Journal Home > Volume 3 , Issue 3
Brain Science Advances 2017, 3(3): 159-175 https://doi.org/10.18679/CN11-6030_R.2017.025
Review Article | Open Access | Issue | Published: 01 September 2017

Strategies to improve the migration of mesenchymal stromal cells in cell therapy

Show Author's Information Gaigai Li1,  Yang Hu1( ),  Yanfang Chen2,  Zhouping Tang1( )
Department of Neurology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
Department of Pharmacology and Toxicology, Wright State University School of Medicine, Dayton, Ohio 45345, USA
Keywords:
migration, cell therapy, MSCs, engraftment efficiency, neurological disorder
Cite this article:
Li G, Hu Y, Chen Y, et al. Strategies to improve the migration of mesenchymal stromal cells in cell therapy. Brain Science Advances, 2017, 3(3): 159-175. https://doi.org/10.18679/CN11-6030_R.2017.025
Download citation
EndNote(RIS)
BibTeX

460

Views

7

Downloads

Citations

3

Crossref

N/A

WoS

N/A

Scopus

N/A

CSCD

Abstract Full text About this article

Mesenchymal stromal/stem cells (MSCs) are multipotent cells under consideration as a potential new therapy for a variety of inflammatory diseases including certain neurological disorders. It is generally thought that the efficacy of cell therapy in attenuating damage after ischemia, inflammation, or injury depends on the quantity of transplanted cells recruited to the target tissue. However, only a small number of systematically infused MSCs can effectively migrate to target sites, which significantly decreases the efficacy of exogenous cell-based therapy. In this review, we discuss specific factors influencing MSC migration, and summarize current strategies that effectively promote the motility of MSCs. In addition, we describe several protocols to improve the migration of stromal cells into the nervous system and, therefore, enhance the efficiency of engraftment as means of treating neurological disorders.


menu
Abstract
Full text
Outline
About this article

Strategies to improve the migration of mesenchymal stromal cells in cell therapy

Show Author's information Gaigai Li1, Yang Hu1( ), Yanfang Chen2, Zhouping Tang1( )
Department of Neurology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
Department of Pharmacology and Toxicology, Wright State University School of Medicine, Dayton, Ohio 45345, USA

Abstract

Mesenchymal stromal/stem cells (MSCs) are multipotent cells under consideration as a potential new therapy for a variety of inflammatory diseases including certain neurological disorders. It is generally thought that the efficacy of cell therapy in attenuating damage after ischemia, inflammation, or injury depends on the quantity of transplanted cells recruited to the target tissue. However, only a small number of systematically infused MSCs can effectively migrate to target sites, which significantly decreases the efficacy of exogenous cell-based therapy. In this review, we discuss specific factors influencing MSC migration, and summarize current strategies that effectively promote the motility of MSCs. In addition, we describe several protocols to improve the migration of stromal cells into the nervous system and, therefore, enhance the efficiency of engraftment as means of treating neurological disorders.

Keywords: migration, cell therapy, MSCs, engraftment efficiency, neurological disorder

References(167)

