted human keratinocyte differentiation both occur via a novel cell cycle involving cellular growth and endoreplication. Oncogene 19, 3278-3289.
50. Garza, L. A., Liu, Y. P., Yang, Z. X., Alagesan, B., Lawson, J. A., Norberg, S. M., Loy, D. E., Zhao, T. L., Blatt, H. B., Stanton, D. C., Carrasco, L., Ahluwalia, G., Fischer, S. M., FitzGerald, G. A. & Cotsarelis, G. (2012). Prostaglandin D-2 inhibits hair growth and is elevated in bald scalp of men with androgenetic alopecia. Science Translational Medicine 4, 123-134.
51. Geyfman, M. & Andersen, B. (2009). How the skin can tell time. Journal of Investigative Dermatology 129, 1063-1066.
52. Geyfman, M. & Andersen, B. (2010). Clock genes, hair growth and aging. Aging (Albany NY) 2, 122-128.
53. Geyfman, M., Gordon, W., Paus, R. & Andersen, B. (2011). Identification of telogen markers underscores that telogen is far from a quiescent hair cycle stage. Journal of Investigative Dermatology 132, 721-724.
54. Geyfman, M., Kumar, V., Liu, Q., Ruiz, R., Gordon, W., Espitia, F., Cam, E., Millar, S. E., Smyth, P., Ihler, A., Takahashi, J. S. & Andersen, B. (2012). Brain and muscle Arnt-like protein-1 (BMAL1) controls circadian cell proliferation and susceptibility to UVB-induced DNA damage in the epidermis. Proceedings of the National Academy of Sciences of the United States of America 109, 11758-11763.
55. Gibson, W. T., Westgate, G. E. & Craggs, R. I. (1991). Immunology of the hair follicle. Annals of the New York Academy of Sciences 642, 291-300.
56. Gilhar, A., Etzioni, A. & Paus, R. (2012). Alopecia areata. The New England Journal of Medicine 366, 1515-1525.
57. Greco, V., Chen, T., Rendl, M., Schober, M., Pasolli, H. A., Stokes, N., Dela Cruz-Racelis, J. & Fuchs, E. (2009). A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4, 155-169.
58. Guarrera, M., Fiorucci, M. C. & Rebora, A. (2013). Methods of hair loss evaluation: a comparison of TrichoScan (R) with the modified wash test. Experimental Dermatology 22, 482-484.
59. Halloy, J., Bernard, B. A., Loussouarn, G. & Goldbeter, A. (2000). Modeling the dynamics of human hair cycles by a follicular automaton. Proceedings of the National Academy of Sciences of the United States of America 97, 8328-8333.
60. Hardman, J.A., Tobin, D.J., Haslam, I.S., Farjo, N., Farjo, B., Al-Nuaimi, Y., Grimaldi, B. & Paus, R. (2014). The peripheral clock regulates human pigmentation. The Journal of Investigative Dermatology.
61. Hashizume, H., Tokura, Y., Takigawa, M. & Paus, R. (1997). Hair cycle-dependent expression of heat shock proteins in hair follicle epithelium. International Journal of Dermatology 36, 587-592.
62. Hausman, G. J., Campion, D. R., Richardson, R. L. & Martin, R. J. (1981). Adipocyte development in the rat hypodermis. American Journal of Anatomy 161, 85-100.
63. Headington, J. T. (1993). Telogen-effluvium - new concepts and review. Archives of Dermatology 129, 356-363.
64. Hebert, J. M., Rosenquist, T., Gotz, J. & Martin, G. R. (1994). Fgf5 as a regulator of the hair-growth cycle - evidence from targeted and spontaneous mutations. Cell 78, 1017-1025.
65. Hibino, T. & Nishiyama, T. (2004). Role of TGF-beta 2 in the human hair cycle. Journal of Dermatological Science 35, 9-18.
66. Higgins, C. A., Richardson, G. D., Westgate, G. E. & Jahoda, C. A. (2009a). Exogen involves gradual release of the hair club fibre in the vibrissa follicle model. Experimental Dermatology 18, 793-795.
67. Higgins, C. A., Westgate, G. E. & Jahoda, C. A. (2009b). From telogen to exogen: mechanisms underlying formation and subsequent loss of the hair club fiber. Journal of Investigative Dermatology 129, 2100-2108.
68. Hoffmann, R., Happle, R. & Paus, R. (1998). Elements of the interleukin-1 signaling system show hair cycle-dependent gene expression in murine skin. European Journal of Dermatology 8, 475-477.
