Enhancing the migration ability of mesenchymal stromal cells by targeting the SDF-1/CXCR4 axis

BioMed Research International

Volumn 2013, Issue , 2013, Pages

  Marquez Curtis, Leah A ^a   Janowska Wieczorek, Anna ^a,b  

^a CANADIAN BLOOD SERVICES   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CXCL12 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; STROMAL CELL DERIVED FACTOR 1;

BIOSYNTHESIS; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; FETUS BLOOD; GENETICS; HUMAN; MESENCHYMAL STROMA CELL; REVIEW; SIGNAL TRANSDUCTION;

CELL DIFFERENTIATION; CELL MOVEMENT; CHEMOKINE CXCL12; FETAL BLOOD; HUMANS; MESENCHYMAL STROMAL CELLS; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION;

EID: 84893735629     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2013/561098     Document Type: Review

References (163)

1. Friedenstein A. J., Gorskaja U. F., Kulagina N. N., Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Experimental Hematology 1976 4 5 267 274 2-s2.0-0017119380
2. Rastegar F., Shenaq D., Huang J., Mesenchymal stem cells: molecular characteristics and clinical applications. World Journal of Stem Cells 2010 2 4 67 80
3. Steinert A. F., Rackwitz L., Gilbert F., Noth U., Tuan R. S., Concise review: the clinical application of mesenchymal stem cells for musculoskeletal regeneration: current status and perspectives. Stem Cells Translational Medicine 2012 1 3 237 247
4. Otto W. R., Wright N. A., Mesenchymal stem cells: from experiment to clinic. Fibrogenesis and Tissue Repair 2011 4 1, article 20 2-s2.0-80053222316 10.1186/1755-1536-4-20
5. Hass R., Kasper C., Bohm S., Jacobs R., Different populations and sources of human mesenchymal stem cells (MSC): a comparison of adult and neonatal tissue-derived MSC. Cell Communication and Signaling 2011 9, article 12 2-s2.0-79955795428 10.1186/1478-811X-9-12
6. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F. C., Krause D. S., Deans R. J., Keating A., Prockop D. J., Horwitz E. M., Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy pos (Pubitemid 44269669)
7. Kim J., Shin J. M., Jeon Y. J., Chung H. M., Chae J.-I., Proteomic validation of multifunctional molecules in mesenchymal stem cells derived from human bone marrow, umbilical cord blood and peripheral blood. PLoS One 2012 7 5 e32350
8. Hu L., Hu J., Zhao J., Side-by-side comparison of the biological characteristics of human umbilical cord and adipose tissue-derived mesenchymal stem cells. BioMed Research International 2013 2013 12 438243 10.1155/2013/438243
9. Neirinckx V., 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 Translational Medicine 2013 2 4 284 296
10. Wu X. B., Tao R., Hepatocyte differentiation of mesenchymal stem cells. Hepatobiliary & Pancreatic Diseases International 2012 11 4 360 371
11. Bianco P., Barker R., Brüstle O., Regulation of stem cell therapies under attack in Europe: for whom the bell tolls. The EMBO Journal 2013 32 11 1489 1495
12. Bianco P., Cao X., Frenette P. S., The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nature Medicine 2013 19 1 35 42
13. da Silva Meirelles L., Fontes A. M., Covas D. T., Caplan A. I., Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine and Growth Factor Reviews 2009 20 5-6 419 427 2-s2.0-70849103924 10.1016/j.cytogfr.2009.10.002
14. Boomsma R. A., Geenen D. L., Mesenchymal stem cells secrete multiple cytokines that promote angiogenesis and have contrasting effects on chemotaxis and apoptosis. PLoS One 2012 7 4 e35685
15. Doorn J., Moll G., Le Blanc K., van Blitterswijk C., De Boer J., Therapeutic applications of mesenchymal stromal cells: paracrine effects and potential improvements. Tissue Engineering B 2012 18 2 101 115 2-s2.0-84858979623 10.1089/ten.teb.2011.0488
16. Ranganath S. H., Levy O., Inamdar M. S., Karp J. M., Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 2012 10 3 244 258 2-s2.0-84857838864 10.1016/j.stem.2012.02.005