[1]
Watt FM, Hogan BLM. Out of Eden: Stem cells and their niches. Science 2000, 287(5457): 1427–1430.
DOI Google Scholar
[2]
Neirinckx V, Coste C, Rogister B, Wislet-Gendebien S. Concise review: Adult mesenchymal stem cells, adult neural crest stem cells, and therapy of neurological pathologies: A state of play. Stem Cells Transl Med 2013, 2(4): 284–296.
DOI Google Scholar
[3]
Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: Implications for cell-based therapies. Tissue Eng 2001, 7(2): 211–228.
DOI Google Scholar
[4]
He XY, Jiang WK, Luo ZR, Qu TJ, Wang ZH, Liu NN, Zhang YQ, Cooper PR, He WX. IFN-γ regulates human dental pulp stem cells behavior via NF-κB and MAPK signaling. Sci Rep 2017, 7: 40681.
DOI Google Scholar
[5]
Futami I, Ishijima M, Kaneko H, Tsuji K, Ichikawa-Tomikawa N, Sadatsuki R, Muneta T, Arikawa-Hirasawa E, Sekiya I, Kaneko K. Isolation and characterization of multipotential mesenchymal cells from the mouse synovium. PLoS One 2012, 7(9): e45517.
DOI Google Scholar
[6]
Troyer DL, Weiss ML. Concise review: Wharton’s Jelly-Derived cells are a primitive stromal cell population. Stem Cells 2008, 26(3): 591–599.
DOI Google Scholar
[7]
Zhang XY, Wang YM, Gao YH, Liu XJ, Bai TT, Li MY, Li LS, Chi GF, Xu H, Liu FL, Liu JY, Li YL. Maintenance of high proliferation and multipotent potential of human hair follicle-derived mesenchymal stem cells by growth factors. Int J Mol Med 2013, 31(4): 913–921.
DOI Google Scholar
[8]
Huang YS, Li IH, Chueh SH, Hueng DY, Tai MC, Liang CM, Lien SB, Sytwu HK, Ma KH. Mesenchymal stem cells from rat olfactory bulbs can differentiate into cells with cardiomyocyte characteristics. J Tissue Eng Regen Med 2015, 9(12): E191–E201.
DOI Google Scholar
[9]
Ankrum J, Karp JM. Mesenchymal stem cell therapy: Two steps forward, one step back. Trends Mol Med 2010, 16(5): 203–209.
DOI Google Scholar
[10]
Salem HK, Thiemermann C. Mesenchymal stromal cells: Current understanding and clinical status. Stem Cells 2010, 28(3): 585–596.
DOI Google Scholar
[11]
Karp JM, Leng Teo GS. Mesenchymal stem cell homing: The devil is in the details. Cell Stem Cell 2009, 4(3): 206–216.
DOI Google Scholar
[12]
Liu S, Zhou JL, Zhang X, Liu Y, Chen J, Hu B, Song JL, Zhang YY. Strategies to optimize adult stem cell therapy for tissue regeneration. Int J Mol Sci 2016, 17(6): 982.
DOI Google Scholar
[13]
Liu XF, Ye RD, Yan T, Yu SP, Wei L, Xu GL, Fan XY, Jiang YJ, Stetler RA, Liu G, Chen JL. Cell based therapies for ischemic stroke: From basic science to bedside. Prog Neurobiol 2014, 115: 92–115.
DOI Google Scholar
[14]
Kuai XL, Li P, Zhang JFeng, Cao W, Yuan WY, Shao N, Guan CQ, Wang ZW. Stromal derived factor-1/CXCR4 axis involved in bone marrow mesenchymal stem cells recruitment to injured liver. Stem Cells Int 2016, 2016: 8906945.
DOI Google Scholar
[15]
Chavakis E, Urbich C, Dimmeler S. Homing and engraftment of progenitor cells: A prerequisite for cell therapy. J Mol Cell Cardiol 2008, 45(4): 514–522.
DOI Google Scholar
[16]
Tang YH, Zhang CF, Wang JX, Lin XJ, Zhang L, Yang Y, Wang YT, Zhang ZJ, Bulte JWM, Yang GY. MRI/SPECT/ fluorescent tri-modal probe for evaluating the homing and therapeutic efficacy of transplanted mesenchymal stem cells in a rat ischemic stroke model. Adv Funct Mater 2015, 25(7): 1024–1034.
DOI Google Scholar
[17]
Burst VR, Gillis M, Pütsch F, Herzog R, Fischer JH, Heid P, Müller-Ehmsen J, Schenk K, Fries JWU, Baldamus CA, Benzing T. Poor cell survival limits the beneficial impact of mesenchymal stem cell transplantation on acute kidney injury. Nephron Exp Nephrol 2010, 114(3): e107–e116.
DOI Google Scholar
[18]
Detante O, Moisan A, Dimastromatteo J, Richard MJ, Riou L, Grillon E, Barbier E, Desruet MD, De Fraipont F, Segebarth C, Jaillard A, Hommel M, Ghezzi C, Remy C. Intravenous administration of 99mTc-HMPAO-labeled human mesenchymal stem cells after stroke: In vivo imaging and biodistribution. Cell Transplant 2009, 18(12): 1369–1379.
DOI Google Scholar
[19]
Chavakis E, Dimmeler S. Homing of progenitor cells to ischemic tissues. Antioxid Redox Signal 2011, 15(4): 967–980.
DOI Google Scholar
[20]
Imhof BA, Aurrand-Lions M. Adhesion mechanisms regulating the migration of monocytes. Nat Rev Immunol 2004, 4(6): 432–444.
DOI Google Scholar
[21]
Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: The leukocyte adhesion cascade updated. Nat Rev Immunol 2007, 7(9): 678–689.
DOI Google Scholar
[22]
Luster AD, Alon R, von Andrian UH. Immune cell migration in inflammation: Present and future therapeutic targets. Nat Immunol 2005, 6(12): 1182–1190.
DOI Google Scholar
[23]
Rüster B, Göttig S, Ludwig RJ, Bistrian R, Müller S, Seifried E, Gille J, Henschler R. Mesenchymal stem cells display coordinated rolling and adhesion behavior on endothelial cells. Blood 2006, 108(12): 3938–3944.
DOI Google Scholar
[24]
Belema-Bedada F, Uchida S, Martire A, Kostin S, Braun T. Efficient homing of multipotent adult mesenchymal stem cells depends on FROUNT-mediated clustering of CCR2. Cell Stem Cell 2008, 2(6): 566–575.
DOI Google Scholar
[25]
Ponte AL, Marais E, Gallay N, Langonné A, Delorme B, Hérault O, Charbord P, Domenech J. The in vitro migration capacity of human bone marrow mesenchymal stem cells: Comparison of chemokine and growth factor chemotactic activities. Stem Cells 2007, 25(7): 1737–1745.
DOI Google Scholar
[26]
Baek SJ, Kang SK, Ra JC. In vitro migration capacity of human adipose tissue-derived mesenchymal stem cells reflects their expression of receptors for chemokines and growth factors. Exp Mol Med 2011, 43(10): 596–603.
DOI Google Scholar
[27]
Almalki SG, Agrawal DK. Effects of matrix metalloproteinases on the fate of mesenchymal stem cells. Stem Cell Res Ther 2016, 7(1): 129.
DOI Google Scholar
[28]
De Becker A, Van Hummelen P, Bakkus M, Vande Broek I, De Wever J, De Waele M, Van Riet I. Migration of culture-expanded human mesenchymal stem cells through bone marrow endothelium is regulated by matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-3. Haematologica 2007, 92(4): 440–449.
