Prevascularized Scaffolds Bearing Human Dental Pulp Stem Cells for Treating Complete Spinal Cord Injury.
regenerative medicine
spinal cord injury
tissue engineering
tissue repair
vascularization
Journal
Advanced healthcare materials
ISSN: 2192-2659
Titre abrégé: Adv Healthc Mater
Pays: Germany
ID NLM: 101581613
Informations de publication
Date de publication:
10 2020
10 2020
Historique:
received:
09
06
2020
revised:
08
08
2020
pubmed:
10
9
2020
medline:
15
5
2021
entrez:
9
9
2020
Statut:
ppublish
Résumé
The regeneration of injured spinal cord is hampered by the lack of vascular supply and neurotrophic support. Transplanting tissue-engineered constructs with developed vascular networks and neurotrophic factors, and further understanding the pattern of vessel growth in the remodeled spinal cord tissue are greatly desired. To this end, highly vascularized scaffolds embedded with human dental pulp stem cells (DPSCs) are fabricated, which possess paracrine-mediated angiogenic and neuroregenerative potentials. The potent pro-angiogenic effect of the prevascularized scaffolds is first demonstrated in a rat femoral bundle model, showing robust vessel growth and blood perfusion induced within these scaffolds postimplantation, as evidenced by laser speckle contrast imaging and 3D microCT dual imaging modalities. More importantly, in a rat complete spinal cord transection model, the implantation of these scaffolds to the injured spinal cords can also promote revascularization, as well as axon regeneration, myelin deposition, and sensory recovery. Furthermore, 3D microCT imaging and novel morphometric analysis on the remodeled spinal cord tissue demonstrate substantial regenerated vessels, more significantly in the sensory tract regions, which correlates with behavioral recovery following prevascularization treatment. Taken together, prevascularized DPSC-embedded constructs bear angiogenic and neurotrophic potentials, capable of augmenting and modulating SCI repair.
Identifiants
pubmed: 32902147
doi: 10.1002/adhm.202000974
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2000974Informations de copyright
© 2020 Wiley-VCH GmbH.
Références
L. A. Rocha, R. A. Sousa, D. A. Learmonth, A. J. Salgado, Front. Pharmacol. 2018, 9, 164.
C. S. Ahuja, J. R. Wilson, S. Nori, M. R. N. Kotter, C. Druschel, A. Curt, M. G. Fehlings, Nat. Rev. Dis. Primers 2017, 3, 17018.
M. T. Ng, A. T. Stammers, B. K. Kwon, Transl. Stroke Res. 2011, 2, 474.
M. Nomi, A. Atala, P. D. Coppi, S. Soker, Mol. Aspects Med. 2002, 23, 463.
S. Levenberg, J. Rouwkema, M. Macdonald, E. S. Garfein, D. S. Kohane, D. C. Darland, R. Marini, C. A. van Blitterswijk, R. C. Mulligan, P. A. D'Amore, R. ,Langer, Nat. Biotechnol. 2005, 23, 879.
Y. Shandalov, D. Egozi, J. Koffler, D. Dado-Rosenfeld, D. Ben-Shimol, A. Freiman, E. Shor, A. Kabala, S. Levenberg, Proc. Natl. Acad. Sci. USA 2014, 111, 6010.
J. Koffler, K. Kaufman-Francis, Y. Shandalov, D. Egozi, D. A. Pavlov, A. Landesberg, S. Levenberg, Proc. Natl. Acad. Sci. USA 2011, 108, 14789.
M. A. Font, A. Arboix, J. Krupinski, Curr. Cardiol. Rev. 2010, 6, 238.
C. A. Jones, D. Y. Li, Curr. Opin. Genet. Dev. 2007, 17, 332.
C. Williams, M. F. Rauch, M. Michaud, R. Robinson, H. Xu, J. Madri, E. Lavik, PLoS One 2012, 7, e53208.
F. Mackenzie, C. Ruhrberg, Development 2012, 139, 1371.
R. L. Zhang, M. Chopp, C. Roberts, X. Liu, M. Wei, S. P. Nejad-Davarani, X. Wang, Z. G. Zhang, PLoS One 2014, 9, e113972.
