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Therapeutic strategy for hair regeneration: hair cycle activation, niche environment modulation, wound-induced follicle neogenesis, and stem cell engineering

, , , , , , , , MD & , MD PhD show all
Pages 377-391 | Published online: 05 Jan 2013

Bibliography

  • Garza LA, Yang CC, Zhao T, Bald scalp in men with androgenetic alopecia retains hair follicle stem cells but lacks CD200-rich and CD34-positive hair follicle progenitor cells. J Clin Invest 2011;121:613-22
  • Gallico GG III, O'Connor NE, Compton CC, Permanent coverage of large burn wounds with autologous cultured human epithelium. N Engl J Med 1984;311:448-51
  • Rosenfield RL. Clinical practice. Hirsutism. N Engl J Med 2005;353:2578-88
  • Chamcheu JC, Siddiqui IA, Syed DN, Keratin gene mutations in disorders of human skin and its appendages. Arch Biochem Biophys 2011;508:123-37
  • Hardy MH. The secret life of the hair follicle. Trends Genet 1992;8:55-61
  • Schmidt-Ullrich R, Paus R. Molecular principles of hair follicle induction and morphogenesis. Bioessays 2005;27:247-61
  • Fuchs E. Scratching the surface of skin development. Nature 2007;445:834-42
  • Chuong CM. Molecular basis of epithelial appendage morphognesis. Molecular biology intelligence unit 1. R.G. Landes; Austin, Tex: 1998
  • Kligman AM, Strauss JS. The formation of vellus hair follicles from human adult epidermis. J Invest Dermatol 1956;27:19-23
  • Greco V, Chen T, Rendl M, A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 2009;4:155-69
  • Hsu YC, Pasolli HA, Fuchs E. Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 2011;144:92-105
  • Stenn KS, Paus R. Controls of hair follicle cycling. Physiol Rev 2001;81:449-94
  • Fuchs E, Merrill BJ, Jamora C, At the roots of a never-ending cycle. Dev Cell 2001;1:13-25
  • Kimura-Ueki M, Oda Y, Oki J, Hair cycle resting phase is regulated by cyclic epithelial FGF18 signaling. J Invest Dermatol 2012;132:1338-45
  • Ragone G, Bresin A, Piermarini F, The Tcl1 oncogene defines secondary hair germ cells differentiation at catagen-telogen transition and affects stem-cell marker CD34 expression. Oncogene 2009;28:1329-38
  • Sato N, Leopold PL, Crystal RG. Induction of the hair growth phase in postnatal mice by localized transient expression of Sonic hedgehog. J Clin Invest 1999;104:855-64
  • Woo WM, Oro AE. SnapShot: hair follicle stem cells. Cell 2011;146:334-334 e2
  • Botchkarev VA, Paus R. Molecular biology of hair morphogenesis: development and cycling. J Exp Zool B Mol Dev Evol 2003;298:164-80
  • Ohyama M, Zheng Y, Paus R, The mesenchymal component of hair follicle neogenesis: background, methods and molecular characterization. Exp Dermatol 2010;19:89-99
  • Morris RJ, Liu Y, Marles L, Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 2004;22:411-17
  • Tumbar T, Guasch G, Greco V, Defining the epithelial stem cell niche in skin. Science 2004;303:359-63
  • Kishimoto J, Burgeson RE, Morgan BA. Wnt signaling maintains the hair-inducing activity of the dermal papilla. Genes Dev 2000;14:1181-5
  • Enshell-Seijffers D, Lindon C, Kashiwagi M, beta-catenin activity in the dermal papilla regulates morphogenesis and regeneration of hair. Dev Cell 2010;18:633-42
  • Driskell RR, Giangreco A, Jensen KB, Sox2-positive dermal papilla cells specify hair follicle type in mammalian epidermis. Development 2009;136:2815-23
  • Chuong CM, Randall VA, Widelitz RB, Physiological regeneration of skin appendages and implications for regenerative medicine. Physiology (Bethesda) 2012;27:61-72
