Hedgehog signaling maintains hair follicle stem cell phenotype in young and aged human skin

Aging Cell

Volumn 8, Issue 6, 2009, Pages 738-751

  Rittié, Laure ^a   Stoll, Stefan W ^a   Kang, Sewon ^a   Voorhees, John J ^a   Fisher, Gary J ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

Bulge; CD200; Hair follicle; Hedgehog; Skin; Stem cells

Indexed keywords

CALVASCULIN; CD200 ANTIGEN; CELL PROTEIN; CONNECTIVE TISSUE GROWTH FACTOR; DICKKOPF 3 PROTEIN; DICKKOPF 4 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; LENTIVIRUS VECTOR; PROTEIN GAS1; PROTEIN KRT15; PROTEIN KRT19; SONIC HEDGEHOG PROTEIN; T CELL FACTOR PROTEIN; T CELL FACTOR PROTEIN 3; TRANSCRIPTION FACTOR GLI1; UNCLASSIFIED DRUG; ANTIGENS, CD200; CELL CYCLE PROTEIN; CYTOKERATIN 15; GAS1 PROTEIN, HUMAN; KRT15 PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; MEMBRANE PROTEIN;

ADULT; AGED; AGING; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; CELL SELECTION; CONTROLLED STUDY; CUTANEOUS PARAMETERS; GENE EXPRESSION PROFILING; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HAIR FOLLICLE; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; PHENOTYPE; PRIORITY JOURNAL; SCALP; SIGNAL TRANSDUCTION; STEM CELL; CELL SEPARATION; CYTOLOGY; METABOLISM;

ERINACEIDAE; LENTIVIRUS;

ADULT; AGED; AGING; ANTIGENS, CD; CELL CYCLE PROTEINS; CELL SEPARATION; HAIR FOLLICLE; HEDGEHOG PROTEINS; HUMANS; KERATIN-15; KERATINOCYTES; MEMBRANE PROTEINS; STEM CELLS;

EID: 74049092761     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2009.00526.x     Document Type: Article

References (71)

