The cycling hair follicle as an ideal systems biology research model

Experimental Dermatology

Volumn 19, Issue 8, 2010, Pages 707-713

  Al Nuaimi, Yusur ^a,b   Baier, Gerold ^a   Watson, Rachel E B ^b   Chuong, Cheng Ming ^c   Paus, Ralf ^b,d  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d UNIVERSITY OF LÜBECK   (Germany)

Author keywords

Anagen; BMP; Chronobiology; Clock genes; Hair cycle; Telogen; WNT

Indexed keywords

ALGORITHM; ARTICLE; CHRONOBIOLOGY; HAIR FOLLICLE; HAIR GROWTH; HUMAN; MATHEMATICAL MODEL; MEDICAL RESEARCH; MESODERM; MODEL; NEUROECTODERM; NONHUMAN; SYSTEMS BIOLOGY;

ALGORITHMS; ANIMALS; CHRONOBIOLOGY PHENOMENA; HAIR FOLLICLE; HUMANS; MICE; MODELS, BIOLOGICAL; MODELS, THEORETICAL; SYSTEMS BIOLOGY;

EID: 77954853515     PISSN: 09066705     EISSN: 16000625     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2010.01114.x     Document Type: Article

References (83)

1. Duncan D E. Discover Dialogue: Sydney Brenner. Discover Science, Technology and the Future 2004, http://discovermagazine.com/2004/apr/discover-dialogue, Powell CSAdcroft PGKeating RWooden TWeintraub P. eds, New York, Discover Media LLC, (Last accessed 6th May 2010)
2. Klipp E, Liebermeister W, Wierling C, Kowald A, Lehrach H, Herwig R. Systems Biology: A textbook 2009, Weinheim, Wiley-VCH
3. Systems Biology: a vision for engineering and medicine. A report from the Academy of Medical Sciences and The Royal Academy of Engineering 2007, 1-65. London, Academy of Medical Sciences and the Royal Academy of Engineering
4. Huang S, Wikswo J. Dimensions of systems biology. Reviews of Physiology Biochemistry and Pharmacology 2006, 81-104. Amara SG, Bamberg EGudermann TLill EHebert SCJahn RLederer WJMiyajima AOffermans S. eds, Berlin, Springer Berlin Heidelberg
5. Westerhoff H V, Palsson B O. The evolution of molecular biology into systems biology. Nature 2004, 22:1249-1252.
6. Bruggeman F J, Westerhoff H V. The Nature of Systems Biology. Trends Microbiol 2006, 15:45-50.
7. Sauer U, Heinemann M, Zamboni N. Getting Closer to the Whole Picture. Science 2007, 316:550-551.
8. Di Ventura B, Lemerle C, Michalodimitrakis K, Serrano L. From in vivo to in silico biology and back. Nature 2006, 443:527-533.
9. Makarow M, Hojgaard L, Ceulemans R. European Science Foundation. Setting Science Agendas for Europe: Advancing Systems Biology for Medical Applications. ESF Science Policy Briefing 2008, 35:1-12.
10. Fuchs E. Beauty is skin deep: the fascinating biology of the epidermis and its appendages. Harvey Lect 1998, 94:47-77.
11. Schneider M R, Schmidt-Ullrich R, Paus R. The Hair Follicle as a Dynamic Miniorgan. Curr Biol 2009, 19:R132-R142.
12. Stenn K S, Paus R. Controls of Hair Follicle Cycling. Physiol Rev 2001, 81:449-494.
13. Paus R, Cotsarelis G. The Biology of Hair Follicles. N Eng J Med 1999, 341:491-497.
14. Fuchs E, Merrill B J, Jamora C, DasGupta R. At the roots of a never-ending cycle. Dev Cell 2001, 1:13-25.
15. Paus R, Foitzik K. In search of the ''hair cycle clock'': a guided tour. Differentiation 2004, 72:489-511.
16. Lin K K, Kumar V, Geyfman M. Circadian Clock Genes Contribute to the Regulation of Hair Follicle Cycling. PLoS Genet 2009, 5:e1000573.
17. Hadshiew I M, Foitzik K, Arck P C, Paus R. Burden of Hair Loss: Stress and the Underestimated Psychosocial Impact of Telogen Effluvium and Androgenetic Alopecia. J Invest Dermatol 2004, 123:455-457.
