Efficient differentiation of human iPSC-derived mesenchymal stem cells to chondroprogenitor cells

Journal of Cellular Biochemistry

Volumn 114, Issue 2, 2013, Pages 480-490

  Guzzo, Rosa M ^a   Gibson, Jason ^a   Xu, Ren He ^a   Lee, Francis Y ^b   Drissi, Hicham ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

Chondrogenic differentiation; High density culture; Human induced pluripotent stem cells; Mesenchymal stem cells

Indexed keywords

AGGRECAN; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN TYPE 1; COLLAGEN TYPE 2; COLLAGEN TYPE 9; MEMBRANE ANTIGEN; PROTEOGLYCAN; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX5; TRANSCRIPTION FACTOR SOX6; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTION FACTOR TWIST;

ADIPOCYTE; ARTICLE; ARTICULAR CARTILAGE; CARTILAGE; CARTILAGE CELL; CARTILAGE INJURY; CARTILAGE STEM CELL; CELL DENSITY; CELL DIFFERENTIATION; CELL FUNCTION; CELL HETEROGENEITY; CELL LINEAGE; CELL POPULATION; CONTROLLED STUDY; FIBROCARTILAGE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MESENCHYMAL STEM CELL; MIXED CELL CULTURE; NUCLEOTIDE SEQUENCE; OSTEOBLAST; PHENOTYPE; PLURIPOTENT STEM CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TRANSIENT CARTILAGE;

ADIPOCYTES; BONE AND BONES; BONE MORPHOGENETIC PROTEIN 2; CARTILAGE, ARTICULAR; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHONDROCYTES; CHONDROGENESIS; COLLAGEN TYPE II; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MESENCHYMAL STROMAL CELLS;

EID: 84872721073     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24388     Document Type: Article

References (43)

