Feasibility of human hair follicle-derived mesenchymal stem cells/CultiSpher®-G constructs in regenerative medicine

Cell and Tissue Research

Volumn 362, Issue 1, 2015, Pages 69-86

  Li, Pengdong ^a,b   Liu, Feilin ^a   Wu, Chunling ^c   Jiang, Wenyue ^b   Zhao, Guifang ^a   Liu, Li ^a   Bai, Tingting ^a   Wang, Li ^a   Jiang, Yixu ^a   Guo, Lili ^d   Qi, Xiaojuan ^a   Kou, Junna ^a   Fan, Ruirui ^a   Hao, Deshun ^a   Lan, Shaowei ^a   Li, Yulin ^a   Liu, Jin Yu ^a,b  

^a Basic Medical College   (China)

^b JILIN UNIVERSITY   (China)

^c INSTITUTE OF PLANT PROTECTION   (China)

^d Jilin Provincial Hospital of Cancer   (China)

Author keywords

3D cell culture; CultiSpher G microbeads; Hair follicle mesenchymal stem cells; Long term expansion; Spinner culture

Indexed keywords

CELL SURFACE MARKER; NESTIN;

ADIPOCYTE; ADULT; APOPTOSIS; ARTICLE; CELL ASSAY; CELL CYCLE; CELL DENSITY; CELL DIFFERENTIATION; CELL EXPANSION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; CULTURE MEDIUM; CULTURE TECHNIQUE; FEASIBILITY STUDY; FEMALE; HAIR FOLLICLE; HAIR FOLLICLE DERIVED MESENCHYMAL STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; MESENCHYMAL STEM CELL; MIDDLE AGED; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGENERATIVE MEDICINE; SMOOTH MUSCLE FIBER; CYTOLOGY; MESENCHYMAL STROMA CELL; METABOLISM;

ADULT; CELL DIFFERENTIATION; CELL PROLIFERATION; FEMALE; HAIR FOLLICLE; HUMANS; MALE; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; REGENERATIVE MEDICINE;

EID: 84941881027     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-015-2182-z     Document Type: Article

References (60)

