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Regenerative medicine: Induced pluripotent stem cells and their benefits on accelerated bone tissue reconstruction using scaffolds

Published online by Cambridge University Press:  22 May 2018

Nowsheen Goonoo
Affiliation:
Biomaterials, Drug Delivery and Nanotechnology Unit, Center for Biomedical and Biomaterials Research (CBBR), University of Mauritius, Réduit 80837, Mauritius
Archana Bhaw-Luximon*
Affiliation:
Biomaterials, Drug Delivery and Nanotechnology Unit, Center for Biomedical and Biomaterials Research (CBBR), University of Mauritius, Réduit 80837, Mauritius
*
a)Address all correspondence to this author. e-mail: a.luximon@uom.ac.mu, abluximon@gmail.com
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Abstract

Induced pluripotent stem cells (iPSCs) offer the possibility to accelerate tissue reconstruction through cell differentiation. The use of iPSCs in bone tissue engineering is promoted by next generation scaffolds which guide bone tissue repair and provide specific cues and molecular recognition to enhance differentiation as well as the bone forming ability of these cells. However, bone tissue repair faces additional challenges such as requirement for a consequent bone vasculature and exhaustion of stem cells in the aging adults. In this context, iPSC reprogramming seems to be unaffected by age and they have better pro-angiogenic potential as well as proliferation rate. The benefits of iPSCs using polymeric scaffolds include access to humanized in vitro models, triggering bone tissue reconstruction through a supply of bone cells via differentiation, compensating mesenchymal stem cells age-related deficiencies in osteodegenerative diseases, and enhancing angiogenesis.

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REVIEW
Copyright
Copyright © Materials Research Society 2018 

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Footnotes

This section of Journal of Materials Research is reserved for papers that are reviews of literature in a given area.

References

REFERENCES

Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S.: Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861 (2007).CrossRefGoogle ScholarPubMed
Takahashi, K. and Yamanaka, S.: Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663 (2006).CrossRefGoogle ScholarPubMed
Ohnuki, M. and Takahashi, K.: Present and future challenges of induced pluripotent stem cells. Philos. Trans. R. Soc., B 370, 20140367 (2015).Google Scholar
Singh, V.K., Kalsan, M.K., Kumar, N., Saini, A., and Chandra, R.: Induced pluripotent stem cells: Applications in regenerative medicine, disease modeling, and drug discovery. Front. Cell Dev. Biol. 3, (2015). doi: 10.3389/fcell.2015.00002.Google Scholar
Ramalingam, M. and Rana, D.: Impact of nanotechnology in induced pluripotent stem cells-driven tissue engineering and regenerative medicine. J. Bionanoscience 9, 13 (2015).Google Scholar
Kingham, E. and Oreffo, R.O.C.: Embryonic and induced pluripotent stem cells: Understanding, creating, and exploiting the nano-niche for regenerative medicine. ACS Nano 7, 1867 (2013).Google Scholar
Keaveny, T.M., Morgan, E.F., Niebur, G.L., and Yeh, O.C.: Biomechanics of trabecular bone. Annu. Rev. Biomed. Eng. 3, 307 (2001).Google Scholar
Barrère, F., Mahmood, T.A., de Groota, K., and van Blitterswijka, C.A.: Advanced biomaterials for skeletal tissue regeneration: Instructive and smart functions. Mater. Sci. Eng., R 59, 38 (2008).Google Scholar
Cooper, D.M., Matyas, J.R., Katzenberg, M.A., and Hallgrimsson, B.: Comparison of microcomputed tomographic and microradiographic measurements of cortical bone porosity. Calcif. Tissue Int. 74, 437 (2004).Google Scholar
Sikavitsas, V.I., Temenoff, J.S., and Mikos, A.G.: Biomaterials and bone mechanotransduction. Biomaterials 22, 2581 (2001).Google Scholar
Temenoff, J.S., Lu, L., and Mikos, A.G.: Bone-tissue engineering using synthetic biodegradable polymer scaffolds. In Bone Engineering, 1st ed., Davies, J.E. and Vacanti, J.P., eds. (EM Squared, Toronto, 1999); p. 454.Google Scholar
Sommerfeldt, D.W. and Rubin, C.T.: Biology of bone and how it orchestrates the form and function of the skeleton. Eur. Spine J. 10, S86 (2001).Google Scholar