17. English K., Mechanisms of mesenchymal stromal cell immunomodulation. Immunology and Cell Biology 2013 19 1 9119 9126
18. Lavoie J. R., Rosu-Myles M., Uncovering the secretes of mesenchymal stem cells. Biochimie 2013 95 12 2212 2221
19. Lee R. H., Pulin A. A., Seo M. J., Kota D. J., Ylostalo J., Larson B. L., Semprun-Prieto L., Delafontaine P., Prockop D. J., Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009 5 1 54 63 2-s2.0-67649171661 10.1016/j.stem.2009.05.003
20. Shin L., Peterson D. A., Human mesenchymal stem cell grafts enhance normal and impaired wound healing by recruiting existing endogenous tissue stem/progenitor cells. Stem Cells Translational Medicine 2013 2 1 33 42
21. Chen F.-M., Wu L.-A., Zhang M., Zhang R., Sun H.-H., Homing of endogenous stem/progenitor cells for in situ tissue regeneration: promises, strategies, and translational perspectives. Biomaterials 2011 32 12 3189 3209 2-s2.0-79951740978 10.1016/j.biomaterials.2010.12.032
22. Yi T., Song S. U., Immunomodulatory properties of mesenchymal stem cells and their therapeutic applications. Archives of Pharmacal Research 2012 35 2 213 221
23. Galipeau J., The mesenchymal stromal cells dilemma-does a negative phase III trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road? Cytotherapy 2013 15 1 2 8
24. Cencioni C., Capogrossi M. C., Napolitano M., The SDF-1/CXCR4 axis in stem cell preconditioning. Cardiovascular Research 2012 94 3 400 407
25. Wu Y., Zhao R. C. H., The role of chemokines in mesenchymal stem cell homing to myocardium. Stem Cell Reviews and Reports 2012 8 1 243 250 2-s2.0-84857658430 10.1007/s12015-011-9293-z
26. Liu X., Duan B., Cheng Z., Jia X., Mao L., Fu H., Che Y., Ou L., Liu L., Kong D., SDF-1/CXCR4 axis modulates bone marrow mesenchymal stem cell apoptosis, migration and cytokine secretion. Protein and Cell 2011 2 10 845 854 2-s2.0-80955157950 10.1007/s13238-011-1097-z
27. Petit I., Jin D., Rafii S., The SDF-1-CXCR4 signaling pathway: a molecular hub modulating neo-angiogenesis. Trends in Immunology 2007 28 7 299 307 2-s2.0-34250724520 10.1016/j.it.2007.05.007 (Pubitemid 46963141)
28. Son B.-R., Marquez-Curtis L. A., Kucia M., Wysoczynski M., Turner A. R., Ratajczak J., Ratajczak M. Z., 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 2-s2.0-33749078198 10.1634/stemcells.2005-0271 (Pubitemid 44464694)
29. Honczarenko M., Le Y., Swierkowski M., Ghiran I., Glodek A. M., Silberstein L. E., Human bone marrow stromal cells express a distinct set of biologically functional chemokine receptors. Stem Cells 2006 24 4 1030 1041 2-s2.0-33745489036 10.1634/stemcells.2005-0319 (Pubitemid 44464736)
30. Ren G., Chen X., Dong F., Concise review: mesenchymal stem cells and translational medicine: emerging issues. Stem Cells Translational Medicine 2012 1 1 51 58
31. Frenette P. S., Pinho S., Lucas D., Scheiermann C., Mesenchymal stem cell: keystone of the hematopoietic stem cell niche and a stepping-stone for regenerative medicine. Annual Review of Immunology 2013 31 285 316
32. Prockop D. J., Youn Oh J., Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. Molecular Therapy 2012 20 1 14 20 2-s2.0-84856973179 10.1038/mt.2011.211
33. Kang K. S., Shin I. S., Ko M. S., Jo J. Y., Ra J. C., Journey of mesenchymal stem cells for homing: strategies to enhance efficacy and safety of stem cell therapy. Stem Cells International 2012 2012 11 342968 10.1155/2012/342968
34. Augello A., Kurth T. B., de Bari C., Mesenchymal stem cells: a perspective from in vitro cultures to in vivo migration and niches. European Cells and Materials 2010 20 121 133 2-s2.0-77957133737