18. Cotsarelis G, Millar S E. Towards a molecular understanding of hair loss and its treatment. Trends Mol Med 2001, 7:293-301.
19. Ito M, Kizawa K, Hamada K, Cotsarelis G. 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 2004, 72:548-557.
20. Yu B D, Mukhopadhyay A, Wong C. Skin and hair: models for exploring organ regeneration. Hum Mol Genet 2008, 17:R54-R59.
21. Batista R T B, Ramirez D B, Santos R D, del Rosario M C I, Mendoza E R. EUCLIS-An information system for circadian systems biology. IET Syst Biol 2007, 1:266-273.
22. Schmidt-Ullrich R, Paus R. Molecular principles of hair follicle induction and morphogenesis. Bioessays 2005, 27:247-261.
23. MacArthur B D, Ma'ayan A, Lemischka I R. Systems biology of stem cell fate and cellular reprogramming. Nat Rev Mol Cell Biol 2009, 10:672-681.
24. Vanag V K, Epstein I R. Pattern formation mechanisms in reaction-diffusion systems. Int J Dev Biol 2009, 53:673-681.
25. Baker R E, Schnell S, Maini P K. Waves and patterning in developmental biology: vertebrate segmentation and feather bud formation as case studies. Int J Dev Biol 2009, 53:783-794.
26. Nagorcka B N, Mooney J R. The role of a reaction-diffusion system in the formation of hair fibres. J Theor Biol 1982, 98:575-607.
27. Nagorcka B N, Mooney J R. The role of a reaction-diffusion system in the initiation of primary hair follicles. J Theor Biol 1985, 114:243-272.
28. Mooney J R, Nagorcka B N. Spatial patterns produced by a reaction-diffusion system in primary hair follicles. J Theor Biol 1985, 115:299-317.
29. Sick S, Reinker S, Timmer J, Schlake T. WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism.[see comment]. Science 2006, 314:1447-1450.
30. Stark J, Andl T, Millar S E. Hairy Math: Insights into Hair-Follicle Spacing and Orientation. Cell 2007, 128:17-20.
31. Kitano H. Systems Biology: A brief overview. Science 2002, 295:1662-1664.
32. Aderem A. Systems Biology: Its Practice and Challenges. Cell 2005, 121:511-513.
33. O'Malley M A, Dupré J. Fundamental issues in systems biology. Bioessays 2005, 27:1270-1276.
34. Noble D. Prologue: Mind Over Molecule: Activating Biological Demons. Ann N Y Acad Sci 2008, 1123:xi-xix.
35. Rendl M, Lewis L, Fuchs E. Molecular Dissection of Mesenchymal-Epithelial Interactions in the Hair Follicle. PLoS Biol 2005, 3:e331.
36. Panteleyev A A, Jahoda C A B, Christiano A M. Hair follicle predetermination. J Cell Sci 2001, 114:3419-3431.
37. Nakamura M, Sundberg J P, Paus P. Mutant laboratory mice with abnormalities in hair follicle morphogenesis, cycling, and/or structure: annotated tables. Exp Dermatol 2001, 10:369-390.
38. Alonso L, Okada H, Pasolli H A. Sgk3 links growth factor signaling to maintenance of progenitor cells in the hair follicle. J Cell Biol 2005, 170:559-570.
39. Sundberg J P, Peters E M J, Paus R. Analysis of Hair Follicles in Mutant Laboratory Mice. J Investig Dermatol Symp Proc 2005, 10:264-270.
40. Mecklenburg L, Tobin D J, Cirlan M V, Craciun C, Paus R. Premature termination of hair follicle morphogenesis and accelerated hair follicle cycling in Iasi congenital atrichia (fzica) mice points to fuzzy as a key element of hair cycle control. Exp Dermatol 2005, 14:561-570.
41. Philpott M P, Sanders D, Westgate G E, Kealey T. Human hair growth in vitro: a model for the study of hair follicle biology. J Dermatol Sci 1994, 7(Suppl):S55-S72.
