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Human Stem Cell Derived Osteocytes in Bone-on-Chip

Published online by Cambridge University Press:  07 March 2018

E. Budyn*
Affiliation:
LMT Laboratory CNRS UMR8535, ENS Cachan, Universite Paris-Saclay, 61 Avenue du Pres. Wilson, 94235 Cachan cedex, France Department of Mechanical Engineering, University of Illinois at Chicago, 842 W. Taylor St., Chicago, IL 60607, U.S.A.
N. Gaci
Affiliation:
LMT Laboratory CNRS UMR8535, ENS Cachan, Universite Paris-Saclay, 61 Avenue du Pres. Wilson, 94235 Cachan cedex, France
S. Sanders
Affiliation:
LMT Laboratory CNRS UMR8535, ENS Cachan, Universite Paris-Saclay, 61 Avenue du Pres. Wilson, 94235 Cachan cedex, France
M. Bensidhoum
Affiliation:
B2OA Laboratory CNRS UMR7052, Universite Paris Diderot, 10 Avenue de Verdun, 75010 Paris, France
E. Schmidt
Affiliation:
Department of Mechanical Engineering, University of Illinois at Chicago, 842 W. Taylor St., Chicago, IL 60607, U.S.A.
B. Cinquin
Affiliation:
LBPA Laboratory CNRS UMR8113, ENS Cachan, Universite Paris-Saclay, 61 Avenue du Pres. Wilson, 94235 Cachan cedex, France
P. Tauc
Affiliation:
LBPA Laboratory CNRS UMR8113, ENS Cachan, Universite Paris-Saclay, 61 Avenue du Pres. Wilson, 94235 Cachan cedex, France
H. Petite
Affiliation:
B2OA Laboratory CNRS UMR7052, Universite Paris Diderot, 10 Avenue de Verdun, 75010 Paris, France
*

Abstract

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Human mesenchymal stem cells were reseeded in decellularized human bone subject to a controlled mechanical loading to create a bone-on-chip that was cultured for over 26 months. The cell morphology and their secretome were characterized using immunohistochemistry and in situ immunofluorescence under confocal microscopy. The presence of stem cell derived osteocytes was confirmed at 547 days. Different cell populations were identified. Some cells were connected by long processes and formed a network. Comparison of the MSCs in vitro reorganization and calcium response to in situ mechanical stimulation were compared to MLOY4 cells reseeded on human bone. The bone-on-chip produced an ECM of which the strength was nearly a quarter of native bone after 109 days and that contained calcium minerals at 39 days and type I collagen at 256 days. The cytoplasmic calcium concentration variations seemed to adapt to the expected in vivo mechanical load at the successive stages of cell differentiation in agreement with studies using fluid shear flow stimulation. Some degree of bone-like formation over a long period of time with the formation of a newly formed matrix was observed.