35. Méndez-Ferrer S., Michurina T. V., Ferraro F., Mazloom A. R., MacArthur B. D., Lira S. A., Scadden D. T., Mag'Ayan A., Enikolopov G. N., Frenette P. S., Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 2010 466 7308 829 834 2-s2.0-77955646193 10.1038/nature09262
36. Vanden Berg-Foels W. S., In situ tissue regeneration: chemoattractants for endogenous stem cell recruitment. Tissue Engineering B 2013 10.1089/ten.teb.2013.0100
37. Stolzing A., Jones E., McGonagle D., Scutt A., Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies. Mechanisms of Ageing and Development 2008 129 3 163 173 2-s2.0-39149093357 10.1016/j.mad.2007.12.002
38. Gurtner G. C., Werner S., Barrandon Y., Longaker M. T., Wound repair and regeneration. Nature 2008 453 7193 314 321 2-s2.0-43749088730 10.1038/nature07039 (Pubitemid 351693137)
39. Orozco L., Munar A., Soler R., Treatment of knee osteoarthritis with autologous mesenchymal stem cells: a pilot study. Transplantation 2013 95 12 1535 1541
40. Haack-Sorensen M., Friis T., Mathiasen A. B., Direct intramyocardial mesenchymal stromal cell injections in patients with severe refractory angina: one-year follow-up. Cell Transplantation 2013 22 3 521 528
41. Kollar K., Cook M. M., Atkinson K., Brooke G., Molecular mechanisms involved in mesenchymal stem cell migration to the site of acute myocardial infarction. International Journal of Cell Biology 2009 2009 8 904682 10.1155/2009/904682
42. Bernardo M. E., Fibbe W. E., Safety and efficacy of mesenchymal stromal cell therapy in autoimmune disorders. Annals of the New York Academy of Sciences 2012 1266 107 117
43. von Bahr L., Sundberg B., Lönnies L., Sander B., Karbach H., Hägglund H., Ljungman P., Gustafsson B., Karlsson H., Le Blanc K., Ringdén O., Long-term complications, immunologic effects, and role of passage for outcome in mesenchymal stromal cell therapy. Biology of Blood and Marrow Transplantation 2012 18 4 557 564 2-s2.0-84858080480 10.1016/j.bbmt.2011. 07.023
44. Keating A., Mesenchymal stromal cells: new directions. Cell Stem Cell 2012 10 6 709 716
45. Bernardo M. E., Fibbe W. E., Mesenchymal stromal cells: sensors and switchers of inflammation. Cell Stem Cell 2013 13 4 392 402
46. Zheng G. P., Ge M. H., Shu Q., Rojas M., Xu J., Mesenchymal stem cells in the treatment of pediatric diseases. World Journal of Pediatrics 2013 9 3 197 211
47. Eggenhofer E., Benseler V., Kroemer A., Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion. Frontiers in Immunology 2012 3, article 297
48. Toma C., Wagner W. R., Bowry S., Schwartz A., Villanueva F., Fate of culture-expanded mesenchymal stem cells in the microvasculature: in vivo observations of cell kinetics. Circulation Research 2009 104 3 398 402 2-s2.0-61949313815 10.1161/CIRCRESAHA.108.187724
49. Guo Y., Su L., Wu J., Zhang D., Zhang X., Zhang G., Li T., Wang J., Liu C., Assessment of the green florescence protein labeling method for tracking implanted mesenchymal stem cells. Cytotechnology 2012 64 4 391 401 2-s2.0-84857428294 10.1007/s10616-011-9417-y
50. Wood J. A., Chung D. J., Park S. A., Periocular and intra-articular injection of canine adipose-derived mesenchymal stem cells: an in vivo imaging and migration study. Journal of Ocular Pharmacology and Therapeutics 2012 28 3 307 317
51. Cheng K., Rai P., Plagov A., Transplantation of bone marrow-derived MSCs improves cisplatinum-induced renal injury through paracrine mechanisms. Experimental and Molecular Pathology 2013 94 3 466 473
52. Hu C., Yong X., Li C., CXCL12/CXCR4 axis promotes mesenchymal stem cell mobilization to burn wounds and contributes to wound repair. The Journal of Surgical Research 2013 183 1 427 434
53. Horwitz E. M., Gordon P. L., Koo W. K. K., Marx J. C., Neel M. D., McNall R. Y., Muul L., Hofmann T., Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proceedings of the National Academy of Sciences of the United States of America 2002 99 13 8932 8937 2-s2.0-0037173116 10.1073/pnas.132252399 (Pubitemid 34693661)