DOI Google Scholar
[29]
De Becker A, Van Riet I. Homing and migration of mesenchymal stromal cells: How to improve the efficacy of cell therapy? World J Stem Cells 2016, 8(3): 73–87.
DOI Google Scholar
[30]
Ma JH, Liu N, Yi B, Zhang XC, Gao BB, Zhang YS, Xu RX, Li X, Dai YW. Transplanted hUCB-MSCs migrated to the damaged area by SDF-1/CXCR4 signaling to promote functional recovery after traumatic brain injury in rats. Neurol Res 2015, 37(1): 50–56.
DOI Google Scholar
[31]
Li J, Guo WC, Xiong M, Han H, Chen J, Mao D, Tang B, Yu HL, Zeng Y. Effect of SDF-1/CXCR4 axis on the migration of transplanted bone mesenchymal stem cells mobilized by erythropoietin toward lesion sites following spinal cord injury. Int J Mol Med 2015, 36(5): 1205–1214.
DOI Google Scholar
[32]
Li L, Wu SZ, Liu Z, Zhuo ZX, Tan KB, Xia HM, Zhuo LS, Deng XJ, Gao YH, Xu YL. Ultrasound-targeted microbubble destruction improves the migration and homing of mesenchymal stem cells after myocardial infarction by upregulating SDF-1/CXCR4: A pilot study. Stem Cells Int 2015, 2015: 691310.
DOI Google Scholar
[33]
Wiehe JM, Kaya Z, Homann JM, Wöhrle J, Vogt K, Nguyen T, Rottbauer W, Torzewski J, Fekete N, Rojewski M, Schrezenmeier H, Moepps B, Zimmermann O. GMP-adapted overexpression of CXCR4 in human mesenchymal stem cells for cardiac repair. Int J Cardiol 2013, 167(5): 2073–2081.
DOI Google Scholar
[34]
Yang JX, Zhang N, Wang HW, Gao P, Yang QP, Wen QP. CXCR4 receptor overexpression in mesenchymal stem cells facilitates treatment of acute lung injury in rats. J Biol Chem 2015, 290(4): 1994–2006.
DOI Google Scholar
[35]
Ryu CH, Park SA, Kim SM, Lim JY, Jeong CH, Jun JA, Oh JH, Park SH, Oh WI, Jeun SS. Migration of human umbilical cord blood mesenchymal stem cells mediated by stromal cell-derived factor-1/CXCR4 axis via Akt, ERK, and p38 signal transduction pathways. Biochem Biophys Res Commun 2010, 398(1): 105–110.
DOI Google Scholar
[36]
Xu LN, Zhao Y, Wang MW, Song W, Li B, Liu W, Jin XB, Zhang HY. Defocused low-energy shock wave activates adipose tissue-derived stem cells in vitro via multiple signaling pathways. Cytotherapy 2016, 18(12): 1503–1514.
DOI Google Scholar
[37]
Guo J, Zhang HF, Xiao JJ, Wu J, Ye Y, Li Z, Zou YZ, Li XL. Monocyte chemotactic protein-1 promotes the myocardial homing of mesenchymal stem cells in dilated cardiomyopathy. Int J Mol Sci 2013, 14(4): 8164–8178.
DOI Google Scholar
[38]
Stamatovic SM, Keep RF, Kunkel SL, Andjelkovic AV. Potential role of MCP-1 in endothelial cell tight junction ‘opening’: Signaling via Rho and Rho kinase. J Cell Sci 2003, 116(22): 4615–4628.
DOI Google Scholar
[39]
Zhang Y, Zheng J, Zhou ZJ, Zhou HD, Wang YJ, Gong ZL, Zhu J. Fractalkine promotes chemotaxis of bone marrow-derived mesenchymal stem cells towards ischemic brain lesions through Jak2 signaling and cytoskeletal reorganization. FEBS J 2015, 282(5): 891–903.
DOI Google Scholar
[40]
Zhu J, Zhou ZJ, Liu Y, Zheng J. Fractalkine and CX3CR1 are involved in the migration of intravenously grafted human bone marrow stromal cells toward ischemic brain lesion in rats. Brain Res 2009, 1287: 173–183.
DOI Google Scholar
[41]
Naaldijk Y, Johnson AA, Ishak S, Meisel HJR, Hohaus C, Stolzing A. Migrational changes of mesenchymal stem cells in response to cytokines, growth factors, hypoxia, and aging. Exp Cell Res 2015, 338(1): 97–104.
DOI Google Scholar
[42]
Son BR, Marquez-Curtis LA, Kucia M, Wysoczynski M, Turner AR, Ratajczak J, Ratajczak MZ, Janowska-Wieczorek A. Migration of bone marrow and cord blood mesenchymal stem cells in vitro is regulated by stromal-derived factor-1-CXCR4 and hepatocyte growth factor-c-met axes and involves matrix metalloproteinases. Stem Cells 2006, 24(5): 1254–1264.
DOI Google Scholar
[43]
Majumdar MK, Keane-Moore M, Buyaner D, Hardy WB, Moorman MA, McIntosh KR, Mosca JD. Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J Biomed Sci 2003, 10(2): 228–241.
DOI Google Scholar
[44]
Fischer UM, Harting MT, Jimenez F, Monzon-Posadas WO, Xue HS, Savitz SI, Laine GA, Cox CS Jr. Pulmonary passage is a major obstacle for intravenous stem cell delivery: The pulmonary first-pass effect. Stem Cells Dev 2009, 18(5): 683–692.
DOI Google Scholar
[45]
Leibacher J, Henschler R. Biodistribution, migration and homing of systemically applied mesenchymal stem/stromal cells. Stem Cell Res Ther 2016, 7(1): 7.
DOI Google Scholar
[46]
Segers VFM, Van Riet I, Andries LJ, Lemmens K, Demolder MJ, De Becker AJML, Kockx MM, De Keulenaer GW. Mesenchymal stem cell adhesion to cardiac microvascular endothelium: Activators and mechanisms. Am J Physiol Heart Circ Physiol 2006, 290(4): H1370–H1377.
DOI Google Scholar
[47]
Constantin G, Marconi S, Rossi B, Angiari S, Calderan L, Anghileri E, Gini B, Bach SD, Martinello M, Bifari F, Galiè M, Turano E, Budui S, Sbarbati A, Krampera M, Bonetti B. Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells 2009, 27(10): 2624–2635.
DOI Google Scholar
[48]
Yilmaz G, Vital S, Yilmaz CE, Stokes KY, Alexander JS, Granger DN. Selectin-mediated recruitment of bone marrow stromal cells in the postischemic cerebral microvasculature. Stroke 2011, 42(3): 806–811.
DOI Google Scholar
[49]
Lawton B, Boyette JR, Hu M, Lian TS. Selectin blockade decreases postischemic recruitment of bone marrow stromal cells. Laryngoscope 2013, 123(12): 2993–2995.
DOI Google Scholar
[50]
Sackstein R, Merzaban JS, Cain DW, Dagia NM, Spencer JA, Lin CP, Wohlgemuth R. Ex vivo glycan engineering of CD44 programs human multipotent mesenchymal stromal cell trafficking to bone. Nat Med 2008, 14(2): 181–187.
DOI Google Scholar
[51]
Brauer PR. Mmps-role in cardiovascular development and disease. Front Biosci 2006, 11(1): 447–478.
DOI Google Scholar
[52]
