A guide to studying human Hair follicle cycling in vivo

Journal of Investigative Dermatology

Volumn 136, Issue 1, 2016, Pages 34-44

  Oh, Ji Won ^a,b,c   Kloepper, Jennifer ^d   Langan, Ewan A ^d   Kim, Yongsoo ^e   Yeo, Joongyeub ^f   Kim, Min Ji ^b   Hsi, Tsai Ching ^c   Rose, Christian ^g   Yoon, Ghil Suk ^h   Lee, Seok Jong ^b   Seykora, John ⁱ   Kim, Jung Chul ^a,b   Sung, Young Kwan ^b   Kim, Moonkyu ^a,b   Paus, Ralf ^j,k   Plikus, Maksim V ^c  

^a Kyungpook National University Hospital   (South Korea)

^b Kyungpook National University School of Medicine   (South Korea)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF LÜBECK   (Germany)

^e NETHERLANDS CANCER INSTITUTE   (Netherlands)

^f Stanford University   (United States)

^g Dermatohistologisches Labor   (Germany)

^h Kyungpook National University   (South Korea)

ⁱ UNIVERSITY OF PENNSYLVANIA   (United States)

^j UNIVERSITY OF MANCHESTER   (United Kingdom)

^k UNIVERSITY OF MÜNSTER   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; MELANIN;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; COMPUTER SIMULATION; GRAFT REJECTION; HAIR; HAIR FOLLICLE; HAIR GROWTH; HAIR ROOT; HAIR TRANSPLANTATION; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE; IN VIVO STUDY; LONG TERM SURVIVAL; MOSAICISM; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCALP; SEBACEOUS GLAND; XENOTRANSPLANTATION; ANATOMY AND HISTOLOGY; ANIMAL; APOPTOSIS; CELL CULTURE; CELL CYCLE; GROWTH, DEVELOPMENT AND AGING; IMMUNOHISTOCHEMISTRY; NEEDLE BIOPSY; PHYSIOLOGY; PRACTICE GUIDELINE; SCID MOUSE; XENOGRAFT;

ANIMALS; APOPTOSIS; BIOPSY, NEEDLE; CELL CYCLE; CELLS, CULTURED; GUIDELINES AS TOPIC; HAIR; HAIR FOLLICLE; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, SCID;

EID: 84959526189     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/JID.2015.354     Document Type: Article

References (86)