Henkel, J., Woodruff, M.A., Epari, D.R., Steck, R., Glatt, V., Dickinson, I.C., Choong, P., Schutz, M.A., and Hutmacher, D.W.: Bone regeneration based on tissue engineering conceptions—A 21st century perspective. Bone Res. 1, 216 (2013).Google Scholar
Ducy, P., Schinke, T., and Karsenty, G.: The osteoblast: A sophisticated fibroblast under central surveillance. Science 289, 1501 (2000).Google Scholar
Mackie, E.J.: Osteoblasts: Novel roles in orchestration of skeletal architecture. Int. J. Biochem. Cell Biol. 35, 1301 (2003).Google Scholar
Nijweide, P.J., Burger, E.H., Nulend, J.K., and Van der Plas, A.: The osteocyte. In Principles of Bone Biology, 1st ed., Bilezikian, J.P., Raisz, L.G., and Rodan, G.A. (Academic, San Diego, CA, 1996); pp. 93115.Google Scholar
Jilka, R.L., Weinstein, R.S., Bellido, T., Parfitt, M., and Manolagas, S.C.: Osteoblast programmed cell death (apoptosis): Modulation by growth factors and cytokines. J. Bone Miner. Res. 13, 793 (1998).Google Scholar
Safadi, F.F., Xu, J., Smock, S.L., Kannan, R.A., Selim, A-H., Odgren, P.R., Marks, S.C. Jr., Owen, T.A., and Popoff, S.N.: Expression of connective tissue growth factor in bone: Its role in osteoblast proliferation and differentiation in vitro and bone formation in vivo. J. Cell. Physiol. 196, 51 (2003).Google Scholar
Hadjidakis, D.J. and Androulakis, I.I.: Bone remodeling. Ann. N. Y. Acad. Sci. 1092, 385 (2006).Google Scholar
Rho, J.Y., Kuhn-Spearing, L., and Zioupos, P.: Mechanical properties and the hierarchical structure of bone. Med. Eng. Phys. 20, 92 (1998).Google Scholar
Hollister, S.J. and Murphy, W.L.: Scaffold translation: Barriers between concept and clinic. Tissue Eng., Part B 17, 459 (2011).CrossRefGoogle ScholarPubMed
O’Loughlin, P.F., Morr, S., Bogunovic, L., Kim, A.D., Park, B., and Lane, J.M.: Selection and development of preclinical models in fracture-healing research. J. Bone Jt. Surg., Am. 90(Suppl. 1), 79 (2008).CrossRefGoogle ScholarPubMed
Muschler, G.F., Nakamoto, C., and Griffith, L.G.: Engineering principles of clinical cell-based tissue engineering. J. Bone Jt. Surg., Am. 86A, 1541 (2004).Google Scholar
Stedman, T.L.: Stedman’s Medical Dictionary, 25th ed. (Williams & Wilkins, Baltimore, 1990); p. 1108.Google Scholar
Burchardt, H.: The biology of bone graft repair. Clin. Orthop. 174, 28 (1983).CrossRefGoogle Scholar
Muschler, G.F. and Lane, J.M.: Orthopedic surgery. In Bone Grafts and Bone Substitutes, Habal, M.B., Reddi, A.H., and Saunders, W.B., eds. (Philadelphia, 1992); pp. 375407.Google Scholar
Aerssens, J., Boonen, S., Lowet, G., and Dequeker, J.: Interspecies differences in bone composition, density, and quality: Potential implications for in vivo bone research. Endocrinology 139, 663 (1998).Google Scholar
Thorwarth, M., Schultze-Mosgau, S., Kessler, P., Wiltfang, J., and Schlegel, K.A.: Bone regeneration in osseous defects using a resorbable nanoparticular hydroxyapatite. J. Oral Maxillofac. Surg. 63, 1626 (2005).Google Scholar
Yamamoto, T., Irisa, T., Sugioka, Y., and Sueishi, K.: Effects of pulse methylprednisolone on bone and marrow tissues: Corticosteroid-induced osteonecrosis in rabbits. Arthritis Rheum. 40, 2055 (1997).Google Scholar
Miyanishi, K., Yamamoto, T., Irisa, T., Yamashita, A., Jingushi, S., Noguchi, Y., and Iwamoto, Y.: Bone marrow fat cell enlargement and a rise in intraosseous pressure in steroid-treated rabbits with osteonecrosis. Bone 30, 185 (2002).Google Scholar
Pearce, A.I., Richards, R.G., Milz, S., Schneider, E., and Pearce, S.G.: Animal models for implant biomaterial research in bone: A review. Eur. Cell. Mater. 13, 1 (2007).Google Scholar
Reinwald, S. and Burr, D.: Review of nonprimate, large animal models for osteoporosis research. J. Bone Miner. Res. 23, 1353 (2008).Google Scholar
Muschler, G.F., Raut, V.P., Patterson, T.E., Wenke, J.C., and Hollinger, J.O.: The design and use of animal models for translational research in bone tissue engineering and regenerative medicine. Tissue Eng., Part B 16, 123 (2010).Google Scholar
O’Driscoll, S.W., Saris, D.B., Ito, Y., and Fitzimmons, J.S.: The chondrogenic potential of periosteum decreases with age. J. Orthop. Res. 19, 95 (2001).Google Scholar
Meyer, R.A. Jr., Tsahakis, P.J., Martin, D.F., Banks, D.M., Harrow, M.E., and Kiebzak, G.M.: Age and ovariectomy impair both the normalization of mechanical properties and the accretion of mineral by the fracture callus in rats. J. Orthop. Res. 19, 428 (2001).CrossRefGoogle ScholarPubMed
