{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,12]],"date-time":"2026-03-12T05:05:42Z","timestamp":1773291942614,"version":"3.50.1"},"reference-count":42,"publisher":"Springer Science and Business Media LLC","issue":"7","license":[{"start":{"date-parts":[[2015,11,18]],"date-time":"2015-11-18T00:00:00Z","timestamp":1447804800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"funder":[{"name":"NSF","award":["CMMI-1300476"],"award-info":[{"award-number":["CMMI-1300476"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Ann Biomed Eng"],"published-print":{"date-parts":[[2016,7]]},"DOI":"10.1007\/s10439-015-1508-z","type":"journal-article","created":{"date-parts":[[2015,11,18]],"date-time":"2015-11-18T19:30:58Z","timestamp":1447875058000},"page":"2123-2131","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Early Passage Dependence of Mesenchymal Stem Cell Mechanics Influences Cellular Invasion and Migration"],"prefix":"10.1007","volume":"44","author":[{"given":"Stephen T.","family":"Spagnol","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wei-Chun","family":"Lin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elizabeth A.","family":"Booth","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Benoit","family":"Ladoux","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hillard M.","family":"Lazarus","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kris Noel","family":"Dahl","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2015,11,18]]},"reference":[{"key":"1508_CR1","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.molmed.2010.02.005","volume":"16","author":"J Ankrum","year":"2010","unstructured":"Ankrum, J., and J. M. Karp. Mesenchymal stem cell therapy: two steps forward, one step back. Trends Mol. Med. 16:203\u2013209, 2010.","journal-title":"Trends Mol. Med."},{"key":"1508_CR2","doi-asserted-by":"crossref","first-page":"529","DOI":"10.2217\/imt.12.41","volume":"4","author":"JJ Auletta","year":"2012","unstructured":"Auletta, J. J., A. M. Bartholomew, R. T. Maziarz, R. J. Deans, R. H. Miller, et al. The potential of mesenchymal stromal cells as a novel cellular therapy for multiple sclerosis. Immunotherapy 4:529\u2013547, 2012.","journal-title":"Immunotherapy"},{"key":"1508_CR3","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.stem.2008.03.002","volume":"2","author":"P Bianco","year":"2008","unstructured":"Bianco, P., P. G. Robey, and P. J. Simmons. Mesenchymal stem cells: revisiting history, concepts, and assays. Cell Stem Cell 2:313\u2013319, 2008.","journal-title":"Cell Stem Cell"},{"key":"1508_CR4","doi-asserted-by":"crossref","first-page":"2197","DOI":"10.1016\/j.jbiomech.2013.11.017","volume":"47","author":"T Bongiorno","year":"2014","unstructured":"Bongiorno, T., J. Kazlow, R. Mezencev, S. Griffiths, R. Olivares-Navarrete, et al. Mechanical stiffness as an improved single-cell indicator of osteoblastic human mesenchymal stem cell differentiation. J. Biomech. 47:2197\u20132204, 2014.","journal-title":"J. Biomech."},{"key":"1508_CR5","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1039\/c3ib20231c","volume":"5","author":"EA Booth-Gauthier","year":"2013","unstructured":"Booth-Gauthier, E. A., V. Du, M. Ghibaudo, A. D. Rape, K. N. Dahl, and B. Ladoux. Hutchinson-Gilford progeria syndrome alters nuclear shape and reduces cell motility in three dimensional model substrates. Integr. Biol. (Camb.) 5:569\u2013577, 2013.","journal-title":"Integr. Biol. (Camb.)"