1. Adolphe C, Narang M, Ellis T, Wicking C, Kaur P, Wainwright B (2004) An in vivo comparative study of sonic, desert and Indian hedgehog reveals that hedgehog pathway activity regulates epidermal stem cell homeostasis. Development 131, 5009-5019.
2. Athar M, Tang XW, Lee JL, Kopelovich L, Kim AL (2006) Hedgehog signalling in skin development and cancer. Exp. Dermatol. 15, 667-677.
3. Barrandon Y, Green H (1987) Three clonal types of keratinocyte with different capacities for multiplication. Proc. Natl Acad. Sci. USA 84, 2302-2306.
4. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E (2004) Selfrenewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118, 635-648.
5. Boyer MJ, Cheng T (2008) The CDK inhibitors: potential targets for therapeutic stem cell manipulations? Gene Ther. 15, 117-125.
6. Chuang PT, McMahon AP (1999) Vertebrate hedgehog signalling modulated by induction of a hedgehog-binding protein. Nature 397, 617-621.
7. Claudinot S, Nicolas M, Oshima H, Rochat A, Barrandon Y (2005) Long-term renewal of hair follicles from clonogenic multipotent stem cells. Proc. Natl Acad. Sci. USA 102, 14677-14682.
8. Commo S, Bernard BA (1997) Immunohistochemical analysis of tissue remodelling during the anagen-catagen transition of the human hair follicle. Br. J. Dermatol. 137, 31-38.
9. Conboy IM, Conboy MJ, Smythe GM, Rando TA (2003) Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575-1577.
10. Cotsarelis G, Sun TT, Lavker RM (1990) Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61, 1329-1337.
11. Di Marcotullio L, Ferretti E, Greco A, De Smaele E, Po A, Sico MA, Alimandi M, Giannini G, Maroder M, Screpanti I, Gulino A (2006) Numb is a suppressor of hedgehog signalling and targets Gli1 for Itch-dependent ubiquitination. Nat. Cell Biol. 8, 1415-1423.
12. Dickson MA, Hahn WC, Ino Y, Ronfard V, Wu JY, Weinberg RA, Louis DN, Li FP, Rheinwald JG (2000). Human keratinocytes that express hTERT and also bypass a p16(INK4a)-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristicsMol. Cell. Biol. 20, 1436-1447.
13. Dierks C, Beigi R, Guo G-R, Zirlik K, Stegert MR, Manley P, Trussell C, Schmitt-Graeff A, Landwerlin K, Veelken H, Warmuth M (2008) Expansion of Bcr-Abl-positive leukemic stem cells is dependent on hedgehog pathway activation. Cancer Cell 14, 238-249.
14. Edelberg JM, Ballard VL (2008). Stem cell review series: regulating highly potent stem cells in aging: environmental influences on plasticity. Aging Cell 7, 599-604.
15. Fiuraskova M, Brychtova S, Kolar Z, Kucerova R, Bienova M (2005) Expression of beta-catenin, p63 and CD34 in hair follicles during the course of androgenetic alopecia. Arch. Dermatol. Res. 297, 143-146.
16. Fuchs E (2008) Skin stem cells: rising to the surface. J. Cell Biol. 180, 273-284.
17. Ghali L, Wong ST, Green J, Tidman N, Quinn AG (1999) Gli1 protein is expressed in basal cell carcinomas, outer root sheath keratinocytes and a subpopulation of mesenchymal cells in normal human skin. J. Invest. Dermatol. 113, 595-599.
18. Giangreco A, Qin M, Pintar JE, Watt FM (2008) Epidermal stem cells are retained in vivo throughout skin aging. Aging Cell 7, 250-259.
19. Gritli-Linde A, Hallberg K, Harfe BD, Reyahi A, Kannius-Janson M, Nilsson J, Cobourne MT, Sharpe PT, McMahon AP, Linde A (2007) Abnormal hair development and apparent follicular transformation to mammary gland in the absence of hedgehog signaling. Dev. Cell 12, 99-112.
20. Grotendorst GR, Okochi H, Hayashi N (1996) A novel transforming growth factor beta response element controls the expression of the connective tissue growth factor gene. Cell Growth Differ. 7, 469-480.
21. Ingham PW, McMahon AP (2001) Hedgehog signaling in animal development: paradigms and principles. Genes Dev. 15, 3059-3087.
22. Iseki S, Araga A, Ohuchi H, Nohno T, Yoshioka H, Hayashi F, Noji S (1996) Sonic hedgehog is expressed in epithelial cells during development of whisker, hair, and tooth. Biochem. Biophys. Res. Commun. 218, 688-693.
23. Ito M, Liu Y, Yang Z, Nguyen J, Liang F, Morris RJ, Cotsarelis G (2005) Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat. Med. 11, 1351-1354.
24. Jaks V, Barker N, Kasper M, van EsJH, Snippert HJ, Clevers H, Toftgard R (2008) Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat. Genet. 40, 1291-1299.
25. INK4a. Nature 443, 421-426.
