From telogen to exogen: Mechanisms underlying formation and subsequent loss of the hair club fiber

Journal of Investigative Dermatology

Volumn 129, Issue 9, 2009, Pages 2100-2108

  Higgins, Claire A ^a   Westgate, Gillian E ^b   Jahoda, Colin A B ^a  

^a DURHAM UNIVERSITY   (United Kingdom)

^b Westgate Consultancy Ltd   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION; CELL DIVISION; DESQUAMATION; EXOGEN; FIBER; HAIR CELL; HAIR FOLLICLE; HAIR GROWTH; HAIR LOSS; HAIR ROOT; HORMONAL REGULATION; HUMAN; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; REVIEW; SCALP HAIR; TELOGEN;

EID: 70349918149     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2009.66     Document Type: Review

References (97)

1. Alonso L, Fuchs E (2006) The hair cycle. J Cell Sci 119:391-393
2. Auber L, Burns M (1947) Replacement of fibres in Sheep. Nature 160:836
3. Bamford JT (1987) A falling out following minoxidil: telogen effluvium. J Am Acad Dermatol 16:144-146
4. Bardelli A, Rebora A (1989) Telogen effluvium and minoxidil. J Am Acad Dermatol 21:572-573
5. Bernot KM, Coulombe PA, McGowan KM (2002) Keratin 16 expression defines a subset of epithelial cells during skin morphogenesis and the hair cycle. J Invest Dermatol 119:1137-1149
6. Berth-Jones J, Shuttleworth D, Hutchinson PE (1990) A study of etretinate alopecia. Br J Dermatol 122:751-755
7. Bisset DL, McBride JF, Patrick LF (1987) Role of protein and calcium in stratum corneum cell cohesion. Arch Dermatol Res 279:184-189
8. Blanpain C, Fuchs E (2006) Epidermal stem cells of the skin. Annu Rev Cell Dev Biol 22:339-373
9. Broekaert D, Cooreman K, Coucke P, Nsabumukunzi S, Reyniers P, Kluyskens P et al. (1982) A quantitative histochemical study of sulphydryl and disulphide content during normal epidermal keratinization. Histochem J 14:573-584
10. Cao T, Racz P, Szauter KM, Groma G, Nakamatsu GY, Fogelgren B et al. (2007) Mutation in Mpzl3, a novel [corrected] gene encoding a predicted [corrected] adhesion protein, in the rough coat (rc) mice with severe skin and hair abnormalities. J Invest Dermatol 127:1375-1386
11. Cash TF (1992) The psychological effects of androgenetic alopecia in men. J Am Acad Dermatol 26:926-931
12. Cash TF (1999) The psychosocial consequences of androgenetic alopecia: a review of the research literature. Br J Dermatol 141:398-405
13. Cash TF, Price VH, Savin RC (1993) Psychological effects of androgenetic alopecia on women: comparisons with balding men and with female control subjects. J Am Acad Dermatol 29:568-575
14. Chapman DM (1992) The anchoring strengths of various chest hair root types. Clin Exp Dermatol 17:421-423
15. Chapman SJ, Walsh A (1990) Desmosomes, corneosomes and desquamation. An ultrastructural study of adult pig epidermis. Arch Dermatol Res 282:304-310
16. Chase HB (1954) Growth of the hair. Physiol Rev 34:113-126
17. Chase HB, Eaton GJ (1959) The growth of hair follicles in waves. Ann NY Acad Sci 83:365-368
18. Courtois M, Loussouarn G, Hourseau C, Grollier JF (1994) Hair cycle and alopecia. Skin Pharmacol 7:84-89
19. Courtois M, Loussouarn G, Hourseau C, Grollier JF (1995) Ageing and hair cycles. Br J Dermatol 132:86-93
20. Dano K, Andreason PA, Grondahl-Hansen J, Kristensen P, Nielsen LS, Skriver L (1985) Plasminogen activators, tissue degredation and cancer. Adv Cancer Res 44:139-266
21. Dry F (1926) The coat of a mouse (Mus musculus). J Genet 16:281-340
22. Ebling FJ (1976) Hair. J Invest Dermatol 67:98-105
23. Ebling FJ, Johnson E (1964) The action of hormones on spontaneous hair growth cycles in the rat. J Endocrinol 29:193-201
24. Egelrud T (2000) Desquamation in the stratum corneum. Acta Derm Venereol Suppl (Stockh) 208:44-45