69. Hofmann, U., Tokura, Y., Nishijima, T., Takigawa, M. & Paus, R. (1996). Hair cycle-dependent changes in skin immune functions: anagen-associated depression of sensitization for contact hypersensitivity in mice. Journal of Investigative Dermatology 106, 598-604.
70. Hofmann, U., Tokura, Y., Ruckert, R. & Paus, R. (1998). The anagen hair cycle induces systemic immunosuppression of contact hypersensitivity in mice. Cellular Immunology 184, 65-73.
71. Horsley, V., Aliprantis, A. O., Polak, L., Glimcher, L. H. & Fuchs, E. (2008). NFATc1 balances quiescence and proliferation of skin stem cells. Cell 132, 299-310.
72. Horsley, V., O'Carroll, D., Tooze, R., Ohinata, Y., Saitou, M., Obukhanych, T., Nussenzweig, M., Tarakhovsky, A. & Fuchs, E. (2006). Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 126, 597-609.
73. Hsu, Y.-C., Li, L. & Fuchs, E. (2014). Emerging interactions between skin stem cells and their niches. Nature Medicine 20, 847-856.
74. Hsu, Y. C., Pasolli, H. A. & Fuchs, E. (2011). Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 144, 92-105.
75. Ishimatsu-Tsuji, Y., Moro, O. & Kishimoto, J. (2005). Expression profiling and cellular localization of genes associated with the hair cycle induced by wax depilation. Journal of Investigative Dermatology 125, 410-420.
76. Ito, M., Kizawa, K., Hamada, K. & Cotsarelis, G. (2004). Hair follicle stem cells in the lower bulge form the secondary germ, a biochemically distinct but functionally equivalent progenitor cell population, at the termination of catagen. Differentiation 72, 548-557.
77. Jackson, A. J. & Price, V. H. (2013). How to diagnose hair loss. Dermatologic Clinics 31, 21-28.
78. Jahoda, C. A. & Reynolds, A. J. (1996). Dermal-epidermal interactions. Adult follicle-derived cell populations and hair growth. Dermatologia Clinica 14, 573-583.
79. Jaks, V., Barker, N., Kasper, M., Van Es, J. H., Snippert, H. J., Clevers, H. & Toftgard, R. (2008). Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nature Genetics 40, 1291-1299.
80. Janich, P., Pascual, G., Merlos-Suarez, A., Batlle, E., Ripperger, J., Albrecht, U., Cheng, H. Y., Obrietan, K., Di Croce, L. & Benitah, S. A. (2011). The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 480, 209-214.
81. Jensen, K. B., Collins, C. A., Nascimento, E., Tan, D. W., Frye, M., Itami, S. & Watt, F. M. (2009). Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 4, 427-439.
82. Johnson, E. (1958). Quantitative studies of hair growth in the albino rat. III. The role of the adrenal glands. Journal of Endocrinology 16, 360-368.
83. Jouvel, C., Maciejewski, P., Garcia, P., Bonnaire, Y., Horning, S. & Popot, M. A. (2000). Detection of diazepam in horse hair samples by mass spectrometric methods. Analyst 125, 1765-1769.
84. Langan, E. A., Foitzik-Lau, K., Goffin, V., Ramot, Y. & Paus, R. (2010). Prolactin: an emerging force along the cutaneous-endocrine axis. Trends in Endocrinology and Metabolism: TEM 21, 569-577.
85. Kandyba, E., Leung, Y., Chen, Y. B., Widelitz, R., Chuong, C. M. & Kobielak, K. (2013). Competitive balance of intrabulge BMP/Wnt signaling reveals a robust gene network ruling stem cell homeostasis and cyclic activation. Proceedings of the National Academy of Sciences of the United States of America 110, 1351-1356.
86. Katayama, M., Aoki, E., Suzuki, H. & Kawana, S. (2007). Foot shock stress prolongs the telogen stage of the spontaneous hair cycle in a non-depilated mouse model. Experimental Dermatology 16, 553-560.
87. Kimura-Ueki, M., Oda, Y., Oki, J., Komi-Kuramochi, A., Honda, E., Asada, M., Suzuki, M. & Imamura, T. (2012). Hair cycle resting phase is regulated by cyclic epithelial FGF18 signaling. Journal of Investigative Dermatology 132, 1338-1345.
88. Kligman, A. M. (1956). Pathophysiology of ringworm infections in animals with skin cycles. Journal of Investigative Dermatology 27, 171-185.
89. Kligman, A. M. (1961). Pathologic dynamics of human hair loss. I. Telogen effuvium. Archives of Dermatology 83, 175-198.
