Differentiation of Mouse Induced Pluripotent Stem Cells (iPSCs) into Nucleus Pulposus-Like Cells In Vitro

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Chen, Jun ^a   Lee, Esther J ^b   Jing, Liufang ^b   Christoforou, Nicolas ^b   Leong, Kam W ^b   Setton, Lori A ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b Duke University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LAMININ;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD24+ CELL; CELL CULTURE; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL ISOLATION; CELL SELECTION; CELL THERAPY; CONTROLLED STUDY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MAGNETIC ACTIVATED CELL SORTING; MOUSE; NONHUMAN; NOTOCHORD; NUCLEUS PULPOSUS; OXYGEN TENSION; PHENOTYPE; PLURIPOTENT STEM CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANTIGENS, CD24; CELL DIFFERENTIATION; CULTURE MEDIA, CONDITIONED; INDUCED PLURIPOTENT STEM CELLS; INTERVERTEBRAL DISC DEGENERATION; MICE; NOTOCHORD; PHENOTYPE;

EID: 84884560038     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0075548     Document Type: Article

References (70)

1. Setton LA, Bonassar L, Masuda K, (2007) Regeneration and Replacement of the Intervertebral Disc in Principles of Tissue Engineering In: Lanza R, Langer R, Vacanti JP, eds. 3rd ed. Elsevier Science.
2. Humzah MD, Soames RW, (1988) Human intervertebral disc: structure and function. Anat Rec 220: 337-356. doi:10.1002/ar.1092200402. PubMed: 3289416.
3. Oegema TR Jr., (1993) Biochemistry of the intervertebral disc. Clin Sports Med 12: 419-439. PubMed: 8364983.
4. Roberts S, Menage J, Duance V, Wotton S, Ayad S, (1991) 1991 Volvo Award in basic sciences. Collagen types around the cells of the intervertebral disc and cartilage end plate: an immunolocalization study. Spine (Phila Pa 197616:: 1030-1038.
5. Yu J, (2002) Elastic tissues of the intervertebral disc. Biochem Soc Trans 30: 848-852. PubMed: 12440931.
6. Gilchrist CL, Chen J, Richardson WJ, Loeser RF, Setton LA, (2007) Functional integrin subunits regulating cell-matrix interactions in the intervertebral disc. J Orthop Res 25: 829-840. doi:10.1002/jor.20343. PubMed: 17318895.
7. Chen J, Jing L, Gilchrist CL, Richardson WJ, Fitch RD, et al. (2009) Expression of Laminin Isoforms, Receptors, and Binding Proteins Unique to Nucleus Pulposus Cells of Immature Intervertebral Disc. Connect Tissue Res 50: 294-306. doi:10.1080/03008200802714925. PubMed: 19863388.
8. Gilchrist CL, Francisco AT, Plopper GE, Chen J, Setton LA, (2011) Nucleus pulposus cell-matrix interactions with laminins. Eur Cells Mater 21: 523-532. PubMed: 21710443.
9. Götz W, Kasper M, Fischer G, Herken R, (1995) Intermediate filament typing of the human embryonic and fetal notochord. Cell Tissue Res 280: 455-462. doi:10.1007/BF00307819. PubMed: 7781042.
10. Herrmann BG, Kispert A, (1994) The T genes in embryogenesis. Trends Genet 10: 280-286. doi:10.1016/0168-9525(90)90011-T. PubMed: 7940757.
11. Fujita N, Miyamoto T, Imai J-i, Hosogane N, Suzuki T, et al. (2005) CD24 is expressed specifically in the nucleus pulposus of intervertebral discs. Biochem Biophys Res Commun 338: 1890-1896. doi:10.1016/j.bbrc.2005.10.166. PubMed: 16288985.
12. Tang X, Jing L, Chen J, (2012) Changes in the molecular phenotype of nucleus pulposus cells with intervertebral disc aging. PLOS ONE 7: e52020. doi:10.1371/journal.pone.0052020. PubMed: 23284858.