Naik, A.A., Xie, C., Zuscik, M.J., Kingsley, P., Schwarz, E.M., Awad, H., Guldberg, R., Drissi, H., Puzas, J.E., Boyce, B., Zhang, X., and O’Keefe, R.J.: Reduced COX-2 expression in aged mice is associated with impaired fracture healing. J. Bone Miner. Res. 24, 251 (2009).Google Scholar
Lu, C., Hansen, E., Sapozhnikova, A., Hu, D., Miclau, T., and Marcucio, R.S.: Effect of age on vascularization during fracture repair. J. Orthop. Res. 26, 1384 (2008).Google Scholar
Malaval, L., Modrowski, D., Gupta, A.K., and Aubin, J.E.: Cellular expression of bone-related proteins during in vitro osteogenesis in rat bone marrow stromal cell cultures. J. Cell. Physiol. 158, 555 (1994).Google Scholar
Majors, A.K., Boehm, C.A., Nitto, H., Midura, R.J., and Muschler, G.F.: Characterization of human bone marrow stromal cells with respect to osteoblastic differentiation. J. Orthop. Res. 15, 546 (1997).Google Scholar
Mathieu, J., Zu, W., Xing, Y., Sperber, H., Ferricio, A., Agoston, Z., Kuppusamy, K.T., Moon, R.T., and Ruohala-Baker, H.: Hypoxia-inducible factors have distinct and stage-specific roles during reprogramming of human cells to pluripotency. Cell Stem Cell 14, 592 (2014).CrossRefGoogle ScholarPubMed
Mordhorst, B.R., Murphy, S.L., Ross, R.M., Samuel, M.S., Salazar, S.R., Ji, T., Behura, S.K., Wells, K.D., Green, J.A., and Prather, R.S.: Pharmacologic reprogramming designed to induce a warburg effect in porcine fetal fibroblasts alters gene expression and quantities of metabolites from conditioned media without increased cell proliferation. Cell. Reprogr. 20, 38 (2018).Google Scholar
Frohlich, M., Grayson, W.L., Wan, L.Q., Marolt, D., Dorbnik, M., and Vunjak-Novakovic, G.: Tissue engineered bone grafts: Biological requirements, tissue culture and clinical relevance. Curr. Stem Cell Res. Ther. 3, 254 (2008).CrossRefGoogle ScholarPubMed
Meijer, G.J., de Bruijn, J.D., Koole, R., and van Blitterswijk, C.A.: Cell-based bone tissue engineering. PLoS Med. 4, e9 (2007).Google Scholar
Kretlow, J.D., Jin, Y.Q., Liu, W., Zhang, W.J., Hong, T-H., Zhou, G., Baggett, L.S., Mikos, A.G., and Cao, Y.: Donor age and cell passage affects differentiation potential of murine bone marrow-derived stem cells. BMC Cell Biol. 9, 60 (2008).Google Scholar
Stenderup, K., Justesen, J., Clausen, C., and Kassem, M.: Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33, 919 (2003).Google Scholar
Jesudason, D. and Clifton, P.: The interaction between dietary protein and bone health. J. Bone Miner. Metabol. 29, 224 (2011).Google Scholar
Bilousova, G., Jun, D.H., King, K.B., Langhe, S.D., Chick, W.S., Torchia, E.C., Chow, K.S., Klemm, D.J., Roop, D.R., and Majka, S.M.: Osteoblasts derived from induced pluripotent stem cells form calcified structures in scaffolds both in vitro and in vivo. Stem Cell. 29, 206 (2011).Google Scholar
Li, F., Bronson, S., and Niyibizi, C.: Derivation of murine induced pluripotent stem cells (iPS) and assessment of their differentiation toward osteogenic lineage. J. Cell. Biochem. 109, 643 (2010).Google Scholar
Wang, P., Liu, X., and Zhao, L.: Bone tissue engineering via human induced pluripotent, umbilical cord and bone marrow mesenchymal stem cells in rat cranium. Acta Biomater. 18, 236 (2015).Google Scholar
de Peppoa, G.M., Marcos-Campos, I., Kahler, D.J., Alsalman, D., Shang, L., Vunjak-Navakovic, G., and Marolt, D.: Engineering bone tissue substitutes from human induced pluripotent stem cells. Proc. Natl. Acad. Sci. U.S.A. 110, 8680 (2013).Google Scholar
Dogaki, Y., Lee, S.Y., Niikura, T., Iwakura, T., Okumachi, E., Waki, T., Kakutani, K., Nishida, K., Kuroda, R., and Kurosaka, M.: Efficient derivation of osteoprogenitor cells from induced pluripotent stem cells for bone regeneration. Int. Orthop. 38, 1779 (2014).Google Scholar
Zou, L., Luo, Y., Chen, M., Wang, G., Ding, M., Petersen, C.C., Kang, R., Dagnaes-Hansen, F., Zeng, Y., Lv, N., Ma, Q., Le, D.Q.S., Bessenbacher, F., Bolund, L., Jensen, T.G., Kjems, J., Pu, W.T., and Bünger, C.: A simple method for deriving functional MSCs and applied for osteogenesis in 3D scaffolds. Sci. Rep. 3, 2243 (2013).Google Scholar
Jin, G.Z., Kim, T.H., Kim, J.H., Won, J.E., Yoo, S.Y., Choi, S.J., Hyun, J.K., and Kim, H.W.: Bone tissue engineering of induced pluripotent stem cells cultured with macrochanneled polymer scaffold. J. Biomed. Mater. Res., Part A 101, 1283 (2013).Google Scholar