1. Al-Nuaimi Y, Hardman JA, Biro T, et al. A meeting of two chronobiological systems: circadian proteins Period1 and BMAL1 modulate the human hair cycle clock. J Invest Dermatol 2014;134:610-9.
2. Arck PC, Handjiski B, Kuhlmei A, et al. Mast cell deficient and neurokinin-1 receptor knockout mice are protected from stress-induced hair growth inhibition. J Mol Med (Berl) 2005;83:386-96.
3. Atanaskova Mesinkovska N, Bergfeld WF. Hair: what is new in diagnosis and management? Female pattern hair loss update: diagnosis and treatment. Dermatol Clin 2013;31:119-27.
4. Bernard BA. The human hair follicle, a bistable organ? Exp Dermatol 2012;21:401-3.
5. Bodo E, Tobin DJ, Kamenisch Y, et al. 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 2007;171:1153-67.
6. Botchkareva NV, Ahluwalia G, Shander D. Apoptosis in the hair follicle. J Invest Dermatol 2006;126:258-64.
7. Botchkareva NV, Kahn M, Ahluwalia G, Shander D. Survivin in the human hair follicle. J Invest Dermatol 2007;127:479-82.
8. Commo S, Bernard BA. Immunohistochemical analysis of tissue remodelling during the anagen-catagen transition of the human hair follicle. Br J Dermatol 1997;137:31-8.
9. Conover WJ. Practical nonparametric statistics. 3rd edition. New York: Wiley; 1999.
10. Cotsarelis G. Gene expression profiling gets to the root of human hair follicle stem cells. J Clin Invest 2006;116:19-22.
11. Courtois M, Loussouarn G, Hourseau C, Grollier JF. Hair cycle and alopecia. Skin Pharmacol 1994;7:84-9.
12. Crabtree JS, Kilbourne EJ, Peano BJ, et al. A mouse model of androgenetic alopecia. Endocrinology 2010;151:2373-80.
13. Dawber RPR. Diseases of the hair and scalp. Hoboken, NJ: Wiley; 1997.
14. De Brouwer B, Tetelin C, Leroy T, Bonfils A, Van Neste D. A controlled study of the effects of RU58841, a non-steroidal antiandrogen, on human hair production by balding scalp grafts maintained on testosterone-conditioned nude mice. Br J Dermatol 1997;137:699-702.
15. Dry FW. The coat of the mouse (Mus musculus). J Gen 1926;16:287-340.
16. Garza LA, Liu Y, Yang Z, et al. Prostaglandin D2 inhibits hair growth and is elevated in bald scalp of men with androgenetic alopecia. Sci Transl Med 2012;90:1179-96.
17. Geyfman M, Plikus MV, Treffeisen E, Andersen B, Paus R. Resting no more: redefining telogen, the maintenance stage of the hair growth cycle. Biol Rev Camb Phil Soc 2014.
18. Gilhar A, Keren A, Shemer A, d'Ovidio R, Ullmann Y, Paus R. Autoimmune disease induction in a healthy human organ: a humanized mouse model of alopecia areata. J Invest Dermatol 2013;133:844-7.
19. Gilhar A, Pillar T, Etzioni A. The effect of topical cyclosporin on the immediate shedding of human scalp hair grafted onto nude mice. Br J Dermatol 1988;119:767-70.
20. Gilhar A, Ullmann Y, Berkutzki T, Assy B, Kalish RS. Autoimmune hair loss (alopecia areata) transferred by T lymphocytes to human scalp explants on SCID mice. J Clin Invest 1998;101:62-7.
21. 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;123:455-7.
22. Halloy J, Bernard BA, Loussouarn G, Goldbeter A. Modeling the dynamics of human hair cycles by a follicular automaton. Proc Natl Acad Sci U S A 2000;97:8328-33.
23. Hardman JA, Tobin DJ, Haslam IS, et al. The peripheral clock regulates human pigmentation. J Invest Dermatol 2015;135:1053-64.
24. Harries MJ, Meyer K, Chaudhry I, et al. Lichen planopilaris is characterized by immune privilege collapse of the hair follicle's epithelial stem cell niche. J Pathol 2013;231:236-47.
25. Harries MJ, Paus R. The pathogenesis of primary cicatricial alopecias. Am J Pathol 2010;177:2152-62.
26. Harrison S, Sinclair R. Telogen effluvium. Clin Exp Dermatol 2002;27:389-5.
27. Hashimoto T, Kazama T, Ito M, et al. Histologic and cell kinetic studies of hair loss and subsequent recovery process of human scalp hair follicles grafted onto severe combined immunodeficient mice. J Invest Dermatol 2000;115:200-6.
28. Hashimoto T, Kazama T, Ito M, et al. Histologic study of the regeneration process of human hair follicles grafted onto SCID mice after bulb amputation. J Investig Dermatol Symp Proc 2001;6:38-42.
29. Hendrix S, Handjiski B, Peters EM, Paus R. A guide to assessing damage response pathways of the hair follicle: lessons from cyclophosphamideinduced alopecia in mice. J Invest Dermatol 2005;125:42-51.
