Clonal multipotency and effect of long-term in vitro expansion on differentiation potential of human hair follicle derived mesenchymal stem cells

Stem Cell Research

Volumn 8, Issue 1, 2012, Pages 74-84

  Bajpai, Vivek K ^a   Mistriotis, Panagiotis ^a   Andreadis, Stelios T ^a,b,c  

^a the State University of New York   (United States)

^b University at Buffalo The State University of New York   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRECAN; ALKALINE PHOSPHATASE; ALPHA SMOOTH MUSCLE ACTIN; CALPONIN; COLLAGEN TYPE 10; GLYCOSAMINOGLYCAN; LEPTIN; LIPOPROTEIN LIPASE; MYOCARDIN; MYOSIN HEAVY CHAIN; OSTEONECTIN; PROTEIN P8; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9; TRANSGELIN;

ADIPOGENESIS; ARTICLE; BONE DEVELOPMENT; BONE MINERALIZATION; CELL CLONE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CHONDROGENESIS; GENE EXPRESSION; GENE EXPRESSION PROFILING; HAIR FOLLICLE; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MESENCHYMAL STEM CELL; MULTIPOTENT STEM CELL; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SENESCENCE;

CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CLONE CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HAIR FOLLICLE; HUMANS; KINETICS; MESENCHYMAL STEM CELLS; MULTIPOTENT STEM CELLS; MUSCLE DEVELOPMENT; TIME FACTORS;

RODENTIA;

EID: 80052859171     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2011.07.003     Document Type: Article

References (45)