90. Koch, P. J., Mahoney, M. G., Cotsarelis, G., Rothenberger, K., Lavker, R. M. & Stanley, J. R. (1998). Desmoglein 3 anchors telogen hair in the follicle. Journal of Cell Science 111(Pt. 17), 2529-2537.
91. Kunz, M., Seifert, B. & Trueb, R. M. (2009). Seasonality of hair shedding in healthy women complaining of hair loss. Dermatology 219, 105-110.
92. Kushlan, J. A. (1980). The evolution of hairlessness in man. The American Naturalist 116, 727-729.
93. Kushlan, J. A. (1985). The vestiary hypothesis of human-hair reduction. Journal of Human Evolution 14, 29-32.
94. Langan, E. A., Hanning, A., Ramot, Y., Poeggeler, B., Biro, T., Gaspar, E., Griffiths, C. E. & Paus, R. (2010). Thyrotropin releasing hormone and 17-beta-estradiol regulate intra-cutaneous prolactin and prolactin receptor expression in human skin and hair follicles; preliminary evidence using serum free organ culture. Experimental Dermatology 19, 1127-1131.
95. Lee, B., Geyfman, M., Andersen, B. & Dai, X. (2013). Analysis of gene expression in skin using laser capture microdissection. Methods in Molecular Biology (Clifton, N.J.) 989, 109-117.
96. Leishman, E., Howard, J. M., Garcia, G. E., Miao, Q., Ku, A. T., Dekker, J. D., Tucker, H. & Nguyen, H. (2013). Foxp1 maintains hair follicle stem cell quiescence through regulation of Fgf18. Development (Cambridge, England) 140, 3809-3818.
97. Lien, W. H., Guo, X. Y., Polak, L., Lawton, L. N., Young, R. A., Zheng, D. Y. & Fuchs, E. (2011). Genome-wide maps of histone modifications unwind in vivo chromatin states of the hair follicle lineage. Cell Stem Cell 9, 219-232.
98. Lin, K. K., Chudova, D., Hatfield, G. W., Smyth, P. & Andersen, B. (2004). Identification of hair cycle-associated genes from time-course gene expression profile data by using replicate variance. Proceedings of the National Academy of Sciences of the United States of America 101, 15955-15960.
99. Lin, K. K., Kumar, V., Geyfman, M., Chudova, D., Ihler, A. T., Smyth, P., Paus, R., Takahashi, J. S. & Andersen, B. (2009). Circadian clock genes contribute to the regulation of hair follicle cycling. PLoS Genetics 5, e1000573.
100. Lin, H. Y. & Yang, L. T. (2013). Differential response of epithelial stem cell populations in hair follicles to TGF-beta signaling. Developmental Biology 373, 394-406.
101. Lindner, G., Botchkarev, V. A., Botchkareva, N. V., Ling, G., van der Veen, C. & Paus, R. (1997). Analysis of apoptosis during hair follicle regression (catagen). The American Journal of Pathology 151, 1601-1617.
102. Lindner, G., Menrad, A., Gherardi, E., Merlino, G., Welker, P., Handjiski, B., Roloff, B. & Paus, R. (2000). Involvement of hepatocyte growth factor/scatter factor and met receptor signaling in hair follicle morphogenesis and cycling. FASEB Journal 14, 319-332.
103. Lowry, W. E., Blanpain, C., Nowak, J. A., Guasch, G., Lewis, L. & Fuchs, E. (2005). Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells. Genes & Development 19, 1596-1611.
104. Ma, L., Liu, J., Wu, T., Plikus, M., Jiang, T. X., Bi, Q., Liu, Y. H., Muller-Rover, S., Peters, H., Sundberg, J. P., Maxson, R., Maas, R. L. & Chuong, C. M. (2003). 'Cyclic alopecia' in Msx2 mutants: defects in hair cycling and hair shaft differentiation. Development 130, 379-389.
105. Mardaryev, A. N., Ahmed, M. I., Vlahov, N. V., Fessing, M. Y., Gill, J. H., Sharov, A. A. & Botchkareva, N. V. (2010). Micro-RNA-31 controls hair cycle-associated changes in gene expression programs of the skin and hair follicle. FASEB Journal 24, 3869-3881.
106. Mardaryev, A. N., Meier, N., Poterlowicz, K., Sharov, A. A., Sharova, T. Y., Ahmed, M. I., Rapisarda, V., Lewis, C., Fessing, M. Y., Ruenger, T. M., Bhawan, J., Werner, S., Paus, R. & Botchkarev, V. A. (2011). Lhx2 differentially regulates Sox9, Tcf4 and Lgr5 in hair follicle stem cells to promote epidermal regeneration after injury. Development 138, 4843-4852.