Pan, L., Yu, G., Zhai, D., Lee, H.R., Zhao, W., Liu, N., Wang, H., Tee, B.C-K., Shi, Y., Cui, Y., and Bao, Z.: Hierarchical nanostructured conducting polymer hydrogel with high electrochemical activity. Proc. Natl. Acad. Sci. U.S.A. 109, 20379 (2012).Google Scholar
Sheyn, D., Ben-David, S., Shapiro, G., De Mel, S., Bez, M., Ornelas, L., Sahabian, A., Sareen, D., Da, X., Pelled, G., Tawakocli, W., Liu, Z., Gazit, D., and Gazit, Z.: Human induced pluripotent stem cells differentiate into functional mesenchymal stem cells and repair bone defects. Stem Cells Transl. Med. 5, 1447 (2016).CrossRefGoogle ScholarPubMed
Kim, K., Doi, A., Wen, B., Ng, K., Zhao, R., Cahan, P., Kim, J., Aryee, M.J., Ji, H., Ehrlich, L.I.R., Yabuuchi, A., Takeuchi, A., Cunniff, K.C., Hongguang, H., McKinney-Freeman, S., Naveiras, O., Yoon, T.J., Irizarry, R.A., Jung, N., Seita, J., Hanna, J., Murakami, P., Jaenisch, R., Weissleder, R., Orkin, S.H., Weissman, I.L., Feinberg, A.P., and Daley, G.Q.: Epigenetic memory in induced pluripotent stem cells. Nature 467, 285 (2010).Google Scholar
Polo, J.M., Liu, S., Figueroa, M.E., Kulalert, W., Eminli, S., Tan, K.Y., Apostolou, E., Stadtfeld, M., Li, Y., Shioda, T., Natesan, S., Wagners, A.J., Melnick, A., Evans, T., and Hochedlinger, K.: Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat. Biotechnol. 28, 848 (2010).Google Scholar
Ishiy, F.A.A., Fanganiello, R.D., Griesi-Oliveira, K., Suzuki, A.M., Kobayashi, G.S., Morales, A.G., Capelo, L.P., and Passos-Bueno, M.R.: Improvement of in vitro osteogenic potential through differentiation of induced pluripotent stem cells from human exfoliated dental tissue towards mesenchymal-like stem cells. Stem Cells Int., 249098, 9 pages (2015). doi: 10.1155/2015/249098.Google Scholar
Hynes, K., Menicanin, D., Mrozik, K., Gronthos, S., and Bartold, P.M.: Generation of functional mesenchymal stem cells from different induced pluripotent stem cell lines. Stem Cells Dev. 23, 1084 (2014).Google Scholar
Nasu, A., Ikeya, M., Yamamoto, T., Watanabe, A., Jin, Y., Matsumoto, Y., Hayakawa, K., Amano, N., Sato, S., Osafune, K., Aoyama, T., Nakamura, T., Kato, T., and Togushida, J.: Genetically matched human iPS cells reveal that propensity for cartilage and bone differentiation differs with clones, not cell type of origin. PLoS One 8, e53771 (2013).Google Scholar
Sparks, N.R.L., Martinez, I.K.C., Soto, C.H., and zur Nieden, N.I.: Low osteogenic yield in human pluripotent stem cells associates with differential neural crest promoter methylation. Stem Cell. 36, 349 (2018).Google Scholar
Li, F. and Niyibizi, C.: Cells derived from murine induced pluripotent stem cells (iPSC) by treatment with members of TGF-beta family give rise to osteoblasts differentiation and form bone in vivo. BMC Cell Biol. 13, 35 (2012).Google Scholar
Liu, J., Chen, W., Zhao, Z., and Xu, H.H.: Reprogramming of mesenchymal stem cells derived from iPSCs seeded on biofunctionalized calcium phosphate scaffold for bone engineering. Biomaterials 34, 7862 (2013).Google Scholar
Tashiro, K., Inamura, M., Kawabata, K., Sakurai, F., Yamanishi, K., Hayakawa, T., and Mizuguchi, H.: Efficient adipocyte and osteoblast differentiation from mouse induced pluripotent stem cells by adenoviral transduction. Stem Cell. 27, 1802 (2009).CrossRefGoogle ScholarPubMed
Ye, J.H., Xu, Y.J., Gao, J., Yan, S-G., Zhao, J., Tu, Q., Zhang, J., Duan, X-J., Sommer, C.A., Mostoslavsky, G., Kaplan, D.L., Wu, Y-N., Zhang, C-P., Wang, L., and Chen, J.: Critical-size calvarial bone defects healing in a mouse model with silk scaffolds and SATB2-modified iPSCs. Biomaterials 32, 5065 (2011).Google Scholar
Villa-Diaz, L.G., Brown, S.E., Liu, Y., Ross, A.M., Lahann, J., Parent, J.M., and Krebsbach, P.H.: Derivation of functional mesenchymal stem cells from human induced pluripotent stem cells cultured on synthetic polymer substrates. Stem Cell. 30, 1174 (2012).Google Scholar
Tang, M., Chen, W., Liu, J., Weir, M.D., Cheng, L., and Xu, H.H.: Human induced pluripotent stem cell-derived mesenchymal stem cell seeding on calcium phosphate scaffold for bone regeneration. Tissue Eng., Part A 20, 1295 (2014).Google Scholar
Diederichs, S. and Tuan, R.S.: Functional comparison of human-induced pluripotent stem cell-derived mesenchymal cells and bone marrow-derived mesenchymal stromal cells from the same donor. Stem Cells Dev. 23, 1594 (2014).Google Scholar
