A meeting of two chronobiological systems: Circadian proteins period1 and bmal1 modulate the human hair cycle clock

Journal of Investigative Dermatology

Volumn 134, Issue 3, 2014, Pages 610-619

  Al Nuaimi, Yusur ^a   Hardman, Jonathan A ^a   Bíró, Tamás ^b   Haslam, Iain S ^a   Philpott, Michael P ^c   Tóth, Balázs I ^b   Farjo, Nilofer ^d   Farjo, Bessam ^d   Baier, Gerold ^e   Watson, Rachel E B ^a   Grimaldi, Benedetto ^f   Kloepper, Jennifer E ^g   Paus, Ralf ^a,g  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d Farjo Medical Centre   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^g UNIVERSITY OF LÜBECK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1A; MESSENGER RNA; MYC PROTEIN; NUCLEAR RECEPTOR NR1D1; PER1 PROTEIN; PROTEIN BMAL1; PROTEIN P21; TRANSCRIPTION FACTOR CLOCK;

ADULT; AGED; ARTICLE; CHRONOBIOLOGY; CIRCADIAN RHYTHM; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE ACTIVITY; GENE EXPRESSION; GENE SILENCING; HAIR; HAIR FOLLICLE; HAIR GROWTH; HUMAN; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; KERATINOCYTE; MALE; MIDDLE AGED; MOLECULAR CLOCK; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCALP; CELL CYCLE REGULATION; GENE CONTROL; GROWTH REGULATION; HAIR ANALYSIS; HUMAN CELL; HYPOTHESIS; ORGAN CULTURE; REGULATORY MECHANISM;

ADULT; AGED; ARNTL TRANSCRIPTION FACTORS; CIRCADIAN RHYTHM; CLOCK PROTEINS; CYCLIN-DEPENDENT KINASE INHIBITOR P21; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; HAIR FOLLICLE; HUMANS; KERATINOCYTES; MALE; MIDDLE AGED; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP D, MEMBER 1; ORGAN CULTURE TECHNIQUES; PERIOD CIRCADIAN PROTEINS; PROTO-ONCOGENE PROTEINS C-MYB; SCALP;

EID: 84894089179     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2013.366     Document Type: Article

References (89)