54. Nagaya N., Fujii T., Iwase T., Ohgushi H., Itoh T., Uematsu M., Yamagishi M., Mori H., Kangawa K., Kitamura S., Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. American Journal of Physiology: Heart and Circulatory Physiology 2004 287 6 H2670 H2676 2-s2.0-9344265225 10.1152/ajpheart.01071.2003 (Pubitemid 39557139)
55. González M. A., González-Rey E., Rico L., Büscher D., Delgado M., Treatment of experimental arthritis by inducing immune tolerance with human adipose-derived mesenchymal stem cells. Arthritis and Rheumatism 2009 60 4 1006 1019 2-s2.0-65249161683 10.1002/art.24405
56. Kanazawa H., Fujimoto Y., Teratani T., Iwasaki J., Kasahara N., Negishi K., Tsuruyama T., Uemoto S., Kobayashi E., Bone marrow-derived mesenchymal stem cells ameliorate hepatic ischemia reperfusion injury in a rat model. PLoS ONE 2011 6 4 2-s2.0-79955706042 10.1371/journal.pone.0019195 e19195
57. Karp J. M., Leng Teo G. S., Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 2009 4 3 206 216 2-s2.0-60849136593 10.1016/j.stem.2009.02.001
58. Crop M. J., Baan C. C., Korevaar S. S., Ijzermans J. N., Pescatori M., Stubbs A. P., van Ijcken W. F., Dahlke M. H., Eggenhofer E., Weimar W., Hoogduijn M. J., Inflammatory conditions affect gene expression and function of human adipose tissue-derived mesenchymal stem cells. Clinical and Experimental Immunology 2010 162 3 474 486 2-s2.0-79952482065
59. Assis A. C. M., Carvalho J. L., Jacoby B. A., Ferreira R. L. B., Castanheira P., Diniz S. O. F., Cardoso V. N., Goes A. M., Ferreira A. J., Time-dependent migration of systemically delivered bone marrow mesenchymal stem cells to the infarcted heart. Cell Transplantation 2010 19 2 219 230 2-s2.0-77951444290 10.3727/096368909X479677
60. Jung S., Panchalingam K. M., Rosenberg L., Behie L. A., Ex vivo expansion of human mesenchymal stem cells in defined serum-free media,. Stem Cells International: 2012 2012 21 123030 10.1155/2012/123030
61. Lee M. W., Kim D. S., Ryu S., Effect of ex vivo culture conditions on immunosuppression by human mesenchymal stem cells. BioMed Research International 2013 2013 10 154919 10.1155/2013/154919
62. Rombouts W. J. C., Ploemacher R. E., Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia 2003 17 1 160 170 2-s2.0-0037269456 10.1038/sj.leu.2402763 (Pubitemid 36175902)
63. Morikawa S., Mabuchi Y., Kubota Y., Nagai Y., Niibe K., Hiratsu E., Suzuki S., Miyauchi-Hara C., Nagoshi N., Sunabori T., Shimmura S., Miyawaki A., Nakagawa T., Suda T., Okano H., Matsuzaki Y., Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. Journal of Experimental Medicine 2009 206 11 2483 2496 2-s2.0-70449701931 10.1084/jem.20091046
64. Li Q., Zhou X., Shi Y., In vivo tracking and comparison of the therapeutic effects of MSCs and HSCs for liver injury. PLoS One 2013 8 4 e62363
65. Song C., Li G., CXCR4 and matrix metalloproteinase-2 are involved in mesenchymal stromal cell homing and engraftment to tumors. Cytotherapy 2011 13 5 549 561 2-s2.0-79954452880 10.3109/14653249.2010.542457
66. Liu L., Eckert M. A., Riazifar H., Kang D.-K., Agalliu D., Zhao W., From blood to the brain: can systemically transplanted mesenchymal stem cells cross the blood-brain barrier? Stem Cells International 2013 2013 7 435093 10.1155/2013/435093
67. Steingen C., Brenig F., Baumgartner L., Schmidt J., Schmidt A., Bloch W., Characterization of key mechanisms in transmigration and invasion of mesenchymal stem cells. Journal of Molecular and Cellular Cardiology 2008 44 6 1072 1084 2-s2.0-44649178243 10.1016/j.yjmcc.2008.03.010
68. Yagi H., Soto-Gutierrez A., Parekkadan B., Kitagawa Y., Tompkins R. G., Kobayashi N., Yarmush M. L., Mesenchymal stem cells: mechanisms of immunomodulation and homing. Cell Transplantation 2010 19 6-7 667 679 2-s2.0-77958572322 10.3727/096368910X508762