107. Marks, F. & Richter, K. H. (1984). A request for a more serious approach to the chalone concept. British Journal of Dermatology 111(Suppl. 27), 58-63.
108. McElwee, K. J., Gilhar, A., Tobin, D. J., Ramot, Y., Sundberg, J. P., Nakamura, M., Bertolini, M., Inui, S., Tokura, Y., King, L. E., Duque-Estrada, B., Tosti, A., Keren, A., Itami, S., Shoenfeld, Y., Zlotogorski, A. & Paus, R. (2013). What causes alopecia areata?: Section Editors: Ralf Paus, Manchester/Lubeck and Raymond Cho, San Francisco. Experimental Dermatology 22, 609-626.
109. Messenger, A. G., Elliott, K., Westgate, G. E. & Gibson, W. T. (1991). Distribution of extracellular matrix molecules in human hair follicles. Annals of the New York Academy of Sciences 642, 253-262.
110. Messenger, A. G., Slater, D. N. & Bleehen, S. S. (1986). Alopecia-areata - alterations in the hair-growth cycle and correlation with the follicular pathology. British Journal of Dermatology 114, 337-347.
111. Milner, Y., Sudnik, J., Filippi, M., Kizoulis, M., Kashgarian, M. & Stenn, K. (2002a). Exogen, shedding phase of the hair growth cycle: characterization of a mouse model. Journal of Investigative Dermatology 119, 639-644.
112. Milner, Y., Sudnik, J., Kizoulis, M., Filippi, M., Kashgarian, M. & Stenn, K. (2002b). The shedding phase of the hair growth cycle, exogen, is coupled to anagen and creates a unique hair shaft base. Journal of Investigative Dermatology 119, 639-644.
113. Miteva, M. & Tosti, A. (2012). The follicular triad: a pathological clue to the diagnosis of early frontal fibrosing alopecia. British Journal of Dermatology 166, 440-442.
114. Montagna, W. & Ellis, R. A. (eds) (1958). The Biology of Hair-Growth. Academic Press, New York.
115. Morris, D. (1967). The Naked Ape. Vintage, London.
116. Muller-Rover, S., Handjiski, B., van der Veen, C., Eichmuller, S., Foitzik, K., McKay, I. A., Stenn, K. S. & Paus, R. (2001). A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. Journal of Investigative Dermatology 117, 3-15.
117. Murray, P. J., Maini, P. K., Plikus, M. V., Chuong, C. M. & Baker, R. E. (2012). Modelling hair follicle growth dynamics as an excitable medium. PLoS Computational Biology 8, e1002804.
118. Myung, P. S., Takeo, M., Ito, M. & Atit, R. P. (2013). Epithelial Wnt ligand secretion is required for adult hair follicle growth and regeneration. Journal of Investigative Dermatology 133, 31-41.
119. Nagao, K., Kobayashi, T., Moro, K., Ohyama, M., Adachi, T., Kitashima, D. Y., Ueha, S., Horiuchi, K., Tanizaki, H., Kabashima, K., Kubo, A., Cho, Y. H., Clausen, B. E., Matsushima, K., Suematsu, M., Furtado, G. C., Lira, S. A., Farber, J. M., Udey, M. C. & Amagai, M. (2012). Stress-induced production of chemokines by hair follicles regulates the trafficking of dendritic cells in skin. Nature Immunology 13, 744-752.
120. Nakamura, M., Schneider, M. R., Schmidt-Ullrich, R. & Paus, R. (2013). Mutant laboratory mice with abnormalities in hair follicle morphogenesis, cycling, and/or structure: an update. Journal of Dermatological Science 69, 6-29.
121. Nieves, A. & Garza, L. A. (2014). Does prostaglandin D2 hold the cure to male pattern baldness? Experimental Dermatology 23, 224-227.
122. Nijhof, J., Braun, K., Giangreco, A., van Pelt, C., Kawamoto, H., Boyd, R., Willemze, R., Mullenders, L., Watt, F., de Gruijl, F. & van Ewijk, W. (2006). The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells. Development 133, 3027-3037.
123. Nishimura, E. K. (2011). Melanocyte stem cells: a melanocyte reservoir in hair follicles for hair and skin pigmentation. Pigment Cell & Melanoma Research 24, 401-410.
124. Nixon, A. J., Ashby, M. G., Saywell, D. P. & Pearson, A. J. (1995). Seasonal fiber growth cycles of ferrets (Mustela putorius furo) and long-term effects of melatonin treatment. Journal of Experimental Zoology 272, 435-445.