25. Egelrud T, Hofer PA, Lundström A (1988) Proteolytic degredation of desmosomes in plantar stratum corneum leads to cell dissociation in vitro. Acta Derm Venereol (Stockh) 68:93-97
26. Gu LH, Coulombe PA (2007) Keratin expression provides novel insight into the morphogenesis and function of the companion layer in hair follicles. J Invest Dermatol 127:1061-1073
27. 0 s scalp. Dermatology 197:335-7
28. Guarrera M, Cipriani C, Rebora A (1998) Delayed telogen replacement in a boy0s scalp. Dermatology 197:335-7 Guarrera M, Rebora A (2005) Kenogen in female androgenetic alopecia. A longitudinal study. Dermatology 210:18-20
29. Hadshiew IM, Foitzik K, Arck PC, Paus R (2004) Burden of hair loss: stress and the underestimated psychosocial impact of telogen effluvium and androgenetic alopecia. J Invest Dermatol 123:455-457
30. Hale PA, Ebling FJ (1975) The effects of epilation and hormones on the activity of rat hair follicles. J Exp Zool 191:49-62
31. Hardy MH (1992) The secret life of the hair follicle. Trends Genet 8:55-61
32. Harrison S, Sinclair R (2002) Telogen effluvium. Clin Exp Dermatol 27:389-395
33. Hayashi K, Cao T, Passmore H, Jourdan-Le Saux C, Fogelgren B, Khan S et al. (2004) Progressive hair loss and myocardial degeneration in rough coat mice: reduced lysyl oxidase-like (LOXL) in the skin and heart. J Invest Dermatol 123:864-871
34. Headington JT (1993) Telogen effluvium. New concepts and review. Arch Dermatol 129:356-363
35. Herron BJ, Liddell RA, Parker A, Grant S, Kinne J, Fisher JK et al. (2005) A mutation in stratifin is responsible for the repeated epilation (Er) phenotype in mice. Nat Genet 37:1210-1212
36. Hibino T, Nishiyama T (2004) Role of TGF-beta2 in the human hair cycle. J Dermatol Sci 35:9-18
37. Higgins CA, Richardson GD, Westgate GE, Jahoda CAB (2009) Exogen involves gradual release of the hair club fibre in the vibrissa follicle model. Exp Dermatol, advance online publication, 6 January 2009, doi:10.1111/j.1600-0625. 2008.00833.x
38. Honda Y, Egawa K, Kuroki M, Ono T (1997) Hair cycle-dependent expression of a nonspecific cross reacting antigen (NCA)-50/90-like molecule on follicular keratinocytes. Arch Dermatol Res 289:457-465
39. Hunt N, McHale S (2005) The psychological impact of alopecia. BMJ 331:951-953
40. Ibrahim L, Wright EA (1975) The growth of rats and mice vibrissae under normal and some abnormal conditions. J Embryol Exp Morphol 33:831-844
41. Ito M, Kizawa K (2001) Expression of calcium-binding S100 proteins A4 and A6 in regions of the epithelial sac associated with the onset of hair follicle regeneration. J Invest Dermatol 116:956-963
42. 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
43. Ito M, Kizawa K, Toyoda M, Morohashi M (2002) Label-retaining cells in the bulge region are directed to cell death after plucking, followed by healing from the surviving hair germ. J Invest Dermatol 119:1310-1316
44. Jensen PJ, Yang T, Yu DW, Baker MS, Risse B, Sun TT et al. (2000) Serpins in the human hair follicle. J Invest Dermatol 114:917-922
45. Johnson E (1972) Moulting cycles. Mammal Rev 1:198-208
46. Johnson E, Ebling FJ (1964) The effect of plucking hairs during different phases of the follicular cycle. J Embryol Exp Morphol 12:465-474
47. Kligman AM (1959) The human hair cycle. J Invest Dermatol 33:307-316
48. Kligman AM (1961) Pathologic dynamics of human hair loss. I. Telogen effuvium. Arch Dermatol 83:175-198
49. Koch PJ, Mahoney MG, Cotsarelis G, Rothenberger K, Lavker RM, Stanley JR (1998) Desmoglein 3 anchors telogen hair in the follicle. J Cell Sci 111(Part 17):2529-2537
50. Lavker RM, Risse B, Brown H, Ginsburg D, Pearson J, Baker MS et al. (1998) Localization of plasminogen activator inhibitor type 2 (PAI-2) in hair and nail: implications for terminal differentiation. J Invest Dermatol 110:917-922