69. Chamberlain G., Smith H., Rainger G. E., Middleton J., Mesenchymal stem cells exhibit firm adhesion, crawling, spreading and transmigration across aortic endothelial cells: effects of chemokines and shear. PLoS ONE 2011 6 9 2-s2.0-80053269532 10.1371/journal.pone.0025663 e25663
70. Wang Y., Deng Y., Zhou G.-Q., SDF-1 α /CXCR4-mediated migration of systemically transplanted bone marrow stromal cells towards ischemic brain lesion in a rat model. Brain Research 2008 1195 104 112 2-s2.0-39149131038 10.1016/j.brainres.2007.11.068
71. Dong F., Harvey J., Finan A., Weber K., Agarwal U., Penn M. S., Myocardial CXCR4 expression is required for mesenchymal stem cell mediated repair following acute myocardial infarction. Circulation 2012 126 3 314 324
72. Rice C. M., Scolding N. J., Adult human mesenchymal cells proliferate and migrate in response to chemokines expressed in demyelination. Cell Adhesion and Migration 2010 4 2 235 240 2-s2.0-77953594323 10.4161/cam.4.2.11404
73. Akram K. M., Samad S., Spiteri M. A., Forsyth N. R., Mesenchymal stem cells promote alveolar epithelial cell wound repair in vitro through distinct migratory and paracrine mechanisms. Respiratory Research 2013 14, article 9
74. Joyce N. C., Harris D. L., Markov V., Zhang Z., Saitta B., Potential of human umbilical cord blood mesenchymal stem cells to heal damaged corneal endothelium. Molecular Vision 2012 18 547 564 2-s2.0-84859054130
75. Manuguerra-Gagne R., Boulos P. R., Ammar A., Transplantation of mesenchymal stem cells promotes tissue regeneration in a glaucoma model through laser-induced paracrine factor secretion and progenitor cell recruitment. Stem Cells 2013 31 6 1136 1148
76. Wise A. F., Ricardo S. D., Mesenchymal stem cells in kidney inflammation and repair. Nephrology 2012 17 1 1 10 2-s2.0-84855161399 10.1111/j.1440-1797. 2011.01501.x
77. Stagg J., Galipeau J., Mechanisms of immune modulation by mesenchymal stromal cells and clinical translation. Current Molecular Medicine 2013 13 5 856 867
78. Smith H., Whittall C., Weksler B., Middleton J., Chemokines stimulate bidirectional migration of human mesenchymal stem cells across bone marrow endothelial cells. Stem Cells and Development 2012 21 3 476 486 2-s2.0-84856745103 10.1089/scd.2011.0025
79. Alexeev V., Donahue A., Uitto J., Igoucheva O., Analysis of chemotactic molecules in bone marrow-derived mesenchymal stem cells and the skin: Ccl27-Ccr10 axis as a basis for targeting to cutaneous tissues. Cytotherapy 2013 15 2 171.e1 184.e1
80. Lee M. W., Kim D. S., Yoo K. H., Human bone marrow-derived mesenchymal stem cell gene expression patterns vary with culture conditions. Blood Research 2013 48 2 107 114
81. 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 2-s2.0-44349088779 10.1016/j.stem.2008.03.003 (Pubitemid 351729213)
82. Kim D.-S., Kim J. H., Kwon Lee J., Choi S. J., Kim J.-S., Jeun S.-S., Oh W., Yang Y. S., Chang J. W., Overexpression of CXC chemokine receptors is required for the superior glioma-tracking property of umbilical cord blood-derived mesenchymal stem cells. Stem Cells and Development 2009 18 3 511 519 2-s2.0-65349149983 10.1089/scd.2008.0050
83. Sordi V., Malosio M. L., Marchesi F., Mercalli A., Melzi R., Giordano T., Belmonte N., Ferrari G., Leone B. E., Bertuzzi F., Zerbini G., Allavena P., Bonifacio E., Piemonti L., Bone marrow mesenchymal stem cells express a restricted set of functionally active chemokine receptors capable of promoting migration to pancreatic islets. Blood 2005 106 2 419 427 2-s2.0-22144491551 10.1182/blood-2004-09-3507 (Pubitemid 40981232)
84. Huang J., Zhang Z., Guo J., Ni A., Deb A., Zhang L., Mirotsou M., Pratt R. E., Dzau V. J., Genetic modification of mesenchymal stem cells overexpressing ccr1 increases cell viability, migration, engraftment, and capillary density in the injured myocardium. Circulation Research 2010 106 11 1753 1762 2-s2.0-77953812469 10.1161/CIRCRESAHA.109.196030