Type
Articles
Copyright
Copyright © Materials Research Society 2018 

References

REFERENCES

Carter, D.R., Hayes, W.C., and Schurman, D.J.. J. Biomech. 9, 211218 (1976).Google Scholar
Carter, D.R. and Hayes, W.C., J. Biomech., 10, 325337 (1977).Google Scholar
Yeni, Y.N. and Fyhrie, D.P., Bone, 30(3), 509514 (2002).CrossRefGoogle ScholarPubMed
Budyn, E., Bensidhoum, M., Marsan, T., Mainnemare, F., Tauc, P., Sasnouski, S., Schmidt, E., Deprez, E., Petite, H., Proc. CMBE 2015, 1, 124127, (2015). ISBN 978-0-9562914-3-1Google Scholar
Taylor, D., Hazenberg, J.G., and Lee, T.C., J. Biomech., 36, 121124 (2003).Google Scholar
Bonewald, L.F., Johnson, M., and Kneissel, M.. Bone, 54, 181, (2013).CrossRefGoogle Scholar
Miller, S.C., Calcified Tissue Internat., 41, 15, (1987).Google Scholar
Boateng, S.Y., Hartman, T.J., Ahluwalia, N., Vidula, H., Desai, T.A., and Russell, B., Osteoporos. Int, 25(Supp 3), S487S489, (2014).Google Scholar
Menton, D.N., Simmons, D.J., Chang, S.L., and Orr, B.Y., Anatom. Rec., 209, 2939, (1984).Google Scholar
Bella, L.S., Kayser, M. and Jones, C.. Am. J. Phys. Anthropol., 137, 449456, (2008).Google Scholar
Wang, Y., McNamara, L.M., Schaffler, M.B., and Weinbaum, S.. PNAS, 104(40), 1594115946, (2007).Google Scholar
McNamara, L.M., Majeska, R.J., Weinbaum, S. Friedrich, V., and Schaffler, M.B.. Anat. Rec., 292, 355363, (2009).Google Scholar
Skedros, J.G., Keenan, K., Cooper, D.M.L., and Bloebaum, R.D.. J. Struct. Biol., 187, 129148, (2014).Google Scholar
Skedros, J.G., Keenan, K, Williams, T.J., and Kiser, C.J., J. Struct. Biol., 181, 95107, (2013).CrossRefGoogle Scholar
Cowin, S.C. and Cardoso, L.. J. Biomech., 48, 842854, (2015).Google Scholar
Mullender, M., El Haj, A.J., Yang, Y., van Duin, M.A., Burger, E.H., and Klein-Nulend, I.J.. Medical and Biol. Eng. Comput., 42, 1421, (2004).CrossRefGoogle Scholar
McGarry, J.C., Klein-Nulend, I.J., and Prendergast, P.J.. Biochem. Biophys. Res. Com., 330, 341348, (2005).Google Scholar
Klein-Nulend, J., M van Oers, R.F., Bakker, A.D., Bacabac, R.G., Vatsa, A., and Weinbaum, S.. Bone, 54, 182190, (2013).Google Scholar
Wang, Y., McNamara, L.M., Schaffler, M.B., and Weinbaum, S.. J. Musculoskelet, Neuronal Interact, 8(4), 332334, (2008).Google Scholar
Sun, X., McLamore, E., Kishore, V., Slipchenko, M., Porterfield, D.M., and Akkus, O., Bone, 50, 581591, (2012).Google Scholar
Weinbaum, S., Cowin, S.C., and Zeng, Y.. J. Biomech., 27(3), 339–, (1994).Google Scholar
Parreno, J., Herd-Buckley, G., De-Hemptinne, I., and Hart, D.A., Mol. Cell. Biochem, 317, 2122, (2008).Google Scholar
Pridaux, M., Wijenayaka, A.R., Kumarasinghe, D.D., Ormsby, R.T., Evdokiou, A., and Findlay, D.M.. Calcif. Tissue Int., 95, 183193, (2014).Google Scholar
Hutmacher, D.W., Biomaterials, 21, 25292543, (2000).CrossRefGoogle Scholar
Stevens, B., Yang, Y., Mohandas, A., Stucker, B., and Nguyen, K.T.. J. Biomed. Mater. Res. B, 85B, 573582, (2008).CrossRefGoogle Scholar
Bose, S., Roy, M., and Bandyopadhay, A.. Trends Biotechnol., 30, 546554, (2012).Google Scholar
Budyn, E., Bensidhoum, M., Marsan, T., Mainnemare, F., Tauc, P., Deprez, E. and Petite, H., Proc. ECCOMAS Coupled Problems, 1:110, (2015).Google Scholar
Woo, S.M., Rosser, J., Dusevich, V., Kalajzic, I., and Bonewald, L.F.. JBMR, 26(11), 2634–46, (2011).CrossRefGoogle Scholar
Davidson, E.H., Reformat, D.D., Orlando Canizares, A.A., Saadeh, P.B. Wagner, I.J., and Warren, S.M.. J. Tisssue Eng. Regen. Med., 6, 769776, (2012).Google Scholar
Marino, S., .A Staines, K., Brown, G, Howard-Jones, R.A., and Adamczyk, M.. BoneKEy Reports, 5(818), 118, (2016).Google Scholar
