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Research Paper

TGF-β3 and IGF-1 synergy ameliorates nucleus pulposus mesenchymal stem cell differentiation towards the nucleus pulposus cell type through MAPK/ERK signaling

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Pages 326-336 | Received 23 Apr 2015, Accepted 26 Aug 2015, Published online: 02 Oct 2015

References

  • Abbushi A, Endres M, Cabraja M, Kroppenstedt SN, Thomale UW, Sittinger M, Hegewald AA, et al. 2008. Regeneration of intervertebral disc tissue by resorbable cell-free polyglycolic acid-based implants in a rabbit model of disc degeneration. Spine (Phila Pa (1976)) 33:1527–1532
  • Adams MA, Roughley PJ. 2006. What is intervertebral disc degeneration, and what causes it? Spine (Phila Pa (1976)) 31:2151–2161
  • Antoniou J, Steffen T, Nelson F, Winterbottom N, Hollander AP, Poole RA, Aebi M, Alini M. 1996. The human lumbar intervertebral disc: Evidence for changes in the biosynthesis and denaturation of the extracellular matrix with growth, maturation, ageing, and degeneration. J Clin Invest 98:996–1003
  • Bian L, Zhai DY, Tous E, Rai R, Mauck RL, Burdick JA. 2011. Enhanced MSC chondrogenesis following delivery of TGF-beta3 from alginate microspheres within hyaluronic acid hydrogels in vitro and in vivo. Biomaterials 32:6425–6434
  • Blanco JF, Graciani IF, Sanchez-Guijo FM, Muntion S, Hernandez-Campo P, Santamaria C, Carrancio S, et al. 2010. Isolation and characterization of mesenchymal stromal cells from human degenerated nucleus pulposus: Comparison with bone marrow mesenchymal stromal cells from the same subjects. Spine (Phila Pa (1976)) 35:2259–2265
  • Boye A, Kan H, Wu C, Jiang Y, Yang X, He S, Yang Y. 2015. MAPK inhibitors differently modulate TGF-beta/Smad signaling in HepG2 cells. Tumour Biol 36:3643–3651
  • Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, et al. 2006. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315–317
  • Dudas M, Nagy A, Laping NJ, Moustakas A, Kaartinen V. 2004. Tgf-beta3-induced palatal fusion is mediated by Alk-5/Smad pathway. Dev Biol 266:96–108
  • Ehlicke F, Freimark D, Heil B, Dorresteijn A, Czermak P. 2010. Intervertebral disc regeneration: Influence of growth factors on differentiation of human mesenchymal stem cells (hMSC). Int J Artif Organs 33:244–252
  • Endres M, Abbushi A, Thomale UW, Cabraja M, Kroppenstedt SN, Morawietz L, Casalis PA, et al. 2010. Intervertebral disc regeneration after implantation of a cell-free bioresorbable implant in a rabbit disc degeneration model. Biomaterials 31:5836–5841
  • Farndale RW, Buttle DJ, Barrett AJ. 1986. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 883:173–177
  • Fortier LA, Mohammed HO, Lust G, Nixon AJ. 2002. Insulin-like growth factor-I enhances cell-based repair of articular cartilage. J Bone Joint Surg Br 84:276–288
  • Gupta MS, Cooper ES, Nicoll SB. 2011. Transforming growth factor-beta 3 stimulates cartilage matrix elaboration by human marrow-derived stromal cells encapsulated in photocrosslinked carboxymethylcellulose hydrogels: Potential for nucleus pulposus replacement. Tissue Eng Part A 17:2903–2910
  • Han B, Wang HC, Li H, Tao YQ, Liang CZ, Li FC, Chen G, Chen QX. 2015. Nucleus pulposus mesenchymal stem cells in acidic conditions mimicking degenerative intervertebral discs give better performance than adipose tissue-derived mesenchymal stem cells. Cells Tissues Organs 199:342–352
  • Hough C, Radu M, Dore JJ. 2012. Tgf-beta induced Erk phosphorylation of smad linker region regulates smad signaling. PLoS One 7:e42513
  • Katz JN. 2006. Lumbar disc disorders and low-back pain: Socioeconomic factors and consequences. J Bone Joint Surg Am 88:21–24