85. Vogel S., Peters C., Etminan N., Migration of mesenchymal stem cells towards glioblastoma cells depends on hepatocyte-growth factor and is enhanced by aminolaevulinic acid-mediated photodynamic treatment. Biochemical and Biophysical Research Communications 2013 431 3 428 432
86. van de Kamp J., Jahnen-Dechent W., Rath B., Knuechel R., Neuss S., Hepatocyte growth factor-loaded biomaterials for mesenchymal stem cell recruitment. Stem Cells International 2013 2013 9 892065 10.1155/2013/892065
87. Herrera M. B., Bussolati B., Bruno S., Morando L., Mauriello-Romanazzi G., Sanavio F., Stamenkovic I., Biancone L., Camussi G., Exogenous mesenchymal stem cells localize to the kidney by means of CD44 following acute tubular injury. Kidney International 2007 72 4 430 441 2-s2.0-34547763362 10.1038/sj.ki.5002334 (Pubitemid 47237610)
88. Kim C., Schneider G., Abdel-Latif A., Ceramide-1-phosphate regulates migration of multipotent stromal cells and endothelial progenitor cells-implications for tissue regeneration. Stem Cells 2013 31 3 500 510
89. Gasque P., Complement: a unique innate immune sensor for danger signals. Molecular Immunology 2004 41 11 1089 1098 2-s2.0-5144222255 10.1016/j.molimm. 2004.06.011 (Pubitemid 39345390)
90. Schraufstatter I. U., DiScipio R. G., Zhao M., Khaldoyanidi S. K., C3a and C5a are chemotactic factors for human mesenchymal stem cells, which cause prolonged ERK1/2 phosphorylation. Journal of Immunology 2009 182 6 3827 3836 2-s2.0-65449147900 10.4049/jimmunol.0803055
91. Qiu Y., Marquez-Curtis L. A., Janowska-Wieczorek A., Mesenchymal stromal cells derived from umbilical cord blood migrate in response to complement C1q. Cytotherapy 2012 14 3 285 295 2-s2.0-84856928657 10.3109/14653249.2011.651532
92. Baglio S. R., Pegtel D. M., Baldini N., Mesenchymal stem cell secreted vesicles provide novel opportunities in (stem) cell-free therapy. Frontiers in Physiology 2012 3, article 359 10.3389/fphys.2012.00359
93. Ratajczak M. Z., Kucia M., Jadczyk T., Greco N. J., Wojakowski W., Tendera M., Ratajczak J., Pivotal role of paracrine effects in stem cell therapies in regenerative medicine-can we translate stem cell-secreted paracrine factors and microvesicles into better therapeutic strategies? Leukemia 2012 26 6 1166 1173 2-s2.0-83455164878 10.1038/leu.2011.389
94. Kim H.-S., Choi D.-Y., Yun S. J., Choi S.-M., Kang J. W., Jung J. W., Hwang D., Kim K. P., Kim D.-W., Proteomic analysis of microvesicles derived from human mesenchymal stem cells. Journal of Proteome Research 2012 11 2 839 849 2-s2.0-84856638286 10.1021/pr200682z
95. Ghadge S. K., Mühlstedt S., Özcelik C., Bader M., SDF-1 α as a therapeutic stem cell homing factor in myocardial infarction. Pharmacology and Therapeutics 2011 129 1 97 108 2-s2.0-78650514210 10.1016/j.pharmthera. 2010.09.011
96. Penn M. S., Pastore J., Miller T., Aras R., SDF-1 in myocardial repair. Gene Therapy 2012 19 6 583 587
97. Yu J., Li M., Qu Z., Yan D., Li D., Ruan Q., SDF-1/CXCR4-mediated migration of transplanted bone marrow stromal cells toward areas of heart myocardial infarction through activation of PI3K/Akt. Journal of Cardiovascular Pharmacology 2010 55 5 496 505 2-s2.0-77953016267 10.1097/FJC.0b013e3181d7a384
98. Liu N., Tian J., Cheng J., Zhang J., Directional migration of CXCR4 gene-modified bone marrow-derived mesenchymal stem cells to the kidney area after acute kidney injury. Journal of Cellular Biochemistry 114 12 2677 2268
99. Stich S., Haag M., Häupl T., Sezer O., Notter M., Kaps C., Sittinger M., Ringe J., Gene expression profiling of human mesenchymal stem cells chemotactically induced with CXCL12. Cell and Tissue Research 2009 336 2 225 236 2-s2.0-67349136795 10.1007/s00441-009-0768-z