Takai, E., Mauck, R.L., Hung, C.T., and Guo, X.E.. J. Bone Min. Res.., 19(9), 1403–10, (2011).Google Scholar
You, J., Yellowhey, C.E., Donahue, H.J., Zhang, Y., Chen, Q., and Jacobs, C.R.. ASME J. Biomech. Eng, 122, 387–, (2000).CrossRefGoogle Scholar
Frost, H.M., Anat. Rec., 219, 195, (1987).CrossRefGoogle Scholar
Frost, H.M.. Anat. Rec. A Discov. Mol. Cell. Evol. Biol., 275, 10811101, (2003).Google Scholar
Al Nazer, R., Lanovaz, J., Kawalilak, C., Johnston, J.D., and Kontulainen, S.. J. Biomech., 45, 2740, (2012).Google Scholar
Klein-Nulend, J., Van Der Plas, A., Semeins, C.M., Ajubi, N.E., Frangos, J.A., Nijweide, P.J., and Burger, E.H.. Res. Com., 9, 441445, (1995).Google Scholar
Bonivtch, A.R., Bonewald, L.F., and Nicolella, D.P.. J. Biomech, 40, 21992206, (2007).Google Scholar
Adachi, T., Aonuma, Y., Hojo, M., Hojo, M., and Kamioka, H.. Biochem. Biophys. Res. Comm., 389, 495500, (2009).CrossRefGoogle Scholar
Adachi, T., Aonuma, Y., Hojo, M., Takano-Yamamoto, T., and Kamioka, H.. J. Biomech., 42, 19891995, (2009).Google Scholar
Adachi, T., Aonuma, Y., Ito, S.-I., Tanaka, M., Hojo, M., Takano-Yamamoto, T., and Kamioka, H.. J. Biomech., 42, 25072512, (2009).Google Scholar
Jing, D., Baik, A. D., Lu, X. L., Zhou, B., Lai, X., Wang, L., Luo, E., and Guo, X. E.. The FASEB J. Res. Comm., 28, 15821592, (2014).Google Scholar
Lopez, E., Vidal, B., Berland, S., Camprasse, S., Camprasse, G., and Silves, C.. Tissue and Cell, 24(5), 667679, (1992).Google Scholar
Sautier, J.M., Nefussi, J.R., Boulekbache, H., and Forest, N., Soc. for in vitro biol.., 26(11):10791085, (1999).Google Scholar
Xynos, I.D., J Hukkanen, M.V., Batten, J.J., Buttery, L.D., Hench, L.L., and Polak, J.M.. Calcif. Tissue Internat., 67, 312329, (2000).Google Scholar
Ishaug, S.L., Crane, G.M., Miller, M.J., Yasko, A.W., Yaszemski, M.J., and Mikos, A.G.. Journal of Biomechanical Materials Research, 36, 1728-, (1997).Google Scholar
Schantz, J.T., Hutmacher, D.W., Ng, K.W., Khor, H.L., Lim, T.C., and Teoh, S.H.. The International Journal of Oral and Maxillofacial Implants, 17(2), 161174, (2002).Google Scholar
Bancroft, G.N., Sikavitsas, V.I., van den Dolder, J., Sheffield, T.L., Ambrose, C.G., Jansen, J.A., and Miko, A.G... PNAS, 99(20), 1260012605, 2002.Google Scholar
Klein-Nulend, J., Van Der Plas, A., Semeins, C. M., Ajubi, N. E., Francos, J.A., Nijweide, P.J., and Burger, E. H.. The FASEB Journal, 9(5), 441445, (1995).Google Scholar
Scheiner, S., Pivonka, P., and Hellmich, C.. Biomech. Model. Mechanobiology, 9, 928, (2016).Google Scholar
Morin, C., and Hellmich, C.. Ultrasonics, 54, 12511269, (2014).Google Scholar
Hellmich, C., Celundova, D., and Ulm, J.. Journal of Engineering Mechanics, 135(5), 382394, (2009).Google Scholar
Nouhou Bako, A., Darboux, F., James, F., Josserand, C. and Lucas, C.. Processes and Landforms, 41(9), 1991210, (2016).Google Scholar
SKYSCAN NV. NRecon User Manual. (2011).Google Scholar
FEI. Avizo 8: Avizo User’s Guide. (2014).Google Scholar
Dassault Syst`emes. Abaqus 6.12: Abaqus/CAE User’s Manual. (2012).Google Scholar
Jonvaux, J., Hoc, T., and Budyn, E., International Journal of Numerical Methods in Biomedical Engineering, 28(9), 974998, (2012).Google Scholar
Hasslinger, P., Vass, V., Dejaco, A., Blanchard, R., Örlygsson, G., Gargiulo, P., and Hellmich, C.. International Journal for Numerical Methods in Engineering Science and Mechanics, 17(3), 222244, (2016).Google Scholar
Sanders, S., Bensidhoum, M., and Budyn, E., ZetaComputational Resources Ltd, Proc. CMBE 2015, 1:132135, (2015). ISBN: 978-0-9562914-3Google Scholar