1. Barberi T, Willis LM, Socci ND, Studer L. 2005. Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2:e161.
2. Barna M, Niswander L. 2007. Visualization of cartilage formation: Insight into cellular properties of skeletal progenitors and chondrodysplasia syndromes. Dev Cell 12:931-941.
3. Baxter MA, Wynn RF, Jowitt SN, Wraith JE, Fairbairn LJ, Bellantuono I. 2004. Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion. Stem Cells 22:675-682.
4. Bigdeli N, Karlsson C, Strehl R, Concaro S, Hyllner J, Lindahl A. 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.
5. Bradley EW, Drissi MH. 2010. WNT5A regulates chondrocyte differentiation through differential use of the CaN/NFAT and IKK/NF-kappaB pathways. Mol Endocrinol 24:1581-1593.
6. Chen FH, Tuan RS. 2008. Mesenchymal stem cells in arthritic diseases. Arthritis Res Ther 10:223.
7. Daniels K, Reiter R, Solursh M. 1996. Micromass cultures of limb and other mesenchyme. Methods Cell Biol 51:237-247.
8. Fischer L, Boland G, Tuan RS. 2002. Wnt signaling during BMP-2 stimulation of mesenchymal chondrogenesis. J Cell Biochem 84:816-831.
9. Gong G, Ferrari D, Dealy CN, Kosher RA. 2010. Direct and progressive differentiation of human embryonic stem cells into the chondrogenic lineage. J Cell Physiol 224:664-671.
10. Harkness L, Taipaleenmaki H, Mahmood A, Frandsen U, Saamanen AM, Kassem M, Abdallah BM. 2009. Isolation and differentiation of chondrocytic cells derived from human embryonic stem cells using dlk1/FA1 as a novel surface marker. Stem Cell Rev 5:353-368.
11. Hwang NS, Varghese S, Elisseeff J. 2008a. Derivation of chondrogenically-committed cells from human embryonic cells for cartilage tissue regeneration. PLoS ONE 3:e2498.
12. Hwang NS, Varghese S, Lee HJ, Zhang Z, Ye Z, Bae J, Cheng L, Elisseeff J. 2008b. In vivo commitment and functional tissue regeneration using human embryonic stem cell-derived mesenchymal cells. Proc Natl Acad Sci USA 105:20641-20646.
13. Jones EA, Kinsey SE, English A, Jones RA, Straszynski L, Meredith DM, Markham AF, Jack A, Emery P, McGonagle D. 2002. Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 46:3349-3360.
14. Karlsson C, Emanuelsson K, Wessberg F, Kajic K, Axell MZ, Eriksson PS, Lindahl A, Hyllner J, Strehl R. 2009. Human embryonic stem cell-derived mesenchymal progenitors - Potential in regenerative medicine. Stem Cell Res 3:39-50.
15. Kramer J, Hegert C, Guan K, Wobus AM, Muller PK, Rohwedel J. 2000. Embryonic stem cell-derived chondrogenic differentiation in vitro: Activation by BMP-2 and BMP-4. Mech Dev 92:193-205.
16. Lefebvre V, Li P, de Crombrugghe B. 1998. A new long form of Sox5 (L-Sox5), Sox6 and Sox9 are coexpressed in chondrogenesis and cooperatively activate the type II collagen gene. EMBO J 17:5718-5733.
17. Lefebvre V, Behringer RR, de Crombrugghe B. 2001. L-Sox5, Sox6 and Sox9 control essential steps of the chondrocyte differentiation pathway. Osteoarthritis Cartilage 9(Suppl. A):S69-S75.
18. Lian Q, Lye E, Suan Yeo K, Khia Way Tan E, Salto-Tellez M, Liu TM, Palanisamy N, El Oakley RM, Lee EH, Lim B, Lim SK. 2007. Derivation of clinically compliant MSCs from CD105+, CD24- differentiated human ESCs. Stem Cells 25:425-436.
19. Lian Q, Zhang Y, Zhang J, Zhang HK, Wu X, Lam FF, Kang S, Xia JC, Lai WH, Au KW, Chow YY, Siu CW, Lee CN, Tse HF. 2010. Functional mesenchymal stem cells derived from human induced pluripotent stem cells attenuate limb ischemia in mice. Circulation 121:1113-1123.
20. Marion RM, Strati K, Li H, Tejera A, Schoeftner S, Ortega S, Serrano M, Blasco MA. 2009. Telomeres acquire embryonic stem cell characteristics in induced pluripotent stem cells. Cell Stem Cell 4:141-154.
21. Martins-Taylor K, Nisler BS, Taapken SM, Compton T, Crandall L, Montgomery KD, Lalande M, Xu RH. 2011. Recurrent copy number variations in human induced pluripotent stem cells. Nat Biotechnol 29:488-491.
22. McAlinden A, Havlioglu N, Liang L, Davies SR, Sandell LJ. 2005. Alternative splicing of type II procollagen exon 2 is regulated by the combination of a weak 5' splice site and an adjacent intronic stem-loop cis element. J Biol Chem 280:32700-32711.