  • Kim BS, Kang HJ, Park JY, Lee J. 2015. Fucoidan promotes osteoblast differentiation via JNK- and ERK-dependent BMP2-Smad 1/5/8 signaling in human mesenchymal stem cells. Exp Mol Med 47:e128. doi: 10.1038/emm.2014.95
  • Kim KW, Chung HN, Ha KY, Lee JS, Kim YY. 2009. Senescence mechanisms of nucleus pulposus chondrocytes in human intervertebral discs. Spine J 9:658–666
  • Le Maitre CL, Richardson SM, Baird P, Freemont AJ, Hoyland JA. 2005. Expression of receptors for putative anabolic growth factors in human intervertebral disc: Implications for repair and regeneration of the disc. J Pathol 207:445–452
  • Lee CR, Sakai D, Nakai T, Toyama K, Mochida J, Alini M, Grad S. 2007a. A phenotypic comparison of intervertebral disc and articular cartilage cells in the rat. Eur Spine J 16:2174–2185
  • Lee MK, Pardoux C, Hall MC, Lee PS, Warburton D, Qing J, Smith SM, Derynck R. 2007b. TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA. EMBO J 26:3957–3967
  • Li H, Tao Y, Liang C, Han B, Li F, Chen G, Chen Q. 2013. Influence of hypoxia in the intervertebral disc on the biological behaviors of rat adipose- and nucleus pulposus-derived mesenchymal stem cells. Cells Tissues Organs 198:266–277
  • Li J, Zhou XD, Yang KH, Fan TD, Chen WP, Jiang LF, Bao JP, et al. 2014. Hinokitiol reduces matrix metalloproteinase expression by inhibiting Wnt/beta-Catenin signaling in vitro and in vivo. Int Immunopharmacol 23:85–91
  • Li TF, O'Keefe RJ, Chen D. 2005. TGF-beta signaling in chondrocytes. Front Biosci 10:681–688
  • Liang CZ, Li H, Tao YQ, Peng LH, Gao JQ, Wu JJ, Li FC, et al. 2013. Dual release of dexamethasone and TGF-beta3 from polymeric microspheres for stem cell matrix accumulation in a rat disc degeneration model. Acta Biomater 9:9423–9433
  • Liu LT, Huang B, Li CQ, Zhuang Y, Wang J, Zhou Y. 2011. Characteristics of stem cells derived from the degenerated human intervertebral disc cartilage endplate. PLoS One 6:e26285
  • Liu X, Hubchak SC, Browne JA, Schnaper HW. 2014. Epidermal growth factor inhibits transforming growth factor-beta-induced fibrogenic differentiation marker expression through ERK activation. Cell Signal 26:2276–2283
  • Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408
  • Longobardi L, Granero-Molto F, O'Rear L, Myers TJ, Li T, Kregor PJ, Spagnoli A. 2009. Subcellular localization of IRS-1 in IGF-I-mediated chondrogenic proliferation, differentiation and hypertrophy of bone marrow mesenchymal stem cells. Growth Factors 27:309–320
  • Madhala-Levy D, Williams VC, Hughes SM, Reshef R, Halevy O. 2012. Cooperation between Shh and IGF-I in promoting myogenic proliferation and differentiation via the MAPK/ERK and PI3K/Akt pathways requires Smo activity. J Cell Physiol 227:1455–1464
  • McGowan KB, Kurtis MS, Lottman LM, Watson D, Sah RL. 2012. Biochemical quantification of DNA in human articular and septal cartilage using PicoGreen and Hoechst 33258. Osteoarthritis Cartilage 10:580–587
  • Mizrahi O, Sheyn D, Tawackoli W, Ben-David S, Su S, Li N, Oh A, et al. 2013. Nucleus pulposus degeneration alters properties of resident progenitor cells. Spine J 13:803–814
  • Okuda S, Myoui A, Ariga K, Nakase T, Yonenobu K, Yoshikawa H. 2001. Mechanisms of age-related decline in insulin-like growth factor-I dependent proteoglycan synthesis in rat intervertebral disc cells. Spine (Phila Pa (1976)) 26:2421–2426
  • Ottley E, Gold E. 2014. microRNA and non-canonical TGF-beta signalling: Implications for prostate cancer therapy. Critical Rev Oncol/Hematol 92:49–60
  • Pelton RW, Saxena B, Jones M, Moses HL, Gold LI. 1991. Immunohistochemical localization of TGF beta 1, TGF beta 2, and TGF beta 3 in the mouse embryo: Expression patterns suggest multiple roles during embryonic development. J Cell Biol 115:1091–1105