13. Sakai D, Nakamura Y, Nakai T, Mishima T, Kato S, et al. (2012) Exhaustion of nucleus pulposus progenitor cells with ageing and degeneration of the intervertebral disc. Nat Commun 3: 1264. doi:10.1038/ncomms2226. PubMed: 23232394.
14. Gilson A, Dreger M, Urban JP, (2010) Differential expression level of cytokeratin 8 in cells of the bovine nucleus pulposus complicates the search for specific intervertebral disc cell markers. Arthritis Res Ther 12: R24. doi:10.1186/ar2931. PubMed: 20152014.
15. Trout JJ, Buckwalter JA, Moore KC, Landas SK, (1982) Ultrastructure of the human intervertebral disc. I. Changes in notochordal cells with age. Tissue Cell 14: 359-369.
16. Buckwalter JA, (1995) Aging and degeneration of the human intervertebral disc. Spine (Phila Pa 197620:: 1307-1314. PubMed: 7660243.
17. Katz JN, (Apr(2006) Lumbar disc disorders and low-back pain: socioeconomic factors and consequences. J Bone Joint Surg Am, Apr: pp. 21-24. PubMed: 16595438.
18. Luo X, Pietrobon R, Sun X,. S, Liu GG, Hey L (2004); Estimates and Patterns of Direct Health Care Expenditures Among Individuals With Back Pain in the United States. Spine 29.
19. Kandel R, Roberts S, Urban JP, (2008) Tissue engineering and the intervertebral disc: the challenges. Eur Spine J 17 (Suppl 4):: 480-491. doi:10.1007/s00586-008-0746-2. PubMed: 19005701.
20. Sakai D, (2008) Future perspectives of cell-based therapy for intervertebral disc disease. Eur Spine J 17 (Suppl 4):: 452-458. doi:10.1007/s00586-008-0743-5. PubMed: 19005704.
21. Longo UG, Papapietro N, Petrillo S, Franceschetti E, Maffulli N, et al. (2012) Mesenchymal stem cell for prevention and management of intervertebral disc degeneration. Stem Cells Int, 2012(2012): 921053. PubMed: 22550520.
22. Nishimura K, Mochida J, (1998) Percutaneous reinsertion of the nucleus pulposus. An experimental study. Spine 23: 1531-1538. doi:10.1097/00007632-199807150-00006. PubMed: 9682309.
23. Nomura T, Mochida J, Okuma M, Nishimura K, Sakabe K, (2001) Nucleus Pulposus Allograft Retards Intervertebral Disc Degeneration. Clin Orthop Relat Res 389: 94-101. PubMed: 11501830.
24. Gruber HE, Johnson TL, Leslie K, Ingram JA, Martin D, et al. (2002) Autologous intervertebral disc cell implantation: a model using Psammomys obesus, the sand rat. Spine 27: 1626-1633. doi:10.1097/00007632-200208010-00007. PubMed: 12163723.
25. Ganey T, Libera J, Moos V, Alasevic O, Fritsch KG, et al. (2003) Disc chondrocyte transplantation in a canine model: a treatment for degenerated or damaged intervertebral disc. Spine (Phila Pa 1976) 28: 2609-2620. doi:10.1097/01.BRS.0000097891.63063.78.
26. Meisel HJ, Siodla V, Ganey T, Minkus Y, Hutton WC, et al. (2007) Clinical experience in cell-based therapeutics: Disc chondrocyte transplantation: A treatment for degenerated or damaged intervertebral disc. Biomol Eng 24: 5-21. doi:10.1016/j.bioeng.2006.07.002. PubMed: 16963315.
27. Richardson SM, Hughes N, Hunt JA, Freemont AJ, Hoyland JA, (2008) Human mesenchymal stem cell differentiation to NP-like cells in chitosan-glycerophosphate hydrogels. Biomaterials 29: 85-93. doi:10.1016/j.biomaterials.2007.09.018. PubMed: 17920676.
28. Risbud MV, Albert TJ, Guttapalli A, Vresilovic EJ, Hillibrand AS, et al. (2004) Differentiation of mesenchymal stem cells towards a nucleus pulposus-like phenotype in vitro: implications for cell-based transplantation therapy. Spine (Phila Pa 197629:: 2627-2632. PubMed: 15564911.