125. Oh, H. S. & Smart, R. C. (1996). An estrogen receptor pathway regulates the telogen-anagen hair follicle transition and influences epidermal cell proliferation. Proceedings of the National Academy of Sciences of the United States of America 93, 12525-12530.
126. Ohnemus, U., Uenalan, M., Conrad, F., Handjiski, B., Mecklenburg, L., Nakamura, M., Inzunza, J., Gustafsson, J.-A. & Paus, R. (2005). Hair cycle control by estrogens: catagen induction via estrogen receptor (ER)-alpha is checked by ER beta signaling. Endocrinology 146, 1214-1225.
127. Ohnemus, U., Uenalan, M., Inzunza, J., Gustafsson, J. A. & Paus, R. (2006). The hair follicle as an estrogen target and source. Endocrine Reviews 27, 677-706.
128. Ohyama, M., Zheng, Y., Paus, R. & Stenn, K. S. (2010). The mesenchymal component of hair follicle neogenesis: background, methods and molecular characterization. Experimental Dermatology 19, 89-99.
129. Oshimori, N. & Fuchs, E. (2012). Paracrine TGF-beta signaling counterbalances BMP-mediated repression in hair follicle stem cell activation. Cell Stem Cell 10, 63-75.
130. Panteleyev, A. A., Jahoda, C. A. & Christiano, A. M. (2001). Hair follicle predetermination. Journal of Cell Science 114, 3419-3431.
131. Parakkal, P. F. (1970). Morphogenesis of hair follicle during catagen. Zeitschrift fur Zellforschung und Mikroskopische Anatomie 107, 174-186.
132. Paus, R. (1998). Principles of hair cycle control. The Journal of Dermatology 25, 793-802.
133. Paus, R., Bottge, J. A., Henz, B. M. & Maurer, M. (1996). Hair growth control by immunosuppression. Archives of Dermatological Research 288, 408-410.
134. Paus, R. & Cotsarelis, G. (1999). The biology of hair follicles. New England Journal of Medicine 341, 491-497.
135. Paus, R. & Czarnetzki, B. M. (1994). The "bulge-activation hypothesis" does not explain hair follicle cycling but may still be valid. American Journal of Dermatopathology 16, 112-114.
136. Paus, R., Eichmüller, S., Hofmann, U., Czarnetzki, B. M. & Robinson, P. (1994). Expression of classical and non-classical MHC class I antigens in murine hair follicles. The British Journal of Dermatology 131, 177-183.
137. Paus, R. & Foitzik, K. (2004). In search of the "hair cycle clock": a guided tour. Differentiation 72, 489-511.
138. Paus, R., Haslam, I. S., Sharov, A. A. & Botchkarev, V. A. (2013). Pathobiology of chemotherapy-induced hair loss. Lancet Oncology 14, 50-59.
139. Paus, R., Heinzelmann, T., Robicsek, S., Czarnetzki, B. M. & Maurer, M. (1995). Substance-P stimulates murine epidermal keratinocyte proliferation and dermal mast-cell degranulation in-situ. Archives of Dermatological Research 287, 500-502.
140. Paus, R., Langan, E. A., Vidali, S., Ramot, Y. & Andersen, B. (2014). Neuroendocrinology of the hair follicle: principles and clinical perspectives. Trends in Molecular Medicine 20, 559-570.
141. Paus, R., Müller-Röver, S. & Botchkarev, V. A. (1999). Chronobiology of the hair follicle: hunting the " hair cycle clock". The Journal of Investigative Dermatology. Symposium Proceedings/The Society for Investigative Dermatology, Inc. [and] European Society for Dermatological Research 4, 338-345.
142. Paus, R., Nickoloff, B. J. & Ito, T. (2005). A "hairy" privilege. Trends in Immunology 26, 32-40.
143. Paus, R., Stenn, K. S. & Elgjo, K. (1991). The epidermal pentapeptide pyroGlu-Glu-Asp-Ser-Glyoh inhibits murine hair-growth in vivo and in vitro. Dermatologica 183, 173-178.
144. Paus, R., Stenn, K. S. & Link, R. E. (1989). The induction of anagen hair-growth in telogen mouse skin by cyclosporine-A administration. Laboratory Investigation 60, 365-369.
145. Paus, R., Stenn, K. S. & Link, R. E. (1990). Telogen skin contains an inhibitor of hair-growth. British Journal of Dermatology 122, 777-784.
146. Paus, R., Theoharides, T. C. & Arck, P. C. (2006). Neuroimmunoendocrine circuitry of the "brain-skin connection". Trends in Immunology 27, 32-39.