Ji, J., Tong, X., Huang, X., Zhang, J., Qin, H., and Hu, Q.: Patient-derived human induced pluripotent stem cells from gingival fibroblasts composited with defined nanohydroxyapatite/chitosan/gelatin porous scaffolds as potential bone graft substitutes. Stem Cells Transl. Med. 5, 95 (2016).Google Scholar
Lepage, S.I., Nagy, K., Sung, H.K., Kandel, R.A., Nagy, A., and Koch, T.G.: Generation, characterization, and multilineage potency of mesenchymal-like progenitors derived from equine induced pluripotent stem cells. Stem Cells Dev. 25, 80 (2015).Google Scholar
Hong, S.G., Winkler, T., Wu, C., Guo, V., Pittaluga, S., Nicolae, A., Donahue, R.E., Metzger, M.E., Price, S.D., Uchida, N., Kuznetsov, S.A., Kilts, T., Li, L., Robey, P.G., and Dunbar, C.E.: Path to the clinic: Assessment of iPSC-based cell therapies in vivo in a nonhuman primate model. Cell Rep. 7, 1298 (2014).Google Scholar
Vining, K.H. and Mooney, D.J.: Mechanical forces direct stem cell behaviour in development and regeneration. Nat. Rev. Mol. Cell Biol. 18, 728 (2017).Google Scholar
Ireland, R.G. and Simmons, C.A.: Human pluripotent stem cell mechanobiology: Manipulating the biophysical microenvironment for regenerative medicine and tissue engineering applications. Stem Cell. 33, 3187 (2015).Google Scholar
Kim, Y.M., Kang, Y.G., Park, S.H., Han, M-K., Kim, J.H., Shin, J.W., and Shin, J-W.: Effects of mechanical stimulation on the reprogramming of somatic cells into human-induced pluripotent stem cells. J. Stem Cell Res. Ther. 8, 139 (2017).Google Scholar
Sarić, T., Halbach, M., Khalil, M., and Er, F.: Induced pluripotent stem cells as cardiac arrhythmic in vitro models and the impact for drug discovery. Expet Opin. Drug Discov. 9, 55 (2014).Google Scholar
Lee, P., Klos, M., Bollensdorff, C., Hou, L., Ewart, P., Kamp, T.J., Zhang, J., Bizy, A., Guerrero-Serna, G., Kohl, P., Jalife, J., and Herron, T.J.: Simultaneous voltage and calcium mapping of genetically purified human induced pluripotent stem cell-derived cardiac myocyte monolayers. Circ. Res. 110, 1556 (2012).Google Scholar
Zhu, R., Blazeski, A., Poon, E., Costa, K.D., Tung, L., and Boheler, K.R.: Physical developmental cues for the maturation of human pluripotent stem cell-derived cardiomyocytes. J. Stem Cell Res. Ther. 5, 117 (2014).Google Scholar
Cao, H., Kang, B.J., Lee, C.A., Shung, K.K., and Hsiai, T.K.: Electrical and mechanical strategies to enable cardiac repair and regeneration. IEEE Rev. Biomed. Eng. 8, 114 (2015).Google Scholar
Ruan, J.L., Tulloch, N.L., Razumova, M.V., Saiget, M., Muskheli, V., Pabon, L., Reinecke, H., Regnier, M., and Murry, C.E.: Mechanical stress conditioning and electrical stimulation promote contractility and force maturation of induced pluripotent stem cell-derived human cardiac tissue. Circulation 134, 1557 (2016).CrossRefGoogle ScholarPubMed
Li, Y.C., Zhu, K., and Young, T.H.: Induced pluripotent stem cells, form in vitro tissue engineering to in vivo allogeneic transplantation. J. Thorac. Dis. 9, 455 (2017).Google Scholar
Kim, D., Kim, C.H., Moon, J.I., Chung, Y-G., Chang, M-Y., Han, B-S., Ko, S., Yang, E., Cha, K.Y., Lanza, R., and Kim, K-S.: Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4, 472 (2009).Google Scholar
Zhou, H., Wu, S., Joo, J.Y., Zhu, S., Han, D.W., Lin, T., Trauger, S., Bien, G., Yao, S., Zhu, Y., Siuzdak, G., Schöler, H.R., Duan, L., and Ding, S.: Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4, 381 (2009).Google Scholar
Hou, P., Li, Y., Zhang, X., Liu, C., Guan, J., Li, H., Zhao, T., Ye, J., Yang, W., Liu, K., Ge, J., Xu, J., Zhang, Q., Zhao, Y., and Deng, H.: Pluripotent stem cells induced from mouse somatic cells by small-molecule compounds. Science 341, 651 (2013).Google Scholar
Shiba, Y., Gomibuchi, T., Seto, T., Wada, Y., Ichimura, H., Tanaka, Y., Ogasawara, T., Okada, K., Shiba, N., Sakamoto, K., Ido, D., Shiina, T., Ohkura, M., Nakai, J., Uno, N., Kazuki, Y., Oshimura, M., Minami, I., and Ikeda, U.: Allogeneic transplantation of iPS cell-derived cardiomyocytes regenerates primate hearts. Nature 538, 388 (2016).Google Scholar
Li, Y.C., Zhang, Y.S., Akpek, A., Shin, S.R., and Khademhosseini, A.: 4D bioprinting: The next-generation technology for biofabrication enabled by stimuli-responsive materials. Biofabrication 9, 012001 (2016).Google Scholar