30. Higgins CA, Westgate GE, Jahoda CA. From telogen to exogen: mechanisms underlying formation and subsequent loss of the hair club fiber. J Invest Dermatol 2009;129:2100-8.
31. Hoffmann R. TrichoScan: combining epiluminescence microscopy with digital image analysis for the measurement of hair growth in vivo. Eur J Dermatol 2001;11:362-8.
32. Hsu YC, Li L, Fuchs E. Emerging interactions between skin stem cells and their niches. Nat Med 2014;20:847-56.
33. Jahoda CA, Oliver RF, Reynolds AJ, Forrester JC, Horne KA. Human hair follicle regeneration following amputation and grafting into the nude mouse. J Invest Dermatol 1996;107:804-7.
34. Katz KA, Cotsarelis G, Gupta R, Seykora JT. Telogen effluvium associated with the dopamine agonist pramipexole in a 55-year-old woman with Parkinson's disease. J Am Acad Dermatol 2006;55:S103e4.
35. Kligman AM. The human hair cycle. J Invest Dermatol 1959;33:307-16.
36. Kloepper JE, Sugawara K, Al-Nuaimi Y, Gáspár E, van Beek N, Paus R. Methods in hair research: howto objectively distinguish between anagen and catagen in human hair follicle organ culture. Exp Dermatol 2010;19:305-12.
37. Kloepper JE, Tiede S, Brinckmann J, et al. Immunophenotyping of the human bulge region: the quest to define useful in situ markers for human epithelial hair follicle stem cells and their niche. Exp Dermatol 2008;17:592-609.
38. Krajcik RA, Vogelman JH, Malloy VL, Orentreich N. Transplants from balding and hairy androgenetic alopecia scalp regrow hair comparably well on immunodeficient mice. J Am Acad Dermatol 2003;48:752-9.
39. Langan EA, Foitzik-Lau K, Goffin V, Ramot Y, Paus R. Prolactin: an emerging force along the cutaneous-endocrine axis. Trends Endocrinol Metab 2010;21:569-77.
40. Langan EA, Philpott MP, Kloepper JE, Paus R. Human hair follicle organ culture: Theory, application and perspectives [e-pub ahead of print]. Exp Dermatol 2015. http://dx.doi.org/10.1111/exd.12836 (accessed 18 August 2015).
41. Lattanand A, Johnson WC. Male pattern alopecia a histopathologic and histochemical study. J Cutan Pathol 1975;2:58-70.
42. 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 1997;151:1601-17.
43. Lu Z, Hasse S, Bodo E, Rose C, Funk W, Paus R. Towards the development of a simplified long-term organ culture method for human scalp skin and its appendages under serum-free conditions. Exp Dermatol 2007;16:37-44.
44. Lyle S, Christofidou-Solomidou M, Liu Y, Elder DE, Albelda S, Cotsarelis G. Human hair follicle bulge cells are biochemically distinct and possess an epithelial stem cell phenotype. J Investig Dermatol Symp Proc 1999;4:296-301.
45. Malgouries S, Donovan M, Thibaut S, Bernard BA. Heparanase 1: a key participant of inner root sheath differentiation program and hair follicle homeostasis. Exp Dermatol 2008a; 17:1017-23.
46. Malgouries S, Thibaut S, Bernard BA. Proteoglycan expression patterns in human hair follicle. Br J Dermatol 2008b; 158:234-42.
47. Mardaryev AN, Meier N, Poterlowicz K, et al. Lhx2 differentially regulates Sox9, Tcf4 and Lgr5 in hair follicle stem cells to promote epidermal regeneration after injury. Development 2011;138:4843-52.
48. Mitchell TM. Machine learning. New York: McGraw-Hill; 1997.
49. Montagna W, Ellis RA. The biology of hair growth. New York, NY: Academic Press; 1958.
50. 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 2001;117:3-15.
51. Nakamura M, Schneider MR, Schmidt-Ullrich R, Paus R. Mutant laboratory mice with abnormalities in hair follicle morphogenesis, cycling, and/or structure: an update. J Dermatol Sci 2013;69:6-29.
52. Oh JW, Hsi TC, Guerrero-Juarez CF, Ramos R, Plikus MV. Organotypic skin culture. J Invest Dermatol 2013;133:e14.
53. Ohnemus U, Uenalan M, Inzunza J, Gustafsson JA, Paus R. The hair follicle as an estrogen target and source. Endocr Rev 2006;27:677-706.
54. Paus R. Therapeutic strategies for treating hair loss. Drug Discov Today 2006;3:101-10.
55. Paus R, Cotsarelis G. The biologyofhair follicles. N Engl J Med 1999;341:491-7.
56. Paus R, Foitzik K. In search of the "hair cycle clock": a guided tour. Differentiation 2004;72:489-511.
57. 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 1994;144:719-34.
58. Paus R, Haslam IS, Sharov AA, Botchkarev VA. Pathobiology of chemotherapy-induced hair loss. Lancet Oncol 2013;14:e50e9.