  • Plikus MV, Mayer JA, de la Cruz D, Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 2008;451:340-4
  • Festa E, Fretz J, Berry R, Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 2011;146:761-71
  • Chen CC, Chuong CM. Multi-layered environmental regulation on the homeostasis of stem cells: the saga of hair growth and alopecia. J Dermatol Sci 2012;66:3-11
  • Garza LA, Liu Y, Yang Z, Prostaglandin D2 inhibits hair growth and is elevated in bald scalp of men with androgenetic alopecia. Sci Transl Med 2012;4:126ra34
  • Oh HS, Smart RC. An estrogen receptor pathway regulates the telogen-anagen hair follicle transition and influences epidermal cell proliferation. Proc Natl Acad Sci USA 1996;93:12525-30
  • Wallace ML, Smoller BR. Estrogen and progesterone receptors in androgenic alopecia versus alopecia areata. Am J Dermatopathol 1998;20:160-3
  • Plikus MV, Baker RE, Chen CC, Self-organizing and stochastic behaviors during the regeneration of hair stem cells. Science 2011;332:586-9
  • Courtois M, Loussouarn G, Hourseau C, Hair cycle and alopecia. Skin Pharmacol 1994;7:84-9
  • Azziz R, Carmina E, Sawaya ME. Idiopathic hirsutism. Endocr Rev 2000;21:347-62
  • Reingold SB, Rosenfield RL. The relationship of mild hirsutism or acne in women to androgens. Arch Dermatol 1987;123:209-12
  • Paus R, Cotsarelis G. The biology of hair follicles. N Engl J Med 1999;341:491-7
  • Hoffmann R, Happle R. Current understanding of androgenetic alopecia. Part I: etiopathogenesis. Eur J Dermatol 2000;10:319-27
  • Hibberts NA, Howell AE, Randall VA. Balding hair follicle dermal papilla cells contain higher levels of androgen receptors than those from non-balding scalp. J Endocrinol 1998;156:59-65
  • Inui S, Fukuzato Y, Nakajima T, Androgen-inducible TGF-beta1 from balding dermal papilla cells inhibits epithelial cell growth: a clue to understand paradoxical effects of androgen on human hair growth. FASEB J 2002;16:1967-9
  • Kwack MH, Sung YK, Chung EJ, Dihydrotestosterone-inducible dickkopf 1 from balding dermal papilla cells causes apoptosis in follicular keratinocytes. J Invest Dermatol 2008;128:262-9
  • Randall VA, Hibberts NA, Hamada K. A comparison of the culture and growth of dermal papilla cells from hair follicles from non-balding and balding (androgenetic alopecia) scalp. Br J Dermatol 1996;134:437-44
  • Bahta AW, Farjo N, Farjo B, Premature senescence of balding dermal papilla cells in vitro is associated with p16(INK4a) expression. J Invest Dermatol 2008;128:1088-94
  • Winiarska A, Mandt N, Kamp H, Effect of 5alpha-dihydrotestosterone and testosterone on apoptosis in human dermal papilla cells. Skin Pharmacol Physiol 2006;19:311-21
  • Hamada K, Randall VA. Inhibitory autocrine factors produced by the mesenchyme-derived hair follicle dermal papilla may be a key to male pattern baldness. Br J Dermatol 2006;154:609-18
  • Hamilton JB. Male hormone stimulation is a prerequisite and an incitant in common baldness. Am J Anat 1942;71:451-80
  • Imperato-McGinley J, Guerrero L, Gautier T, Steroid 5alpha-reductase deficiency in man: an inherited form of male pseudohermaphroditism. Science 1974;186:1213-15
  • Ellis JA, Sinclair R, Harrap SB. Androgenetic alopecia: pathogenesis and potential for therapy. Expert Rev Mol Med 2002;4:1-11
  • Klemp P, Peters K, Hansted B. Subcutaneous blood flow in early male pattern baldness. J Invest Dermatol 1989;92:725-6
  • Hillmer AM, Hanneken S, Ritzmann S, Genetic variation in the human androgen receptor gene is the major determinant of common early-onset androgenetic alopecia. Am J Hum Genet 2005;77:140-8
