Enrichment and characterization of human dermal stem/progenitor cells by intracellular granularity

Stem Cells and Development

Volumn 22, Issue 8, 2013, Pages 1264-1274

  Shim, Joong Hyun ^a   Lee, Tae Ryong ^a   Shin, Dong Wook ^a  

^a AmorePacific Corporation   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; AGGRECAN; COLLAGEN TYPE 2; COLLAGEN TYPE 4; CORIN; FATTY ACID BINDING PROTEIN 4; LEPTIN; MICROTUBULE ASSOCIATED PROTEIN 2; NESTIN; OSTEOGLYCIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN; PROTEIN S100B; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SOX2; TWIST1 PROTEIN; UNCLASSIFIED DRUG; VERSICAN; VIMENTIN;

ADIPOCYTE; ADULT; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; DERMAL STEM CELL; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HAIR FOLLICLE; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; OSTEOBLAST; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL;

ADOLESCENT; ADULT; ADULT STEM CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CYTOPLASMIC GRANULES; DERMIS; FEMALE; GENE EXPRESSION; HUMANS; INFANT, NEWBORN; INTERMEDIATE FILAMENT PROTEINS; MALE; MICROSCOPY, FLUORESCENCE; MULTIPOTENT STEM CELLS; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; S100 PROTEINS; SERINE ENDOPEPTIDASES; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; TWIST TRANSCRIPTION FACTOR; VERSICANS; VIMENTIN;

EID: 84876160161     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0244     Document Type: Article

References (59)