147. Paus, R., van der Veen, C., Eichmüller, S., Kopp, T., Hagen, E., Müller-Röver, S. & Hofmann, U. (1998). Generation and cyclic remodeling of the hair follicle immune system in mice. The Journal of Investigative Dermatology 111, 7-18.
148. Pearson, A. J., Ashby, M. G., Wildermoth, J. E., Craven, A. J. & Nixon, A. J. (1999). Effect of exogenous prolactin on the hair growth cycle. Experimental Dermatology 8, 358-360.
149. Petho-Schramm, A., Muller, H. J. & Paus, R. (1996). FGF5 and the murine hair cycle. Archives of Dermatological Research 288, 264-266.
150. Philpott, M. P. & Kealey, T. (1994). Effects of Egf on the morphology and patterns of DNA-synthesis in isolated human hair-follicles. Journal of Investigative Dermatology 102, 186-191.
151. Plikus, M. V. (2012). New activators and inhibitors in the hair cycle clock: targeting stem cells' state of competence. Journal of Investigative Dermatology 132, 1321-1324.
152. Plikus, M. V., Baker, R. E., Chen, C. C., Fare, C., de la Cruz, D., Andl, T., Maini, P. K., Millar, S. E., Widelitz, R. & Chuong, C. M. (2011). Self-organizing and stochastic behaviors during the regeneration of hair stem cells. Science 332, 586-589.
153. Plikus, M. V. & Chuong, C. M. (2008). Complex hair cycle domain patterns and regenerative hair waves in living rodents. Journal of Investigative Dermatology 128, 1071-1080.
154. Plikus, M. V. & Chuong, C. M. (2014). Macroenvironmental regulation of hair cycling and collective regenerative behavior. Cold Spring Harbor Perspectives in Medicine 4, a015198.
155. Plikus, M. V., Mayer, J. A., de la Cruz, D., Baker, R. E., Maini, P. K., Maxson, R. & Chuong, C. M. (2008). Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451, 340-344.
156. Plikus, M. V., Vollmers, C., de la Cruz, D., Chaix, A., Ramos, R., Panda, S. & Chuong, C. M. (2013). Local circadian clock gates cell cycle progression of transient amplifying cells during regenerative hair cycling. Proceedings of the National Academy of Sciences of the United States of America 110, 2106-2115.
157. Plikus, M. V., Widelitz, R. B., Maxson, R. & Chuong, C. M. (2009). Analyses of regenerative wave patterns in adult hair follicle populations reveal macro-environmental regulation of stem cell activity. International Journal of Developmental Biology 53, 857-868.
158. Posner, M. I. (2008). Measuring alertness. Molecular and Biophysical Mechanisms of Arousal, Alertness, and Attention 1129, 193-199.
159. Purba, T. S., Haslam, I. S., Poblet, E., Jiménez, F., Gandarillas, A., Izeta, A. & Paus, R. (2014). Human epithelial hair follicle stem cells and their progeny: current state of knowledge, the widening gap in translational research and future challenges. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 36, 513-525.
160. Rabbani, P., Takeo, M., Chou, W. C., Myung, P., Bosenberg, M., Chin, L., Taketo, M. M. & Ito, M. (2011). Coordinated activation of Wnt in epithelial and melanocyte stem cells initiates pigmented hair regeneration. Cell 145, 941-955.
161. Randall, V. A. (2007). Hormonal regulation of hair follicles exhibits a biological paradox. Seminars in Cell & Developmental Biology 18, 274-285.
162. Randall, V. A. & Ebling, F. J. G. (1991). Seasonal-changes in human hair-growth. British Journal of Dermatology 124, 146-151.
163. Risek, B., Klier, F. G. & Gilula, N. B. (1992). Multiple gap junction genes are utilized during rat skin and hair development. Development (Cambridge, England) 116, 639-651.
164. Rogers, G. E. (2006). Biology of the wool follicle: an excursion into a unique tissue interaction system waiting to be re-discovered. Experimental Dermatology 15, 931-949.
165. Rompolas, P., Mesa, K. R. & Greco, V. (2013). Spatial organization within a niche as a determinant of stem-cell fate. Nature 502, 513-518.
166. Rose, J., Oldfield, J. & Stormshak, F. (1987). Apparent role of melatonin and prolactin in initiating winter fur growth in mink. General and Comparative Endocrinology 65, 212-215.
167. Rose, J., Stormshak, F., Oldfield, J. & Adair, J. (1985). The effects of photoperiod and melatonin on serum prolactin levels of mink during the autumn molt. Journal of Pineal Research 2, 13-19.