100. Kitaori T., Ito H., Schwarz E. M., Tsutsumi R., Yoshitomi H., Oishi S., Nakano M., Fujii N., Nagasawa T., Nakamura T., Stromal cell-derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model. Arthritis and Rheumatism 2009 60 3 813 823 2-s2.0-61649090805 10.1002/art.24330
101. Burns J. M., Summers B. C., Wang Y., Melikian A., Berahovich R., Miao Z., Penfold M. E. T., Sunshine M. J., Littman D. R., Kuo C. J., Wei K., McMaster B. E., Wright K., Howard M. C., Schall T. J., A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival, cell adhesion, and tumor development. Journal of Experimental Medicine 2006 203 9 2201 2213 2-s2.0-33748474838 10.1084/jem.20052144 (Pubitemid 44352240)
102. Liu H., Liu S., Li Y., 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
103. Zabel B. A., Wang Y., Lewén S., Berahovich R. D., Penfold M. E. T., Zhang P., Powers J., Summers B. C., Miao Z., Zhao B., Jalili A., Janowska-Wieczorek A., Jaen J. C., Schall T. J., Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. Journal of Immunology 2009 183 5 3204 3211 2-s2.0-70349234110 10.4049/jimmunol.0900269
104. Liu N., Patzak A., Zhang J., CXCR4-overexpressing bone marrow-derived mesenchymal stem cells improve repair of acute kidney injury. American Journal of Physiology: Renal Physiology 2013 305 7 F1064 F1073 10.1152/ajprenal.00178. 2013
105. Gheisari Y., Azadmanesh K., Ahmadbeigi N., Genetic modification of mesenchymal stem cells to overexpress CXCR4 and CXCR7 does not improve the homing and therapeutic potentials of these cells in experimental acute kidney injury. Stem Cells and Development 2012 21 16 2969 2980
106. Cao J., Wang L., Du Z.-J., Recruitment of exogenous mesenchymal stem cells in mandibular distraction osteogenesis by the stromal cell-derived factor-1/chemokine receptor-4 pathway in rats. British Journal of Oral and Maxillofacial Surgery 2013 10.1016/j.bjoms.2013.05.003
107. Yu X., Chen D., Zhang Y., Wu X., Huang Z., Zhou H., Zhang Y., Zhang Z., Overexpression of CXCR4 in mesenchymal stem cells promotes migration, neuroprotection and angiogenesis in a rat model of stroke. Journal of the Neurological Sciences 2012 316 1-2 141 149 2-s2.0-84859444967 10.1016/j.jns.2012.01.001
108. Wynn R. F., Hart C. A., Corradi-Perini C., O'Neill L., Evans C. A., Wraith J. E., Fairbairn L. J., Bellantuono I., A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow. Blood 2004 104 9 2643 2645 2-s2.0-7244224904 10.1182/blood-2004-02-0526 (Pubitemid 39434942)
109. Maijenburg M. W., van der Schoot C. E., Voermans C., Mesenchymal stromal cell migration: possibilities to improve cellular therapy. Stem Cells and Development 2012 21 1 19 29 2-s2.0-84855457616 10.1089/scd.2011.0270
110. Thomas Kean J., Paul Lin, Arnold Caplan I., James Dennis E., MSCs: delivery routes and engraftment, cell-targeting strategies, and immune modulation. Stem Cells International 2013 2013 13 732742 10.1155/2013/732742
111. Sarkar D., Spencer J. A., Phillips J. A., Zhao W., Schafer S., Spelke D. P., Mortensen L. J., Ruiz J. P., Vemula P. K., Sridharan R., Kumar S., Karnik R., Lin C. P., Karp J. M., Engineered cell homing. Blood 2011 118 25 e184 e191 2-s2.0-84055223060 10.1182/blood-2010-10-311464
112. Ko I. K., Kim B.-G., Awadallah A., Mikulan J., Lin P., Letterio J. J., Dennis J. E., Targeting improves MSC treatment of inflammatory bowel disease. Molecular Therapy 2010 18 7 1365 1372 2-s2.0-77954242073 10.1038/mt.2010.54
113. Levy O., Zhao W., Mortensen L. J., mRNA-engineered mesenchymal stem cells for targeted delivery of interleukin-10 to sites of inflammation. Blood 2013 122 14 e23 e32
114. Yao W., Guan M., Jia J., Reversing Bone Loss by Directing Mesenchymal Stem Cells to the Bone. Stem Cells 2013 31 9 2003 2014 10.1002/stem.1461