Hoveizi, E., Ebrahimi-Barough, S., Tavakol, S., and Nabiuni, M.: In vitro comparative survey of cell adhesion and proliferation of human induced pluripotent stem cells on surfaces of polymeric electrospun nanofibrous and solution-cast film scaffolds. J. Biomed. Mater. Res., Part A 103, 2952 (2015).Google Scholar
Ardeshirylajimi, A., Dinarvand, P., Seyedjafari, E., Langroudi, L., Adegani, F.J., and Soleimani, M.: Enhanced reconstruction of rat calvarial defects achieved by plasma-treated electrospun scaffolds and induced pluripotent stem cells. Cell Tissue Res. 354, 849 (2013).Google Scholar
Liu, J., Nie, H., Xu, Z., Niu, X., Guo, S., Yin, J., Guo, F., Li, G., Wang, Y., and Zhang, C.: The effect of 3D nanofibrous scaffolds on the chondrogenesis of induced pluripotent stem cells and their application in restoration of cartilage defects. PLoS One 9, e111566 (2014).Google Scholar
Liu, L., Hindieh, J., Leong, D.J., and Sun, S.D.: Advances of stem cell based-therapeutic approaches for tendon repair. J. Orthop. Translat. 9, 69 (2017).Google Scholar
Higuchi, A., Kumar, S.S., Ling, Q.D., and Alarfaj, A.F.: Polymeric design of cell culture materials that guide the differentiation of human pluripotent stem cells. Prog. Polym. Sci. 65, 83 (2017).Google Scholar
Wang, P., Liu, X., Zhao, L., Weir, M.D., Sun, J., Chen, W., Man, Y., and Xu, H.H.K.: Bone tissue engineering via human induced pluripotent, umbilical cord and bone marrow mesenchymal stem cells in rat cranium. Acta Biomater. 18, 236 (2015).Google Scholar
Wang, P., Song, Y., Weir, M.D., Sun, J., Zhao, L., Simon, C.G., and Xu, H.H.K.: A self-setting iPSMSC-alginate-calcium phosphate paste for bone tissue engineering. Dent. Mater. 32, 252 (2016).CrossRefGoogle ScholarPubMed
Ji, J., Tong, X., Huang, X., Wang, T., Lin, Z., Cao, Y., Zhang, J., Dong, L., Qin, H., and Hu, Q.: Sphere-shaped nano-hydroxyapatite/chitosan/gelatin 3D porous scaffolds increase proliferation and osteogenic differentiation of human induced pluripotent stem cells from gingival fibroblasts. Biomed. Mater. 10, (2015). doi: 10.1088/1748-6041/10/4/045005.Google Scholar
Xie, J., Peng, C., Zhao, Q., Wang, X., Yuan, H., Yang, L., Li, K., Lou, X., and Zhang, Y.: Osteogenic differentiation and bone regeneration of iPSC-MSCs supported by a biomimetic nanofibrous scaffold. Acta Biomater. 29, 365 (2016).Google Scholar
Ardeshirylajimi, A., Hosseinkhani, S., Parivar, K., Yaghmaie, P., and Soleimani, M.: Nanofiber-based polyethersulfone scaffold and efficient differentiation of human induced pluripotent stem cells into osteoblastic lineage. Mol. Biol. Rep. 40, 4287 (2013).Google Scholar
Chien, K-H., Chang, Y-L., Wang, M-L., Chuang, J-H., Yang, Y-C., Tai, M-C., Wang, C-Y., Liu, Y-Y., Li, H-Y., Chen, J-T., Kao, S-Y., Chen, H-L.i., and Lo, W-L.: Promoting induced pluripotent stem cell-driven biomineralization and periodontal regeneration in rats with maxillary-molar defects using injectable BMP-6 hydrogel. Sci. Rep. 8, 114 (2018).Google Scholar
Goonoo, N.: Modulating immunological responses of electrospun fibers for tissue engineering. Adv. Biosyst. (2017). doi: 10.1002/adbi.201700093.Google Scholar
Zhang, C., Hu, K., Liu, X., Reynolds, M.A., Bao, C., Wang, P., Zhao, L., and Xu, H.H.K.: Novel hiPSC-based tri-culture for pre-vascularization of calcium phosphate scaffold to enhance bone and vessel formation. Mater. Sci. Eng., C 79, 296 (2017).Google Scholar
Liu, X., Chen, W., Zhang, C., Thein-Han, W., Hu, K., Reynolds, M.A., Bao, C., Wang, P., Zhao, L., and Xu, H.H.K.: Co-seeding human endothelial cells with human-induced pluripotent stem cell-derived mesenchymal stem cells on calcium phosphate scaffold enhances osteogenesis and vascularization in rats. Tissue Eng., Part A 23, 546 (2017).Google Scholar
Jeon, O.H., Panicker, L.M., Lu, Q., Chae, J.J., Feldman, R.A., and Eliseeff, J.: Human iPSC-derived osteoblasts and osteoclasts together promote bone regeneration in 3D biomaterials. Sci. Rep. 6, 26761 (2016).Google Scholar
Ravichandran, R., Venugopal, J.R., Sundarrajan, S., Mukherjee, S., and Ramakrishna, S.: Precipitation of nanohydroxyapatite on PLLA/PBLG/collagen nanofibrous structures for the differentiation of adipose derived stem cells to osteogenic lineage. Biomaterials 33, 846 (2012).Google Scholar
