Human induced pluripotent stem cells differentiated into chondrogenic lineage via generation of mesenchymal progenitor cells

Stem Cells and Development

Volumn 22, Issue 1, 2013, Pages 102-113

  Koyama, Noriaki ^a   Miura, Masako ^a   Nakao, Kazumasa ^a   Kondo, Eri ^a   Fujii, Toshihito ^a   Taura, Daisuke ^a   Kanamoto, Naotetsu ^a   Sone, Masakatsu ^a   Yasoda, Akihiro ^a   Arai, Hiroshi ^a   Bessho, Kazuhisa ^a   Nakao, Kazuwa ^a  

^a KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; CELL LINEAGE; CELL STRUCTURE; CONTROLLED STUDY; CULTURE TECHNIQUE; EMBRYOID BODY; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; MONOLAYER CULTURE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL;

ADULT; ANIMALS; ANTIGENS, DIFFERENTIATION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; COCULTURE TECHNIQUES; EMBRYOID BODIES; FEMALE; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MESENCHYMAL STROMAL CELLS; MICE; TRANSCRIPTOME;

EID: 84871448242     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0127     Document Type: Article

References (64)

1. Nejadnik H, JH Hui, EP Feng Choong, BC Tai and EH Lee. (2010). Autologous bone marrow-derived mesenchymal stem cells versus autologous chondrocyte implantation: an observational cohort study. Am J Sports Med 38:1110-1116.
2. Wakitani S, T Okabe, S Horibe, T Mitsuoka, M Saito, T Koyama, M Nawata, K Tensho, H Kato, et al. (2011). Safety of autologous bone marrow-derived mesenchymal stem cell transplantation for cartilage repair in 41 patients with 45 joints followed for up to 11 years and 5 months. J Tissue Eng Regen Med 5:146-150.
3. Wakitani S, M Nawata, K Tensho, T Okabe, H Machida and H Ohgushi. (2007). Repair of articular cartilage defects in the patello-femoral joint with autologous bone marrow mesenchymal cell transplantation: three case reports involving nine defects in five knees. J Tissue Eng Regen Med 1:74-79.
4. 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 adult human mesenchymal stem cells. Science 284:143-147. (Pubitemid 29282067)
5. 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. (Pubitemid 35471185)
6. Segawa Y, T Muneta, H Makino, A Nimura, T Mochizuki, YJ Ju, Y Ezura, A Umezawa and I Sekiya. (2009). Mesenchymal stem cells derived from synovium, meniscus, anterior cruciate ligament, and articular chondrocytes share similar gene expression profiles. J Orthop Res 27:435-441.
7. Miura M, S Gronthos, M Zhao, B Lu, LW Fisher, PG Robey and S Shi. (2003). SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A 100:5807-5812. (Pubitemid 36576889)
8. Gronthos S, M Mankani, J Brahim, PG Robey and S Shi. (2000). Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci U S A 97:13625-13630.
9. Stenderup K, J Justesen, C Clausen and M Kassem. (2003). Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone33:919-926. (Pubitemid 37543568)
10. Payne KA, DM Didiano and CR Chu. (2010). Donor sex and age influence the chondrogenic potential of human femoral bone marrow stem cells. Osteoarthritis Cartilage 18:705-713.
11. 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. (Pubitemid 350138099)
12. Yu J, MA Vodyanik, K Smuga-Otto, J Antosiewicz-Bourget, JL Frane, S Tian, J Nie, GA Jonsdottir, V Ruotti, et al. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318:1917-1920.
13. Maherali N, T Ahfeldt, A Rigamonti, J Utikal, C Cowan and K Hochedlinger. (2008). A high-efficiency system for the generation and study of human induced pluripotent stem cells. Cell Stem Cell 3:340-345.