Ries C, Egea V, Karow M, Kolb H, Jochum M, Neth P. MMP-2, MT1-MMP, and TIMP-2 are essential for the invasive capacity of human mesenchymal stem cells: Differential regulation by inflammatory cytokines. Blood 2007, 109(9): 4055–4063.
DOI Google Scholar
[53]
Tajiri N, Kaneko Y, Shinozuka K, Ishikawa H, Yankee E, McGrogan M, Case C, Borlongan CV. Stem cell recruitment of newly formed host cells via a successful seduction? Filling the gap between neurogenic niche and injured brain site. PLoS One 2013, 8(9): e74857.
DOI Google Scholar
[54]
Tajiri N, Duncan K, Antoine A, Pabon M, Acosta SA, de la Pena I, Hernadez-Ontiveros DG, Shinozuka K, Ishikawa H, Kaneko Y, Yankee E, McGrogan M, Case C, Borlongan CV. Stem cell-paved biobridge facilitates neural repair in traumatic brain injury. Front Syst Neurosci 2014, 8: 116.
DOI Google Scholar
[55]
Liska MG, Crowley MG, Nguyen H, Borlongan CV. Biobridge concept in stem cell therapy for ischemic stroke. J Neurosurg Sci 2017, 61(2): 173–179.
DOI Google Scholar
[56]
Duncan K, Gonzales-Portillo GS, Acosta SA, Kaneko Y, Borlongan CV, Tajiri N. Stem cell-paved biobridges facilitate stem transplant and host brain cell interactions for stroke therapy. Brain Res 2015, 1623: 160–165.
DOI Google Scholar
[57]
Rombouts WJC, Ploemacher RE. Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia 2003, 17(1): 160–170.
DOI Google Scholar
[58]
Cheng NC, Hsieh TY, Lai HS, Young TH. High glucose-induced reactive oxygen species generation promotes stemness in human adipose-derived stem cells. Cytotherapy 2016, 18(3): 371–383.
DOI Google Scholar
[59]
Barbash IM, Chouraqui P, Baron J, Feinberg MS, Etzion S, Tessone A, Miller L, Guetta E, Zipori D, Kedes LH, Kloner RA, Leor J. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: Feasibility, cell migration, and body distribution. Circulation 2003, 108(7): 863–868.
DOI Google Scholar
[60]
Beggs KJ, Lyubimov A, Borneman JN, Bartholomew A, Moseley A, Dodds R, Archambault MP, Smith AK, Mcintosh KR. Immunologic consequences of multiple, high-dose administration of allogeneic mesenchymal stem cells to baboons. Cell Transplant 2006, 15(8–9): 711–721.
DOI Google Scholar
[61]
Walczak P, Zhang J, Gilad AA, Kedziorek DA, Ruiz-Cabello J, Young RG, Pittenger MF, van Zijl PCM, Huang J, Bulte JWM. Dual-modality monitoring of targeted intraarterial delivery of mesenchymal stem cells after transient ischemia. Stroke 2008, 39(5): 1569–1574.
DOI Google Scholar
[62]
Wei N, Yu SP, Gu XH, Taylor TM, Song D, Liu XF, Wei L. Delayed intranasal delivery of hypoxic-preconditioned bone marrow mesenchymal stem cells enhanced cell homing and therapeutic benefits after ischemic stroke in mice. Cell Transplant 2013, 22(6): 977–991.
DOI Google Scholar
[63]
Rosová I, Dao M, Capoccia B, Link D, Nolta JA. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells. Stem Cells 2008, 26(8): 2173–2182.
DOI Google Scholar
[64]
Kubo M, Li TS, Kamota T, Ohshima M, Qin SL, Hamano K. Increased expression of CXCR4 and integrin αM in hypoxia-preconditioned cells contributes to improved cell retention and angiogenic potency. J Cell Physiol 2009, 220(2): 508–514.
DOI Google Scholar
[65]
Naderi-Meshkin H, Bahrami AR, Bidkhori HR, Mirahmadi M, Ahmadiankia N. Strategies to improve homing of mesenchymal stem cells for greater efficacy in stem cell therapy. Cell Biol Int 2015, 39(1): 23–34.
DOI Google Scholar
[66]
Liu HB, Xue WJ, Ge GQ, Luo XH, Li Y, Xiang HL, Ding XM, Tian PX, Tian XH. Hypoxic preconditioning advances CXCR4 and CXCR7 expression by activating HIF-1α in MSCs. Biochem Biophys Res Commun 2010, 401(4): 509–515.
DOI Google Scholar
[67]
Liu HB, Liu SB, Li Y, Wang XH, Xue WJ, Ge GQ, Luo XH. The role of SDF-1-CXCR4/CXCR7 axis in the therapeutic effects of hypoxia-preconditioned mesenchymal stem cells for renal ischemia/reperfusion injury. PLoS One 2012, 7(4): e34608.
DOI Google Scholar
[68]
Cerrada I, Ruiz-Saurí A, Carrero R, Trigueros C, Dorronsoro A, Sanchez-Puelles JM, Diez-Juan A, Montero JA, Sepúlveda P. Hypoxia-inducible factor 1 Alpha contributes to cardiac healing in mesenchymal stem cells-mediated cardiac repair. Stem Cells Dev 2013, 22(3): 501–511.
DOI Google Scholar
[69]
Yu Q, Liu LZ, Lin J, Wang Y, Xuan XB, Guo Y, Hu SJ. SDF-1α/CXCR4 axis mediates the migration of mesenchymal stem cells to the hypoxic-ischemic brain lesion in a rat model. Cell J 2015, 16(4): 440–447.
Google Scholar
[70]
Choi JH, Lee YB, Jung J, Hwang SG, Oh IH, Kim GJ. Hypoxia inducible factor-1α regulates the migration of bone marrow mesenchymal stem cells via integrin α4. Stem Cells Int 2016, 2016: 7932185.
DOI Google Scholar
[71]
Shi MX, Li J, Liao LM, Chen B, Li BZ, Chen L, Jia HR, Zhao RC. Regulation of CXCR4 expression in human mesenchymal stem cells by cytokine treatment: Role in homing efficiency in nod/scid mice. Haematologica 2007, 92(7): 897–904.
DOI Google Scholar
[72]
Li YX, Yu XY, Lin SG, Li XH, Zhang SD, Song YH. Insulin-like growth factor 1 enhances the migratory capacity of mesenchymal stem cells. Biochem Biophys Res Commun 2007, 356(3): 780–784.
DOI Google Scholar
[73]
Xinaris C, Morigi M, Benedetti V, Imberti B, Fabricio AS, Squarcina E, Benigni A, Gagliardini E, Remuzzi G. A novel strategy to enhance mesenchymal stem cell migration capacity and promote tissue repair in an injury specific fashion. Cell Transplant 2013, 22(3): 423–436.
DOI Google Scholar
[74]
Fan HY, Zhao GF, Liu L, Liu F, Gong W, Liu XQ, Yang L, Wang JJ, Hou YY. Pre-treatment with IL-1β enhances the efficacy of MSC transplantation in DSS-induced colitis. Cell Mol Immunol 2012, 9(6): 473–481.
DOI Google Scholar
[75]
Duijvestein M, Wildenberg ME, Welling MM, Hennink S, Molendijk I, van Zuylen VL, Bosse T, Vos ACW, de Jonge-Muller ESM, Roelofs H, van der Weerd L, Verspaget HW, Fibbe WE, te Velde AA, van den Brink GR, Hommes DW. Pretreatment with interferon-γ enhances the therapeutic activity of mesenchymal stromal cells in animal models of colitis. Stem Cells 2011, 29(10): 1549–1558.
DOI Google Scholar
[76]