1. Ackermann K, Dehghani F, Bux R et al. (2007) Day-night expression patterns of clock genes in the human pineal gland. J Pineal Res 43:185-944
2. Akashi M, Soma H, Yamamoto T et al. (2010) Noninvasive method for assessing the human circadian clock using hair follicle cells. PNAS 107: 15643-88
3. Al-Nuaimi Y, Baier G, Watson RE et al. (2010) The cycling hair follicle as an ideal systems biology research model. Exp Dermatol 19:707-133
4. Al-Nuaimi Y, Goodfellow M, Paus R et al. (2012) A prototypic mathematical model of the human hair cycle. J Theor Biol 310:143-599
5. Albrecht U (2012) Timing to perfection: the biology of central and peripheral circadian clocks. Neuron 74:246-600
6. Balsalobre A, Brown SA, Marcacci L et al. (2000) Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science 289:2344-77
7. Bass J (2012) Circadian topology of metabolism. Nature 491:348-566
8. Bedrosian TA, Nelson RJ (2012) Pro: Alzheimer's disease and circadian dysfunction: chicken or egg? Alzheimers Res Ther 4:255
9. Brown SA, Kowalska E, Dallmann R (2012) (Re)inventing the circadian feedback loop. Dev Cell 22:477-877
10. Brown SA, Kunz D, Dumas A et al. (2008) Molecular insights into human daily behavior. PNAS 105:1602-77
11. Bull JJ, Muller-Rover S, Patel SV et al. (2001) Contrasting localization of c-Myc with other Myc superfamily transcription factors in the human hair follicle and during the hair growth cycle. J Invest Dermatol 116:617-222
12. Bull JJ, Pelengaris S, Hendrix S et al. (2005) Ectopic expression of c-Myc in the skin affects the hair growth cycle and causes an enlargement of the sebaceous gland. Br J Dermatol 152:1125-333
13. Bunger MK, Wilsbacher LD, Moran SM et al. (2000) Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 103:1009-177
14. Chen J, Roop DR (2012) Mimicking hair disorders by genetic manipulation of organ-cultured human hair. J Invest Dermatol 132:2312-44
15. Chen Z, Yoo SH, Takahashi JS (2012) Small molecule modifiers of circadian clocks. Cell Mol Life Sci 70:2985-988
16. Chen-Goodspeed M, Lee CC (2007) Tumor suppression and circadian function. J Biol Rhythm 22:291-88
17. Chourasia R, Jain SK (2009) Drug targeting through pilosebaceous route. Curr Drug Target 10:950-677
18. Cotsarelis G (2006) Epithelial stem cells: a folliculocentric view. J Invest Dermatol Symp Proc 126:1459-688
19. Cotsarelis G, Millar SE (2001) Towards a molecular understanding of hair loss and its treatment. Trend Mol Med 7:293-3011
20. Dardente H, Cermakian N (2007) Molecular circadian rhythms in central and peripheral clocks in mammals. Chronobiol Int 24:195-2133
21. De Bodinat C, Guardiola-Lemaitre B, Mocaer E et al. (2010) Agomelatine, the first melatonergic antidepressant: discovery, characterization. Nat Rev Drug Discov 9:628-422
22. Dunlap JC, Loros JJ, DeCoursey PJ (2004) Chronobiology: Biological Timekeeping, Sinauer, Sunderland, Massachusetts, 213-555
23. Etain B, Milhiet V, Bellivier F et al. (2011) Genetics of circadian rhythms and mood spectrum disorders. Eur Neuropsychopharmacol 21(Suppl 4): S676-822
24. Feng D, Lazar MA (2012) Clocks, metabolism, and the epigenome. Mol Cell 47:158-677
25. Fu L, Pelicano H, Liu J et al. (2002) The circadian gene Period2 plays an important role in tumor suppression and DNA damage response in vivo. Cell 111:41-500
26. Fuchs E (2009) The tortoise and the hair: slow-cycling cells in the stem cell race. Cell 137:811-99
27. Geyfman M, Andersen B (2010) Clock genes, hair growth and aging. Aging 2:122-88
28. Geyfman M, Gordon W, Paus R et al. (2012a) Identification of telogen markers underscores that telogen is far from a quiescent hair cycle phase. J Invest Dermatol 132:721-44
29. Geyfman M, Kumar V, Liu Q et al. (2012b) Brain and muscle Arnt-like protein- 1 (BMAL1) controls circadian cell proliferation and susceptibility to UVBinduced DNA damage in the epidermis. PNAS 109:11758-633
30. Gu X, Xing L, Shi G et al. (2012) The circadian mutation PER2(S662G) is linked to cell cycle progression and tumorigenesis. Cell Death Differ 19:397-4055
31. Halloy J, Bernard BA, Loussouarn G et al. (2002) The follicular automaton model: effect of stochasticity and of synchronization of hair cycles. J Theor Biol 214:469-799