},{"key":"1508_CR6","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1002\/(SICI)1097-4644(199702)64:2<278::AID-JCB11>3.0.CO;2-F","volume":"64","author":"SP Bruder","year":"1997","unstructured":"Bruder, S. P., N. Jaiswal, and S. E. Haynesworth. Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J. Cell. Biochem. 64:278\u2013294, 1997.","journal-title":"J. Cell. Biochem."},{"key":"1508_CR7","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1002\/jcp.21200","volume":"213","author":"AI Caplan","year":"2007","unstructured":"Caplan, A. I. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J. Cell. Physiol. 213:341\u2013347, 2007.","journal-title":"J. Cell. Physiol."},{"key":"1508_CR8","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/j.stem.2008.08.008","volume":"3","author":"AI Caplan","year":"2008","unstructured":"Caplan, A. I. All MSCs are pericytes? Cell Stem Cell 3:229\u2013230, 2008.","journal-title":"Cell Stem Cell"},{"key":"1508_CR9","doi-asserted-by":"crossref","first-page":"2739","DOI":"10.1634\/stemcells.2007-0197","volume":"25","author":"G Chamberlain","year":"2007","unstructured":"Chamberlain, G., J. Fox, B. Ashton, and J. Middleton. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 25:2739\u20132749, 2007.","journal-title":"Stem Cells"},{"key":"1508_CR10","doi-asserted-by":"crossref","first-page":"455","DOI":"10.2217\/rme.12.45","volume":"7","author":"EJ Culme-Seymour","year":"2012","unstructured":"Culme-Seymour, E. J., N. L. Davie, D. A. Brindley, S. Edwards-Parton, and C. Mason. A decade of cell therapy clinical trials (2000-2010). Regenerative Med. 7:455\u2013462, 2012.","journal-title":"Regenerative Med."},{"key":"1508_CR11","doi-asserted-by":"crossref","first-page":"10271","DOI":"10.1073\/pnas.0601058103","volume":"103","author":"KN Dahl","year":"2006","unstructured":"Dahl, K. N., P. Scaffidi, M. F. Islam, A. G. Yodh, K. L. Wilson, and T. Misteli. Distinct structural and mechanical properties of the nuclear lamina in Hutchinson-Gilford progeria syndrome. Proc. Natl. Acad. Sci. USA 103:10271\u201310276, 2006.","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"1508_CR12","doi-asserted-by":"crossref","first-page":"201","DOI":"10.3389\/fimmu.2013.00201","volume":"4","author":"AM Dimarino","year":"2013","unstructured":"Dimarino, A. M., A. I. Caplan, and T. L. Bonfield. Mesenchymal stem cells in tissue repair. Front. Immunol. 4:201, 2013.","journal-title":"Front. Immunol."},{"key":"1508_CR13","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1080\/14653240600855905","volume":"8","author":"M Dominici","year":"2006","unstructured":"Dominici, M., K. Le Blanc, I. Mueller, I. Slaper-Cortenbach, F. Marini, et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315\u2013317, 2006.","journal-title":"Cytotherapy"},{"key":"1508_CR14","doi-asserted-by":"crossref","first-page":"557","DOI":"10.3233\/BIR-1991-28607","volume":"28","author":"C Dong","year":"1991","unstructured":"Dong, C., R. Skalak, and K. L. Sung. Cytoplasmic rheology of passive neutrophils. Biorheology 28:557\u2013567, 1991.","journal-title":"Biorheology"},{"key":"1508_CR15","doi-asserted-by":"crossref","first-page":"677","DOI":"10.1016\/j.cell.2006.06.044","volume":"126","author":"AJ Engler","year":"2006","unstructured":"Engler, A. J., S. Sen, H. L. Sweeney, and D. E. Discher. Matrix elasticity directs stem cell lineage specification. Cell 126:677\u2013689, 2006.","journal-title":"Cell"},{"key":"1508_CR16","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1006\/excr.2001.5408","volume":"272","author":"TM Freyman","year":"2002","unstructured":"Freyman, T. M., I. V. Yannas, R. Yokoo, and L. J. Gibson. Fibroblast contractile force is independent of the stiffness which resists the contraction. Exp. Cell Res. 272:153\u2013162, 2002.","journal-title":"Exp. Cell Res."