  • Hillmer AM, Brockschmidt FF, Hanneken S, Susceptibility variants for male-pattern baldness on chromosome 20p11. Nat Genet 2008;40:1279-81
  • Paus R, Handjiski B, Eichmuller S, Chemotherapy-induced alopecia in mice. Induction by cyclophosphamide, inhibition by cyclosporine A, and modulation by dexamethasone. Am J Pathol 1994;144:719-34
  • Matsuo K, Mori O, Hashimoto T. Plucking during telogen induces apoptosis in the lower part of hair follicles. Arch Dermatol Res 2003;295:33-7
  • Silver AF, Chase HB, Arsenault CT. Early anagen initiated by plucking compared with early spontaneous anagen. Adv Biol Skin 1967;9:265-86
  • Cotsarelis G, Sun TT, Lavker RM. Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 1990;61:1329-37
  • Lavker RM, Sun TT. Hair follicle stem cells: present concepts. J Invest Dermatol 1995;104:38S-9S
  • Morris RJ, Potten CS. Highly persistent label-retaining cells in the hair follicles of mice and their fate following induction of anagen. J Invest Dermatol 1999;112:470-5
  • Ito M, Kizawa K, Toyoda M, 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 2002;119:1310-16
  • Yang CC, Cotsarelis G. Review of hair follicle dermal cells. J Dermatol Sci 2010;57:2-11
  • Jahoda CA, Horne KA, Oliver RF. Induction of hair growth by implantation of cultured dermal papilla cells. Nature 1984;311:560-2
  • Jahoda CA. Induction of follicle formation and hair growth by vibrissa dermal papillae implanted into rat ear wounds: vibrissa-type fibres are specified. Development 1992;115:1103-9
  • Reynolds AJ, Lawrence C, Cserhalmi-Friedman PB, Trans-gender induction of hair follicles. Nature 1999;402:33-4
  • Zheng Y, Du X, Wang W, Organogenesis from dissociated cells: generation of mature cycling hair follicles from skin-derived cells. J Invest Dermatol 2005;124:867-76
  • Weinberg WC, Goodman LV, George C, Reconstitution of hair follicle development in vivo: determination of follicle formation, hair growth, and hair quality by dermal cells. J Invest Dermatol 1993;100:229-36
  • Jahoda CA, Oliver RF, Reynolds AJ, Trans-species hair growth induction by human hair follicle dermal papillae. Exp Dermatol 2001;10:229-37
  • Ehama R, Ishimatsu-Tsuji Y, Iriyama S, Hair follicle regeneration using grafted rodent and human cells. J Invest Dermatol 2007;127:2106-15
  • Gibson WT, Westgate GE, Craggs RI. Immunology of the hair follicle. Ann N Y Acad Sci 1991;642:291-300
  • Streilein JW. Unraveling immune privilege. Science 1995;270:1158-9
  • Ito M, Yang Z, Andl T, Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 2007;447:316-20
  • Chuong CM. Regenerative biology: new hair from healing wounds. Nature 2007;447:265-6
  • Seifert AW, Kiama SG, Seifert MG, Skin shedding and tissue regeneration in African spiny mice (Acomys). Nature 2012;489:561-5
  • Lacassagne A, Latarjet R. Action of methylcholanthrene on certain scars of the skin in mice. Cancer Res 1946;6:183-8
  • Breedis C. Regeneration of hair follicles and sebaceous glands from the epithelium of scars in the rabbit. Cancer Res 1954;14:575-9
  • Billingham RE, Russell PS. Incomplete wound contracture and the phenomenon of hair neogenesis in rabbits' skin. Nature 1956;177:791-2
  • Davies GC, Thornton MJ, Jenner TJ, Novel and established potassium channel openers stimulate hair growth in vitro: implications for their modes of action in hair follicles. J Invest Dermatol 2005;124:686-94
  • Bishop GH. Regeneration after experimental removal of skin in man. Am J Anat 1945;76:153-81
  • Martinot V, Mitchell V, Fevrier P, Comparative study of split thickness skin grafts taken from the scalp and thigh in children. Burns 1994;20:146-50
