The CD44+ALDH+ population of human keratinocytes is enriched for epidermal stem cells with long-term repopulating ability

Stem Cells

Volumn 31, Issue 4, 2013, Pages 786-799

  Szabo, Akos Z ^a   Fong, Stephen ^a   Yue, Lili ^a   Zhang, Kai ^a   Strachan, Lauren R ^a   Scalapino, Kenneth ^b   Mancianti, Maria Laura ^c   Ghadially, Ruby ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Alta Bates Medical Center   (United States)

Author keywords

Aldehyde dehydrogenase; CD44; Epidermis; Human; Keratinocyte; Stem cell

Indexed keywords

ALDEHYDE DEHYDROGENASE; ALPHA6 INTEGRIN; BMI1 PROTEIN; CD71 ANTIGEN; HERMES ANTIGEN;

ADULT; ARTICLE; CELL GROWTH; CELL POPULATION; CELL RENEWAL; CONTROLLED STUDY; EPIDERMIS CELL; FLUORESCENCE ACTIVATED CELL SORTING; HAIR FOLLICLE; HUMAN; HUMAN CELL; IN VITRO STUDY; KERATINOCYTE; NEWBORN; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REGENERATION; STEM CELL;

ALDEHYDE DEHYDROGENASE; ANIMALS; ANTIGENS, CD44; EPIDERMIS; FLOW CYTOMETRY; HUMANS; KERATINOCYTES; MICE; MICE, INBRED NOD; MICE, SCID; REGENERATION; STEM CELLS;

EID: 84875778857     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1329     Document Type: Article

References (76)