42. Kloepper J E, Sugawara K, Al-Nuaimi Y, Gáspár E, van Beek N, Paus R. Methods in hair research: how to objectively distinguish between anagen and catagen in human hair follicle organ culture. Exp Dermatol 2010, 19:305-312.
43. Bodo E, Biro T, Telek A. A hot new twist to hair biology: involvement of vanilloid receptor-1 (VR1/TRPV1) signaling in human hair growth control. Am J Pathol 2005, 166:985-998.
44. Bodo E, Tobin D J, Kamenisch Y. 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, 171:1153-1167.
45. Rogers G E, Hynd P I. Animal Models and Culture Methods in the Study of Hair Growth. Clin Dermatol 2001, 19:105-119.
46. Maurer M, Peters E M J, Botchkarev V A, Paus R. Intact hair follicle innervation is not essential for anagen induction and development. Arch Dermatol Res 1998, 290:574-578.
47. Philpott M P, Green M R, Kealey T. Human hair growth in vitro. J Cell Sci 1990, 97:463-471.
48. Philpott M P, Sanders D A, Kealey T. Whole hair follicle culture. Dermatol Clin 1996, 14:595-607.
49. Paus R, Muller-Rover S, Botchkarev V A. Chronobiology of the hair follicle: hunting the " hair cycle clock" J Investig Dermatol Symp Proc 1999, 4:338-345.
50. Plikus M V, Mayer J A, de la Cruz D. Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 2008, 451:340-344.
51. Plikus M V, Widelitz R B, Maxson R, Chuong C M. Analyses of regenerative wave patterns in adult hair follicle populations reveal macro-environmental regulation of stem cell activity. Int J Dev Biol 2009, 53:857-868.
52. Tobin D J, Gunin A, Magerl M, Handijski B, Paus R. Plasticity and cytokinetic dynamics of the hair follicle mesenchyme: implications for hair growth control. J Invest Dermatol 2003, 120:895-904.
53. Hu M, Polyak K. Molecular characterisation of the tumour microenvironment in breast cancer. Eur J Cancer 2008, 44:2760-2765.
54. Faratian D, Clyde R G, Crawford J W, Harrison D J. Systems pathology-taking molecular pathology into a new dimension. Nat Rev Clin Oncol 2009, 6:455-464.
55. Widelitz R B, Baker R E, Plikus M. Distinct Mechanisms Underlie Pattern Formation in the Skin and Skin Appendages. Birth Defects Res 2006, 78:280-291.
56. Chuong C M, Dhouailly D, Gilmore S. What is the biological basis of pattern formation of skin lesions? Exp Dermatol 2006, 15:547-564.
57. Rudman S M, Philpott M P, Thomas G A, Kealey T. The role of IGF-I in human skin and its appendages: morphogen as well as mitogen? J Invest Dermatol 1997, 109:770-777.
58. Jindo T, Tsuboi R, Takamori K, Ogawa H. Local injection of hepatocyte growth factor/scatter factor (HGF/SF) alters cyclic growth of murine hair follicles. J Invest Dermatol 1998, 110:338-342.
59. Jindo T, Tsuboi R, Imai R, Takamori K, Rubin J S, Ogawa H. The effect of hepatocyte growth factor/scatter factor on human hair follicle growth. J Dermatol Sci 1995, 10:229-232.
60. Lindner G, Menrad A, Gherardi E. Involvement of hepatocyte growth factor/scatter factor and met receptor signaling in hair follicle morphogenesis and cycling. FASEB J 2000, 14:319-332.
61. Kawano M, Komi-Kuramochi A, Asada M. Comprehensive analysis of FGF and FGFR expression in skin: FGF18 is highly expressed in hair follicles and capable of inducing anagen from telogen stage hair follicles. J Invest Dermatol 2005, 124:877-885.
62. Hebert J M, Rosenquist T, Gotz J, Martin G R. FGF5 as a regulator of the hair growth cycle: evidence from targeted and spontaneous mutations. Cell 1994, 78:1017-1025.