  • Langton AK, Herrick SE, Headon DJ. An extended epidermal response heals cutaneous wounds in the absence of a hair follicle stem cell contribution. J Invest Dermatol 2008;128:1311-18
  • Ito M, Cotsarelis G. Is the hair follicle necessary for normal wound healing? J Invest Dermatol 2008;128:1059-61
  • Ito M, Liu Y, Yang Z, Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 2005;11:1351-4
  • Levy V, Lindon C, Zheng Y, Epidermal stem cells arise from the hair follicle after wounding. FASEB J 2007;21:1358-66
  • Nowak JA, Polak L, Pasolli HA, Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 2008;3:33-43
  • Fernandes KJ, McKenzie IA, Mill P, A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 2004;6:1082-93
  • Toma JG, McKenzie IA, Bagli D, Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 2005;23:727-37
  • Vierbuchen T, Ostermeier A, Pang ZP, Direct conversion of fibroblasts to functional neurons by defined factors. Nature 2010;463:1035-41
  • Huang P, He Z, Ji S, Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors. Nature 2011;475:386-9
  • Kishimoto J, Ehama R, Wu L, Selective activation of the versican promoter by epithelial- mesenchymal interactions during hair follicle development. Proc Natl Acad Sci USA 1999;96:7336-41
  • Enshell-Seijffers D, Lindon C, Morgan BA. The serine protease Corin is a novel modifier of the Agouti pathway. Development 2008;135:217-25
  • Chi WY, Enshell-Seijffers D, Morgan BA. De novo production of dermal papilla cells during the anagen phase of the hair cycle. J Invest Dermatol 2010;130:2664-6
  • Lichti U, Weinberg WC, Goodman L, In vivo regulation of murine hair growth: insights from grafting defined cell populations onto nude mice. J Invest Dermatol 1993;101:124S-9S
  • Lichti U, Anders J, Yuspa SH. Isolation and short-term culture of primary keratinocytes, hair follicle populations and dermal cells from newborn mice and keratinocytes from adult mice for in vitro analysis and for grafting to immunodeficient mice. Nat Protoc 2008;3:799-810
  • Lee LF, Jiang TX, Garner W, A simplified procedure to reconstitute hair-producing skin. Tissue Eng Part C Methods 2011;17:391-400
  • Inamatsu M, Matsuzaki T, Iwanari H, Establishment of rat dermal papilla cell lines that sustain the potency to induce hair follicles from afollicular skin. J Invest Dermatol 1998;111:767-75
  • Osada A, Iwabuchi T, Kishimoto J, Long-term culture of mouse vibrissal dermal papilla cells and de novo hair follicle induction. Tissue Eng 2007;13:975-82
  • Rendl M, Polak L, Fuchs E. BMP signaling in dermal papilla cells is required for their hair follicle-inductive properties. Genes Dev 2008;22:543-57
  • Young TH, Lee CY, Chiu HC, Self-assembly of dermal papilla cells into inductive spheroidal microtissues on poly(ethylene-co-vinyl alcohol) membranes for hair follicle regeneration. Biomaterials 2008;29:3521-30
  • Young TH, Tu HR, Chan CC, The enhancement of dermal papilla cell aggregation by extracellular matrix proteins through effects on cell-substratum adhesivity and cell motility. Biomaterials 2009;30:5031-40
  • Yen CM, Chan CC, Lin SJ. High-throughput reconstitution of epithelial-mesenchymal interaction in folliculoid microtissues by biomaterial-facilitated self-assembly of dissociated heterotypic adult cells. Biomaterials 2010;31:4341-52
  • Plikus MV, Widelitz RB, Maxson R, Analyses of regenerative wave patterns in adult hair follicle populations reveal macro-environmental regulation of stem cell activity. Int J Dev Biol 2009;53:857-68

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