29. Allon AA, Schneider RA, Lotz JC, (2009) Co-culture of Adult Mesenchymal Stem Cells and Nucleus Pulposus Cells in Bilaminar Pellets for Intervertebral Disc Regeneration. SAS J 3: 41-49. doi:10.1016/S1935-9810(09)70006-4.
30. Li X, Lee JP, Balian G, Greg Anderson D, (2005) Modulation of Chondrocytic Properties of Fat-Derived Mesenchymal Cells in Co-Cultures with Nucleus Pulposus. Connect Tissue Res 46: 75-82. doi:10.1080/03008200590954104. PubMed: 16019417.
31. Korecki CL, Taboas JM, Tuan RS, Iatridis JC, (2010) Notochordal cell conditioned medium stimulates mesenchymal stem cell differentiation toward a young nucleus pulposus phenotype. Stem Cell Res Ther 1: 1-8. doi:10.1186/scrt1. PubMed: 20565707.
32. Purmessur D, Schek RM, Abbott RD, Ballif BA, Godburn KE, et al. (2011) Notochordal conditioned media from tissue increases proteoglycan accumulation and promotes a healthy nucleus pulposus phenotype in human mesenchymal stem cells. Arthritis Res Ther 13: R81. doi:10.1186/ar3344. PubMed: 21627827.
33. Chon BH, Jing L, Setton LA, Chen J, (2011) Human umbilical cord mesenchymal stromal cells (HUCMSCs) exhibit immature nucleus pulposus cell phenotype in a laminin-rich pseudo-3D culture system. Tansactions of the Orthopaedic Research Society. p. pp. 36. p.
34. Pattappa G, Li Z, Peroglio M, Wismer N, Alini M, et al. (2012) Diversity of intervertebral disc cells: phenotype and function. J Anat 221: 480-496. doi:10.1111/j.1469-7580.2012.01521.x. PubMed: 22686699.
35. Sakai D, Mochida J, Yamamoto Y, Nomura T, Okuma M, et al. (2003) Transplantation of mesenchymal stem cells embedded in Atelocollagen gel to the intervertebral disc: a potential therapeutic model for disc degeneration. Biomaterials 24: 3531-3541. doi:10.1016/S0142-9612(03)00222-9. PubMed: 12809782.
36. Crevensten G, Walsh AJL, Ananthakrishnan D, Page P, Wahba GM, et al. (2004) Intervertebral disc cell therapy for regeneration: Mesenchymal stem cell implantation in rat intervertebral discs. Ann Biomed Eng 32: 430-434. doi:10.1023/B:ABME.0000017545.84833.7c. PubMed: 15095817.
37. Takahashi K, Yamanaka S, (2006) Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors. Cell 126: 663-676. doi:10.1016/j.cell.2006.07.024. PubMed: 16904174.
38. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, et al. (2007) Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors. Cell 131: 861-872. doi:10.1016/j.cell.2007.11.019. PubMed: 18035408.
39. Liu H, Zhu F, Yong J, Zhang P, Hou P, et al. (2008) Generation of Induced Pluripotent Stem Cells from Adult Rhesus Monkey Fibroblasts. Cell Stem Cell 3: 587-590. doi:10.1016/j.stem.2008.10.014. PubMed: 19041774.
40. Ezashi T, Telugu BPVL, Alexenko AP, Sachdev S, Sinha S, et al. (2009) Derivation of induced pluripotent stem cells from pig somatic cells. Proc Natl Acad Sci USA 106: 10993-10998. doi:10.1073/pnas.0905284106. PubMed: 19541600.
41. Liao J, Cui C, Chen S, Ren J, Chen J, et al. (2009) Generation of Induced Pluripotent Stem Cell Lines from Adult Rat Cells. Cell Stem Cell 4: 11-15. doi:10.1016/j.stem.2008.11.013. PubMed: 19097959.