},{"key":"1508_CR17","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1097\/00007890-197404000-00001","volume":"17","author":"AJ Friedenstein","year":"1974","unstructured":"Friedenstein, A. J., R. K. Chailakhyan, N. V. Latsinik, A. F. Panasyuk, and I. V. Keiliss-Borok. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17:331\u2013340, 1974.","journal-title":"Transplantation"},{"key":"1508_CR18","first-page":"440","volume":"6","author":"AJ Friedenstein","year":"1978","unstructured":"Friedenstein, A. J., A. A. Ivanov-Smolenski, R. K. Chajlakjan, U. F. Gorskaya, A. I. Kuralesova, et al. Origin of bone marrow stromal mechanocytes in radiochimeras and heterotopic transplants. Exp. Hematol. 6:440\u2013444, 1978.","journal-title":"Exp. Hematol."},{"key":"1508_CR19","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1039\/C0LC00221F","volume":"11","author":"M Ghibaudo","year":"2011","unstructured":"Ghibaudo, M., J. M. Di Meglio, P. Hersen, and B. Ladoux. Mechanics of cell spreading within 3D-micropatterned environments. Lab Chip 11:805\u2013812, 2011.","journal-title":"Lab Chip"},{"key":"1508_CR20","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1111\/wrr.12173","volume":"22","author":"WU Hassan","year":"2014","unstructured":"Hassan, W. U., U. Greiser, and W. Wang. Role of adipose-derived stem cells in wound healing. Wound Repair Regen. 22:313\u2013325, 2014.","journal-title":"Wound Repair Regen."},{"key":"1508_CR21","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/S0021-9290(99)00175-X","volume":"33","author":"RM Hochmuth","year":"2000","unstructured":"Hochmuth, R. M. Micropipette aspiration of living cells. J. Biomech. 33:15\u201322, 2000.","journal-title":"J. Biomech."},{"key":"1508_CR22","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1146\/annurev.bioeng.10.061807.160511","volume":"11","author":"BD Hoffman","year":"2009","unstructured":"Hoffman, B. D., and J. C. Crocker. Cell mechanics: dissecting the physical responses of cells to force. Annu. Rev. Biomed. Eng. 11:259\u2013288, 2009.","journal-title":"Annu. Rev. Biomed. Eng."},{"key":"1508_CR23","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1016\/j.stem.2009.02.001","volume":"4","author":"JM Karp","year":"2009","unstructured":"Karp, J. M., and G. S. Leng Teo. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 4:206\u2013216, 2009.","journal-title":"Cell Stem Cell"},{"key":"1508_CR24","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1200\/JCO.2000.18.2.307","volume":"18","author":"ON Koc","year":"2000","unstructured":"Koc, O. N., S. L. Gerson, B. W. Cooper, S. M. Dyhouse, S. E. Haynesworth, et al. Rapid hematopoietic recovery after coinfusion of autologous-blood stem cells and culture-expanded marrow mesenchymal stem cells in advanced breast cancer patients receiving high-dose chemotherapy. J. Clin. Oncol. 18:307\u2013316, 2000.","journal-title":"J. Clin. Oncol."},{"key":"1508_CR25","doi-asserted-by":"crossref","first-page":"3127","DOI":"10.1039\/C0SM00833H","volume":"7","author":"P Kollmannsberger","year":"2011","unstructured":"Kollmannsberger, P., C. T. Mierke, and B. Fabry. Nonlinear viscoelasticity of adherent cells is controlled by cytoskeletal tension. Soft Matter 7:3127\u20133132, 2011.","journal-title":"Soft Matter"},{"key":"1508_CR26","first-page":"557","volume":"16","author":"HM Lazarus","year":"1995","unstructured":"Lazarus, H. M., S. E. Haynesworth, S. L. Gerson, N. S. Rosenthal, and A. I. Caplan. Ex vivo expansion and subsequent infusion of human bone marrow-derived stromal progenitor cells (mesenchymal progenitor cells): implications for therapeutic use. Bone Marrow Transplant. 