  • Risbud MV, Di Martino A, Guttapalli A, Seghatoleslami R, Denaro V, Vaccaro AR, Albert TJ, Shapiro IM. 2006. Toward an optimum system for intervertebral disc organ culture: TGF-beta 3 enhances nucleus pulposus and anulus fibrosus survival and function through modulation of TGF-beta-R expression and ERK signaling. Spine (Phila Pa (1976)) 31:884–890
  • Risbud MV, Guttapalli A, Tsai TT, Lee JY, Danielson KG, Vaccaro AR, Albert TJ, et al. 2007. Evidence for skeletal progenitor cells in the degenerate human intervertebral disc. Spine (Phila Pa (1976)) 32:2537–2544
  • Roughley PJ. 2004. Biology of intervertebral disc aging and degeneration: Involvement of the extracellular matrix. Spine (Phila Pa (1976)) 29:2691–2699
  • Sakai D, Andersson GB. 2015. Stem cell therapy for intervertebral disc regeneration: Obstacles and solutions. Nature Rev Rheumatol 11:243–256
  • Steck E, Bertram H, Abel R, Chen B, Winter A, Richter W. 2005. Induction of intervertebral disc-like cells from adult mesenchymal stem cells. Stem Cells 23:403–411
  • Tao YQ, Liang CZ, Li H, Zhang YJ, Li FC, Chen G, Chen QX. 2013. Potential of co-culture of nucleus pulposus mesenchymal stem cells and nucleus pulposus cells in hyperosmotic microenvironment for intervertebral disc regeneration. Cell Biol Int 37:826–834
  • Tsirimonaki E, Fedonidis C, Pneumaticos SG, Tragas AA, Michalopoulos I, Mangoura D. 2013. PKCepsilon signalling activates ERK1/2, and regulates aggrecan, ADAMTS5, and miR377 gene expression in human nucleus pulposus cells. PLoS One 8:e82045
  • Urano T, Narusawa K, Shiraki M, Usui T, Sasaki N, Hosoi T, Ouchi Y, et al. 2008. Association of a single nucleotide polymorphism in the insulin-like growth factor-1 receptor gene with spinal disc degeneration in postmenopausal Japanese women. Spine (Phila Pa (1976)) 33:1256–1261
  • Vadala G, Russo F, Di Martino A, Denaro V. 2013. Intervertebral disc regeneration: From the degenerative cascade to molecular therapy and tissue engineering. J Tissue Eng Regen Med 9:679–690
  • Vadala G, Sowa G, Hubert M, Gilbertson LG, Denaro V, Kang JD. 2012. Mesenchymal stem cells injection in degenerated intervertebral disc: Cell leakage may induce osteophyte formation. J Tissue Eng Regen Med 6:348–355
  • van der Kraan PM, Blaney Davidson EN, Blom A, van den Berg WB. 2009. TGF-beta signaling in chondrocyte terminal differentiation and osteoarthritis: Modulation and integration of signaling pathways through receptor-Smads. Osteoarthritis Cartilage 17:1539–1545
  • Woiciechowsky C, Abbushi A, Zenclussen ML, Casalis P, Kruger JP, Freymann U, Endres M, Kaps C. 2012. Regeneration of nucleus pulposus tissue in an ovine intervertebral disc degeneration model by cell-free resorbable polymer scaffolds. J Tissue Eng Regen Med 8:811–820
  • Xiong CJ, Huang B, Zhou Y, Cun YP, Liu LT, Wang J, Li CQ, et al. 2012. Macrophage migration inhibitory factor inhibits the migration of cartilage end plate-derived stem cells by reacting with CD74. PLoS One 7:e43984
  • Yang X, Wei A, Liu Y, He G, Zhou Z, Yu Z. 2013. IGF-1 protects retinal ganglion cells from hypoxia-induced apoptosis by activating the Erk-1/2 and Akt pathways. Mol Vis 19:1901–1912
  • Zhou X, Tao Y, Wang J, Liang C, Wang J, Li H, Chen Q. 2015. Roles of FGF-2 and TGF-beta/FGF-2 on differentiation of human mesenchymal stem cells towards nucleus pulposus-like phenotype. Growth Factors 33:23–30
  • Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, et al. 2001. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng 7:211–228

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