Dissecting the bulge in hair regeneration

Journal of Clinical Investigation

Volumn 122, Issue 2, 2012, Pages 448-454

  Myung, Peggy ^a   Ito, Mayumi ^b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL MEMBRANE POTENTIAL; CELL POPULATION; CELL PROLIFERATION; CELL STRUCTURE; EPIDERMIS; EPITHELIUM CELL; HAIR FOLLICLE; HAIR GROWTH; HUMAN; NONHUMAN; PIGMENTATION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; HAIR FOLLICLE; HUMANS; MELANOCYTES; REGENERATION; STEM CELL NICHE; STEM CELLS;

EID: 84856526083     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI57414     Document Type: Review

References (65)

1. Mackenzie I. Relationship between mitosis and the ordered structure of the stratum corneum in mouse epidermis. Nature. 1970;226(5246):653-655.
2. Potten C. The epidermal proliferative unit: the possible role of the central basal cell. Cell Tissue Kinet. 1974;7(1):77-88.
3. Cotsarelis G. Epithelial stem cells: A folliculocentric view. J invest Dermatol. 2006;126(7):1459-1468.
4. Paus R, Cotsarelis G. The biology of hair follicles. N Engl J Med. 1999;341(7):491-497. (Pubitemid 29372890)
5. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell. 2004;118(5):635-648. (Pubitemid 39179715)
6. Morris RJ, et al. Capturing and profiling adult hair follicle stem cells. Nat Biotechnol. 2004;22(4):411-417. (Pubitemid 38451371)
7. Oshima H, Rochat A, Kedzia C, Kobayashi K, Barrandon Y. Morphogenesis and renewal of hair follicles from adult multipotent stem cells. Cell. 2001;104(2):233-245. (Pubitemid 32174839)
8. Ito M, et al. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med. 2005;11(12):1351-1354. (Pubitemid 41752917)
9. Levy V, Lindon C, Harfe BD, Morgan BA. Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev Cell. 2005;9(6):855-861. (Pubitemid 41724112)
10. Taylor G, Lehrer MS, Jensen PJ, Sun TT, Lavker RM. Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell. 2000;102(4):451-461.
11. Tumbar T, et al. Defining the epithelial stem cell niche in skin. Science. 2004;303(5656):359-363. (Pubitemid 38095773)
12. 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(7):1329-1337.
13. Lyle S, Christofidou-Solomidou M, Liu Y, Elder DE, Albelda S, Cotsarelis G. The C8/144B monoclonal antibody recognizes cytokeratin 15 and defines the location of human hair follicle stem cells. J Cell Sci. 1998;111(pt 21):3179-3188. (Pubitemid 28532428)
14. Trempus CS, et al. Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J Invest Dermatol. 2003;120(4):501-511. (Pubitemid 36343991)
15. Horsley V, Aliprantis AO, Polak L, Glimcher LH, Fuchs E. NFATc1 balances quiescence and proliferation of skin stem cells. Cell. 2008;132(2):299-310. (Pubitemid 351172432)
16. Jaks V, et al. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet. 2008;40(11):1291-1299.
17. Nguyen H, Rendl M, Fuchs E. Tcf3 governs stem cell features and represses cell fate determination in skin. Cell. 2006;127(1):171-183. (Pubitemid 44466637)
18. Nowak JA, Polak L, Pasolli HA, Fuchs E. Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell. 2008;3(1):33-43.
19. Rhee H, Polak L, Fuchs E. Lhx2 maintains stem cell character in hair follicles. Science. 2006;312(5782):1946-1949. (Pubitemid 43993720)
20. Vidal VP, et al. Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment. Curr Biol. 2005;15(15):1340-1351. (Pubitemid 41097538)
21. Horsley V, et al. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell. 2006;126(3):597-609. (Pubitemid 44163616)
22. Ito M, Kizawa K, Toyoda M, Morohashi 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(6):1310-1316. (Pubitemid 36005614)
23. Jensen KB, et al. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell. 2009;4(5):427-439.
24. Snippert HJ, et al. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science. 2010;327(5971):1385-1389.
25. Stohr P. Entwicklungsgeschichte des menschlichen wollhaares. Anat Hefte Abt 1. 1904;23:1-66.
26. Unna P. Beitrage zur histologie und entwicklungsgeschichte der menschlichen oberhaut und ihrer anhangsgebilde. Arch mikroskop Anat Entwicklungsmech. 1876;12:665-741.
27. Madsen A. Studies on the "bulge" (wulst) in superficial basal epitheliomas. Arch Dermatol. 1964;89:698-708.
28. Pinkus H. Embryology Of Hair. New York, New York, USA: Academy Press; 1958.
29. Liu Y, Lyle S, Yang Z, Cotsarelis G. Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J Invest Dermatol. 2003;121(5):963-968. (Pubitemid 37430960)
30. Chase HB, Rauch R, Smith VW. Critical stages of hair development and pigmentation in the mouse. Physiol Zool. 1951;24(1):1-8.
31. Silver AF, Chase HB. DNA synthesis in the adult hair germ during dormancy (telogen) and activation (early anagen). Dev Biol. 1970;21(3):440-451.
32. Silver AF, Chase HB, Arsenault CT. Early anagen initiated by plucking compared with early spontaneous anagen. In: Montagna W, Kenshalo DR, eds. Advances in Biology of Skin. Vol. 9. London, United Kingdom: Pergamon Press; 1967:265-289.