51. Li Q, Lu Q, Estepa G, Verma IM (2005) Identification of 14-3-3 ó mutation causing cutaneous abnormality in repeated-epilation mutant mouse. Proc Natl Acad Sci USA 102:15977-15982
52. Lundström A, Egelrud T (1988) Cell shedding from human plantar skin in vitro: evidence of its dependence on endogenous proteolysis. J Invest Dermatol 91:340-343
53. Lynfield YL (1960) Effect of pregnancy on the human hair cycle. J Invest Dermatol 35:323-327
54. Lyons-Giordano B, Loskutoff D, Chen CS, Lazarus G, Keeton M, Jensen PJ (1994) Expression of plasminogen activator inhibitor type 2 in normal and psoriatic epidermis. Histochemistry 101:105-112 (Pubitemid 24110023)
55. Ma L, Liu J, Wu T, Plikus M, Jiang TX, Bi Q et al. (2003) 0 Cyclic alopecia0 in Msx2 mutants: defects in hair cycling and hair shaft differentiation. Development 130:379-389
56. Matsuo K, Mori O, Hashimoto T (2003) Plucking during telogen induces apoptosis in the lower part of hair follicles. Arch Dermatol Res 295:33-37
57. Maurer F. Die epidermis und ihre Abkömmlinge. Leipzig: Wilhelm Engelmann, 1895
58. Milner Y, Sudnik J, Filippi M, Kizoulis M, Kashgarian M, Stenn K (2002) Exogen, shedding phase of the hair growth cycle: characterization of a mouse model. J Invest Dermatol 119:639-644
59. Muller-Rover S, Handjiski B, van der Veen C, Eichmuller S, Foitzik K, McKay IA et al. (2001) A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J Invest Dermatol 117:3-15
60. Orwin DF, Chase HB, Silver AF (1967) Catagen in the hairless house mouse. Am J Anat 121:489-507
61. Panteleyev AA, Botchkareva NV, Sundberg JP, Christiano AM, Paus R (1999) The role of the hairless (hr) gene in the regulation of hair follicle catagen transformation. Am J Pathol 155:159-171
62. Panteleyev AA, van der Veen C, Rosenbach T, Muller-Rover S, Sokolov VE, Paus R (1998) Towards defining the pathogenesis of the hairless phenotype. J Invest Dermatol 110:902-907
63. Paus R, Foitzik K (2004) In search of the "hair cycle clock": a guided tour. Differentiation 72:489-511
64. Paus R, Muller-Rover S, Botchkarev VA (1999) Chronobiology of the hair follicle: hunting the "hair cycle clock". J Investig Dermatol Symp Proc 4:338-345 (Pubitemid 30085832)
65. Pena JC, Kelekar A, Fuchs EV, Thompson CB (1999) Manipulation of outer root sheath cell survival perturbs the hair-growth cycle. EMBO J 18:3596-3603
66. Pierard-Franchimont C, Goffin V, Henry F, Uhoda I, Braham C, Pierard GE (2002) Nudging hair shedding by antidandruff shampoos. A comparison of 1% ketoconazole, 1% piroctone olamine and 1% zinc pyrithione formulations. Int J Cosmet Sci 24:249-256
67. Pierard-Franchimont C, Pierard GE (2001) Teloptosis, a turning point in hair shedding biorhythms. Dermatology 203:115-117
68. Pierard-Franchimont C, Xhauflaire-Uhoda E, Loussouarn G, Saint Leger D, Pierard GE (2006) Dandruff-associated smouldering alopecia: a chron-obiological assessment over 5 years. Clin Exp Dermatol 31:23-26
69. Pinkus H (1969) "Sebaceous cysts" are trichilemmal cysts. Arch Dermatol 99:544-555
70. Pinkus H, Iwasaki T, Mishima Y (1981) Outer root sheath keratinization in anagen and catagen of the mammalian hair follicle. A seventh distinct type of keratinization in the hair follicle: trichilemmal keratinization. J Anat 133:19-35
71. Plikus MV, Chuong CM (2008) Complex hair cycle domain patterns and regenerative hair waves in living rodents. J Invest Dermatol 128:1071-1080
72. Plikus MV, Mayer JA, de la Cruz D, Baker RE, Maini PK, Maxson R et al. (2008) Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451:340-344
73. Plonka PM, Michalczyk D, Popik M, Handjiski B, Paus R (2008) Electron paramagnetic resonance (EPR) spectroscopy for investigating murine telogen skin after spontaneous or depilation-induced hair growth. J Dermatol Sci 49:227-240