K. Arai, G. Jin, D. Navaratna, E. H. Lo, FEBS J. 2009, 276, 4644.
J. Ganz, E. Shor, S. Guo, A. Sheinin, I. Arie, I. Michaelevski, S. Pitaru, D. Offen, S. Levenberg, Front. Neurosci. 2017, 11, 589.
J. Koffler, W. Zhu, X. Qu, O. Platoshyn, J. N. Dulin, J. Brock, L. Graham, P. Lu, J. Sakamoto, M. Marsala, S. Chen, M. H. Tuszynski, Nat. Med. 2019, 25, 263.
Y. D. Teng, E. B. Lavik, X. Qu, K. I. Park, J. Ourednik, D. Zurakowski, R. Langer, E. Y. Snyder, Proc. Natl. Acad. Sci. USA 2002, 99, 3024.
D. Liu, X. Li, Z. Xiao, W. Yin, Y. Zhao, J. Tan, B. Chen, X. Jiang, J. Dai, Biomaterials 2019, 214, 119230.
N. Nuti, C. Corallo, B. M. Chan, M. Ferrari, B. Gerami-Naini, Stem Cell Rev. Rep. 2016, 12, 511.
V. Tirino, F. Paino, A. De Rosa, G. Papaccio, Methods Mol. Biol. 2012, 879, 443.
C. Gandia, A. Arminan, J. M. Garcia-Verdugo, E. Lledo, A. Ruiz, M. D. Minana, J. Sanchez-Torrijos, R. Paya, V. Mirabet, F. Carbonell-Uberos, M. Llop, J. A. Montero, P. Sepulveda, Stem Cells 2008, 26, 638.
M. Nakashima, K. Iohara, M. Sugiyama, Cytokine Growth Factor Rev. 2009, 20, 435.
K. Iohara, L. Zheng, M. Ito, R. Ishizaka, H. Nakamura, T. Into, K. Matsushita, M. Nakashima, Regener. Med 2009, 4, 377.
K. Sakai, A. Yamamoto, K. Matsubara, S. Nakamura, M. Naruse, M. Yamagata, K. Sakamoto, R. Tauchi, N. Wakao, S. Imagama, H. Hibi, K. Kadomatsu, N. Ishiguro, M. Ueda, J. Clin. Invest. 2012, 122, 80.
B. Mead, A. Logan, M. Berry, W. Leadbeater, B. A. Scheven, PLoS One 2014, 9, e109305.
L. Luo, Y. He, X. Wang, B. Key, B. H. Lee, H. Li, Q. Ye, Stem Cells Int. 2018, 2018, 1731289.
P. C. Demircan, A. E. Sariboyaci, Z. S. Unal, G. Gacar, C. Subasi, E. Karaoz, Cytotherapy 2011, 13, 1205.
J. Blumenthal, S. I. Cohen-Matsliah, S. Levenberg, Tissue Eng., Part A 2013, 19, 2284.
S. Landau, S. Guo, S. Levenberg, Front. Bioeng. Biotechnol. 2018, 6, 2.
S. Landau, A. A. Szklanny, G. C. Yeo, Y. Shandalov, E. Kosobrodova, A. S. Weiss, S. Levenberg, Biomaterials 2017, 122, 72.
T. Kaufman, B. Kaplan, L. Perry, Y. Shandalov, S. Landau, I. Srugo, D. Ad-El, S. Levenberg, Am. J. Transplant. 2019, 19, 37.
S. Guo, N. Perets, O. Betzer, S. Ben-Shaul, A. Sheinin, I. Michaelevski, R. Popovtzer, D. Offen, S. Levenberg, ACS Nano 2019, 13, 10015.
M. F. Rauch, S. R. Hynes, J. Bertram, A. Redmond, R. Robinson, C. Williams, H. Xu, J. A. Madri, E. B. Lavik, Eur. J. Neurosci. 2009, 29, 132.
K. A. Tran, P. P. Partyka, Y. Jin, J. Bouyer, I. Fischer, P. A. Galie, Acta Biomater. 2020, 104, 76.
Z. Fan, X. Liao, Y. Tian, X. Xuzhuzi, Y. Nie, Acta Biomater. 2020, 101, 304.
K. De Clercq, E. Persoons, T. Napso, C. Luyten, T. N. Parac-Vogt, A. N. Sferruzzi-Perri, G. Kerckhofs, J. Vriens, Proc. Natl. Acad. Sci. USA 2019, 116, 13927.