23. Mello MA, Tuan RS. 1999. High density micromass cultures of embryonic limb bud mesenchymal cells: An in vitro model of endochondral skeletal development. In Vitro Cell Dev Biol Anim 35:262-269.
24. Murdoch AD, Grady LM, Ablett MP, Katopodi T, Meadows RS, Hardingham TE. 2007. Chondrogenic differentiation of human bone marrow stem cells in transwell cultures: Generation of scaffold-free cartilage. Stem Cells 25:2786-2796.
25. Nakagawa T, Lee SY, Reddi AH. 2009. Induction of chondrogenesis from human embryonic stem cells without embryoid body formation by bone morphogenetic protein 7 and transforming growth factor beta1. Arthritis Rheum 60:3686-3692.
26. Nakayama N, Umeda K. 2011. From Pluripotent stem cells to lineage-specific chondrocytes: Essential signaling and cellular intermediates. In: Atwood C, editor. Embryonic stem cells: The hormonal regulation of pluripotency and embryogenesis. Manhattan, New York: InTech.
27. Oldershaw RA, Baxter MA, Lowe ET, Bates N, Grady LM, Soncin F, Brison DR, Hardingham TE, Kimber SJ. 2010. Directed differentiation of human embryonic stem cells toward chondrocytes. Nat Biotechnol 28:1187-1194.
28. Pizette S, Niswander L. 2000. BMPs are required at two steps of limb chondrogenesis: Formation of prechondrogenic condensations and their differentiation into chondrocytes. Dev Biol 219:237-249.
29. Prockop DJ. 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71-74.
30. Sethe S, Scutt A, Stolzing A. 2006. Aging of mesenchymal stem cells. Ageing Res Rev 5:91-116.
31. Sieber C, Kopf J, Hiepen C, Knaus P. 2009. Recent advances in BMP receptor signaling. Cytokine Growth Factor Rev 20:343-355.
32. Smith N, Dong Y, Lian JB, Pratap J, Kingsley PD, van Wijnen AJ, Stein JL, Schwarz EM, O'Keefe RJ, Stein GS, Drissi MH. 2005. Overlapping expression of Runx1(Cbfa2) and Runx2(Cbfa1) transcription factors supports cooperative induction of skeletal development. J Cell Physiol 203:133-143.
33. Soung do Y, Dong Y, Wang Y, Zuscik MJ, Schwarz EM, O'Keefe RJ, Drissi H. 2007. Runx3/AML2/Cbfa3 regulates early and late chondrocyte differentiation. J Bone Miner Res 22:1260-1270.
34. Steinert AF, Ghivizzani SC, Rethwilm A, Tuan RS, Evans CH, Noth U. 2007. Major biological obstacles for persistent cell-based regeneration of articular cartilage. Arthritis Res Ther 9:213.
35. Stolzing A, Jones E, McGonagle D, Scutt A. 2008. Age-related changes in human bone marrow-derived mesenchymal stem cells: Consequences for cell therapies. Mech Ageing Dev 129:163-173.
36. Toh WS, Guo XM, Choo AB, Lu K, Lee EH, Cao T. 2009. Differentiation and enrichment of expandable chondrogenic cells from human embryonic stem cells in vitro. J Cell Mol Med 13:3570-3590.
37. Toh WS, Lee EH, Richards M, Cao T. 2010. In vitro derivation of chondrogenic cells from human embryonic stem cells. Methods Mol Biol 584:317-331.
38. Toh WS, Lee EH, Cao T. 2011. Potential of human embryonic stem cells in cartilage tissue engineering and regenerative medicine. Stem Cell Rev 7:544-559.
39. Wang Y, Belflower RM, Dong YF, Schwarz EM, O'Keefe RJ, Drissi H. 2005. Runx1/AML1/Cbfa2 mediates onset of mesenchymal cell differentiation toward chondrogenesis. J Bone Miner Res 20:1624-1636.
40. Yoon BS, Lyons KM. 2004. Multiple functions of BMPs in chondrogenesis. J Cell Biochem 93:93-103.
41. Yoon BS, Ovchinnikov DA, Yoshii I, Mishina Y, Behringer RR, Lyons KM. 2005. Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc Natl Acad Sci USA 102:5062-5067.
42. Zhang X, Ziran N, Goater JJ, Schwarz EM, Puzas JE, Rosier RN, Zuscik M, Drissi H, O'Keefe RJ. 2004. Primary murine limb bud mesenchymal cells in long-term culture complete chondrocyte differentiation: TGF-beta delays hypertrophy and PGE2 inhibits terminal differentiation. Bone 34:809-817.
43. Zhang L, Su P, Xu C, Yang J, Yu W, Huang D. 2010. Chondrogenic differentiation of human mesenchymal stem cells: A comparison between micromass and pellet culture systems. Biotechnol Lett 32:1339-1346.