74. Poblet E, Jimenez F, de Cabo C, Prieto-Martin A, Sanchez-Prieto R (2005) The calcium-binding protein calretinin is a marker of the companion cell layer of the human hair follicle. Br J Dermatol 152:1316-1320
75. Price ML, Griffiths WA (1985) Normal body hair-a review. Clin Exp Dermatol 10:87-97
76. Randall VA, Ebling FJ (1991) Seasonal changes in human hair growth. Br J Dermatol 124:146-151
77. Rebora A, Guarrera M (2002) Kenogen. A new phase of the hair cycle? Dermatology 205:108-110
78. Rebora A, Guarrera M (2004) Teloptosis and kenogen: two new concepts in human trichology. Arch Dermatol 140:619-620
79. Roersma ME, Douven LF, Lefki K, Oomens CW (2001) The failure behavior of the anchorage of hairs during slow extraction. J Biomech 34:319-325
80. Rook A (1965) Endocrine influences on hair growth. Br Med J 1:609-614
81. Rook A, Dawber RPR (1982) Diseases of the hair and scalp. In: The Comparative Physiology, Embryology and Physiology of Human Hair. (Rook A, Dawber RPR, eds), Oxford, UK: Blackwell Publishing, 1-17
82. Roth W, Deussing J, Botchkarev VA, Pauly-Evers M, Saftig P, Hafner A et al. (2000) Cathepsin L deficiency as molecular defect of furless: hyperpro-liferation of keratinocytes and pertubation of hair follicle cycling. FASEB J 14:2075-2086
83. Saitoh M, Uzuka M, Sakamoto M (1970) Human hair cycle. J Invest Dermatol 54:65-81
84. Schmidt S (2003) Female alopecia: the mediating effect of attachment patterns on changes in subjective health indicators. Br J Dermatol 148:1205-1211
85. Seago SV, Ebling FJ (1985) The hair cycle on the human thigh and upper arm. Br J Dermatol 113:9-16
86. Segall A (1918) Ueber die Entwicklung und den Wechsel der Haare beim Meerschweinschen (Cavia Cobaya Schreb). Arch Mikrobiol Anat 91:218-291
87. Silver AF, Chase HB, Arsenault CT (1969) Early anagen initiated by plucking compared with early spontaneous anagen. In: Advances in Biology of Skin. (Montagna W, Dobson RL, eds), Vol.9. London: Pergamon, 265-286
88. Stenn K (2005) Exogen is an active, separately controlled phase of the hair growth cycle. J Am Acad Dermatol 52:374-375
89. Stenn KS, Parimoo S, Prouty S (1998) Growth of the hair follicle: a cycling and regenerating biological system. In: Molecular Basis of Epithelial Appendage Morphogenesis. (Chuong C-M, ed), Austin Tx: RG Landes Company, 111-130
90. Stenn KS, Paus R (2001) Controls of hair follicle cycling. Physiol Rev 81:449-494
91. Tobin DJ, Foitzik K, Reinheckel T, Mecklenburg L, Botchkarev VA, Peters C et al. (2002) The lysosomal protease cathepsin L is an important regulator of keratinocyte and melanocyte differentiation during hair follicle morphogenesis and cycling. Am J Pathol 160:1807-1821
92. Uyttendaele H, Panteleyev AA, de Berker D, Tobin DT, Christiano AM (2004) Activation of Notch1 in the hair follicle leads to cell-fate switch and Mohawk alopecia. Differentiation 72:396-409
93. Van Neste D, Leroy T, Conil S (2007) Exogen hair characterization in human scalp. Skin Res Technol 13:436-443
94. Vandevelde C, Allaerts W (1984) Trichilemmal keratinisation: a causal factor in loosening the murine telogen club hair from the trichilemmal sac. J Anat 138(Part 4):745-756
95. Williamson D, Gonzalez M, Finlay AY (2001) The effect of hair loss on quality of life. J Eur Acad Dermatol Venereol 15:137-139
96. Winter H, Langbein L, Praetzel S, Jacobs M, Rogers MA, Leigh IM et al. (1998) A novel human type II cytokeratin, K6hf, specifically expressed in the companion layer of the hair follicle. J Invest Dermatol 111:955-962
97. Ya-Xian Z, Suetake T, Tagami H (1999) Number of cell layer of the stratum corneum in normal skin-relationship to the anatomical location on the body, age, sex and physical parameters. Arch Dermatol Res 291:555-559