63. Rosenquist T A, Martin G R. Fibroblast growth factor signalling in the hair growth cycle: expression of the fibroblast growth factor receptor and ligand genes in the murine hair follicle. Dev Dyn 1996, 205:379-386.
64. Botchkarev V A, Botchkareva N V, Welker P. A new role for neurotrophins: involvement of brain-derived neurotrophic factor and neurotrophin-4 in hair cycle control. FASEB J 1999, 13:395-410.
65. Botchkarev V A, Welker P, Albers K M. A New Role for Neurotrophin-3. Involvement in the Regulation of Hair Follicle Regression (Catagen). Am J Pathol 1998, 153:785-799.
66. Stenn K S, Prouty S M, Seiberg M. Molecules of the cycling hair follicle - a tabulated review. J Dermatol Sci 1994, 7(Suppl):S109-S124.
67. Thibaut S, Collin C, Langbein L, Schweizer J, Gautier B, Bernard B A. Hair keratin pattern in human hair follicles grown in vitro. Exp Dermatol 2003, 12:160-164.
68. Whiting D A. The Structure of the Human Hair Follicle. Light Microscopy of Vertical and Horizontal Sections of Scalp Biopsies 2004, Fairfield, Canfield Publishing
69. Whittington M A, Traubb R D, Kopellc N, Ermentroutd B, Buhl E H. Inhibition-based rhythms: experimental and mathematical observations on network dynamics. Int J Psychophysiol 2000, 38:315-336.
70. Zanello S B, Jackson D M, Holick M F. Expression of the Circadian Clock Genes clock and period1 in Human Skin. J Invest Dermatol 2000, 115:757-760.
71. Bjarnson G A, Jordan R C K, Wood P A. Circadian Expression of Clock Genes in Human Oral Mucosa and Skin Association with Specific Cell-Cycle Phases. Am J Pathol 2001, 158:1793-1801.
72. Bjarnson G A, Jordan R. Rhythms in Human Gastrointestinal Mucosa and Skin. Chronobiol Int 2002, 19:129-140.
73. Kawara S, Mydlarski R, Mamelak A J. Low-dose Ultraviolet B Rays Alter the mRNA Expression of the Circadian Clock Genes in Cultured Human Keratinocytes. J Invest Dermatol 2002, 119:1220-1223.
74. Mehling A, Fluhr J W. Chronobiology: Biological Clocks and Rhythms of the Skin. Skin Pharmacol Physiol 2006, 19:182-189.
75. Tanioka M, Yamada H, Doi M. Molecular Clocks in Mouse Skin. J Invest Dermatol 2009, 129:1225-1232.
76. Lin K K, Chudova D, Hatfield G W, Smyth P, Andersen B. Identification of hair cycle-associated genes from time-course gene expression profile data by using replicate variance. Proc Natl Acad Sci USA 2004, 101:15955-15960.
77. Halloy J, Bernard B A, Loussouarn G, Goldbeter A. Modeling the dynamics of human hair cycles by a follicular automaton. Proc Natl Acad Sci USA 2000, 97:8328-8333.
78. Halloy J, Bernard B A, Loussouarn G, Goldbeter A. The follicular automaton model: effect of stochasticity and of synchronization of hair cycles. J Theor Biol 2002, 214:469-479.
79. Ma L, Liu J, Wu T. 'Cyclic alopecia' in Msx2 mutants: defects in hair cycling and hair shaft differentiation. Development 2003, 130:379-389.
80. Suzuki N, Hirata M, Kondo S. Traveling stripes on the skin of a mutant mouse. PNAS 2003, 100:9680-9685.
81. Jimenez F, Ruifernández J M. Distribution of Human Hair in Follicular Units. Dermatol Surg 1999, 25:294-298.
82. Kolinko V, Littler C M. Mathematical modeling for the prediction and optimization of laser hair removal. Lasers Surg Med 2000, 26:164-176.
83. Al-Nuaimi Y, Philpott M, Kloepper J. A role for clock-related genes in human hair growth control? J Invest Dermatol 2009, 129:S67.