26. Kasper M, Schnidar H, Neill GW, Hanneder M, Klingler S, Blaas L, Schmid C, Hauser-Kronberger C, Regl G, Philpott MP, Aberger F (2006) Selective modulation of Hedgehog/GLI target gene expression by epidermal growth factor signaling in human keratinocytes. Mol. Cell. Biol. 26, 6283-6298.
27. Katoh Y, Katoh M (2006) Hedgehog signaling pathway and gastrointestinal stem cell signaling network (review). Int. J. Mol. Med. 18, 1019-1023.
28. Kloepper JE, Tiede S, Brinckmann J, Reinhardt DP, Meyer W, Faessler R, Paus R (2008) Immunophenotyping of the human bulge region: the quest to define useful in situ markers for human epithelial hair follicle stem cells and their niche. Exp. Dermatol. 17, 592-609.
29. Krause K, Foitzik K (2006) Biology of the hair follicle: the basics. Semin. Cutan. Med. Surg. 25, 2-10.
30. Krishnamurthy J, Ramsey MR, Ligon KL, Torrice C, Koh A, Bonner-Weir S, Sharpless NE (2006) p16INK4a induces an age-dependent decline in islet regenerative potential. Nature 443, 453-457.
31. Levy V, Lindon C, Harfe BD, Morgan BA (2005) Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev. Cell 9, 855-861.
32. Levy V, Lindon C, Zheng Y, Harfe BD, Morgan BA (2007) Epidermal stem cells arise from the hair follicle after wounding. FASEB J. 21, 1358-1366.
33. Li L, Mignone J, Yang M, Matic M, Penman S, Enikolopov G, Hoffman RM (2003) Nestin expression in hair follicle sheath progenitor cells. Proc. Natl Acad. Sci. USA 100, 9958-9961.
34. Limat A, French LE, Blal L, Saurat J-H, Hunziker T, Salomon D (2003) Organotypic cultures of autologous hair follicle keratinocytes for the treatment of recurrent leg ulcers. J. Am. Acad. Dermatol. 48, 207-214.
35. Liu Y, Lyle S, Yang Z, Cotsarelis G (2003) Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J. Invest. Dermatol. 121, 963-968.
36. Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, Suri P, Wicha MS (2006) Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 66, 6063-6071.
37. Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, Corbin JG, Gritli-Linde A, Dellovade T, Porter JA, Rubin LL, Dudek H, McMahon AP, Fishell G (2003) Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39, 937-950.
38. Martinelli DC, Fan CM (2007) Gas1 extends the range of hedgehog action by facilitating its signaling. Genes Dev. 21, 1231-1243.
39. Michel M, Torok N, Godbout MJ, Lussier M, Gaudreau P, Royal A, Germain L (1996) Keratin 19 as a biochemical marker of skin stem cells in vivo and in vitro: keratin 19 expressing cells are differentially localized in function of anatomic sites, and their number varies with donor age and culture stage. J. Cell Sci. 109, 1017-1028.
40. Molofsky AV, Slutsky SG, Joseph NM, He S, Pardal R, Krishnamurthy J, Sharpless NE, Morrison SJ (2006) Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 443, 448-452.
41. Morris RJ, Liu Y, Marles L, Yang Z, Trempus C, Li S, Lin JS, Sawicki JA, Cotsarelis G (2004) Capturing and profiling adult hair follicle stem cells. Nat. Biotechnol. 22, 411-417.
42. Neill GW, Harrison WJ, Ikram MS, Williams TD, Bianchi LS, Nadendla SK, Green JL, Ghali L, Frischauf AM, O'Toole EA, Aberger F, Philpott MP (2008) GLI1 repression of ERK activity correlates with colony formation and impaired migration in human epidermal keratinocytes. Carcinogenesis 29, 738-746.
43. Nielsen CM, Williams J, van denBrink GR, Lauwers GY, Roberts DJ (2004) Hh pathway expression in human gut tissues and in inflammatory gut diseases. Lab. Invest. 84, 1631-1642.
44. Niemann C, Unden AB, Lyle S, Zouboulis CC, Toftgard R, Watt FM (2003) Indian hedgehog and beta-catenin signaling: role in the sebaceous lineage of normal and neoplastic mammalian epidermis. Proc. Natl Acad. Sci. USA 100, 11873-11880.
45. Ninkovic J, Stigloher C, Lillesaar C, Bally-Cuif L (2008) Gsk3beta/PKA and Gli1 regulate the maintenance of neural progenitors at the midbrain-hindbrain boundary in concert with E(Spl) factor activity. Development 135, 3137-3148.
46. Ohyama M, Terunuma A, Tock CL, Radonovich MF, Pise-Masison CA, Hopping SB, Brady JN, Udey MC, Vogel JC (2006) Characterization and isolation of stem cell-enriched human hair follicle bulge cells. J. Clin. Invest. 116, 249-260.
47. Olsen CL, Hsu PP, Glienke J, Rubanyi GM, Brooks AR (2004) Hedgehog-interacting protein is highly expressed in endothelial cells but down-regulated during angiogenesis and in several human tumors. BMC Cancer 4, 43.