L. Schaad, R. Hlushchuk, S. Barre, R. Gianni-Barrera, D. Haberthur, A. Banfi, V. Djonov, Sci. Rep. 2017, 7, 41842.
Y. Cao, Y. Zhou, S. Ni, T. Wu, P. Li, S. Liao, J. Hu, H. Lu, J. Neurotrauma 2017, 34, 1187.
A. Freiman, Y. Shandalov, D. Rosenfeld, E. Shor, D. Ben-David, S. Meretzki, S. Levenberg, D. Egozi, J. Tissue Eng. Regener. Med. 2018, 12, e130.
K. K. Yap, G. C. Yeoh, W. A. Morrison, G. M. Mitchell, Trends Biotechnol. 2018, 36, 1011.
B. Zhang, M. Montgomery, M. D. Chamberlain, S. Ogawa, A. Korolj, A. Pahnke, L. A. Wells, S. Masse, J. Kim, L. Reis, A. Momen, S. S. Nunes, A. R. Wheeler, K. Nanthakumar, G. Keller, M. V. Sefton, M. Radisic, Nat. Mater. 2016, 15, 669.
M. A. Davis, S. M. Kazmi, A. K. Dunn, J. Biomed. Opt. 2014, 19, 086001.
K. P. Das, T. M. Freudenrich, W. R. Mundy, Neurotoxicol. Teratol. 2004, 26, 397.
J. A. Sierra-Fonseca, O. Najera, J. Martinez-Jurado, E. M. Walker, A. Varela-Ramirez, A. M. Khan, M. Miranda, N. S. Lamango, S. Roychowdhury, BMC Neurosci. 2014, 15, 132.
S. Koizumi, M. L. Contreras, Y. Matsuda, T. Hama, P. Lazarovici, G. Guroff, J. Neurosci. 1988, 8, 715.
J. Kjell, L. Olson, Dis. Model Mech. 2016, 9, 1125.
The Spinal Cord: A Christopher and Dana Reeve Foundation Text and Atlas (Eds: C. Watson, G. Paxinos, G. Kayalioglu), Academic, London 2009.
A. E. Mautes, M. R. Weinzierl, F. Donovan, L. J. Noble, Phys. Ther. 2000, 80, 673.
T. Dvir, A. Kedem, E. Ruvinov, O. Levy, I. Freeman, N. Landa, R. Holbova, M. S. Feinberg, S. Dror, Y. Etzion, J. Leor, S. Cohen, Proc. Natl. Acad. Sci. USA 2009, 106, 14990.
S. Ben-Shaul, S. Landau, U. Merdler, S. Levenberg, Proc. Natl. Acad. Sci. USA 2019, 116, 2955.
H. Zhang, F. Wu, X. Kong, J. Yang, H. Chen, L. Deng, Y. Cheng, L. Ye, S. Zhu, X. Zhang, Z. Wang, H. Shi, X. Fu, X. Li, H. Xu, L. Lin, J. Xiao, J. Transl. Med. 2014, 12, 130.
R. J. Grill, A. Blesch, M. H. Tuszynski, Exp. Neurol. 1997, 148, 444.
E. Shor, U. Merdler, I. Brosh, S. Shoham, S. Levenberg, Biomaterials 2018, 180, 1.
A. Lesman, M. Habib, O. Caspi, A. Gepstein, G. Arbel, S. Levenberg, L. Gepstein, Tissue Eng., Part A 2010, 16, 115.
C. Dray, G. Rougon, F. Debarbieux, Proc. Natl. Acad. Sci. USA 2009, 106, 9459.
A. Saliani, B. Perraud, T. Duval, N. Stikov, S. Rossignol, J. Cohen-Adad, Front. Neuroanat. 2017, 11, 129.
A. E. Haggerty, I. Maldonado-Lasuncion, M. Oudega, Biomed. Mater. 2018, 13, 044105.
M. H. Tuszynski, O. Steward, Neuron 2012, 74, 777.
S. Liu, S. R. Levine, H. R. Winn, J. Exp. Stroke Transl. Med. 2010, 3, 47.
R. Liu, H. Yuan, F. Yuan, S. H. Yang, Neurol. Res. 2012, 34, 331.
Y. Li, A. M. Lucas-Osma, S. Black, M. V. Bandet, M. J. Stephens, R. Vavrek, L. Sanelli, K. K. Fenrich, A. F. Di Narzo, S. Dracheva, I. R. Winship, K. Fouad, D. J. Bennett, Nat. Med. 2017, 23, 733.