168. Roth, W., Deussing, J., Botchkarev, V. A., Pauly-Evers, M., Saftig, P., Hafner, A., Schmidt, P., Schmahl, W., Scherer, J., Anton-Lamprecht, I., Von Figura, K., Paus, R. & Peters, C. (2000). Cathepsin L deficiency as molecular defect of furless: hyperproliferation of keratinocytes and pertubation of hair follicle cycling. FASEB Journal 14, 2075-2086.
169. Rudman, S. M., Philpott, M. P., Thomas, G. A. & Kealey, T. (1997). The role of IGF-I in human skin and its appendages: morphogen as well as mitogen? Journal of Investigative Dermatology 109, 770-777.
170. Sato-Miyaoka, M., Hisatsune, C., Ebisui, E., Ogawa, N., Takahashi-Iwanaga, H. & Mikoshiba, K. (2012). Regulation of hair shedding by the type 3 IP3 receptor. Journal of Investigative Dermatology 132, 2137-2147.
171. Schlake, T., Beibel, M., Weger, N. & Boehm, T. (2004). Major shifts in genomic activity accompany progression through different stages of the hair cycle. Gene Expression Patterns 4, 141-152.
172. Schmidt, B. & Horsley, V. (2012). Unravelling hair follicle-adipocyte communication. Experimental Dermatology 21, 827-830.
173. Schneider, M. R. (2011). The first description of the hair follicle bulge by Franz von Leydig. Dermatology 223, 29-31.
174. Schneider, M. R. & Paus, R. (2014). Deciphering the functions of the hair follicle infundibulum in skin physiology and disease. Cell and Tissue Research.
175. Schneider, M. R., Schmidt-Ullrich, R. & Paus, R. (2009). The hair follicle as a dynamic miniorgan. Current Biology 19, 132-142.
176. Sennett, R. & Rendl, M. (2012). Mesenchymal-epithelial interactions during hair follicle morphogenesis and cycling. Seminars in Cell & Developmental Biology 23, 917-927.
177. Shimomura, Y. & Christiano, A. M. (2010). Biology and genetics of hair. Annual Review of Genomics and Human Genetics 11, 109-132.
178. Shipman, M., Chase, H. B. & Montagna, W. (1955). Glycogen in skin of the mouse during cycles of hair growth. Proceedings of the Society for Experimental Biology and Medicine 88, 449-451.
179. Silver, A. F. & Chase, H. B. (1970). DNA synthesis in the adult hair germ during dormancy (telogen) and activation (early anagen). Developmental Biology 21, 440-451.
180. Snippert, H. J., Haegebarth, A., Kasper, M., Jaks, V., van Es, J. H., Barker, N., van de Wetering, M., van den Born, M., Begthel, H., Vries, R. G., Stange, D. E., Toftgard, R. & Clevers, H. (2010). Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 327, 1385-1389.
181. Sohnle, P. G., Collinslech, C. & Hahn, B. (1986). Effect of hair-growth cycles on experimental cutaneous candidiasis in mice. Journal of Investigative Dermatology 86, 556-559.
182. Stenn, K. (2005). Exogen is an active, separately controlled phase of the hair growth cycle. Journal of the American Academy of Dermatology 52, 374-375.
183. Stenn, K. S. & Paus, R. (2001). Controls of hair follicle cycling. Physiological Reviews 81, 449-494.
184. Stenn, K. S., Paus, R., Dutton, T. & Sarba, B. (1993). Glucocorticoid effect on hair-growth initiation - a reconsideration. Skin Pharmacology 6, 125-134.
185. Sundberg, J. P., Peters, E. M. J. & Paus, R. (2005). Analysis of hair follicles in mutant laboratory mice. Journal of Investigative Dermatology Symposium Proceedings 10, 264-270.
186. Suzuki, S., Ota, Y., Ozawa, K. & Imamura, T. (2000). Dual-mode regulation of hair growth cycle by two Fgf-5 gene products. Journal of Investigative Dermatology 114, 456-463.
187. Takeda, N., Jain, R., LeBoeuf, M. R., Padmanabhan, A., Wang, Q. H., Li, L., Lu, M. M., Millar, S. E. & Epstein, J. A. (2013). Hopx expression defines a subset of multipotent hair follicle stem cells and a progenitor population primed to give rise to K6(+) niche cells. Development 140, 1655-1664.
188. Tang, Y. Y., Rothbart, M. K. & Posner, M. I. (2012). Neural correlates of establishing, maintaining, and switching brain states. Trends in Cognitive Sciences 16, 330-337.