32. Hatfield CF, Herbert J, van Someren EJ et al. (2004) Disrupted daily activity/rest cycles in relation to daily cortisol rhythms of home-dwelling patients with early Alzheimer's dementia. Brain 127:1061-744
33. Hazlerigg D, Loudon A (2008) New insights into ancient seasonal review life timers. Curr Biol 18:R795-8044
34. Ito T, Ito N, Saathoff M et al. (2005) Interferon-gamma is a potent inducer of catagen-like changes in cultured human anagen hair follicles. Br J Dermatol 152:623-311
35. Janich P, Pascual G, Merlos-Suarez A et al. (2011) The circadian molecular clock creates epidermal stem cell heterogeneity. Nature 480:209-144
36. Kawara S, Mydlarski R, Mamelak AJ et al. (2002) Low-dose ultraviolet B rays alter the mRNA expression of the circadian clock. J Invest Dermatol 119:1220-33
37. Khapre RV, Samsa WE, Kondratov RV (2010) Circadian regulation of cell cycle: molecular connections between aging and the circadian clock. Ann Med 42:404-155
38. Kligman AM (1959) The human hair cycle. J Invest Dermatol 33:307-166
39. Kloepper JE, Sugawara K, Al-Nuaimi Y et al. (2010) Methods in hair research: how to objectively distinguish between anagen and catagen in human hair follicle organ culture. Exp Dermatol 19:305-122
40. Knuever J, Poeggeler B, Gaspar E et al. (2012) Thyrotropin-releasing hormone controls mitochondrial biology in human epidermis. J Clin Endocrinol Metab 97:978-866
41. Kwon OS, Oh JK, Kim MH et al. (2006) Human hair growth ex vivo is correlated with in vivo hair growth: selective categorization of hair follicles for more reliable hair follicle organ culture. Arch Dermatol Res 297:367-711
42. Langmesser S, Tallone T, Bordon A et al. (2008) Interaction of circadian clock proteins PER2 and CRY with BMALI and CLOCK. BMC Mol Biol 9:411
43. Lavker RM, Sun TT, Oshima H et al. (2003) Hair follicle stem cells. J Investig Dermatol Symp Proc 8:28-388
44. Lee C (2005) The circadian clock and tumor suppression by mammalian Period genes. Method Enzymol 393:852-611
45. Lee CC (2006) Tumor suppression by the mammalian Period genes. Cancer Causes Control 17:525-300
46. Lee J, Moulik M, Fang Z et al. (2013) Bmal1 and beta-Cell clock are required for adaptation to circadian disruption, and their loss of function leads to oxidative stress-induced beta-cell failure in mice. Mol Cell Biol 33:2327-388
47. Lin KK, Kumar V, Geyfman M et al. (2009) Circadian clock genes contribute to the regulation of hair follicle cycling. PLOS Genet 5:e10005733
48. Liu X, Grice JE, Lademann J et al. (2011) Hair follicles contribute significantly to penetration through human skin only at. Br J Clin Pharmacol 72: 768-744
49. Lowrey PL, Takahashi JS (2004) Mammalian circadian biology: elucidating genome-wide levels of temporal organisation. Annu Rev Genomics Hum Genet 5:407-411
50. Lowrey PL, Takahashi JS (2011) Genetics of circadian rhythms in mammalian model organisms. Adv Genet 74:175-2300
51. Matsuo T, Yamaguchi S, Mitsui S et al. (2003) Control mechanism of the circadian clock for timing of cell division in vivo. Science 302:255-99
52. Miller BH, L. ME, Panda S et al. (2007) Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. PNAS 104:3342-77
53. Mitsui S, Ohuchi A, Adachi-Yamada T et al. (2001) Cyclin-dependent kinase inhibitors, p21(waf1/cip1) and p27(kip1), are expressed site- and hair cycle-dependently in rat hair follicles. J Dermatol Sci 25:164-99
54. Ohtani N, Imamura Y, Yamakoshi K et al. (2007) Visualizing the dynamics of p21(Waf1/Cip1) cyclin-dependent kinase inhibitor expression in living animals. PNAS 104:15034-99
55. Ota T, Fustin JM, Yamada H et al. (2012) Circadian clock signals in the adrenal cortex. Mol Cell Endocrinol 349:30-77
56. Patzelt A, Richter H, Knorr F et al. (2011) Selective follicular targeting by modification of the particle sizes. J Control Release 150:45-88
57. Paus R (2006) Therapeutic strategies for treating hair loss. Drug Discov Today 3:101-100
58. Paus R, Cotsarelis G (1999) The biology of hair follicles. N Engl J Med 341: 491-77
59. Paus R, Foitzik K (2004) In search of the ''hair cycle clock'': a guided tour. Differentiation 72:489-5111
60. Peters EMJ, Stieglitz MG, Liezman C et al. (2006) p75 Neurotrophin receptormediated signalling promotes human hair follicle regression (catagen). Am J Pathol 168:221-344