14. Yu J, K Hu, K Smuga-Otto, S Tian, R Stewart, II Slukvin and JA Thomson. (2009). Human induced pluripotent stem cells free of vector and transgene sequences. Science 324:797-801.
15. Jia F, KD Wilson, N Sun, DM Gupta, M Huang, Z Li, NJ Panetta, ZY Chen, RC Robbins, et al. (2010). A nonviral minicircle vector for deriving human iPS cells. Nat Methods 7:197-199.
16. Okita K, Y Matsumura, Y Sato, A Okada, A Morizane, S Okamoto, H Hong, M Nakagawa, K Tanabe, et al. (2011). A more efficient method to generate integration-free human iPS cells. Nat Methods 8:409-412.
17. Johnstone B, TM Hering, AI Caplan, VM Goldberg and JU Yoo. (1998). In vitro chondrogenesis of bone marrowderived mesenchymal progenitor cells. Exp Cell Res 238:265-272. (Pubitemid 28366150)
18. Yoo JU, TS Barthel, K Nishimura, L Solchaga, AI Caplan, VM Goldberg and B Johnstone. (1998). The chondrogenic potential of human bone-marrow-derived mesenchymal progenitor cells. J Bone Joint Surg Am 80:1745-1757. (Pubitemid 29013807)
19. Holtzer H, J Abbott, J Lash and S Holtzer. (1960). The loss of phenotypic traits by differentiated cells in vitro, I. Dedifferentiation of cartilage cells. Proc Natl Acad Sci U S A 46:1533-1542.
20. Bigdeli N, C Karlsson, R Strehl, S Concaro, J Hyllner and A Lindahl. (2009). Coculture of human embryonic stem cells and human articular chondrocytes results in significantly altered phenotype and improved chondrogenic differentiation. Stem Cells 27:1812-1821.
21. Sui Y, T Clarke and JS Khillan. (2003). Limb bud progenitor cells induce differentiation of 1pluripotent embryonic stem cells into chondrogenic lineage. Differentiation 71:578-585. (Pubitemid 38091100)
22. Hwang YS, JM Polak and A Mantalaris. (2008). In vitro direct chondrogenesis of murine embryonic stem cells by bypassing embryoid body formation. Stem Cells Dev 17:971-978.
23. Kim JH, HJ Do, HM Yang, JH Oh, SJ Choi, DK Kim, KY Cha and HM Chung. (2005). Overexpression of SOX9 in mouse embryonic stem cells directs the immediate chondrogenic commitment. Exp Mol Med 37:261-268.
24. Vinatier C, D Mrugala, C Jorgensen, J Guicheux and D Noe?l. (2009). Cartilage engineering: a crucial combination of cells, biomaterials and biofactors. Trends Biotechnol 27:307-314.
25. Medvedev SP, EV Grigor'eva, AI Shevchenko, AA Malakhova,EV Dementyeva, AA Shilov, EA Pokushalov, AM Zaidman, MA Aleksandrova, et al. (2011). Human induced pluripotent stem cells derived from fetal neural stem cells successfully undergo directed differentiation into cartilage. Stem Cells Dev 20:1099-1112.
26. Thomson JA, J Itskovitz-Eldor, SS Shapiro, MA Waknitz, JJ Swiergiel, VS Marshall and JM Jones. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147. (Pubitemid 28516247)
27. Fujioka T, K Yasuchika, Y Nakamura, N Nakatsuji and H Suemori. (2004). A simple and efficient cryopreservation method for primate embryonic stem cells. Int J Dev Biol 48:1149-1154. (Pubitemid 40179582)
28. Koyama N, Y Okubo, K Nakao, K Osawa, K Fujimura and K Bessho. (2011). Pluripotency of mesenchymal cells derived from synovial fluid in patients with temporomandibular joint disorder. Life Sci 89:741-747.
29. Dominici M, K Le Blanc, I Mueller, I Slaper-Cortenbach, F Marini, D Krause, R Deans, A Keating, DJ Prockop and E Horwitz. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for cellular therapy position statement. Cytotherapy 8:315-317. (Pubitemid 44269669)
30. Salem HK and C Thiemermann. (2010). Mesenchymal stromal cells: current understanding and clinical status. Stem Cells 28:585-596.