59. Paus R, Langan EA, Vidali S, Ramot Y, Andersen B. Neuroendocrinology of the hair follicle: principles and clinical perspectives. Trends Mol Med 2014;20:559-70.
60. Philpott MP, Green MR, Kealey T. Human hair growth in vitro. J Cell Sci 1990;97(Pt 3):463-71.
61. Plikus MV, Baker RE, Chen CC, et al. Self-organizing and stochastic behaviors during the regeneration of hair stem cells. Science 2011;332:586-9.
62. Plikus MV, Chuong CM. Macroenvironmental regulation of hair cycling and collective regenerative behavior. Cold Spring Harb Perspect Med 2014;4:a015198.
63. Plikus MV, Mayer JA, delaCruz D, et al. Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 2008;451:340-4.
64. Poeggeler B, Bodó E, Nadrowitz R, Dunst J, Paus R. A simple assay for the study of human hair follicle damage induced by ionizing irradiation. Exp Dermatol 2010;19:e306e9.
65. Purba TS, Haslam IS, Poblet E, et al. Human epithelial hair follicle stem cells and their progeny: current state of knowledge, the widening gap in translational research and future challenges. BioEssays 2014;36:513-25.
66. Purba TS, Haslam IS, Shahmalak A, Bhogal RK, Paus R. Mapping the expression of epithelial hair follicle stem cell-related transcription factors LHX2 and SOX9 in the human hair follicle. Exp Dermatol 2015;24:462-7.
67. Ramot Y, Paus R. Harnessing neuroendocrine controls of keratin expression: a new therapeutic strategy for skin diseases? BioEssays 2014;36:672-86.
68. Rebora A, Guarrera M. Kenogen. A new phase of the hair cycle? Dermatology 2002;205:108-10.
69. Schneider MR, Schmidt-Ullrich R, Paus R. The hair follicle as a dynamic miniorgan. Curr Biol 2009;19:R132e42.
70. Shapiro J. Clinical practice. Hair loss in women. N Engl J Med 2007;357:1620-30.
71. Sharova TY, Poterlowicz K, Botchkareva NV, et al. Complex changes in the apoptotic and cell differentiation programs during initiation of the hair follicle response to chemotherapy. J Invest Dermatol 2014;134:2873-82.
72. Sintov A, Serafimovich S, Gilhar A. New topical antiandrogenic formulations can stimulate hair growth in human bald scalp grafted onto mice. Int J Pharm 2000;194:125-34.
73. Slominski A, Wortsman J, Plonka PM, Schallreuter KU, Paus R, Tobin DJ. Hair follicle pigmentation. J Invest Dermatol 2005;124:13-21.
74. Sperling LC, Cowper SE, Knopp EA. An atlas of hair pathology with clinical correlations. 2nd edition. New York, NY: Taylor & Francis; 2012.
75. Stenn K. Exogen is an active, separately controlled phase of the hair growth cycle. J Am Acad Dermatol 2005;52:374-5.
76. Sundberg JP, Beamer WG, Uno H, Van Neste D, King LE. Androgenetic alopecia: in vivo models. Exp Mol Pathol 1999;67:118-30.
77. Sundberg JP, Peters EM, Paus R. Analysis of hair follicles in mutant laboratory mice. J Investig Dermatol Symp Proc 2005;10:264-70.
78. Tang L, Madani S, Lui H, Shapiro J. Regeneration of a new hair follicle from the upper half of a human hair follicle in a nude mouse. J Invest Dermatol 2002;119:983-4.
79. Tiede S, Kloepper JE, Whiting DA, Paus R. The 'follicular trochanter': an epithelial compartment of the human hair follicle bulge region in need of further characterization. Br J Dermatol 2007;157:1013-6.
80. Tobin DJ. The cell biology of human hair follicle pigmentation. Pigment Cell Melanoma Res 2011;24:75-88.
81. Unger WP. Hair transplantation: current concepts and techniques. J Investig Dermatol Symp Proc 2005;10:225-9.
82. Van Neste D, De Brouwer B, Dumortier M. Reduced linear hair growth rates of vellus and of terminal hairs produced by human balding scalp grafted onto nude mice. Ann N Y Acad Sci 1991;642:480-2.
83. Van Neste D, Trueb RM. Critical study of hair growth analysis with computerassisted methods. J Eur Acad Dermatol Venereol 2006;20:578-83.
84. Van Neste D, Warnier G, Thulliez M, Van Hoof F. Human hair follicle grafts onto nude mice: morphological study. In: Van Neste D, Lachapelle JM, Antoine JL, editors. Trends in human hair growth and alopecia research. Dordrecht, the Netherlands: Springer; 1989. p. 117e31.
85. Van Neste MD. Assessment of hair loss: clinical relevance of hair growth evaluation methods. Clin Exp Dermatol 2002;27:358-65.
86. Whiting DA. The structure of the human hair follicle: light microscopy of vertical and horizontal sections of scalp biopsies. NJ: Canfield Publishing; 2004.