Cui X, Chen JL, Zacharek A, Li Y, Roberts C, Kapke A, Savant-Bhonsale S, Chopp M. Nitric oxide donor upregulation of stromal cell-derived factor-1/chemokine (CXC motif) receptor 4 enhances bone marrow stromal cell migration into ischemic brain after stroke. Stem Cells 2007, 25(11): 2777–2785.
DOI Google Scholar
[77]
Qiu YY, Marquez-Curtis LA, Janowska-Wieczorek A. Mesenchymal stromal cells derived from umbilical cord blood Migrate in response to complement C1q. Cytotherapy 2012, 14(3): 285–295.
DOI Google Scholar
[78]
Yu Q, Chen L, You Y, Zou C, Zhang YS, Liu QH, Cheng FJ. Erythropoietin combined with granulocyte colony-stimulating factor enhances MMP-2 expression in mesenchymal stem cells and promotes cell migration. Mol Med Rep 2011, 4(1): 31–36.
DOI Google Scholar
[79]
Tsai LK, Wang ZF, Munasinghe J, Leng Y, Leeds P, Chuang DM. Mesenchymal stem cells primed with valproate and lithium robustly migrate to infarcted regions and facilitate recovery in a stroke model. Stroke 2011, 42(10): 2932–2939.
DOI Google Scholar
[80]
Linares GR, Chiu CT, Scheuing L, Leng Y, Liao HM, Maric D, Chuang DM. Preconditioning mesenchymal stem cells with the mood stabilizers lithium and valproic acid enhances therapeutic efficacy in a mouse model of Huntington’s disease. Exp Neurol 2016, 281: 81–92.
DOI Google Scholar
[81]
Dendorfer A, Heidbreder M, Hellwig-Bürgel T, Jöhren O, Qadri F, Dominiak P. Deferoxamine induces prolonged cardiac preconditioning via accumulation of oxygen radicals. Free Radic Biol Med 2005, 38(1): 117–124.
DOI Google Scholar
[82]
Nouri F, Salehinejad P, Nematollahi-Mahani SN, Kamarul T, Zarrindast MR, Sharifi AM. Deferoxamine preconditioning of neural-like cells derived from human Wharton’s Jelly mesenchymal stem cells as a strategy to promote their tolerance and therapeutic potential: An in vitro study. Cell Mol Neurobiol 2016, 36(5): 689–700.
DOI Google Scholar
[83]
Knowles HJ, Tian YM, Mole DR, Harris AL. Novel mechanism of action for hydralazine: Induction of hypoxia-inducible factor-1α, vascular endothelial growth factor, and angiogenesis by inhibition of prolyl hydroxylases. Circ Res 2004, 95(2): 162–169.
DOI Google Scholar
[84]
Yu XF, Lu CL, Liu H, Rao SX, Cai JR, Liu SP, Kriegel AJ, Greene AS, Liang MY, Ding XQ. Hypoxic preconditioning with cobalt of bone marrow mesenchymal stem cells improves cell migration and enhances therapy for treatment of ischemic acute kidney injury. PLoS One 2013, 8(5): e62703.
DOI Google Scholar
[85]
Pourjafar M, Saidijam M, Mansouri K, Ghasemibasir H, Karimi Dermani F, Najafi R. All-trans retinoic acid preconditioning enhances proliferation, angiogenesis and migration of mesenchymal stem cell in vitro and enhances wound repair in vivo. Cell Prolif 2017, 50(1): e12315.
DOI Google Scholar
[86]
Mortezaee K, Pasbakhsh P, Ragerdi Kashani I, Sabbaghziarani F, Omidi A, Zendedel A, Ghasemi S, Dehpour AR. Melatonin pretreatment enhances the homing of bone marrow-derived mesenchymal stem cells following transplantation in a rat model of liver fibrosis. Iran Biomed J 2016, 20(4): 207–216.
Google Scholar
[87]
Zhang W, Schmull S, Du M, Liu J, Lu Z, Zhu H, Xue S, Lian F. Estrogen receptor α and β in mouse: Adipose-derived stem cell proliferation, migration, and brown adipogenesis in vitro. Cell Physiol Biochem 2016, 38(6): 2285–2299.
DOI Google Scholar
[88]
Chen ZQ, Wei QS, Hong GJ, Chen D, Liang J, He W, Chen MH. Polydatin induces bone marrow stromal cells migration by activation of ERK1/2. Biomed Pharmacother 2016, 82: 49–53.
DOI Google Scholar
[89]
Ma Q, Yang JJ, Zhou H, Zhang Y, Chen YD. Exenatide promotes chemotactic migration of adipose-derived stem cells through SDF-1/CXCR-4/Rho GTPase pathway. Journal of Southern Medical University 2016, 36(8): 1034–1040.
Google Scholar
[90]
Heinelt M, Karp JM, Levy O. Cell therapy-showing cells the way home. Oncotarget 2015, 6(20): 17857–17858.
DOI Google Scholar
[91]
Levy O, Mortensen LJ, Boquet G, Tong ZX, Perrault C, Benhamou B, Zhang JD, Stratton T, Han E, Safaee H, Musabeyezu J, Yang ZJ, Multon MC, Rothblatt J, Deleuze JF, Lin CP, Karp JM. A small-molecule screen for enhanced homing of systemically infused cells. Cell Rep 2015, 10(8): 1261–1268.
DOI Google Scholar
[92]
Jang S, Cho HH, Cho YB, Park JS, Jeong HS. Functional neural differentiation of human adipose tissue-derived stem cells using bFGF and forskolin. BMC Cell Biol 2010, 11(1): 25.
DOI Google Scholar
[93]
Abdullah RH, Yaseen NY, Salih SM, Al-Juboory AA, Hassan A, Al-Shammari AM. Induction of mice adult bone marrow mesenchymal stem cells into functional motor neuron-like cells. J Chem Neuroanat 2016, 77: 129–142.
DOI Google Scholar
[94]
Marei HE, El-Gamal A, Althani A, Afifi N, Abd-Elmaksoud A, Farag A, Cenciarelli C, Caceci T, Hasan A. Cholinergic and dopaminergic neuronal differentiation of human adipose tissue derived mesenchymal stem cells. J Cell Physiol, in Press, .
DOI Google Scholar
[95]
Salehi H, Amirpour N, Niapour A, Razavi S. An overview of neural differentiation potential of human adipose derived stem cells. Stem Cell Rev Rep 2016, 12(1): 26–41.
DOI Google Scholar
[96]
Nowakowski A, Walczak P, Lukomska B, Janowski M. Genetic engineering of mesenchymal stem cells to induce their migration and survival. Stem Cells Int 2016, 2016: 4956063.
DOI Google Scholar
[97]
Yu XL, Chen DP, Zhang Y, Wu XL, Huang ZX, Zhou HT, Zhang YD, Zhang ZJ. Overexpression of CXCR4 in mesenchymal stem cells promotes migration, neuroprotection and angiogenesis in a rat model of stroke. J Neurol Sci 2012, 316(1–2): 141–149.
DOI Google Scholar
[98]
Wang YL, Fu W, Zhang SC, He XM, Liu ZA, Gao D, Xu TJ. CXCR-7 receptor promotes SDF-1α-induced migration of bone marrow mesenchymal stem cells in the transient cerebral ischemia/reperfusion rat hippocampus. Brain Res 2014, 1575: 78–86.
DOI Google Scholar
[99]
Li H, Jiang YM, Jiang XX, Guo XM, Ning HM, Li YH, Liao L, Yao HY, Wang XY, Liu YL, Zhang Y, Chen H, Mao N. CCR7 guides migration of mesenchymal stem cell to secondary lymphoid organs: A novel approach to separate GvHD from GvL effect. Stem Cells 2014, 32(7): 1890–1903.