1. Paus R., Cotsarelis G. The biology of hair follicles. N Engl J. Med. 1999, 341:491-497.
2. Cotsarelis G., Sun T.T., Lavker R.M. Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 1990, 61:1329-1337.
3. Morris R.J., Liu Y., Marles L., Yang Z., Trempus C., Li S., Lin J.S., Sawicki J.A., Cotsarelis G. Capturing and profiling adult hair follicle stem cells. Nat. Biotechnol. 2004, 22:411-417.
4. Tumbar T., Guasch G., Greco V., Blanpain C., Lowry W.E., Rendl M., Fuchs E. Defining the epithelial stem cell niche in skin. Science 2004, 303:359-363.
5. Alonso L., Fuchs E. The hair cycle. J. Cell Sci. 2006, 119:391-393.
6. Taylor G., Lehrer M.S., Jensen P.J., Sun T.T., Lavker R.M. Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 2000, 102:451-461.
7. Amoh Y., Li L., Katsuoka K., Penman S., Hoffman R.M. Multipotent nestin-positive, keratin-negative hair-follicle bulge stem cells can form neurons. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:5530-5534.
8. Yu H., Kumar S.M., Kossenkov A.V., Showe L., Xu X. Stem cells with neural crest characteristics derived from the bulge region of cultured human hair follicles. J. Investig. Dermatol. 2010, 130:1227-1236.
9. Schneider M.R., Schmidt-Ullrich R., Paus R. The hair follicle as a dynamic miniorgan. Curr. Biol. 2009, 19:R132-R142.
10. Jahoda C.A., Horne K.A., Oliver R.F. Induction of hair growth by implantation of cultured dermal papilla cells. Nature 1984, 311:560-562.
11. McElwee K.J., Kissling S., Wenzel E., Huth A., Hoffmann R. Cultured peribulbar dermal sheath cells can induce hair follicle development and contribute to the dermal sheath and dermal papilla. J. Investig. Dermatol. 2003, 121:1267-1275.
12. Reynolds A.J., Lawrence C., Cserhalmi-Friedman P.B., Christiano A.M., Jahoda C.A. Trans-gender induction of hair follicles. Nature 1999, 402:33-34.
13. Jahoda C.A., Whitehouse J., Reynolds A.J., Hole N. Hair follicle dermal cells differentiate into adipogenic and osteogenic lineages. Exp. Dermatol. 2003, 12:849-859.
14. Hoogduijn M.J., Gorjup E., Genever P.G. Comparative characterization of hair follicle dermal stem cells and bone marrow mesenchymal stem cells. Stem Cells Dev. 2006, 15:49-60.
15. Lako M., Armstrong L., Cairns P.M., Harris S., Hole N., Jahoda C.A. Hair follicle dermal cells repopulate the mouse haematopoietic system. J. Cell Sci. 2002, 115:3967-3974.
16. Liu J.Y., Peng H.F., Gopinath S., Tian J., Andreadis S.T. Derivation of functional smooth muscle cells from multipotent human hair follicle mesenchymal stem cells. Tissue engineering. Part A 2010, 16:2553-2564.
17. Liu J.Y., Peng H.F., Andreadis S.T. Contractile smooth muscle cells derived from hair-follicle stem cells. Cardiovasc. Res. 2008, 79:24-33.
18. Peng H.F., Liu J.Y., Andreadis S.T., Swartz D.D. Hair follicle-derived smooth muscle cells and small intestinal submucosa for engineering mechanically robust and vasoreactive vascular media. Tissue Eng. Part A 2011, 17:981-990.
19. Kinner B., Zaleskas J.M., Spector M. Regulation of smooth muscle actin expression and contraction in adult human mesenchymal stem cells. Exp. Cell Res. 2002, 278:72-83.
20. Narita Y., Yamawaki A., Kagami H., Ueda M., Ueda Y. Effects of transforming growth factor-beta 1 and ascorbic acid on differentiation of human bone-marrow-derived mesenchymal stem cells into smooth muscle cell lineage. Cell Tissue Res. 2008, 333:449-459.
21. Owens G.K. Regulation of differentiation of vascular smooth muscle cells. Physiol. Rev. 1995, 75:487-517.
22. Wang Z., Wang D.Z., Pipes G.C., Olson E.N. Myocardin is a master regulator of smooth muscle gene expression. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:7129-7134.
23. Ailhaud G. Early adipocyte differentiation. Biochem. Soc. Trans. 1996, 24:400-402.
24. MacDougald O.A., Hwang C.S., Fan H., Lane M.D. Regulated expression of the obese gene product (leptin) in white adipose tissue and 3 T3-L1 adipocytes. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:9034-9037.
25. Gregoire F.M., Smas C.M., Sul H.S. Understanding adipocyte differentiation. Physiol. Rev. 1998, 78:783-809.
26. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M., Sato M., Okamoto R., Kitamura Y., Yoshiki S., Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89:755-764.
27. Akiyama H., Chaboissier M.C., Martin J.F., Schedl A., de Crombrugghe B. The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 2002, 16:2813-2828.
28. Zuscik M.J., Hilton M.J., Zhang X., Chen D., O'Keefe R.J. Regulation of chondrogenesis and chondrocyte differentiation by stress. J Clin Invest 2008, 118:429-438.
29. Yu H., Fang D., Kumar S.M., Li L., Nguyen T.K., Acs G., Herlyn M., Xu X. Isolation of a novel population of multipotent adult stem cells from human hair follicles. Am. J. Pathol. 2006, 168:1879-1888.
30. Wagner W., Horn P., Castoldi M., Diehlmann A., Bork S., Saffrich R., Benes V., Blake J., Pfister S., Eckstein V., Ho A.D. Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS One 2008, 3:e2213.
31. Barman J.M., Astore I., Pecoraro V. The normal trichogram of the adult. J. Investig. Dermatol. 1965, 44:233-236.
32. Ducy P., Zhang R., Geoffroy V., Ridall A.L., Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 1997, 89:747-754.
33. Sekiya I., Tsuji K., Koopman P., Watanabe H., Yamada Y., Shinomiya K., Nifuji A., Noda M. SOX9 enhances aggrecan gene promoter/enhancer activity and is up-regulated by retinoic acid in a cartilage-derived cell line, TC6. J. Biol. Chem. 2000, 275:10738-10744.
34. Chawla A., Schwarz E.J., Dimaculangan D.D., Lazar M.A. Peroxisome proliferator-activated receptor (PPAR) gamma: adipose-predominant expression and induction early in adipocyte differentiation. Endocrinology 1994, 135:798-800.
35. Tontonoz P., Hu E., Graves R.A., Budavari A.I., Spiegelman B.M. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev 1994, 8:1224-1234.
36. Kern S., Eichler H., Stoeve J., Kluter H., Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 2006, 24:1294-1301.
37. Banfi A., Bianchi G., Notaro R., Luzzatto L., Cancedda R., Quarto R. Replicative aging and gene expression in long-term cultures of human bone marrow stromal cells. Tissue Eng 2002, 8:901-910.
38. Kretlow J.D., Jin Y.Q., Liu W., Zhang W.J., Hong T.H., Zhou G., Baggett L.S., Mikos A.G., Cao Y. Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol 2008, 9:60.
39. Mauney J.R., Volloch V., Kaplan D.L. Matrix-mediated retention of adipogenic differentiation potential by human adult bone marrow-derived mesenchymal stem cells during ex vivo expansion. Biomaterials 2005, 26:6167-6175.
40. Chen F.G., Zhang W.J., Bi D., Liu W., Wei X., Chen F.F., Zhu L., Cui L., Cao Y. Clonal analysis of nestin(-) vimentin(+) multipotent fibroblasts isolated from human dermis. J. Cell Sci. 2007, 120:2875-2883.
41. Mastrogiacomo M., Cancedda R., Quarto R. Effect of different growth factors on the chondrogenic potential of human bone marrow stromal cells. Osteoarthr. Cartil. 2001, 9(Suppl A):S36-S40.
42. Biernaskie J., Paris M., Morozova O., Fagan B.M., Marra M., Pevny L., Miller F.D. SKPs derive from hair follicle precursors and exhibit properties of adult dermal stem cells. Cell Stem Cell 2009, 5:610-623.
43. Toma J.G., Akhavan M., Fernandes K.J., Barnabe-Heider F., Sadikot A., Kaplan D.R., Miller F.D. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 2001, 3:778-784.
44. Asahina I., Sampath T.K., Nishimura I., Hauschka P.V. Human osteogenic protein-1 induces both chondroblastic and osteoblastic differentiation of osteoprogenitor cells derived from newborn rat calvaria. J Cell Biol 1993, 123:921-933.
45. Abramoff M.D., Magelhaes P.J., Ram S.J. Image processing with ImageJ. Biophotonics Int. 2004, 11:36-42.