1. Amoh Y, Li L, Campillo R, Kawahara K, Katsuoka K, Penman S, Hoffman RM (2005a) 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
2. Amoh Y, Li L, Hamada Y, Katsuoka K, Hoffman RM (2005b) Multipotent nestin-positive, keratin-negative hair-follicle bulge stem cells can form neurons. J Investig Dermatol 125:A5
3. Amoh Y, Li L, Katsuoka K, Penman S, Hoffman RM (2005c) Multipotent nestin-positive, keratin-negative hair-follicle bulge stem cells can form neurons. Proc Natl Acad Sci U S A 102:5530–5534
4. Amoh Y, Li L, Katsuoka K, Hoffman RM (2008) Multipotent hair follicle stem cells promote repair of spinal cord injury and recovery of walking function. Cell Cycle 7:1865–1869
5. Bajpai VK, Mistriotis P, Andreadis ST (2012) Clonal multipotency and effect of long-term in vitro expansion on differentiation potential of human hair follicle derived mesenchymal stem cells. Stem Cell Res 8:74–84
6. Barman JM, Astore I, Pecoraro V (1965) The Normal Trichogram of the Adult. J Invest Dermatol 44:233–236
7. Chen M, Wang X, Ye Z, Zhang Y, Zhou Y, Tan WS (2011) A modular approach to the engineering of a centimeter-sized bone tissue construct with human amniotic mesenchymal stem cells-laden microcarriers. Biomaterials 32:7532–7542
8. Chen AK, Reuveny S, Oh SK (2013) Application of human mesenchymal and pluripotent stem cell microcarrier cultures in cellular therapy: achievements and future direction. Biotechnol Adv 31:1032–1046
9. Choi JS, Kim BS, Kim JD, Choi YC, Lee EK, Park K, Lee HY, Cho YW (2011) In vitro expansion of human adipose-derived stem cells in a spinner culture system using human extracellular matrix powders. Cell Tissue Res 345:415–423
10. Duong J, Mii S, Uchugonova A, Liu F, Moossa AR, Hoffman RM (2012) Real-time confocal imaging of trafficking of nestin-expressing multipotent stem cells in mouse whiskers in long-term 3-D histoculture. In Vitro Cell Dev Biol Anim 48:301–305
11. Hayashi M, Sofuni T, Ishidate M Jr (1983) An application of Acridine Orange fluorescent staining to the micronucleus test. Mutat Res 120:241–247
12. Higgins CA, Itoh M, Inoue K, Richardson GD, Jahoda CAB, Christiano AM (2012) Reprogramming of Human Hair Follicle Dermal Papilla Cells into Induced Pluripotent Stem Cells. J Investig Dermatol 132:1725–1727
13. Hodgkinson T, Yuan XF, Bayat A (2009) Adult stem cells in tissue engineering. Expert Rev Med Devices 6:621–640
14. Hoffman RM (2006) The hair follicle and its stem cells as drug delivery targets. Expert Opin Drug Deliv 3:437–443
15. Hoffman RM (2007) The potential of nestin-expressing hair follicle stem cells in regenerative medicine. Expert Opin Biol Ther 7:289–291
16. in’t Anker PS, Noort WA, Scherjon SA, Kleijburg-van der Keur C, Kruisselbrink AB, van Bezooijen RL, Beekhuizen W, Willemze R, Kanhai HH, Fibbe WE (2003) Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica 88:845–852
17. Ito T, Sawada R, Fujiwara Y, Seyama Y, Tsuchiya T (2007) FGF-2 suppresses cellular senescence of human mesenchymal stem cells by down-regulation of TGF-beta2. Biochem Biophys Res Commun 359:108–114
18. Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33:245–254
19. Jahoda CAB, Whitehouse CJ, Reynolds AJ, Hole N (2003) Hair follicle dermal cells differentiate into adipogenic and osteogenic lineages. Exp Dermatol 12:849–859
20. Ji SZ, Xiao SC, Luo PF, Huang GF, Wang GY, Zhu SH, Wu MJ, Xia ZF (2011) An epidermal stem cells niche microenvironment created by engineered human amniotic membrane. Biomaterials 32:7801–7811
21. Kim I, Park H, Shin Y, Kim M (2009) Adipogenic Differentiation of Adipose-Derived Stem Cells on Collagen Microbeads. Tissue Eng Regen Med 6:924–930
22. Krishan A (1975) Rapid flow cytofluorometric analysis of mammalian cell cycle by propidium iodide staining. J Cell Biol 66:188–193
23. Kruger K, Blume-Peytavi U, Orfanos CE (1999) Basal cell carcinoma possibly originates from the outer root sheath and or the bulge region of the vellus hair follicle. Arch Dermatol Res 291:253–259
24. Lako M, Armstrong L, Cairns PM, Harris S, Hole N, Jahoda CA (2002) Hair follicle dermal cells repopulate the mouse haematopoietic system. J Cell Sci 115:3967–3974
25. Li Y, Zhao X (2014) Concise review: Fragile X proteins in stem cell maintenance and differentiation. Stem Cells 32:1724–1733
26. 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 U S A 100:9958–9961
27. Liu JY, Hafner J, Dragieva G, Burg G (2004a) Bioreactor microcarrier cell culture system (Bio-MCCS) for large-scale production of autologous melanocytes. Cell Transplant 13:809–816
28. Liu JY, Hafner J, Dragieva G, Seifert B, Burg G (2004b) Autologous cultured keratinocytes on porcine gelatin microbeads effectively heal chronic venous leg ulcers. Wound Repair Regen 12:148–156
29. Liu JY, Peng HF, Andreadis ST (2008) Contractile smooth muscle cells derived from hair-follicle stem cells. Cardiovasc Res 79:24–33
30. Liu JY, Peng HF, Gopinath S, Tian J, Andreadis ST (2010) Derivation of functional smooth muscle cells from multipotent human hair follicle mesenchymal stem cells. Tissue Eng Part A 16:2553–2564
31. Liu F, Uchugonova A, Kimura H, Zhang C, Zhao M, Zhang L, Koenig K, Duong J, Aki R, Saito N, Mii S, Amoh Y, Katsuoka K, Hoffman RM (2011) The bulge area is the major hair follicle source of nestin-expressing pluripotent stem cells which can repair the spinal cord compared to the dermal papilla. Cell Cycle 10:830–839
32. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25:402–408
33. Lutz SE, Lengfeld J, Agalliu D (2014) Stem cell-based therapies for multiple sclerosis: recent advances in animal models and human clinical trials. Regen Med 9:129–132
34. Martin Y, Eldardiri M, Lawrence-Watt DJ, Sharpe JR (2011) Microcarriers and their potential in tissue regeneration. Tissue Eng B 17:71–80
35. Mii S, Uehara F, Yano S, Tran B, Miwa S, Hiroshima Y, Amoh Y, Katsuoka K, Hoffman RM (2013) Nestin-Expressing Stem Cells Promote Nerve Growth in Long-Term 3-Dimensional Gelfoam(R)-Supported Histoculture. PLoS ONE 8:e67153
36. Minguell JJ, Erices A, Conget P (2001) Mesenchymal stem cells. Exp Biol Med (Maywood) 226:507–520
37. Motaln H, Schichor C, Lah TT (2010) Human mesenchymal stem cells and their use in cell-based therapies. Cancer 116:2519–2530
38. Olmer R, Haase A, Merkert S, Cui W, Palecek J, Ran C, Kirschning A, Scheper T, Glage S, Miller K, Curnow EC, Hayes ES, Martin U (2010) Long term expansion of undifferentiated human iPS and ES cells in suspension culture using a defined medium. Stem Cell Res 5:51–64
39. Peng HF, Liu JY, Andreadis ST, Swartz DD (2011) Hair follicle-derived smooth muscle cells and small intestinal submucosa for engineering mechanically robust and vasoreactive vascular media. Tissue Eng Part A 17:981–990
40. Phillips HJ, Terryberry JE (1957) Counting actively metabolizing tissue cultured cells. Exp Cell Res 13:341–347
41. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143–147
42. Rubin JP, Bennett JM, Doctor JS, Tebbets BM, Marra KG (2007) Collagenous microbeads as a scaffold for tissue engineering with adipose-derived stem cells. Plast Reconstr Surg 120:414–424
43. Salic A, Mitchison TJ (2008) A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc Natl Acad Sci U S A 105:2415–2420
44. Sart S, Schneider YJ, Agathos SN (2009) Ear mesenchymal stem cells: An efficient adult multipotent cell population fit for rapid and scalable expansion. J Biotechnol 139:291–299
45. Sart S, Agathos SN, Li Y (2013) Engineering stem cell fate with biochemical and biomechanical properties of microcarriers. Biotechnol Prog 29:1354–1366
46. Schop D, van Dijkhuizen-Radersma R, Borgart E, Janssen FW, Rozemuller H, Prins HJ, de Bruijn JD (2010) Expansion of human mesenchymal stromal cells on microcarriers: growth and metabolism. J Tissue Eng Regen Med 4:131–140
47. Shim KJ, Han I (2007) Use of hair follicular cells for cultured skin substitutes. Tissue Eng Regen Med 4:191–196
48. Sun LY, Hsieh DK, Yu TC, Chiu HT, Lu SF, Luo GH, Kuo TK, Lee OK, Chiou TW (2009) Effect of pulsed electromagnetic field on the proliferation and differentiation potential of human bone marrow mesenchymal stem cells. Bioelectromagnetics 30:251–260
49. Sun LY, Hsieh DK, Syu WS, Li YS, Chiu HT, Chiou TW (2010) Cell proliferation of human bone marrow mesenchymal stem cells on biodegradable microcarriers enhances in vitro differentiation potential. Cell Prolif 43:445–456
50. Sun LY, Lin SZ, Li YS, Harn HJ, Chiou TW (2011) Functional cells cultured on microcarriers for use in regenerative medicine research. Cell Transplant 20:49–62
51. Timmins NE, Kiel M, Gunther M, Heazlewood C, Doran MR, Brooke G, Atkinson K (2012) Closed system isolation and scalable expansion of human placental mesenchymal stem cells. Biotechnol Bioeng 109:1817–1826
52. Uchugonova A, Duong J, Zhang N, Konig K, Hoffman RM (2011) The bulge area is the origin of nestin-expressing pluripotent stem cells of the hair follicle. J Cell Biochem 112:2046–2050
53. Wagner W, Horn P, Castoldi M, Diehlmann A, Bork S, Saffrich R, Benes V, Blake J, Pfister S, Eckstein V, Ho AD (2008) Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLoS ONE 3:e2213
54. Wang YM, Liu JY, Tan XH, Li GF, Gao YH, Liu XJ, Zhang LH, Li YL (2013) Induced pluripotent stem cells from human hair follicle mesenchymal stem cells. Stem Cell Rev Rep 9:451–460
55. Wu QF, Wu CT, Dong B, Wang LS (2003) Cultivation of human mesenchymal stem cells on macroporous CultiSpher G microcarriers. Zhongguo Shi Yan Xue Ye Xue Za Zhi 11:15–21
56. Wu C, Liu F, Li P, Zhao G, Lan S, Jiang W, Meng X, Tian L, Li G, Li Y, Liu JY (2014) Engineered hair follicle mesenchymal stem cells overexpressing controlled-release insulin reverse hyperglycemia in mice with type l diabetes. Cell Transplant. doi:10.3727/096368914X681919
57. Yang Y, Rossi FM, Putnins EE (2007) Ex vivo expansion of rat bone marrow mesenchymal stromal cells on microcarrier beads in spin culture. Biomaterials 28:3110–3120
58. Yuan Y, Kallos MS, Hunter C, Sen A (2012) Improved expansion of human bone marrow-derived mesenchymal stem cells in microcarrier-based suspension culture. J Tissue Eng Regen Med 8(3):210–225
59. Zhang X, Wang Y, Gao Y, Liu X, Bai T, Li M, Li L, Chi G, Xu H, Liu F, Liu JY, Li Y (2013) Maintenance of high proliferation and multipotent potential of human hair follicle-derived mesenchymal stem cells by growth factors. Int J Mol Med 31:913–921
60. Zhou Y, Yan Z, Zhang H, Lu W, Liu S, Huang X, Luo H, Jin Y (2011) Expansion and delivery of adipose-derived mesenchymal stem cells on three microcarriers for soft tissue regeneration. Tissue Eng Part A 17:2981–2997