R. Kalluri, V. S. LeBleu, Science 2020, 367, eaau6977.
P. Assinck, G. J. Duncan, B. J. Hilton, J. R. Plemel, W. Tetzlaff, Nat. Neurosci. 2017, 20, 637.
K. Kadoya, P. Lu, K. Nguyen, C. Lee-Kubli, H. Kumamaru, L. Yao, J. Knackert, G. Poplawski, J. N. Dulin, H. Strobl, Y. Takashima, J. Biane, J. Conner, S. C. Zhang, M. H. Tuszynski, Nat. Med. 2016, 22, 479.
K. Liu, Y. Lu, J. K. Lee, R. Samara, R. Willenberg, I. Sears-Kraxberger, A. Tedeschi, K. K. Park, D. Jin, B. Cai, B. Xu, L. Connolly, O. Steward, B. Zheng, Z. He, Nat. Neurosci. 2010, 13, 1075.
D. Jin, Y. Liu, F. Sun, X. Wang, X. Liu, Z. He, Nat. Commun. 2015, 6, 8074.
K. Du, S. Zheng, Q. Zhang, S. Li, X. Gao, J. Wang, L. Jiang, K. Liu, J. Neurosci. 2015, 35, 9754.
K. J. Christie, C. A. Webber, J. A. Martinez, B. Singh, D. W. Zochodne, J. Neurosci. 2010, 30, 9306.
E. S. Rosenzweig, J. H. Brock, P. Lu, H. Kumamaru, E. A. Salegio, K. Kadoya, J. L. Weber, J. J. Liang, R. Moseanko, S. Hawbecker, J. R. Huie, L. A. Havton, Y. S. Nout-Lomas, A. R. Ferguson, M. S. Beattie, J. C. Bresnahan, M. H. Tuszynski, Nat. Med. 2018, 24, 484.
M. A. Anderson, T. M. O'Shea, J. E. Burda, Y. Ao, S. L. Barlatey, A. M. Bernstein, J. H. Kim, N. D. James, A. Rogers, B. Kato, A. L. Wollenberg, R. Kawaguchi, G. Coppola, C. Wang, T. J. Deming, Z. He, G. Courtine, M. V. Sofroniew, Nature 2018, 561, 396.
J. Park, Y. Zhang, E. Saito, S. J. Gurczynski, B. B. Moore, B. J. Cummings, A. J. Anderson, L. D. Shea, Proc. Natl. Acad. Sci. USA 2019, 116, 14947.
A. Lesman, J. Koffler, R. Atlas, Y. J. Blinder, Z. Kam, S. Levenberg, Biomaterials 2011, 32, 7856.
C. Thery, S. Amigorena, G. Raposo, A. Clayton, Curr. Protoc. Cell Biol. 2006, 30, 3.22.1.
D. M. Basso, M. S. Beattie, J. C. Bresnahan, J. Neurotrauma 1995, 12, 1.
A. E. Ropper, D. K. Thakor, I. Han, D. Yu, X. Zeng, J. E. Anderson, Z. Aljuboori, S. W. Kim, H. Wang, R. L. Sidman, R. D. Zafonte, Y. D. Teng, Proc. Natl. Acad. Sci. USA 2017, 114, E820.
K. Gale, H. Kerasidis, J. R. Wrathall, Exp. Neurol. 1985, 88, 123.
M. R. Detloff, L. C. Fisher, R. J. Deibert, D. M. Basso, J. Visualized Exp. 2012, 62, e3247.
M. R. Detloff, L. M. Clark, K. J. Hutchinson, A. D. Kloos, L. C. Fisher, D. M. Basso, Exp. Neurol. 2010, 225, 366.
S. M'Dahoma, S. Bourgoin, V. Kayser, S. Barthelemy, C. Chevarin, F. Chali, D. Orsal, M. Hamon, PLoS One 2014, 9, e102027.