1. Young HE, C Duplaa, R Katz, T Thompson, KC Hawkins, AN Boev, NL Henson, M Heaton, R Sood, et al. (2005). Adult-derived stem cells and their potential for use in tissue repair and molecular medicine. J Cell Mol Med 9:753-769.
2. Pereira RF, KW Halford, MD O'Hara, DB Leeper, BP Sokolov, MD Pollard, O Bagasra and DJ Prockop. (1995). Cultured adherent cells from marrow can serve as longlasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci U S A 92:4857-4861.
3. Pittenger MF, AM Mackay, SC Beck, RK Jaiswal, R Douglas, JD Mosca, MA Moorman, DW Simonetti, S Craig and DR Marshak. (1999). Multilineage potential of human mesenchymal stem cells. Science 284:143-147.
4. Anderson DJ, FH Gage and IL Weissman. (2001). Can stem cells cross lineage boundaries? Nat Med 7:393-395.
5. Jiang Y, BN Jahagirdar, RL Reinhardt, RE Schwartz, CD Keene, XR Ortiz-Gonzalez, M Reyes, T Lenvik, et al. (2002). Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49.
6. Jiang Y, B Vaessen, T Lenvik, M Blackstad, M Reyes and CM Verfaillie. (2002). Multipotent progenitor cells can be isolated from postnatal murine bone marrow, muscle, and brain. Exp Hematol 30:896-904.
7. Zuk PA, M Zhu, H Mizuno, J Huag, JW Futrell, AJ Katz, P Benhaim, HP Lorenz and MH Hedrick. (2001). Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng 7:211-218.
8. Zuk PA, M Zhu, P Ashjian, DA De Ugarte, JI Huang, H Mizuno, ZC Alfonso, JK Fraser, P Benhaim and MH Hedrick. (2002). Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279-4295.
9. Lee MW, MS Yang, JS Park, HC Kim, YJ Kim and J Choi. (2005). Isolation of mesenchymal stem cells from cryopreserved human umbilical cord blood. Int J Hematol 81: 126-130.
10. Fukuchi Y, H Nakajima, D Sugiyama, I Hirose, T Kitamura and K Tsuji. (2004). Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 22:649-658.
11. Blanpain C and E Fuchs. (2006). Epidermal stem cells of the skin. Annu Rev Cell Dev Biol 22:339-373.
12. Fuchs E. (2009). Finding one's niche in the skin. Cell Stem Cell 4:499-502.
13. Toma JG, M Akhavan, KJ Fernandes, F Barnabé-Heider, A Sadikot, DR Kaplan and FD Miller. (2001). Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3:778-784.
14. Fernandes KJ, IA McKenzie, P Mill, KM Smith, M Akhavan, F Barnabé-Heider, J Biernaskie, A Junek, NR Kobayashi, et al. (2004). A dermal niche for multipotent adult skin-derived precursor cells. Nat Cell Biol 6:1082-1093.
15. Toma JG, IA McKenzie, D Bagli and FD Miller. (2005). Isolation and characterization of multipotent skin-derived precursors from human skin. Stem Cells 23:727-737.
16. Chen FG, WJ Zhang, D Bi, W Liu, X Wei, FF Chen, L Zhu, L Cui and Y Cao. (2007). Clonal analysis of nestin (-) vimentin (+) multipotent fibroblasts isolated from human dermis. J Cell Sci 120:2875-2883.
17. Deng Y, JC Hu and KA Athanasiou. (2007). Isolation and chondroinduction of a dermis isolated, aggrecan-sensitive subpopulation with high chondrogenic potential. Arthritis Rheum 56:168-176.
18. Biernaskie J, M Paris, O Morozova, BM Fagan, M Marra, L Pevny and FD Miller. (2009). SKPs derive from hair follicle precursors and exhibit properties of adult dermal stem cells. Cell Stem Cell 5:610-623.
19. Driskell RR, A Giangreco, KB Jensen, KW Mulder and FM Watt. (2009). Sox2-positive dermal papilla cells specify hair follicle type in mammalian epidermis. Development 7136: 2815-2823.
20. Junker JP, P Sommar, M Skog, H Johnson and G Kratz. (2010). Adipogenic, chondrogenic and osteogenic differentiation of clonally derived human dermal fibroblasts. Cells Tissues Organs 191:105-118.
21. Amoh Y, L Li, R Campillo, K Kawahara, K Katsuoka, S Penman and RM Hoffman. (2005). Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Proc Natl Acad Sci U S A 102:17734-17738.
22. Ohyama M, A Terunuma, CL Tock, MF Radonovich, CA Pise-Masison, SB Hopping, JN Brady, MC Udey and JC Vogel. (2006). Characterization and isolation of stem cellenriched human hair follicle bulge cells. J Clin Invest 116:249-260.
23. Rendl M, L Lewis and E Fuchs. (2005). Molecular dissection of mesenchymal-epithelial interactions in the hair follicle. PLoS Biol 3:e331.
24. Wegner M and CC Stolt. (2005). From stem cells to neurons and glia: A Soxist's view of neural development. Trends Neurosci 28:583-588.
25. Takahashi K and S Yamanaka. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676.
26. Takahashi K, K Tanabe, M Ohnuki, M Narita, T Ichisaka, K Tomoda and S Yamanaka. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872.
27. Park SB, KW Seo, AY So, MS Seo, KR Yu, SK Kang and KS Kang. (2011). SOX2 has a crucial role in the lineage determination and proliferation of mesenchymal stem cells through Dickkopf-1 and c-MYC. Cell Death Differ 19:534-545.
28. Shim JH, HH Kang, TR Lee and DW Shin. (2012). Enrichment and characterization of human dermal stem/progenitor cells using collagen, Type IV. J Dermatol Sci 67:202-205.
29. Scott MA, VT Nguyen, B Levi and AW James. (2011). Current methods of adipogenic differentiation of mesenchymal stem cells. Stem Cells Dev 10:1793-1804.
30. Montemurro T, G Andriolo, E Montelatici, G Weissmann, M Crisan, MR Colnaghi, P Rebulla, F Mosca, B Péault and L Lazzari. (2011). Differentiation and migration properties of human foetal umbilical cord perivascular cells: Potential for lung repair. J Cell Mol Med 15:796-808.
31. Gao L, R McBeath and CS Chen. (2010). Stem cell shape regulates a chondrogenic versus myogenic fate through Rac1 and N-cadherin. Stem Cells 28:564-572.