DOI Google Scholar
[100]
Kim SM, Kim DS, Jeong CH, Kim DH, Kim JH, Jeon HB, Kwon SJ, Jeun SS, Yang YS, Oh W, Chang JW. CXC chemokine receptor 1 enhances the ability of human umbilical cord blood-derived mesenchymal stem cells to migrate toward gliomas. Biochem Biophys Res Commun 2011, 407(4): 741–746.
DOI Google Scholar
[101]
Meng FB, Rui YF, Xu LL, Wan C, Jiang XH, Li G. Aqp1 enhances migration of bone marrow mesenchymal stem cells through regulation of FAK and β-catenin. Stem Cells Dev 2014, 23(1): 66–75.
DOI Google Scholar
[102]
Maijenburg MW, Gilissen C, Melief SM, Kleijer M, Weijer K, ten Brinke A, Roelofs H, Van Tiel CM, Veltman JA, de Vries CJM, van der Schoot CE, Voermans C. Nuclear receptors Nur77 and Nurr1 modulate mesenchymal stromal cell migration. Stem Cells Dev 2012, 21(2): 228–238.
DOI Google Scholar
[103]
Zhang X, Yan G, Diao Z, Sun H, Hu Y. NUR77 inhibits the expression of TIMP2 and increases the migration and invasion of HTR-8/SVneo cells induced by CYR61. Placenta 2012, 33(7): 561–567.
DOI Google Scholar
[104]
Xu LL, Huang S, Hou YH, Liu Y, Ni M, Meng FB, Wang KX, Rui YF, Jiang XH, Li G. Sox11-modified mesenchymal stem cells (MSCs) accelerate bone fracture healing: Sox11 regulates differentiation and migration of MSCs. FASEB J 2015, 29(4): 1143–1152.
DOI Google Scholar
[105]
Kumar S, Ponnazhagan S. Bone homing of mesenchymal stem cells by ectopic α4 integrin expression. FASEB J 2007, 21(14): 3917–3927.
DOI Google Scholar
[106]
Liao WB, Pham V, Liu LN, Riazifar M, Pone EJ, Zhang SX, Ma FX, Lu MR, Walsh CM, Zhao WA. Mesenchymal stem cells engineered to express selectin ligands and IL-10 exert enhanced therapeutic efficacy in murine experimental autoimmune encephalomyelitis. Biomaterials 2016, 77: 87–97.
DOI Google Scholar
[107]
Hu XY, Chen PP, Wu Y, Wang K, Xu YC, Chen H, Zhang L, Wu RR, Webster KA, Yu H, Zhu W, Wang JA. MiR-211/STAT5A signaling modulates migration of mesenchymal stem cells to improve its therapeutic efficacy. Stem Cells 2016, 34(7): 1846–1858.
DOI Google Scholar
[108]
Zhu AS, Kang NX, He LH, Li XY, Xu XJ, Zhang HX. MiR-221 and miR-26b regulate chemotactic migration of MSCs toward HGF through activation of Akt and FAK. J Cell Biochem 2016, 117(6): 1370–1383.
DOI Google Scholar
[109]
Ko IK, Kim BG, Awadallah A, Mikulan J, Lin P, Letterio JJ, Dennis JE. Targeting improves MSC treatment of inflammatory bowel disease. Mol Ther 2010, 18(7): 1365– 1372.
DOI Google Scholar
[110]
Sarkar D, Vemula PK, Zhao WA, Gupta A, Karnik R, Karp JM. Engineered mesenchymal stem cells with self-assembled vesicles for systemic cell targeting. Biomaterials 2010, 31(19): 5266–5274.
DOI Google Scholar
[111]
Sarkar D, Vemula PK, Teo GSL, Spelke D, Karnik R, Wee LY, Karp JM. Chemical engineering of mesenchymal stem cells to induce a cell rolling response. Bioconjugate Chem 2008, 19(11): 2105–2109.
DOI Google Scholar
[112]
Yin K, Zhu R, Wang S, Zhao RC. Low-level laser effect on proliferation, migration, and antiapoptosis of mesenchymal stem cells. Stem Cells Dev 2017, 26(10): 762–775.
DOI Google Scholar
[113]
Babona-Pilipos R, Droujinine IA, Popovic MR, Morshead CM. Adult subependymal neural precursors, but not differentiated cells, undergo rapid cathodal migration in the presence of direct current electric fields. PLoS One 2011, 6(8): e23808.
DOI Google Scholar
[114]
Feng JF, Liu J, Zhang XZ, Zhang L, Jiang JY, Nolta J, Zhao M. Guided migration of neural stem cells derived from human embryonic stem cells by an electric field. Stem Cells 2012, 30(2): 349–355.
DOI Google Scholar
[115]
Griffin M, Iqbal SA, Sebastian A, Colthurst J, Bayat A. Degenerate wave and capacitive coupling increase human MSC invasion and proliferation while reducing cytotoxicity in an in vitro wound healing model. PLoS One 2011, 6(8): e23404.
DOI Google Scholar
[116]
Zhang R, Liu Y, Yan K, Chen L, Chen XR, Li P, Chen FF, Jiang XD. Anti-inflammatory and immunomodulatory mechanisms of mesenchymal stem cell transplantation in experimental traumatic brain injury. J Neuroinflammation 2013, 10(1): 871.
DOI Google Scholar
[117]
Karamouzian S, Nematollahi-Mahani SN, Nakhaee N, Eskandary H. Clinical safety and primary efficacy of bone marrow mesenchymal cell transplantation in subacute spinal cord injured patients. Clin Neurol Neurosurg 2012, 114(7): 935–939.
DOI Google Scholar
[118]
Alexanian AR, Fehlings MG, Zhang ZY, Maiman DJ. Transplanted neurally modified bone marrow-derived mesenchymal stem cells promote tissue protection and locomotor recovery in spinal cord injured rats. Neurorehabil Neural Repair 2011, 25(9): 873–880.
DOI Google Scholar
[119]
Bang OY, Lee JS, Lee PH, Lee G. Autologous mesenchymal stem cell transplantation in stroke patients. Ann Neurol 2005, 57(6): 874–882.
DOI Google Scholar
[120]
Honmou O, Houkin K, Matsunaga T, Niitsu Y, Ishiai S, Onodera R, Waxman SG, Kocsis JD. Intravenous administration of auto serum-expanded autologous mesenchymal stem cells in stroke. Brain 2011, 134(6): 1790–1807.
DOI Google Scholar
[121]
Sasaki Y, Honmou O. Bone marrow stem cell therapy for stroke. Nihon Rinsho 2011, 69(12): 2203–2208. (in Japanese)
Google Scholar
[122]
Honmou O. Cell therapy for stroke. Rinsho Shink 2013, 53(11): 1175–1176. (in Japanese)
DOI Google Scholar
[123]
Zhang Y, Deng H, Pan C, Hu Y, Wu Q, Liu N, Tang ZP. Mesenchymal stromal cell therapy in ischemic stroke. J Neurorestoratol 2016, 4: 79–83.
DOI Google Scholar
[124]
Fatar M, Stroick M, Griebe M, Marwedel I, Kern S, Bieback K, Giesel FL, Zechmann C, Kreisel S, Vollmar F, Vollmar, Alonso A, Back W, Meairs S, Hennerici MG. Lipoaspirate-derived adult mesenchymal stem cells improve functional outcome during intracerebral hemorrhage by proliferation of endogenous progenitor cells: Stem cells in intracerebral hemorrhages. Neurosci Lett 2008, 443(3): 174–178.