189. Tanioka, M., Yamada, H., Doi, M., Bando, H., Yamaguchi, Y., Nishigori, C. & Okamura, H. (2009). Molecular clocks in mouse skin. Journal of Investigative Dermatology 129, 1225-1231.
190. Tiede, S., Kloepper, J. E., Bodo, E., Tiwari, S., Kruse, C. & Paus, R. (2007). Hair follicle stem cells: walking the maze. European Journal of Cell Biology 86, 355-376.
191. Tobin, D. J., Foitzik, K., Reinheckel, T., Mecklenburg, L., Botchkarev, V. A., Peters, C. & Paus, R. (2002). The lysosomal protease cathepsin L is an important regulator of keratinocyte and melanocyte differentiation during hair follicle morphogenesis and cycling. American Journal of Pathology 160, 1807-1821.
192. Tornqvist, G., Sandberg, A., Hagglund, A. C. & Carisson, L. (2010). Cyclic expression of Lhx2 regulates hair formation. PLoS Genetics 6, e1000904.
193. Umeda-Ikawa, A., Shimokawa, I. & Doi, K. (2009). Time-course expression profiles of hair cycle-associated genes in male mini rats after depilation of telogen-plhase. International Journal of Molecular Sciences 10, 1967-1977.
194. Van Neste, D., Leroy, T. & Conil, S. (2007). Exogen hair characterization in human scalp. Skin Research and Technology 13, 436-443.
195. Vidali, S., Knuever, J., Lerchner, J., Giesen, M., Bíró, T., Klinger, M., Kofler, B., Funk, W., Poeggeler, B. & Paus, R. (2014). Hypothalamic-pituitary-thyroid axis hormones stimulate mitochondrial function and biogenesis in human hair follicles. The Journal of Investigative Dermatology 134, 33-42.
196. Weger, N. & Schlake, T. (2005). Igfbp3 modulates cell proliferation in the hair follicle. Journal of Investigative Dermatology 125, 847-849.
197. Whittem, T., Davis, C., Beresford, G. D. & Gourdie, T. (1998). Detection of morphine in mane hair of horses. Australian Veterinary Journal 76, 426-427.
198. Wojciechowicz, K., Gledhill, K., Ambler, C. A., Manning, C. B. & Jahoda, C. A. B. (2013). Development of the mouse dermal adipose layer occurs independently of subcutaneous adipose tissue and is marked by restricted early expression of FABP4. PLos One 8, e59811.
199. Woo, W. M. & Oro, A. E. (2011). Snapshot: hair follicle stem cells. Cell 146, 334.
200. Xiong, Y. Q., Li, W., Shang, C., Chen, R. M., Han, P., Yang, J., Stankunas, K., Wu, B. R., Pan, M. G., Zhou, B., Longaker, M. T. & Chang, C. P. (2013). Brg1 governs a positive feedback circuit in the hair follicle for tissue regeneration and repair. Developmental Cell 25, 169-181.
201. Yang, C.-C., Sheu, H.-M., Chung, P.-L., Chang, C.-H., Tsai, Y.-S., Hughes, M.W., Tuan, T.-L. & Huang, L.L.H. (2014). Leptin of dermal adipose tissue is differentially expressed during the hair cycle and contributes to adipocyte-mediated growth inhibition of anagen-phase vibrissa hair. Experimental Dermatology.
202. Yucel, G., Altindag, B., Gomez-Ospina, N., Rana, A., Panagiotakos, G., Lara, M. F., Dolmetsch, R. & Oro, A. E. (2013). State-dependent signaling by Ca(v)1.2 regulates hair follicle stem cell function. Genes & Development 27, 1217-1222.
203. Zanello, S. B., Jackson, D. M. & Holick, M. F. (2000). Expression of the circadian clock genes clock and period1 in human skin. FASEB Journal 115, 757-760.
204. Zanet, J., Freije, A., Ruiz, M., Coulon, V., Sanz, J. R., Chiesa, J. & Gandarillas, A. (2010). A mitosis block links active cell cycle with human epidermal differentiation and results in endoreplication. PLoS ONE 5, e15701.
205. Zanet, J., Pibre, S., Jacquet, C., Ramirez, A., de Alboran, I. M. & Gandarillas, A. (2005). Endogenous Myc controls mammalian epidermal cell size, hyperproliferation, endoreplication and stem cell amplification. Journal of Cell Science 118, 1693-1704.
206. Zhang, Y. V., Cheong, J., Ciapurin, N., McDermitt, D. J. & Tumbar, T. (2009). Distinct Self-renewal and differentiation ptases in the niche of infrequently dividing hair follicle stem cells. Cell Stem Cell 5, 267-278.