32. D'Ippolito G, S Diabira, GA Howard, P Menei, BA Roos and PC Schiller. (2004). Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci 117:2971-2981.
33. Alexander CM, J Puchalski, KS Klos, N Badders, L Ailles, CF Kim, P Dirks and MJ Smalley. (2009). Separating stem cells by flow cytometry: Reducing variability for solid tissues. Cell Stem Cell 5:579-583.
34. Hughes OR, R Stewart, I Dimmick and EA Jones. (2009). A critical appraisal of factors affecting the accuracy of results obtained when using flow cytometry in stem cell investigations: Where do you put your gates? Cytometry A 75: 803-810.
35. Pochampally R. (2008). Colony forming unit assays for MSCs. Methods Mol Biol 449:83-91.
36. Morris RJ, Y Liu, L Marles, Z Yang, C Trempus, S Li, JS Lin, JA Sawicki and G Cotsarelis. (2004). Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 22:411-417.
37. Sekiya I, BL Larson, JR Smith, R Pochampally, JG Cui and DJ Prockop. (2002). Expansion of human adult stem cells from bone marrow stroma: Conditions that maximize the yields of early progenitors and evaluate their quality. Stem Cells 20:530-541.
38. Joannides A, P Gaughwin, C Schwiening, H Majed, J Sterling, A Compston and S Chandran. (2004). Efficient generation of neural precursors from adult human skin: Astrocytes promote neurogenesis from skin-derived stem cells. Lancet 364:172-178.
39. Prockop DJ. (1997). Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71-77.
40. Weissman IL. (2000). Stem cells: Units of development, units of regeneration, and units in evolution. Cell 100:157-168.
41. Mezey E, S Key, G Vogelsang, I Szalayova, GD Lange and B Crain. (2003). Transplanted bone marrow generates new neurons in human brains. Proc Natl Acad Sci U S A 100: 1364-1369.
42. Li L and H Clevers. (2010). Coexistence of quiescent and active adult stem cells in mammals. Science 327:542-545.
43. Lysy PA, F Smets, C Sibille, M Najimi and EM Sokal. (2007). Human skin fibroblasts: From mesodermal to hepatocytelike differentiation. Hepatology 46:1574-1585.
44. Bi D, FG Chen, WJ Zhang, GD Zhou, L Cui, W Liu and Y Cao. (2010) Differentiation of human multipotent dermal fibroblasts into islet-like cell clusters. BMC Cell Biol 11:46.
45. Manini I, L Gulino, B Gava, E Pierantozzi, C Curina, D Rossi, A Brafa, C D'Aniello and V Sorrentino. (2011). Multipotent progenitors in freshly isolated and cultured human mesenchymal stem cells: A comparison between adipose and dermal tissue. Cell Tissue Res 344:85-95.
46. Bez A, E Corsini, D Curti, M Biggiogera, A Colombo, RF Nicosia, SF Pagano and EA Parati.(2003). Neurosphere and neurosphere-forming cells: Morphological and ultrastructural characterization. Brain Res 993:18-29.
47. Romano AC, EM Espana, SH Yoo, MT Budak, JM Wolosin and SC Tseng. (2003). Different cell sizes in human limbal and central corneal basal epithelia measured by confocal microscopy and flow cytometry. Invest Ophthalmol Vis Sci 44:5125-5129.
48. Murayama A, Y Matsuzaki, A Kawaguchi, T Shimazaki and H Okano. (2002). Flow cytometric analysis of neural stem cells in the developing and adult mouse brain. J Neurosci Res 69:837-847.
49. Fauquier T, K Rizzoti, M Dattani, R Lovell-Badge and IC Robinson. (2008). SOX2-expressing progenitor cells generate all of the major cell types in the adult mouse pituitary gland. Proc Natl Acad Sci U S A 105:2907-2912.
50. Liu S, S Liu, X Wang, J Zhou, Y Cao, F Wang and E Duan. (2011). The PI3K-Akt pathway inhibits senescence and promotes self-renewal of human skin-derived precursors in vitro. Aging Cell 10:661-674.
51. Su X, M Paris, YJ Gi, KY Tsai, MS Cho, YL Lin, JA Biernaskie, S Sinha, C Prives, et al. (2009). TAp63 prevents premature aging by promoting adult stem cell maintenance. Cell Stem Cell 5:64-75.
52. Gago N, V Pérez-Ló pez, JP Sanz-Jaka, P Cormenzana, I Eizaguirre, A Bernad and A Izeta. (2009). Age-dependent depletion of human skin-derived progenitor cells. Stem Cells 27:1164-1172.
53. Shimizu R, K Okabe, Y Kubota, A Nakamura-Ishizu, H Nakajima and K Kishi. (2011). Sphere formation restores and confers hair-inducing capacity in cultured mesenchymal cells. Exp Dermatol 20:679-681.
54. Ylöstalo JH, TJ Bartosh, K Coble and DJ Prockop. (2012). Human mesenchymal stem/stromal cells cultured as spheroids are self-activated to produce prostaglandin E2 that directs stimulated macrophages into an anti-inflammatory phenotype. Stem Cells 30:2283-2296.
55. Yu KR, SR Yang, JW Jung, H Kim, K Ko, DW Han, SB Park, SW Choi, SK Kang, H Schöler and KS Kang. (2012). CD49f enhances multipotency and maintains stemness through the direct regulation of OCT4 and SOX2. Stem Cells 30:876-887.
56. Riekstina U, R Muceniece, I Cakstina, I Muiznieks and J Ancans. (2008). Characterization of human skin-derived mesenchymal stem cell proliferation rate in different growth conditions. Cytotechnology 58:153-162.
57. Riekstina U, I Cakstina, V Parfejevs, M Hoogduijn, G Jankovskis, I Muiznieks, R Muceniece and J Ancans. (2009). Embryonic stem cell marker expression pattern in human mesenchymal stem cells derived from bone marrow, adipose tissue, heart and dermis. Stem Cell Rev 5:378-386.
58. Jahoda CA, J Whitehouse, AJ Reynolds and N Hole. (2003). Hair follicle dermal cells differentiate into adipogenic and osteogenic lineages. Exp Dermatol 12:849-859.
59. Hoogduijn MJ, Gorjup E and Genever PG. (2006). Comparative characterization of hair follicle dermal stem cells and bone marrow mesenchymal stem cells. Stem Cells Dev 15:49-60.