33. Ito M, Kizawa K. 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. 2001;116(6):956-963. (Pubitemid 32554384)
34. 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(9-10):548-557. (Pubitemid 41702109)
35. Greco V, et al. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell. 2009;4(2):155-169.
36. Zhang YV, Cheong J, Ciapurin N, McDermitt DJ, Tumbar T. Distinct self-renewal and differentiation phases in the niche of infrequently dividing hair follicle stem cells. Cell Stem Cell. 2009;5(3):267-278.
37. Nishimura EK, et al. Dominant role of the niche in melanocyte stem-cell fate determination. Nature. 2002;416(6883):854-860. (Pubitemid 34453742)
38. Hsu YC, Pasolli HA, Fuchs E. Dynamics between stem cells, niche, and progeny in the hair follicle. Cell. 2011;144(1):92-105.
39. Millar S. Molecular mechanisms regulating hair follicle development. J Invest Dermatol. 2002;118(2):216-225. (Pubitemid 34158473)
40. Schmidt-Ullrich R, Paus R. Molecular principles of hair follicle induction and morphogenesis. Bioessays. 2005;27(3):247-261. (Pubitemid 40476488)
41. Merrill BJ, Gat U, DasGupta R, Fuchs E. Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev. 2001;15(13):1688-1705. (Pubitemid 32702590)
42. Nishimura EK, Granter SR, Fisher DE. Mechanisms of hair graying: incomplete melanocyte stem cell maintenance in the niche. Science. 2005;307(5710):720-724. (Pubitemid 40194641)
43. Tanimura S, et al. Hair follicle stem cells provide a functional niche for melanocyte stem cells. Cell Stem Cell. 2011;8(2):177-187.
44. Rabbani P, et al. Coordinated activation of Wnt in epithelial and melanocyte stem cells initiates pigmented hair regeneration. Cell. 2011;145(6):941-955.
45. Billingham RE, Russell PS. Incomplete wound contracture and the phenomenon of hair neogenesis in rabbits' skin. Nature. 1956;177(4513):791-792.
46. Breedis C. Regeneration of hair follicles and sebaceous glands from the epithelium of scars in the rabbit. Cancer Res. 1954;14(8):575-579.
47. Kligman AM, Strauss JS. The formation of vellus hair follicles from human adult epidermis. J Invest Dermatol. 1956;27(1):19-23.
48. Lacassagne A, Latarjet R. Action of methylcholanthrene on certain scars of the skin in mice. Cancer Res. 1946;6:183-188.
49. Ito M, et al. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature. 2007;447(7142):316-320. (Pubitemid 46788832)
50. Nijhof JG, et al. The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells. Development. 2006;133(15):3027-3037. (Pubitemid 44314279)
51. Brownell I, Guevara E, Bai CB, Loomis CA, Joyner AL. Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell. 2011;8(5):552-565.
52. Sellheyer K, Krahl D. Blimp-1: a marker of terminal differentiation but not of sebocytic progenitor cells. J Cutan Pathol. 2010;37(3):362-370.
53. Ortonne JP, MacDonald DM, Micoud A, Thivolet J. PUVA-induced repigmentation of vitiligo: a histochemical (split-DOPA) and ultrastructural study. Br J Dermatol. 1979;101(1):1-12. (Pubitemid 10134309)
54. Mobini N, Tam S, Kamino H. Possible role of the bulge region in the pathogenesis of inflammatory scarring alopecia: lichen planopilaris as the prototype. J Cutan Pathol. 2005;32(10):675-679. (Pubitemid 41719747)
55. Garza LA, et al. 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(2):613-622.
56. Miller DL, Weinstock MA. Nonmelanoma skin cancer in the United States: incidence. J Am Acad Dermatol. 1994;30(5 pt 1):774-778. (Pubitemid 24157120)
57. Leiter U, Garbe C. Epidemiology of melanoma and nonmelanoma skin cancer - the role of sunlight. Adv Exp Med Biol. 2008;624:89-103.
58. Rubin AI, Chen EH, Ratner D. Basal-cell carcinoma. N Engl J Med. 2005;353(21):2262-2269. (Pubitemid 41697289)
59. Epstein EH. Basal cell carcinomas: attack of the hedgehog. Nat Rev Cancer. 2008;8(10):743-754.
60. Teglund S, Toftgard R. Hedgehog beyond medulloblastoma and basal cell carcinoma. Biochim Biophys Acta. 2010;1805(2):181-208.
61. Youssef KK, et al. Identification of the cell lineage at the origin of basal cell carcinoma. Nat Cell Biol. 2010;12(3):299-305.
62. Wang GY, Wang J, Mancianti ML, Epstein EH Jr. Basal cell carcinomas arise from hair follicle stem cells in Ptch1(+/-) mice. Cancer Cell. 2011;19(1):114-124.
63. Grachtchouk M, et al. Basal cell carcinomas in mice arise from hair follicle stem cells and multiple epithelial progenitor populations. J Clin Invest. 2011;121(5):1768-1781.
64. Gupta S, Takebe N, Lorusso P. Targeting the Hedgehog pathway in cancer. Ther Adv Med Oncol. 2010;2(4):237-250.
65. Kiesslich T, et al. Current status of therapeutic targeting of developmental signalling pathways in oncology [published online ahead of print May 24, 2011]. Curr Pharm Biotechnol. doi:10.2174/1389211216050742010.