Deng, Y., Yang, Y., and Wie, S.: Peptide-decorated nanofibrous niche augments in vitro directed osteogenic conversion of human pluripotent stem cells. Biomacromolecules 18, 587 (2017).Google Scholar
Watts, N.B. and Diab, D.L.: Long-term use of bisphosphonates in osteoporosis. J. Clin. Endocrinol. Metab. 95, 1555 (2010).Google Scholar
Jorgensen, N.R. and Schwarz, P.: Effects of anti-osteoporosis medications on fracture healing. Curr. Osteoporos. Rep. 9, 149 (2011).Google Scholar
Larsson, S. and Fazzalari, N.L.: Anti-osteoporosis therapy and fracture healing. Curr. Osteoporos. Rep. 134, 291 (2014).Google Scholar
Hegde, V., Jo, J.E., Andreopoulou, P., and Lane, J.M.: Effect of osteoporosis medications on fracture healing. Osteoporos. Int. 27, 861 (2016).Google Scholar
Vannucci, L. and Luisa, M.: Healing of the bone with anti-fracture drugs. Brandi Journal Expert Opinion on Pharmacotherapy 17, 2267 (2016).Google Scholar
Csobonyeiova, M., Polak, S., Zamborsky, R., and Danisovic, L.: iPS cell technologies and their prospect for bone regeneration and disease modeling: A mini review. J. Adv. Res. 8, 321 (2017).CrossRefGoogle ScholarPubMed
US National Library of Medicine: Available at: https://ghr.nlm.nih.gov/condition/fibrodysplasia-ossificans-progressiva (accessed April 4, 2018).Google Scholar
Matssmoto, Y., Hayashi, Y., Schlieve, C.R., Ikeya, M., Kim, H., Nguyen, T.D., Sami, S., Baba, S., Barruet, E., Nasu, A., Asaka, I., Otsuka, T., Yamanaka, S., Conklin, B.R., Toguchida, J., and Hsiao, E.C.: Induced pluripotent stem cells from patients with human fibrodysplasia ossificans progressiva show increased mineralization and cartilage formation. Orphanet J. Rare Dis. 8, 190 (2013).Google Scholar
Matsumoto, Y., Ikeya, M., Hino, K., Horigome, K., Fukuta, M., Watanabe, M., Nagata, S., Yamamoto, T., Otsuka, T., and Toguchida, J.: New protocol to optimize iPS cells for genome analysis of fibrodysplasia ossificans progressiva. Stem Cell. 33, 1730 (2015).Google Scholar
Cai, J., Orlova, V.V., Cai, X., Eekhoff, E.M.W., Zhang, K., Pei, D., Pan, G., Mummery, C.L., and Dijke, P.T.: Induced pluripotent stem cells to model human fibrodysplasia ossificans progressiva. Stem Cell Rep. 5, 963 (2015).Google Scholar
Chen, I.P., Wang, C.J., Strecker, S., Koczon-Jaremko, B., Boskey, A., and Reichenberger, E.J.: Introduction of a Phe377del mutation in ANK creates a mouse model for craniometaphyseal dysplasia. J. Bone Miner. Res. 24, 1206 (2009).Google Scholar
Hu, Y., Chen, I.P., de Almeida, S., Tiziani, V., Raposo Do Amaral, C.M., Gowrishankar, K., Passos-Bueno, M.R., and Reichenberger, E.J.: A novel autosomal recessive GJA1 missense mutation linked to craniometaphyseal dysplasia. PLoS One 12, e73576 (2013).Google Scholar
Chen, I.P., Wang, L., Jiang, X., Aguila, E.J., and Reichenberger, H.I.: A Phe377del mutation in ANK leads to impaired osteoblastogenesis and osteoclastogenesis in a mouse model for craniometaphyseal dysplasia (CMD). Hum. Mol. Genet. 20, 948 (2011).Google Scholar
Chen, I.P., Fukuda, K., Fusaki, N., Iida, A., Hasegawa, M., Lichtler, A., and Reichenberger, E.J.: Induced pluripotent stem cell reprogramming by integration-free sendai virus vectors from peripheral blood of patients with craniometaphyseal dysplasia. Cell. Reprogram. 15, 503 (2013).Google Scholar
Granata, A., Serrano, F., Bernard, W.G., McNamara, M., Low, L., Sastry, P., and Sinha, S.: An iPSC-derived vascular model of Marfan syndrome identifies key mediators of smooth muscle cell death. Nat. Genet. 49, 97 (2017).Google Scholar
Carta, L., Pereira, L., Artega-Solis, E., Lee-Arteaga, S.Y., Lenart, B., Starcher, B., Merkel, C.A., Sukoyan, M., Kerkis, A., Hazeki, N., Keene, D.R., Sakai, L.Y., and Ramirez, F.: Fibrillins 1 and 2 perform partially overlapping functions during aortic development. J. Biol. Chem. 281, 8016 (2006).Google Scholar
Byers, P.H.: Determination of the molecular basis of marfan syndrome: A growth industry. J. Clin. Invest. 114, 172 (2004).Google Scholar
Eldadah, Z.A., Brenn, T., Furthmayr, H., and Dietz, H.C.: Expression of a mutant human fibrillin allele upon a normal human or murine genetic background recapitulates a Marfan cellular phenotype. J. Clin. Invest. 95, 874 (1995).Google Scholar
Charbonneau, N.L., Carlson, E.J., Tufa, S., Sengle, G., Manalo, E.C., Carlberg, V.M., Ramirez, F., Keene, D.R., and Sakai, L.Y.: In vivo studies of mutant fibrillin-1 microfibrils. J. Biol. Chem. 285, 24943 (2010).Google Scholar