16:557\u2013564, 1995.","journal-title":"Bone Marrow Transplant."},{"key":"1508_CR27","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1016\/j.bbmt.2005.02.001","volume":"11","author":"HM Lazarus","year":"2005","unstructured":"Lazarus, H. M., O. N. Koc, S. M. Devine, P. Curtin, R. T. Maziarz, et al. Cotransplantation of HLA-identical sibling culture-expanded mesenchymal stem cells and hematopoietic stem cells in hematologic malignancy patients. Biol. Blood Marrow Transpl. 11:389\u2013398, 2005.","journal-title":"Biol. Blood Marrow Transpl."},{"key":"1508_CR28","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1016\/S0091-679X(07)83017-2","volume":"83","author":"B Lincoln","year":"2007","unstructured":"Lincoln, B., F. Wottawah, S. Schinkinger, S. Ebert, and J. Guck. High-throughput rheological measurements with an optical stretcher. Methods Cell Biol. 83:397\u2013423, 2007.","journal-title":"Methods Cell Biol."},{"key":"1508_CR29","doi-asserted-by":"crossref","first-page":"1011","DOI":"10.1039\/c2lc41104k","volume":"13","author":"AJ Mach","year":"2013","unstructured":"Mach, A. J., O. B. Adeyiga, and D. Di Carlo. Microfluidic sample preparation for diagnostic cytopathology. Lab Chip 13:1011\u20131026, 2013.","journal-title":"Lab Chip"},{"key":"1508_CR30","doi-asserted-by":"crossref","first-page":"2479","DOI":"10.1016\/j.bpj.2010.08.052","volume":"99","author":"JM Maloney","year":"2010","unstructured":"Maloney, J. M., D. Nikova, F. Lautenschlager, E. Clarke, R. Langer, et al. Mesenchymal stem cell mechanics from the attached to the suspended state. Biophys. J. 99:2479\u20132487, 2010.","journal-title":"Biophys. J."},{"key":"1508_CR31","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1089\/ten.teb.2012.0014","volume":"18","author":"PS Mathieu","year":"2012","unstructured":"Mathieu, P. S., and E. G. Loboa. Cytoskeletal and focal adhesion influences on mesenchymal stem cell shape, mechanical properties, and differentiation down osteogenic, adipogenic, and chondrogenic pathways. Tissue Eng. B 18:436\u2013444, 2012.","journal-title":"Tissue Eng. B"},{"key":"1508_CR32","doi-asserted-by":"crossref","first-page":"056004","DOI":"10.1088\/1478-3975\/11\/5\/056004","volume":"11","author":"KM McAndrews","year":"2014","unstructured":"McAndrews, K. M., D. J. McGrail, N. D. Quach, and M. R. Dawson. Spatially coordinated changes in intracellular rheology and extracellular force exertion during mesenchymal stem cell differentiation. Phys. Biol. 11:056004, 2014.","journal-title":"Phys. Biol."},{"key":"1508_CR33","doi-asserted-by":"crossref","first-page":"e54","DOI":"10.1038\/emm.2013.94","volume":"45","author":"MB Murphy","year":"2013","unstructured":"Murphy, M. B., K. Moncivais, and A. I. Caplan. Mesenchymal stem cells: environmentally responsive therapeutics for regenerative medicine. Exp. Mol. Med. 45:e54, 2013.","journal-title":"Exp. Mol. Med."