31. Nishikawa SI, S Nishikawa, M Hirashima, N Matsuyoshi and H Kodama. (1998). Progressive lineage analysis by cell sorting and culture identifies FLK1 + VE-cadherin + cells at a diverging point of endothelial and hemopoietic lineages. Development 125:1747-1757. (Pubitemid 28256742)
32. Simmons PJ and B Torok-Storb. (1991). Identification of stromal cell precursors in human bone marrow by a novel monoclonal antibody, STRO-1. Blood 78:55-62.
33. Ning H, G Lin, TF Lue and CS Lin. (2011). Mesenchymal stem cell marker Stro-1 is a 75 kD endothelial antigen. Biochem Biophys Res Commun 413:353-357.
34. Barberi T, LM Willis, ND Socci and L Studer. (2005). Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2:e161.
35. Liu Y, AJ Goldberg, JE Dennis, GA Gronowicz and LT Kuhn. (2012). One-step derivation of mesenchymal stem cell (MSC)-like cells from human pluripotent stem cells on a fibrillar collagen coating. PLos One 7:e33225.
36. Wu R, B Gu, X Zhao, Z Tan, L Chen, J Zhu and M Zhang. (2011). Derivation of multipotent nestin (+) /CD271 (-)/ STRO-1 (-) mesenchymal-like precursors from human embryonic stem cells in chemically defined conditions. Hum Cell [Epub ahead of print]; DOI:10.1007/s13577-011-0022-3.
37. Honczarenko M, Y Le, M Swierkowski, I Ghiran, AM Glodek and LE Silberstein. (2006). Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells 24:1030-1041. (Pubitemid 44464736)
38. Wagner W, P Horn, M Castoldi, A Diehlmann, S Bork, R Saffrich, V Benes, J Blake, S Pfister, V Eckstein and AD Ho. (2008). Replicative senescence of mesenchymal stem cells: a continuous and organized process. PLos One 3:e2213.
39. Jung EM, O Kwon, KS Kwon, YS Cho, SK Rhee, JK Min and DB Oh. (2011). Evidences for correlation between the reduced VCAM-1 expression and hyaluronan synthesis during cellular senescence of human mesenchymal stem cells. Biochem Biophys Res Commun 404:463-469.
40. Toh WS, Z Yang, H Liu, BC Heng, EH Lee and T Cao. (2007). Effects of culture conditions and bone morphogenetic protein 2 on extent of chondrogenesis from human embryonic stem cells. Stem Cells 25:950-960. (Pubitemid 46572592)
41. Nakagawa M, M Koyanagi, K Tanabe, K Takahashi, T Ichisaka, T Aoi, K Okita, Y Mochiduki, N Takizawa and S Yamanaka. (2008). Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 26:101-106.
42. Suemori H, K Yasuchika, K Hasegawa, T Fujioka, N Tsuneyoshi and N Nakatsuji. (2006). Efficient establishment of human embryonic stem cell lines and long-term maintenancewith stable karyotype by enzymatic bulk passage. Biochem Biophys Res Commun 345:926-932. (Pubitemid 43776486)
43. Akiyama H, MC Chaboissier, JF Martin, A Schedl and B de Crombrugghe. (2002). 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 16:2813-2828. (Pubitemid 35253149)
44. Han Y and V Lefebvre. (2008). L-Sox5 and Sox6 drive expression of the aggrecan gene in cartilage by securing binding of Sox9 to a far-upstream enhancer. Mol Cell Biol 28:4999-5013.
45. Lefebvre V and P Smits. (2005). Transcriptional control of chondrocyte fate and differentiation. Birth Defects Res C Embryo Today 75:200-212. (Pubitemid 41456322)
46. Puetzer JL, JN Petitte and EG Loboa. (2010). Comparativereview of growth factors for induction of three-dimensional in vitro chondrogenesis in human mesenchymal stem cells isolated from bone marrow and adipose tissue. Tissue Eng Part B Rev 16:435-444.
47. Hwang NS, S Varghese, Z Zhang and J Elisseeff. (2006). Chondrogenic differentiation of human embryonic stem cellderived cells in arginine-glycine-aspartate-modified hydrogels. Tissue Eng 12:2695-2706. (Pubitemid 46141292)