Neptune, E.R., Frischmeyer, P.A., Arking, D.E., Myers, L., Bunton, T.E., Gayraud, B., Ramirez, F., Sakai, L.Y., and Dietz, H.C.: Dysregulation of TGF-beta activation contributes to pathogenesis in Marfan syndrome. Nat. Genet. 33, 407 (2003).CrossRefGoogle ScholarPubMed
Quarto, R., Mastrogiacomo, M., Cancedda, R., Kutepov, S.M., Mukhachev, V., Lavroukov, A., Kon, E., and Marcacci, M.: Repair of large bone defects with the use of autologous bone marrow stromal cells. N. Engl. J. Med. 344, 386 (2001).Google Scholar
Salazar-Noratto, G.E., Barry, F.P., and Guldberg, R.E.: Application of biomaterials to in vitro pluripotent stem cell disease modeling of the skeletal system. J. Mater. Chem. B 4, 3482 (2016).Google Scholar
Boyette, L.B. and Tuan, R.S.: Adult stem cells and diseases of aging. J. Clin. Med. 3, 88 (2014).Google Scholar
Kiernan, J., Davies, J.E., and William, S.L.: Concise review: Musculoskeletal stem cells to treat age-related osteoporosis. Stem Cells Transl. Med. (2017). doi: 10.1002/sctm.17-0054.Google Scholar
Jones, E.A., Giannoudis, P.V., and Kouroupis, D.: Bone repair with skeletal stem cells: Rationale, progress to date and clinical application. Ther. Adv. Musculoskeletal Dis. 8, 57 (2016).Google Scholar
Kiernan, J., Davies, J.E., and Stanford, W.L.: Concise review: Musculoskeletal stem cells to treat age-related osteoporosis. Stem Cells Transl. Med. 6, 1930 (2017).Google Scholar
Marcacci, M., Kon, E., Moukhachev, V., Lavroukov, A., Kutepov, S., Quarto, R., Mastrogiacomo, M., and Cancedda, R.: Stem cells associated with macroporous bioceramics for long bone repair: 6- to 7-year outcome of a pilot clinical study. Tissue Eng. 13, 947 (2007).Google Scholar
Jaeger, M., Herten, M., Fochtmann, U., Fischer, J., Hernigou, P., Zilkens, C., Hendrich, C., and Krauspe, R.: Bridging the gap: Bone marrow aspiration concentrate reduces autologous bone grafting in osseous defects. J. Orthop. Res. 29, 173 (2011). doi: 10.1002/jor.21230.Google Scholar
Aldahmash, A.: Skeletal stem cells and their contribution to skeletal fragility: Senescence and rejuvenation. Biogerontology 17, 297 (2016).Google Scholar
Roobrouck, V.D., Ulloa-Montoya, F., and Verfaillie, C.M.: Self-renewal and differentiation capacity of young and aged stem cells. Exp. Cell Res. 314, 1937e44 (2008).Google Scholar
Steinert, A.F., Ghivizzani, S.C., Rethwilm, A., Tuan, R.S., Evans, C.H., and Noth, U.: Major biological obstacles for persistent cell-based regeneration of articular cartilage. Arthritis Res. Ther. 9, 213 (2007).Google Scholar
McCarraher, K. and Fournier-Bell, C.A.: Identifying nurses’ perceptions of barriers to research at an orthopedic specialty hospital (2017). doi: 10.1016/j.jot.2017.03.005.Google Scholar
Li, H., Collado, M., Villasante, A., Strati, K., Ortega, S., Canamero, M., Blasco, M.A., and Serrano, M.: The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 460, 1136 (2009).Google Scholar
Cheng, Z., Ito, S., Nishio, N., Xiao, H., Zhang, R., Suzuki, H., Okawa, Y., Murohara, T., and Isobe, K-I.: Establishment of induced pluripotent stem cells from aged mice using bone marrow-derived myeloid cells. J. Mol. Cell Biol. 3, 91 (2011).Google Scholar
Mahmoudi, S. and Brunet, A.: Aging and reprogramming: A two-way street. Curr. Opin. Cell Biol. 24, 744 (2012).Google Scholar
Levi, B., Hyun, J.S., Montoro, D.T., Lo, D.D., Chan, C.K., and Hu, S.: In vivo directed differentiation of pluripotent stem cells for skeletal regeneration. Proc. Natl. Acad. Sci. U.S.A. 109, 20379 (2012).Google Scholar
Zou, L., Chen, Q., Quanbeck, Z., Bechtold, J.E., and Kaufman, D.S.: Angiogenic activity mediates bone repair from human pluripotent stem cell-derived osteogenic cells. Sci. Rep. 6, 22868 (2016).Google Scholar
Ardeshirylajimi, A.R., Soleimani, M., Hosseinkhani, S., Parivar, K., and Yaghmaei, P.: A comparative study of osteogenic differentiation human induced pluripotent stem cells and adipose tissue derived mesenchymal stem cells. Cell J. 16, 235 (2014).Google Scholar
Hynes, K., Menicanin, D., Han, J., Marino, V., Mrozik, K., Gronthos, S., and Barthold, P.M.: Mesenchymal stem cells from iPS cells facilitate periodontal regeneration. J. Dent. Res. 92, 833 (2013).Google Scholar
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