1. Ghazizadeh S, Taichman LB. Organization of stem cells and their progeny in human epidermis. J Invest Dermatol 2005;124:367-72.
2. Li A, Pouliot N, Redvers R et al. Extensive tissue-regenerative capacity of neonatal human keratinocyte stem cells and their progeny. J Clin Invest 2004;113:390-400.
3. Muffler S, Stark H-J, Amoros M et al. A stable niche supports longterm maintenance of human epidermal stem cells in organotypic cultures. Stem Cells 2008;26:2506-2515.
4. Pouliot N, Redvers RP, Ellis S et al. Optimization of a transplant model to assess skin reconstitution from stem cell-enriched primary human keratinocyte populations. Exp Dermatol 2005;14:60-69.
5. Paquet-Fifield S, Redvers RP, Pouliot N, Kaur P. A transplant model for human epidermal skin regeneration. Methods Mol Biol 2010;585: 369-382.
6. Silver SG, Ho VCY. Benign epithelial tumors. In: Freedberg I, Eisen A, Wolff K et al. Fitzpatrick's Dermatology in General Medicine. Columbus, OH: McGraw-Hill, 2003:778-780.
7. Hall JP, Sheffey RJ, Chagares WE et al. Epidermal inclusion cyst in the foot of a Vietnam Veteran. J Am Pediatr Med Assoc 2006;96: 445-447.
8. Ohnishi T, Watanabe S. Immunohistochemical observation of cytokeratins in keratinous cysts including plantar epidermoid cyst. J Cutan Pathol 1999;26:424-429.
9. Doran TI, Vidrich A, Sun TT. Intrinsic and extrinsic regulation of the differentiation of skin, corneal and esophageal epithelial cells. Cell 1980;22(1 pt 1):17-25.
10. Lavker RM, Sun TT. Rapid modulation of keratinocyte differentiation by the external environment. J Invest Dermatol 1983;80:228-237.
11. Yu W, Fang X, Ewald A et al. Formation of cysts by alveolar type II cells in three-dimensional culture reveals a novel mechanism for epithelial morphogenesis. Mol Biol Cell 2007;18:1693-1700.
12. Debnath J, Brugge JS. Modelling glandular epithelial cancers in threedimensional cultures. Nat Rev Cancer 2005;5:675-688.
13. Takahashi K, Tanabe K, Ohnuki M et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007; 131:861-872.
14. Jones PH, Watt FM. Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 1993;73:713-724.
15. Jones PH, Harper S, Watt FM. Stem cell patterning and fate in human epidermis. Cell 1995;80:83-93.
16. Li A, Simmons PJ, Kaur P. Identification and isolation of candidate human keratinocyte stem cells based on cell surface phenotype. Proc Natl Acad Sci USA 1998;95:3902-3907.
17. Webb A, Li A, Kaur P. Location and phenotype of human adult keratinocyte stem cells of the skin. Differentiation 2004;72:387-395.
18. Belicchi M, Pisati F, Lopa R et al. Human skin-derived stem cells migrate throughout forebrain and differentiate into astrocytes after injection into adult mouse brain. J Neurosci Res 2004;77:475-486.
19. Pellegrini G, Dellambra E, Golisano O et al. p63 identifies keratinocyte stem cells. Proc Natl Acad Sci USA 2001;98:3156-3161.
20. Lyle S, Christofidou-Solomidou M, Liu Y et al. 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.
21. Terunuma A, Jackson KL, Kapoor V et al. Side population keratinocytes resembling bone marrow side population stem cells are distinct from label-retaining keratinocyte stem cells. J Invest Dermatol 2003; 121:1095-1103.
22. Triel C, Vestergaard ME, Bolund L et al. Side population cells in human and mouse epidermis lack stem cell characteristics. Exp Cell Res 2004;295:79-90.
23. Lowell S, Jones P, Le Roux I et al. Stimulation of human epidermal differentiation by delta-notch signalling at the boundaries of stem-cell clusters. Curr Biol 2000;10:491-500.
24. Li A, Kaur P. Epidermal Cells: FACS enrichment of human keratinocyte stem cells. Methods Mol Biol. 2005;289:87-96.
25. Marchitti SA, Brocker C, Stagos D et al. Non-P450 aldehyde oxidizing enzymes: The aldehyde dehydrogenase superfamily. Expert Opin Drug Metab Toxicol 2008;4:697-720.
26. Chute JP, Muramoto GG, Whitesides J et al. Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc Natl Acad Sci USA 2006;103: 11707-11712.
27. Armstrong L, Stojkovic M, Dimmick I et al. Phenotypic characterization of murine primitive hematopoietic progenitor cells isolated on basis of aldehyde dehydrogenase activity. Stem Cells 2004;22: 1142-1151.
28. Christ O, Lucke K, Imren S et al. Improved purification of hematopoietic stem cells based on their elevated aldehyde dehydrogenase activity. Haematologica 2007;92:1165-1172.
29. Hess DA, Meyerrose TE, Wirthlin L et al. Functional characterization of highly purified human hematopoietic repopulating cells isolated according to aldehyde dehydrogenase activity. Blood 2004;104: 1648-1655.
30. Corti S, Locatelli F, Papadimitriou D et al. Identification of a primitive brain-derived neural stem cell population based on aldehyde dehydrogenase activity. Stem Cells 2006;24:975-985.
31. Corti S, Locatelli F, Papadimitriou D et al.. Transplanted ALDHhiSSClo neural stem cells generate motor neurons and delay disease progression of nmd mice, an animal model of SMARD1. Hum Mol Genet 2006;15:167-187.
32. Ginestier C, Hur MH, Charafe-Jauffret E et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007;1:555-567.
33. Liu AY, True LD, LaTray L et al. Cell-cell interaction in prostate gene regulation and cytodifferentiation. Proc Natl Acad Sci USA 1997;94:10705-10710.
34. Al-Hajj M, Wicha MS, Benito-Hernandez A et al. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci 2003; 100:3983-3988.
35. Prince ME, Sivanandan R, Kaczorowski A et al. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci USA 2007;104: 973-978.
36. Patrawala L, Calhoun T, Schneider-Broussard R et al. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 2006;25:1696-1708.
37. Charruyer A, Strachan LR, Yue L et al. CD133 is a marker for longterm repopulating murine epidermal stem cells. J Invest Dermatol 2012;132:2522-2533.
38. Yahata T, Takanashi T, Muguruma Y et al. Accumulation of oxidative DNA damage restricts the self-renewal capacity of human hematopoietic stem cells. Blood 2011;118:2941-2950.