42. Wernig M, Zhao J-P, Pruszak J, Hedlund E, Fu D, et al. (2008) Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc Natl Acad Sci USA 105: 5856-5861. doi:10.1073/pnas.0801677105. PubMed: 18391196.
43. Karumbayaram S, Novitch BG, Patterson M, Umbach JA, Richter L, et al. (2009) Directed Differentiation of Human-Induced Pluripotent Stem Cells Generates Active Motor Neurons. Stem Cells 27: 806-811. doi:10.1002/stem.31. PubMed: 19350680.
44. Gai H, Leung EL-H, Costantino PD, Aguila JR, Nguyen DM, et al. (2009) Generation and characterization of functional cardiomyocytes using induced pluripotent stem cells derived from human fibroblasts. Cell Biol Int 33: 1184-1193. doi:10.1016/j.cellbi.2009.08.008. PubMed: 19729070.
45. Christoforou N, Liau B, Chakraborty S, Chellapan M, Bursac N, et al. (2013) Induced pluripotent stem cell-derived cardiac progenitors differentiate to cardiomyocytes and form biosynthetic tissues. PLOS ONE 8: e65963. doi:10.1371/journal.pone.0065963. PubMed: 23785459.
46. Choi K-D, Yu J, Smuga-Otto K, Salvagiotto G, Rehrauer W, et al. (2009) Hematopoietic and Endothelial Differentiation of Human Induced Pluripotent Stem Cells. Stem Cells 27: 559-567. doi:10.1634/stemcells.2008-0922. PubMed: 19259936.
47. Diekman BO, Christoforou N, Willard VP, Sun H, Sanchez-Adams J, et al. (2012) Cartilage tissue engineering using differentiated and purified induced pluripotent stem cells. Proc Natl Acad Sci U S A 109: 19172-19177. doi:10.1073/pnas.1210422109. PubMed: 23115336.
48. Kim MJ, Son MJ, Son MY, Seol B, Kim J, et al. (2011) Generation of human induced pluripotent stem cells from osteoarthritis patient-derived synovial cells. Arthritis Rheum 63: 3010-3021. doi:10.1002/art.30488. PubMed: 21953087.
49. Wei Y, Zeng W, Wan R, Wang J, Zhou Q, et al. (2012) Chondrogenic differentiation of induced pluripotent stem cells from osteoarthritic chondrocytes in alginate matrix. Eur Cells Mater 23: 1-12. PubMed: 22241609.
50. Dahia CL, Mahoney EJ, Durrani AA, Wylie C, (2009) Postnatal growth, differentiation, and aging of the mouse intervertebral disc. Spine (Phila Pa 197634:: 447-455. PubMed: 19247165.
51. Risbud MV, Schaer TP, Shapiro IM, (2010) Toward an understanding of the role of notochordal cells in the adult intervertebral disc: From discord to accord. Dev Dynam 239: 2141-2148. doi:10.1002/dvdy.22350. PubMed: 20568241.
52. Choi KS, Cohn MJ, Harfe BD, (2008) Identification of nucleus pulposus precursor cells and notochordal remnants in the mouse: implications for disk degeneration and chordoma formation. Dev Dyn 237: 3953-3958. doi:10.1002/dvdy.21805. PubMed: 19035356.
53. McCann MR, Tamplin OJ, Rossant J, Seguin CA, (2012) Tracing notochord-derived cells using a Noto-cre mouse: implications for intervertebral disc development. Dis Model. J Mech 5: 73-82.
54. Gilchrist CL, Darling EM, Chen J, Setton LA, (2011) Extracellular Matrix Ligand Stiffness Modulate Immature Nucleus Pulposus Cell-Cell Interactions. PLOS ONE 6: e27170. doi:10.1371/journal.pone.0027170. PubMed: 22087260.
55. Boyd LM, Chen J, Kraus VB, Setton LA, (2004) Conditioned medium differentially regulates matrix protein gene expression in cells of the intervertebral disc. Spine (Phila Pa 197629:: 2217-2222. PubMed: 15480131.