48. Orringer JS, Hammerberg C, Lowe L, Kang S, Johnson TM, Hamilton T, Voorhees JJ, Fisher GJ (2006) The effects of laser-mediated hair removal on immunohistochemical staining properties of hair follicles. J. Am. Acad. Dermatol. 55, 402-407.
49. Palma V, Lim DA, Dahmane N, Sanchez P, Brionne TC, Herzberg CD, Gitton Y, Carleton A, Alvarez-Buylla A, Ruiz i Altaba A (2005) Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 132, 335-344.
50. Poblet E, Jimenez-Acosta F, Rocamora A (1994) QBEND/10 (anti-CD34 antibody) in external root sheath cells and follicular tumors. J. Cutan. Pathol. 21, 224-228.
51. Poblet E, Jimenez F, Godinez JM, Pascual-Martin A, Izeta A (2006) The immunohistochemical expression of CD34 in human hair follicles: a comparative study with the bulge marker CK15. Clin. Exp. Dermatol. 31, 807-812.
52. Ressler S, Bartkova J, Niederegger H, Bartek J, Scharffetter-Kochanek K, Jansen-Durr P, Wlaschek M (2006) p16INK4A is a robust in vivo biomarker of cellular aging in human skin. Aging Cell 5, 379-389.
53. Rittié L, Kang S, Voorhees JJ, Fisher GJ (2008) Induction of collagen by estradiol: difference between sun-protected and photodamaged human skin in vivo. Arch. Dermatol. 144, 1129-1140.
54. Rittié L, Fisher GJ, Voorhees JJ (2010) Aging and photoaging of the skin. In Therapy of Skin Diseases. (Krieg T, Bickers DR, Miyachi Y, eds). Berlin/Heidelberg/New York: Springer-Verlag. In Press.
55. Rosenblum MD, Yancey KB, Olasz EB, Truitt RL (2006) CD200, a "no danger" signal for hair follicles. J. Dermatol. Sci. 41, 165-174.
56. Ross J, Li L (2006) Recent advances in understanding extrinsic control of hematopoietic stem cell fate. Curr. Opin. Hematol. 13, 237-242.
57. Rubin LL, de Sauvage FJ (2006) Targeting the hedgehog pathway in cancer. Nat. Rev. Drug Discov. 5, 1026-1033.
58. Secker GA, Shortt AJ, Sampson E, Schwarz QP, Schultz GS, Daniels JT (2008) TGFbeta stimulated re-epithelialisation is regulated by CTGF and Ras/MEK/ERK signalling. Exp. Cell Res. 314, 131-142.
59. Seppala M, Depew MJ, Martinelli DC, Fan CM, Sharpe PT, Cobourne MT (2007) Gas1 is a modifier for holoprosencephaly and genetically interacts with sonic hedgehog. J. Clin. Invest. 117, 1575-1584.
60. Shapiro GI (2006) Cyclin-dependent kinase pathways as targets for cancer treatment. J. Clin. Oncol. 24, 1770-1783.
61. Sherr CJ, Roberts JM (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13, 1501-1512.
62. Sicklick JK, Li YX, Melhem A, Schmelzer E, Zdanowicz M, Huang JW, Caballero M, Fair JH, Ludlow JW, McClelland RE, Reid LM, Diehl AM (2006) Hedgehog signaling maintains resident hepatic progenitors throughout lifeAm. J. Physiol. 290, G859-G870.
63. Stoll SW, Johnson JL, Bhasin A, Johnston A, Gudjonsson JE, Rittié L, Elder JT (2009) Metalloproteinase-mediated, context-dependent function of amphiregulin and HB-EGF in human keratinocytes and skin. J. Invest. Dermatol. In Press.
64. Sudo K, Ema H, Morita Y, Nakauchi H (2000) Age-associated characteristics of murine hematopoietic stem cells. J. Exp. Med. 192, 1273-1280.
65. Trowbridge JJ, Scott MP, Bhatia M (2006) Hedgehog modulates cell cycle regulators in stem cells to control hematopoietic regeneration. Proc. Natl Acad. Sci. USA 103, 14134-14139.
66. Tumbar T, Guasch G, Greco V, Blanpain C, Lowry WE, Rendl M, Fuchs E (2004) Defining the epithelial stem cell niche in skin. Science 303, 359-363.
67. Vidal VPI, Chaboissier MC, Lutzkendorf S, Cotsarelis S, Mill P, Hui CC, Ortonne N, Ortonne JP, Schedl A (2005) Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment. Curr. Biol. 15, 1340-1351.
68. Vincent S, Perrimon N, Axelrod JD (2008) Hedgehog and wingless stabilize but do not induce cell fate during Drosophila dorsal embryonic epidermal patterning. Development 135, 2767-2775.
69. Zhao C, Chen A, Jamieson CH, Fereshteh M, Abrahamsson A, Blum J, Kwon HY, Kim J, Chute JP, Rizzieri D, Munchhof M, VanArsdale T, Beachy PA, Reya T (2009) Hedgehog signalling is essential for maintenance of cancer stem cells in myeloid leukaemia. Nature 458, 776-779.
70. Zhou JX, Jia LW, Liu WM, Miao CL, Liu S, Cao YJ, Duan EK (2006) Role of sonic hedgehog in maintaining a pool of proliferating stem cells in the human fetal epidermis. Hum. Reprod. 21, 1698-1704.
71. Zouboulis CC, Adjaye J, Akamatsu H, Moe-Behrens G, Niemann C (2008) Human skin stem cells and the ageing process. Exp. Gerontol. 43, 986 997.