},{"key":"1508_CR34","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1126\/science.284.5411.143","volume":"284","author":"MF Pittenger","year":"1999","unstructured":"Pittenger, M. F., A. M. Mackay, S. C. Beck, R. K. Jaiswal, R. Douglas, et al. Multilineage potential of adult human mesenchymal stem cells. Science 284:143\u2013147, 1999.","journal-title":"Science"},{"key":"1508_CR35","doi-asserted-by":"crossref","first-page":"1335","DOI":"10.1007\/s00018-012-1115-1","volume":"70","author":"WJ Polacheck","year":"2013","unstructured":"Polacheck, W. J., I. K. Zervantonakis, and R. D. Kamm. Tumor cell migration in complex microenvironments. Cell. Mol. Life Sci. CMLS 70:1335\u20131356, 2013.","journal-title":"Cell. Mol. Life Sci. CMLS"},{"key":"1508_CR36","doi-asserted-by":"crossref","first-page":"1280","DOI":"10.1016\/j.jbiomech.2012.01.032","volume":"45","author":"AJ Ribeiro","year":"2012","unstructured":"Ribeiro, A. J., S. Tottey, R. W. Taylor, R. Bise, T. Kanade, et al. Mechanical characterization of adult stem cells from bone marrow and perivascular niches. J. Biomech. 45:1280\u20131287, 2012.","journal-title":"J. Biomech."},{"key":"1508_CR37","doi-asserted-by":"crossref","first-page":"20141351","DOI":"10.1098\/rsif.2014.1351","volume":"12","author":"BD Riehl","year":"2015","unstructured":"Riehl, B. D., J. S. Lee, L. Ha, and J. Y. Lim. Fluid-flow-induced mesenchymal stem cell migration: role of focal adhesion kinase and RhoA kinase sensors. J. R. Soc. Interface 12:20141351, 2015.","journal-title":"J. R. Soc. Interface"},{"key":"1508_CR38","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1111\/j.1423-0410.2009.01227.x","volume":"98","author":"L Sensebe","year":"2010","unstructured":"Sensebe, L., M. Krampera, H. Schrezenmeier, P. Bourin, and R. Giordano. Mesenchymal stem cells for clinical application. Vox Sang. 98:93\u2013107, 2010.","journal-title":"Vox Sang."},{"key":"1508_CR39","doi-asserted-by":"crossref","first-page":"047010","DOI":"10.1117\/1.3470124","volume":"15","author":"I Sraj","year":"2010","unstructured":"Sraj, I., C. D. Eggleton, R. Jimenez, E. Hoover, J. Squier, et al. Cell deformation cytometry using diode-bar optical stretchers. J. Biomed. Opt. 15:047010, 2010.","journal-title":"J. Biomed. Opt."},{"key":"1508_CR40","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1146\/annurev-biophys-042910-155306","volume":"41","author":"Y Sun","year":"2012","unstructured":"Sun, Y., C. S. Chen, and J. Fu. Forcing stem cells to behave: a biophysical perspective of the cellular microenvironment. Annu. Rev. Biophys. 41:519\u2013542, 2012.","journal-title":"Annu. Rev. Biophys."},{"key":"1508_CR41","doi-asserted-by":"crossref","first-page":"736","DOI":"10.1016\/j.tcb.2011.09.006","volume":"21","author":"K Wolf","year":"2011","unstructured":"Wolf, K., and P. Friedl. Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol. 21:736\u2013744, 2011.","journal-title":"Trends Cell Biol."},{"key":"1508_CR42","first-page":"26","volume-title":"Cell Mechanics","author":"Y-L Wang","year":"2007","unstructured":"Wang, Y.-L., and D. E. Discher. Cell Mechanics, Vol. 608. Amsterdam: Elsevier, p. 26, 2007."}],"container-title":["Annals of Biomedical Engineering"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s10439-015-1508-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s10439-015-1508-z\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s10439-015-1508-z","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,9,1]],"date-time":"2019-09-01T17:38:13Z","timestamp":1567359493000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s10439-015-1508-z"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,11,18]]},"references-count":42,"journal-issue":{"issue":"7","published-print":{"date-parts":[[2016,7]]}},"alternative-id":["1508"],"URL":"https:\/\/doi.org\/10.1007\/s10439-015-1508-z","relation":{},"ISSN":["0090-6964","1573-9686"],"issn-type":[{"value":"0090-6964","type":"print"},{"value":"1573-9686","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,11,18]]}}}