61. Philpott MP, Green MR, Kealey T (1990) Human hair growth in vitro. J Cell Sci 97:463-711
62. Philpott MP, Sanders D, Westgate GE et al. (1994) Human hair growth in vitro: a model for the study of hair follicle biology. J Dermatol Sci 7(Suppl):S55-722
63. Plikus MV (2012) New activators and inhibitors in the hair cycle clock: targeting stem cells'. J Invest Dermatol 132:1321-44
64. Plikus MV, Baker RE, Chen C-C et al. (2011) Self-organizing and stochastic behaviors during the regeneration of hair stem cells. Science 332:586-99
65. Plikus MV, Gay DL, Treffeisen E et al. (2012) Epithelial stem cells and implications for wound repair. Semin Cell Dev Biol 23:946-533
66. Plikus MV, Mayer JA, de la Cruz D et al. (2008) Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451:340-44
67. Plikus MV, Vollmers C, de la Cruz D et al. (2013) Local circadian clock gates cell cycle progression of transient amplifying cells during regenerative hair cycling. PNAS 110:E2106-155
68. Razorenova OV (2012) Brain and muscle ARNT-like protein BMAL1 regulates ROS homeostasis and senescence: a possible link to hypoxia-inducible factor-mediated pathway. Cell Cycle 11:213-44
69. Robinson M, Reynolds AJ, Jahoda CA (1997) Hair cycle stage of the mouse vibrissa follicle determines subsequent fiber growth and follicle behavior in vitro. J Invest Dermatol 108:495-5000
70. Rosenwasser AM (2010) Circadian clock genes: non-circadian roles in sleep, addiction, and psychiatric disorders? Neurosci Biobehav Rev 34:1249-555
71. Sahar S, Sassone-Corsi P (2009) Metabolism and cancer: the circadian clock connection. Nat Rev Cancer 9:886-966
72. Saini C, Suter DM, Liani A et al. (2011) The mammalian circadian timing system: synchronization of peripheral clocks. Cold Spring Harb Symp Quant Biol 76:39-477
73. Samuelov L, Sprecher E, Tsuruta D et al. (2012) P-cadherin regulates human hair growth and cycling via canonical Wnt signaling. J Invest Dermatol 132:2332-411
74. Sanders DA, Philpott MP, Nicolle FV et al. (1994) The isolation and maintenance of the human pilosebaceous unit. Br J Dermatol 131:166-766
75. Sandu C, Dumas M, Malan A et al. (2012) Human skin keratinocytes, melanocytes, and fibroblasts contain distinct circadian clock machinerie. Cell Mol Life Sci 69:3329-399
76. Schibler U, Sassone-Corsi P (2002) A web of circadian pacemakers. Cell 111:919-222
77. Schneider MR, Schmidt-Ullrich R, Paus R (2009) The hair follicle as a dynamic miniorgan. Curr Biol 19:R132-422
78. Sporl F, Schellenberg K, Blatt T et al. (2011) A circadian clock in HaCaT keratinocytes. J Invest Dermatol 131:338-488
79. Stenn KS, Paus R (2001) Controls of hair follicle cycling. Physiol Rev 81: 449-944
80. Takahashi JS, Hong H-K, Ko CH et al. (2008) The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat Rev Genet 9:764-755
81. Takita E, Yokota S, Tahara Y et al. (2012) Biological clock dysfunction exacerbates contact hypersensitivity in mice. Br J Dermatol 168:39-466
82. Tanioka M, Yamada H, Doi M et al. (2009) Molecular clocks in mouse skin. J Invest Dermatol 129:1225-311
83. Tonsfeldt KJ, Chappell PE (2012) Clocks on top: the role of the circadian clock in the hypothalamic and pituitary. Mol Cell Endocrinol 349:3-122
84. van Beek N, Bodo E, Kromminga A et al. (2008) Thyroid hormones directly alter human hair follicle functions: anagen prolongation and stimulation of both hair matrix keratinocyte proliferation and hair pigmentation. J Clin Endocrinol Metab 93:4381-88
85. Wager-Smith K, Kay SA (2000) Circadian rhythm genetics: from flies to mice to humans. Nat Genet 26:23-77
86. Ware JV, Nelson OL, Robbins CT et al. (2012) Temporal organization of activity in the brown bear (Ursus arctos): roles of. Am J Physiol Regul Integr Comp Physiol 303:R890-9022
87. Xu X, Lyle S, Liu Y et al. (2003) Differential expression of cyclin D1 in the human hair follicle. Am J Pathol 163:969-788
88. Yang X, Wood PA, Ansell CM et al. (2009) The circadian clock gene Per11 supresses cancer cell proliferation and tumor growth at specific times of day. Chronobiol Int 26:1323-399
89. Zanello SB, Jackson DM, Holick MF (2000) Expression of the circadian clock genes clock and period1 in human Skin. J Invest Dermatol 115:757-600