DOI Google Scholar
[125]
Camp DM, Loeffler DA, Farrah DM, Borneman JN, Lewitt PA. Cellular immune response to intrastriatally implanted allogeneic bone marrow stromal cells in a rat model of Parkinson’s disease. J Neuroinflammation 2009, 6(1): 17.
DOI Google Scholar
[126]
Teixeira FG, Carvalho MM, Panchalingam KM, Rodrigues AJ, Mendes-Pinheiro B, Anjo S, Manadas B, Behie LA, Sousa N, Salgado AJ. Impact of the secretome of human mesenchymal stem cells on brain structure and animal behavior in a rat model of Parkinson’s disease. Stem Cells Transl Med 2017, 6(2): 634–646.
DOI Google Scholar
[127]
Karussis D, Karageorgiou C, Vaknin-Dembinsky A, Gowda-Kurkalli B, Gomori JM, Kassis I, Bulte JW, Petrou P, Ben-Hur T, Abramsky O, Slavin S. Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Arch Neurol 2010, 67(10): 1187–1194.
DOI Google Scholar
[128]
Agah EM, Parivar K, Joghataei MT. Therapeutic effect of transplanted human Wharton’s Jelly stem cell-derived oligodendrocyte progenitor cells (hWJ-MSC-derived OPCs) in an animal model of multiple sclerosis. Mol Neurobiol 2014, 49(2): 625–632.
DOI Google Scholar
[129]
Hou Y, Ryu CH, Park KY, Kim SM, Jeong CH, Jeun SS. Effective combination of human bone marrow mesenchymal stem cells and minocycline in experimental autoimmune encephalomyelitis mice. Stem Cell Res Ther 2013, 4(4): 77.
DOI Google Scholar
[130]
Mazzini L, Ferrero I, Luparello V, Rustichelli D, Gunetti M, Mareschi K, Testa L, Stecco A, Tarletti R, Miglioretti M, Vercelli R, Oggioni GD, Carriero A, Cantello R, Monaco F, Fagioli F. Mesenchymal stem cell transplantation in amyotrophic lateral sclerosis: A phase I clinical trial. Exp Neurol 2010, 223(1): 229–237.
DOI Google Scholar
[131]
Vercelli A, Mereuta OM, Garbossa D, Muraca G, Mareschi K, Rustichelli D, Ferrero I, Mazzini L, Madon E, Fagioli F. Human mesenchymal stem cell transplantation extends survival, improves motor performance and decreases neuroinflammation in mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 2008, 31(3): 395–405.
DOI Google Scholar
[132]
Yun HM, Kim HS, Park KR, Shin JM, Kang AR, Lee KI, Song S, Kim YB, Han SB, Chung HM, Hong JT. Placenta-derived mesenchymal stem cells improve memory dysfunction in an Aβ1–42-infused mouse model of Alzheimer’s disease. Cell Death Dis 2013, 4(12): e958.
DOI Google Scholar
[133]
Lin YT, Chern Y, Shen CKJ, Wen HL, Chang YC, Li H, Cheng TH, Hsieh-Li HM. Human mesenchymal stem cells prolong survival and ameliorate motor deficit through trophic support in Huntington’s disease mouse models. PLoS One 2011, 6(8): e22924.
DOI Google Scholar
[134]
Snyder BR, Chiu AM, Prockop DJ, Chan AWS. Human multipotent stromal cells (MSCs) increase neurogenesis and decrease atrophy of the striatum in a transgenic mouse model for Huntington’s disease. PLoS One 2010, 5(2): e9347.
DOI Google Scholar
[135]
Sadan O, Shemesh N, Barzilay R, Dadon-Nahum M, Blumenfeld-Katzir T, Assaf Y, Yeshurun M, Djaldetti R, Cohen Y, Melamed E, Offen D. Mesenchymal stem cells induced to secrete neurotrophic factors attenuate quinolinic acid toxicity: A potential therapy for Huntington’s disease. Exp Neurol 2012, 234(2): 417–427.
DOI Google Scholar
[136]
Koniusz S, Andrzejewska A, Muraca M, Srivastava AK, Janowski M, Lukomska B. Extracellular vesicles in physiology, pathology, and therapy of the immune and central nervous system, with focus on extracellular vesicles derived from mesenchymal stem cells as therapeutic tools. Front Cell Neurosci 2016, 10: 109.
DOI Google Scholar
[137]
Gervois P, Wolfs E, Ratajczak J, Dillen Y, Vangansewinkel T, Hilkens P, Bronckaers A, Lambrichts I, Struys T. Stem cell-based therapies for ischemic stroke: Preclinical results and the potential of imaging-assisted evaluation of donor cell fate and mechanisms of brain regeneration. Med Res Rev 2016, 36(6): 1080–1126.
DOI Google Scholar
[138]
Daviaud N, Garbayo E, Schiller PC, Perez-Pinzon M, Montero-Menei CN. Organotypic Cultures as tools for optimizing central nervous system cell therapies. Exp Neurol 2013, 248: 429–440.
DOI Google Scholar
[139]
Danielyan L, Schäfer R, von Ameln-Mayerhofer A, Buadze M, Geisler J, Klopfer T, Burkhardt U, Proksch B, Verleysdonk S, Ayturan M, Buniatian GH, Gleiter CH, Frey II WH. Intranasal delivery of cells to the brain. Eur J Cell Biol 2009, 88(6): 315–324.
DOI Google Scholar
[140]
Lanza C, Morando S, Voci A, Canesi L, Principato MC, Serpero LD, Mancardi G, Uccelli A, Vergani L. Neuroprotective mesenchymal stem cells are endowed with a potent antioxidant effect in vivo. J Neurochem 2009, 110(5): 1674–1684.
DOI Google Scholar
[141]
Fransson M, Piras E, Wang H, Burman J, Duprez I, Harris RA, LeBlanc K, Magnusson PU, Brittebo E, Loskog ASI. Intranasal delivery of central nervous system-retargeted human mesenchymal stromal cells prolongs treatment efficacy of experimental autoimmune encephalomyelitis. Immunology 2014, 142(3): 431–441.
DOI Google Scholar
[142]
Donega V, Nijboer CH, van Tilborg G, Dijkhuizen RM, Kavelaars A, Heijnen CJ. Intranasally administered mesenchymal stem cells promote a regenerative niche for repair of neonatal ischemic brain injury. Exp Neurol 2014, 261: 53–64.
DOI Google Scholar
[143]
Abbott NJ, Patabendige AAK, Dolman DEM, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis 2010, 37(1): 13–25.
DOI Google Scholar
[144]
Matsushita T, Kibayashi T, Katayama T, Yamashita Y, Suzuki S, Kawamata J, Honmou O, Minami M, Shimohama S. Mesenchymal stem cells transmigrate across brain microvascular endothelial cell monolayers through transiently formed inter-endothelial gaps. Neurosci Lett 2011, 502(1): 41–45.
DOI Google Scholar
[145]
Liu LN, Eckert MA, Riazifar H, Kang DK, Agalliu D, Zhao WA. From blood to the brain: Can systemically transplanted mesenchymal stem cells cross the blood-brain barrier? Stem Cells Int 2013, 2013: 435093.
DOI Google Scholar
[146]