Oliver, W. and Pharr, G.M.. Journal of Materials Research, 7(6), 15641583, (1992).Google Scholar
Budyn, E., Bensidhoum, M., Marsan, T., Mainnemare, F., Sasnouski, S., Tauc, P., Deprez, E., and Perite, H.. Coupled Problems in Science and Engineering VI, 6th International Conference on Computational Methods for Coupled Problems in Science and Engineering (Coupled Problems), 1, 566575, (2015).Google Scholar
Budyn, E., Jonvaux, J., and Hoc, T.. International Journal for Numerical Methods in Biomedical Engineering, 28(8), 815837, (2012).Google Scholar
Budyn, E., Jonvaux, J., and Hoc, T.. Journal of Applied Mechanics – Transaction of the ASME, 79(2), 021001, (2012).Google Scholar
Budyn, E., and Hoc, T.. Proceedings of the ASME 11th Biennal Conference on Engineering Systems design and Analysis, vol. 4, 271278, (2012).Google Scholar
Budyn, E., Jonvaux, J., Funfschilling, C., and Hoc, T.. Journal of Applied Mechanics – Transaction of the ASME, 79(1), 011008, (2012).Google Scholar
Blanchard, R., Dejaco, A., Bongaers, E., and Hellmich, C.. Journal of Biomechanics, 46, 27102721, (2013).Google Scholar
Renders, G.A.P., Mulder, L., van Ruijven, L.J., Langenbach, G.E.J., and van Eijden, M. G. J., Journal of Biomechanics, 44, 402407, (2011).CrossRefGoogle Scholar
Swadener, J.G., Rho, J.Y. and Pharr, G.M.. Journal of Biomedical Materials Research, 57, 108112, (2001).Google Scholar
Salguero, L., Saadat, F., and Savostianov, I.. Journal of Biomechanics, 47, 32793287, (2014).CrossRefGoogle Scholar
Schneider, C.A., Rasband, W.S. and Eliceiri, K.W., Nat. Methods. 9(7), 671675. (2012).Google Scholar
Geuzaine, C. and Remacle, J.F., Int. J. Num. Meth. Eng., 79(11), 13091331, (2009).Google Scholar
Vaughan, T.J., Mullen, C.A., Verbruggen, SW. and McNamara, L.M., Biomech Model Mechanobiol., 14, 703718 (2016).Google Scholar
Varga, P., Hesse, B, Langer, M., Schrof, S, annicke, N.M., Suhonen, H., Pacureanu, A., Pahr, D. Peyrin, F., and Raum, K.. Biomech Model Mechanobiol, 14, 267282, (2015).Google Scholar
Budyn, E., Bensidhoum, M., Sanders, S., Schmidt, E., Tauc, P., Deprez, E. and Petite, H.. European Cell and Materials Conferences, 32(supp. 4), 32, (2016).Google Scholar
Wittkowske, C., Reilly, G.C., Lacroix, D., and Perrault, C.M.. Frontiers in Bioengineering and Biotechnology, 4:122, (2016).Google Scholar
Duncan, R.L. and Turner, C.H.. Calcif. Tissue Int., 57, 344–58, (1995).Google Scholar
Klein-Nulend, J., Bacabac, R.G., and Bakker, A.D.. Eur. Cell. Mater., 24, 278291, (2012).CrossRefGoogle Scholar
Bonewald, L. F. Journal of Bone and Mineral Research, 26(2), 229238, (2013).Google Scholar
Bonewald, L.F. and Johnson, M.L., Bone, 42(4), 606615, (2008).Google Scholar
Pridaux, M., Findlay, D.M., and Atkins, G.J.. Curr. Opin. Pharmacol., 28, 2430, (2016).Google Scholar
Nather, A., David, V., Teng, J.W.H., Lee, C.W., and Pereira, B.P., Annals Academy of Medicine, 39(8), 599606, (2010).Google Scholar
Runyan, C.M., Vu, A.T., Rumburg, A., Bove, K., Racadio, J., Billmire, D.A., and Taylor, J.A. Plastic and reconstructive surgery, 136(4), 461473, (2015).CrossRefGoogle Scholar
Thompson, W.R., Uzer, G., Brobst, K.E., Xie, Z., Sen, B., Yen, S.S., Styner, M. and Rubin, J., Sci. Report, 5, 11049, (2015).Google Scholar
Klein-Nulend, J., Bakker, A.D., and Bacabac, R.G., Osteoporosis Int., 25, 14271437, (2014).Google Scholar
Pastrama, M.I., Scheiner, S., Pivonka, P., and Hellmich, C.. Bone, 107, 208221, (2018).Google Scholar
Goldsztein, G.H.. SIAM Journal of Applied Mathematics, 65(6), 21282140, (2005).Google Scholar
Jones, D.B., Nolte, H., Scholübbers, J.G., Turner, E., and Veltel, D.. Biomaterials, 12, 101110, (1991).Google Scholar