56. Chen J, Baer AE, Paik PY, Yan W, Setton LA, (2002) Matrix protein gene expression in intervertebral disc cells subjected to altered osmolarity. Biochem Biophys Res Commun 293: 932-938. doi:10.1016/S0006-291X(02)00314-5. PubMed: 12051748.
57. Boyd LM, Richardson WJ, Allen KD, Flahiff C, Jing L, et al. (2008) Early-onset degeneration of the intervertebral disc and vertebral end plate in mice deficient in type IX collagen. Arthritis Rheum 58: 164-171. doi:10.1002/art.23231. PubMed: 18163498.
58. Farndale RW, Sayers CA, Barrett AJ, (1982) A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures. Connect Tissue Res 9: 247-248. doi:10.3109/03008208209160269. PubMed: 6215207.
59. Choi KS, Harfe BD, (2011) Hedgehog signaling is required for formation of the notochord sheath and patterning of nuclei pulposi within the intervertebral discs. Proc Natl Acad Sci U S A 108: 9484-9489. doi:10.1073/pnas.1007566108. PubMed: 21606373.
60. Maier JA, Lo Y, Harfe BD, (2013) Foxa1 and Foxa2 are required for formation of the intervertebral discs. PLOS ONE 8: e55528. doi:10.1371/journal.pone.0055528. PubMed: 23383217.
61. Dahia CL, Mahoney EJ, Durrani AA, Wylie C, (2009) Intercellular signaling pathways active during intervertebral disc growth, differentiation, and aging. Spine (Phila Pa 197634:: 456-462. PubMed: 19212276.
62. Ma W, Tavakoli T, Derby E, Serebryakova Y, Rao MS, et al. (2008) Cell-extracellular matrix interactions regulate neural differentiation of human embryonic stem cells. BMC Dev Biol 8: 90. doi:10.1186/1471-213X-8-90. PubMed: 18808690.
63. Masuda K, An HS, (2004) Growth factors and the intervertebral disc. Spine J 4: 330S-340S. doi:10.1016/j.spinee.2004.07.028. PubMed: 15541686.
64. Erwin WM, Ashman K, O'Donnel P, Inman RD, (2006) Nucleus pulposus notochord cells secrete connective tissue growth factor and up-regulate proteoglycan expression by intervertebral disc chondrocytes. Arthritis Rheum 54: 3859-3867. doi:10.1002/art.22258. PubMed: 17136753.
65. Abbott RD, Purmessur D, Monsey RD, Iatridis JC, (2012) Regenerative potential of TGFbeta3 + Dex and notochordal cell conditioned media on degenerated human intervertebral disc cells. J Orthop Res 30: 482-488. doi:10.1002/jor.21534. PubMed: 21866573.
66. Jiang W, Sui X, Zhang D, Liu M, Ding M, et al. (2011) CD24: A Novel Surface Marker for PDX1-Positive Pancreatic Progenitors Derived from Human Embryonic Stem Cells. Stem Cells 29: 609-617. doi:10.1002/stem.608. PubMed: 21308865.
67. von Furstenberg RJ, Gulati AS, Baxi A, Doherty JM, Stappenbeck TS, et al. (2011) Sorting mouse jejunal epithelial cells with CD24 yields a population with characteristics of intestinal stem cells. Am J Physiol Gastrointest Liver Physiol 300: G409-G417. doi:10.1152/ajpgi.00453.2010. PubMed: 21183658.
68. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, et al. (2004) Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118: 149-161. doi:10.1016/j.cell.2004.07.004. PubMed: 15260986.
69. Martinez C, Hofmann TJ, Marino R, Dominici M, Horwitz EM, (2007) Human bone marrow mesenchymal stromal cells express the neural ganglioside GD2: a novel surface marker for the identification of MSCs. Blood 109: 4245-4248. doi:10.1182/blood-2006-08-039347. PubMed: 17264296.
70. Xu J, Liao W, Gu D, Liang L, Liu M, et al. (2009) Neural ganglioside GD2 identifies a subpopulation of mesenchymal stem cells in umbilical cord. Cell Physiol Biochem 23: 415-424. doi:10.1159/000218188. PubMed: 19471109.