39. Kunimoto H, Fukuchi Y, Sakurai M et al. Tet2 disruption leads to enhanced self-renewal and altered differentiation of fetal liver hematopoietic stem cells. Sci Rep 2012;2:273.
40. Barrandon Y, Green H. Three clonal types of keratinocyte with different capacities for multiplication. Proc Natl Acad Sci USA 1987;84: 2302-2306.
41. Pellegrini G, Ranno R, Stracuzzi G et al. The control of epidermal stem cells (holoclones) in the treatment of massive full-thickness burns with autologous keratinocytes cultured on fibrin. Transplantation 1999;6:868-879.
42. Sangiorgi E, Capecchi MR. Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 2008;40:915-20.
43. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003;423:255-60.
44. Leung C, Lingbeek M, Shakhova O et al. Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 2004;428:337-341.
45. Molofsky AV, Pardal R, Iwashita T et al. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003;425:962-967.
46. Ehama R, Ishimatsu-Tsuji Y, Iriyama S et al. Hair follicle regeneration using grafted rodent and human cells. J Invest Dermatol 2007; 127:2106-2115.
47. Bickenbach JR, Holbrook KA. Label-retaining cells in human embryonic and fetal epidermis. J Invest Dermatol 1987;88:42-46.
48. Moser FG, Dorman BP, Ruddle FH. Mouse-human heterokaryon analysis with a 33258 Hoechst-Giemsa technique. J Cell Biol 1975;66: 676-680.
49. Cunha GR, Vanderslice KD. Identification in histological sections of species origin of cells from mouse, rat and human. Stain Technol 1984;59:7-12.
50. Kuperwasser C, Chavarria T, Wu M et al. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc Natl Acad Sci USA 2004;101:4966-4971.
51. Parrott JA, Nilsson E, Mosher R et al. Stromal-epithelial interactions in the progression of ovarian cancer: Influence and source of tumor stromal cells. Mol Cell Endocrinol 2001;175:29-39.
52. Bonnefoix T, Bonnefoix P, Verdiel P et al. Fitting limiting dilution experiments with generalized linear models results in a test of the single-hit Poisson assumption. J Immunol Methods 1996;194:113-119.
53. Szilvassy SJ, Humphries RK, Lansdorp PM et al. Quantitative assay for totipotent reconstituting hematopoietic stem cells by a competitive repopulation strategy. Proc Natl Acad Sci USA 1990;87:8736-8740.
54. Moll R, Franke WW, Schiller DL et al. The catalog of human cytokeratins: Patterns of expression in normal epithelia, tumors and cultured cells. Cell 1982;31:11-24.
55. van der Velden LA, Schaafsma HE, Manni JJ et al. Cytokeratin and vimentin expression in normal epithelium and benign lesions of the vocal cords. Acta Otolaryngol 1996;116:325-331.
56. Gerritsen MJ, Elbers ME, de Jong EM et al. Recruitment of cycling epidermal cells and expression of filaggrin, involucrin and tenascin in the margin of the active psoriatic plaque, in the uninvolved skin of psoriatic patients and in the normal healthy skin. J Dermatol Sci 1997;14:179-188.
57. Murphy GF, Flynn TC, Rice RH et al. Involucrin expression in normal and neoplastic human skin: A marker for keratinocyte differentiation. J Invest Dermatol 1984;82:453-457.
58. Kanitakis J. Anatomy, histology and immunohistochemistry of normal human skin. Eur J Dermatol 2002;12:390-399, quiz 400-401.
59. Strachan LR, Scalapino KJ, Lawrence HJ et al. Rapid adhesion to collagen isolates murine keratinocytes with limited long-term repopulating ability in vivo despite high clonogenicity in vitro. Stem Cells 2008;26:235-243.
60. Charruyer A, Barland CO, Yue L et al. Transit-amplifying cell frequency and cell cycle kinetics are altered in aged epidermis. J Invest Dermatol 2009;129:2574-2583.
61. Schneider TE, Barland C, Alex AM et al. Measuring stem cell frequency in epidermis: A quantitative in vivo functional assay for longterm repopulating cells. Proc Natl Acad Sci USA 2003;100: 11412-11417.
62. Ferraris C, Bernard BA, Dhouailly D. Adult epidermal keratinocytes are endowed with pilosebaceous forming abilities. Int J Dev Biol 1997;41:491-498.
63. Tani H, Morris RJ, Kaur P. Enrichment for murine keratinocyte stem cells based on cell surface phenotype. Proc Natl Acad Sci USA 2000; 97:10960-10965.
64. Grimwood RE, Baskin JB, Nielsen LD et al. Fibronectin extracellular matrix assembly by human epidermal cells implanted into athymic mice. J Invest Dermatol 1988;90:434-440.
65. Cotsarelis G. Epithelial stem cells: A folliculocentric view. J Invest Dermatol 2006;126:1459-1468.
66. Horsley V, O'Carroll D, Tooze R et al. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 2006;126:597-609.
67. Wan H, Stone MG, Simpson C et al. Desmosomal proteins, including desmoglein 3, serve as novel negative markers for epidermal stem cell-containing population of keratinocytes. J Cell Sci 2003;116 (pt 20):4239-4248.
68. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997;91: 661-672.
69. Akashi K, Traver D, Miyamoto T et al. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 2000; 404:193-197.
70. Sutherland HJ, Lansdorp PM, Henkelman DH et al. Functional characterization of individual human hematopoietic stem cells cultured at limiting dilution on supportive marrow stromal layers. Proc Natl Acad Sci USA 1990;87:3584-3588.
71. Haylock DN, To LB, Dowse TL et al. Ex vivo expansion and maturation of peripheral blood CD34+ cells into the myeloid lineage. Blood 1992;80:1405-1412.
72. Budak MT, Alpdogan OS, Zhou M et al. Ocular surface epithelia contain ABCG2-dependent side population cells exhibiting features associated with stem cells. J Cell Sci 2005;118 (pt 8):1715-1724.
73. Pavlovitch JH, Rizk-Rabin M, Jaffray P et al. Characteristics of homogeneously small keratinocytes from newborn rat skin: Possible epidermal stem cells. Am J Physiol 1991;261(6 pt 1):C964-C972.
74. Jones PH, Simons BD, Watt FM. Sic transit gloria: Farewell to the epidermal transit amplifying cell? Cell Stem Cell 2007;1:371-381.
75. Jones P, Simons BD. Epidermal homeostasis: Do committed progenitors work while stem cells sleep? Nat. Rev Mol Cell Biol 2008;9: 82-88.
76. Clayton E, Doupé DP, Klein AM et al. A single type of progenitor cell maintains normal epidermis. Nature 2007;446:185-189.