Lin MN, Shang DS, Sun W, Li B, Xu X, Fang WG, Zhao WD, Cao L, Chen YH. Involvement of PI3K and ROCK signaling pathways in migration of bone marrow-derived mesenchymal stem cells through human brain microvascular endothelial cell monolayers. Brain Res 2013, 1513: 1–8.
DOI Google Scholar
[147]
Feng Y, Yu HM, Shang DS, Fang WG, He ZY, Chen YH. The involvement of CXCL11 in bone marrow-derived mesenchymal stem cell migration through human brain microvascular endothelial cells. Neurochem Res 2014, 39(4): 700–706.
DOI Google Scholar
[148]
Xiong XB, Sun Y, Sattiraju A, Jung Y, Mintz A, Hayasaka S, Li KCP. Remote spatiotemporally controlled and biologically selective permeabilization of blood-brain barrier. J Control Release 2015, 217: 113–120.
DOI Google Scholar
[149]
Rahmi G, Pidial L, Silva AKA, Blondiaux E, Meresse B, Gazeau F, Autret G, Balvay D, Cuenod CA, Perretta S, Tavitian B, Wilhelm C, Cellier C, Clément O. Designing 3D mesenchymal stem cell sheets merging magnetic and fluorescent features: When cell sheet technology meets image-guided cell therapy. Theranostics 2016, 6(5): 739– 751.
DOI Google Scholar
[150]
Yang BX, Brahmbhatt A, Nieves Torres E, Thielen B, McCall DL, Engel S, Bansal A, Pandey MK, Dietz AB, Leof EB, DeGrado TR, Mukhopadhyay D, Misra S. Tracking and therapeutic value of human adipose tissue-derived mesenchymal stem cell transplantation in reducing venous neointimal hyperplasia associated with arteriovenous fistula. Radiology 2016, 279(2): 513–522.
DOI Google Scholar
[151]
Ribot EJ, Gaudet JM, Chen YH, Gilbert KM, Foster PJ. In vivo MR detection of fluorine-labeled human MSC using the bSSFP sequence. Int J Nanomedicine 2014, 9: 1731–1739.
DOI Google Scholar
[152]
Dong SS, Liu N, Hu Y, Zhang P, Pan C, Zhang YP, Tang YX, Tang ZP. Transplantation of neural progenitor cells differentiated from adipose tissue-derived stem cells for treatment of sciatic nerve injury. Transl Neurosci Clin 2016, 2(2): 108–119.
DOI Google Scholar
[153]
Lee SH, Kim Y, Rhew D, Kim A, Jo KR, Yoon Y, Choi KU, Jung T, Kim WH, Kweon OK. Impact of local injection of brain-derived neurotrophic factor–expressing mesenchymal stromal cells (MSCs) combined with intravenous MSC delivery in a canine model of chronic spinal cord injury. Cytotherapy 2017, 19(1): 75–87.
DOI Google Scholar
[154]
Ezquer M, Ezquer F, Ricca M, Allers C, Conget P. Intravenous administration of multipotent stromal cells prevents the onset of non-alcoholic steatohepatitis in obese mice with metabolic syndrome. J Hepatol 2011, 55(5): 1112–1120.
DOI Google Scholar
[155]
Li M, Zhang YX, Zhang Z, Zhou XY, Zuo XL, Cong YZ, Li YQ. Endomicroscopy will track injected mesenchymal stem cells in rat colitis models. Inflamm Bowel Dis 2015, 21(9): 2068–2077.
DOI Google Scholar
[156]
Jasmin, de Souza GT, Andrade Louzada R, Rosado-de-Castro PH, Mendez-Otero R, de Carvalho ACC. Tracking stem cells with superparamagnetic iron oxide nanoparticles: Perspectives and considerations. Int J Nanomedicine 2017, 12: 779–793.
DOI Google Scholar
[157]
Mahmoudi M, Hosseinkhani H, Hosseinkhani M, Boutry S, Simchi A, Journeay WS, Subramani K, Laurent S. Magnetic resonance imaging tracking of stem cells in vivo using iron oxide nanoparticles as a tool for the advancement of clinical regenerative medicine. Chem Rev 2011, 111(2): 253–280.
DOI Google Scholar
[158]
Lee S, Yoon HI, Na JH, Jeon S, Lim S, Koo H, Han SS, Kang SW, Park SJ, Moon SH, Park JH, Cho YW, Kim BS, Kim SK, Lee T, Kim D, Lee S, Pomper MG, Kwon IC, Kim K. In vivo stem cell tracking with imageable nanoparticles that bind bioorthogonal chemical receptors on the stem cell surface. Biomaterials 2017, 139: 12–29.
DOI Google Scholar
[159]
Gerrits A, Dykstra B, Kalmykowa OJ, Klauke K, Verovskaya E, Broekhuis MJC, de Haan G, Bystrykh LV. Cellular barcoding tool for clonal analysis in the hematopoietic system. Blood 2010, 115(13): 2610–2618.
DOI Google Scholar
[160]
Maijenburg MW, van der Schoot CE, Voermans C. Mesenchymal stromal cell migration: Possibilities to improve cellular therapy. Stem Cells Dev 2012, 21(1): 19–29.
DOI Google Scholar
[161]
Li AA, Gong H, Zhang B, Wang QD, Yan C, Wu JP, Liu Q, Zeng SQ, Luo QM. Micro-optical sectioning tomography to obtain a high-resolution atlas of the mouse brain. Science 2010, 330(6009): 1404–1408.
DOI Google Scholar
[162]
Gong H, Xu DL, Yuan J, Li XN, Guo CD, Peng J, Li YX, Schwarz LA, Li AA, Hu BH, Xiong BY, Sun QT, Zhang YL, Liu JP, Zhong QY, Xu TH, Zeng SQ, Luo QM. High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level. Nat Commun 2016, 7: 12142.
DOI Google Scholar
[163]
Gong H, Zeng SQ, Yan C, Lv XH, Yang ZQ, Xu TH, Feng Z, Ding WX, Qi XL, Li AA, Wu JP, Luo QM. Continuously tracing brain-wide long-distance axonal projections in mice at a one-micron voxel resolution. NeuroImage 2013, 74: 87–98.
DOI Google Scholar
[164]
Osten P, Margrie TW. Mapping brain circuitry with a light microscope. Nat Methods 2013, 10(6): 515–523.
DOI Google Scholar
[165]
Pan C, Liu N, Zhang P, Wu Q, Deng H, Xu F, Lian LF, Liang QM, Hu Y, Zhu SQ, Tang ZP. EGB761 ameliorates neuronal apoptosis and promotes angiogenesis in experimental intracerebral hemorrhage via RSK1/GSK3β pathway. Mol Neurobiol, in Press, .
DOI Google Scholar
[166]
Janowski M, Walczak P, Date I. Intravenous route of cell delivery for treatment of neurological disorders: A meta-analysis of preclinical results. Stem Cells Dev 2010, 19(1): 5–16.
DOI Google Scholar
[167]
Konala VBR, Mamidi MK, Bhonde R, Das AK, Pochampally R, Pal R. The current landscape of the mesenchymal stromal cell secretome: A new paradigm for cell-free regeneration. Cytotherapy 2016, 18(1): 13–24.
DOI Google Scholar
Publication history
Copyright
Rights and permissions

Publication history

Received: 23 May 2017
Revised: 17 June 2017
Accepted: 20 July 2017
Published: 01 September 2017
Issue date: September 2017

Copyright

© The authors 2017.

Rights and permissions

This article is published with open access at www.TNCjournal.com

Return