48. Xu C, J Jiang, V Sottile, J McWhir, J Lebkowski and MK Carpenter. (2004). Immortalized fibroblast-like cells derived from human embryonic stem cells support undifferentiated cell growth. Stem Cells 22:972-980. (Pubitemid 39507084)
49. Lian Q, E Lye, K Suan Yeo, E Khia Way Tan, M Salto-Tellez, TM Liu, N Palanisamy, RM El Oakley, EH Lee, B Lim and SK Lim. (2007). Derivation of clinically compliant MSCs from CD105 +, CD24- differentiated human ESCs. Stem Cells 25:425-436. (Pubitemid 46232798)
50. Teramura T, Y Onodera, T Mihara, Y Hosoi, C Hamanishi and K Fukuda. (2010). Induction of mesenchymal progenitor cells with chondrogenic property from mouse-induced pluripotent stem cells. Cell Reprogram 12:249-261.
51. Foster JW, MA Dominguez-Steglich, S Guioli, C Kwok, PA Weller, M Stevanović, J Weissenbach, S Mansour, ID Young, et al. (1994). Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene. Nature 372:525-530. (Pubitemid 24368528)
52. Wagner T, J Wirth, J Meyer, B Zabel, M Held, J Zimmer, J Pasantes, FD Bricarelli, J Keutel, et al. (1994). Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79:1111-1120.
53. Bi W, W Huang, DJ Whitworth, JM Deng, Z Zhang, RR Behringer and B de Crombrugghe. (2001). Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization. Proc Natl Acad Sci U S A 98:6698-6703. (Pubitemid 32538279)
54. Gong G, D Ferrari, CN Dealy and RA Kosher. (2010). Direct and progressive differentiation of human embryonic stem cells into the chondrogenic lineage. J Cell Physiol 224:664-671.
55. Toh WS, XM Guo, AB Choo, K Lu, EH Lee and T Cao. (2009). Differentiation and enrichment of expandable chondrogenic cells from human embryonic stem cells in vitro. J Cell Mol Med 13:3570-3590.
56. Oldershaw RA, MA Baxter, ET Lowe, N Bates, LM Grady, F oncin, DR Brison, TE Hardingham and SJ Kimber. (2010). Directed differentiation of human embryonic stem cells toward chondrocytes. Nat Biotechnol 28:1187-1194.
57. Lafont JE, S Talma, C Hopfgarten and CL Murphy. (2008). Hypoxia promotes the differentiated human articular chondrocyte phenotype through SOX9-dependent andindependent pathways. J Biol Chem 283:4778-4786.
58. Khan WS, AB Adesida and TE Hardingham. (2007). Hypoxic conditions increase hypoxia-inducible transcription factor 2alpha and enhance chondrogenesis in stem cells from the infrapatellar fat pad of osteoarthritis patients. Arthritis Res Ther 9:R55.
59. Grayson WL, F Zhao, B Bunnell and T Ma. (2007). Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 358: 948-953. (Pubitemid 46802482)
60. Krinner A, M Zscharnack, A Bader, D Drasdo and J Galle. (2009). Impact of oxygen environment on mesenchymal stem cell expansion and chondrogenic differentiation. Cell Prolif 42:471-484.
61. Feng G, Y Wan, G Balian, CT Laurencin and X Li. (2008). Adenovirus-mediated expression of growth and differentiation factor-5 romotes chondrogenesis of adipose stem cells. Growth Factors 26:132-142. (Pubitemid 351911395)
62. Vinardell T, RA Rolfe, CT Buckley, EG Meyer, M Ahearne, P Murphy and DJ Kelly. (2012). Hydrostatic pressure acts to stabilise a chondrogenic phenotype in porcine joint tissue derived stem cells. Eur Cell Mater 23:121-132.
63. Miura K, Y Okada, T Aoi, A Okada, K Takahashi, K Okita, M Nakagawa, M Koyanagi, K Tanabe, et al. (2009). Variation in the safety of induced pluripotent stem cell lines. Nat Biotechnol 27:743-745.
64. Kulkeaw K, Y Horio, C Mizuochi, M Ogawa and D Sugiyama.(2010). Variation in hematopoietic potential of induced pluripotent stem cell lines. Stem Cell Rev 6:381-389.