115. Xinaris C., Morigi M., Benedetti V., A novel strategy to enhance mesenchymal stem cell migration capacity and promote tissue repair in an injury specific fashion. Cell Transplantion 2013 22 3 423 436
116. Hahn J.-Y., Cho H.-J., Kang H.-J., Kim T.-S., Kim M.-H., Chung J.-H., Bae J.-W., Oh B.-H., Park Y.-B., Kim H.-S., Pre-treatment of mesenchymal stem cells with a combination of growth factors enhances gap junction formation, cytoprotective effect on cardiomyocytes, and therapeutic efficacy for myocardial infarction. Journal of the American College of Cardiology 2008 51 9 933 943 2-s2.0-39549105786 10.1016/j.jacc.2007.11.040 (Pubitemid 351282455)
117. Jones G. N., Moschidou D., Lay K., pregulating CXCR4 in human fetal mesenchymal stem cells enhances engraftment and bone mechanics in a mouse model of osteogenesis imperfecta. Stem Cells Translational Medicine 2012 1 1 70 78
118. Kim Y. S., Noh M. Y., Kim J. Y., Direct GSK-3beta inhibition enhances mesenchymal stromal cell migration by increasing expression of beta-PIX and CXCR4. Molecular Neurobiology 2013 47 2 811 820
119. Yu Q., Chen L., You Y., Zou C., Zhang Y., Liu Q., Cheng F., Erythropoietin combined with granulocyte colony-stimulating factor enhances MMP-2 expression in mesenchymal stem cells and promotes cell migration. Molecular Medicine Reports 2011 4 1 31 36 2-s2.0-78651383672 10.3892/mmr.2010.387
120. Noiseux N., Borie M., Desnoyers A., Preconditioning of stem cells by oxytocin to improve their therapeutic potential. Endocrinology 2012 153 11 5361 5372
121. Xie J., Wang H., Song T., Tanshinone IIA and astragaloside IV promote the migration of mesenchymal stem cells by up-regulation of CXCR4. Protoplasma 2013 250 2 521 530
122. Gul H., Marquez-Curtis L. A., Jahroudi N., Lo J., Turner A. R., Janowska-Wieczorek A., Valproic acid increases CXCR4 expression in hematopoietic stem/progenitor cells by chromatin remodeling. Stem Cells and Development 2009 18 6 831 838 2-s2.0-67651119931 10.1089/scd.2008.0235
123. Liu L., Yu Q., Lin J., Lai X., Cao W., Du K., Wang Y., Wu K., Hu Y., Zhang L., Xiao H., Duan Y., Huang H., Hypoxia-inducible factor-1 α is essential for hypoxia-induced mesenchymal stem cell mobilization into the peripheral blood. Stem cells and development 2011 20 11 1961 1971 2-s2.0-80053604985
124. Vertelov G., Kharazi L., Muralidhar M. G., Sanati G., Tankovich T., Kharazi A., High targeted migration of human mesenchymal stem cells grown in hypoxia is associated with enhanced activation of RhoA. Stem Cell Research & Therapy 2013 4 1: article 5
125. Zhao Z., Watt C., Karystinou A., Roelofs A. J., McCaig C. D., Gibson I. R., De Bari C., Directed migration of human bone marrow mesenchymal stem cells in a physiological direct current electric field. European Cells & Materials 2011 22 344 358 2-s2.0-84857955548
126. Burks S. R., Ziadloo A., Kim S. J., Nguyen B. A., Frank J. A., Noninvasive pulsed focused ultrasound allows spatiotemporal control of targeted homing for multiple stem cell types in murine skeletal muscle and the magnitude of cell homing can be increased through repeated applications. Stem Cells 2013 31 11 2551 2560 10.1002/stem.1495
127. Yuan L., Sakamoto N., Song G., Sato M., Low-level shear stress induces human mesenchymal stem cell migration through the SDF-1/CXCR4 axis via MAPK signaling pathways. Stem Cells and Development 2013 22 17 2384 2393 10.1089/scd.2012.0717
128. Zhou S. B., Wang J., Chiang C. A., Sheng L. L., Li Q. F., Mechanical stretch upregulates Sdf-1alpha in skin tissue and induces migration of circulating bone marrow-derived stem cells into the expanded skin. Stem Cells 2013 10.1002/stem.1479
129. Zhang D., Fan G.-C., Zhou X., Zhao T., Pasha Z., Xu M., Zhu Y., Ashraf M., Wang Y., Over-expression of CXCR4 on mesenchymal stem cells augments myoangiogenesis in the infarcted myocardium. Journal of Molecular and Cellular Cardiology 2008 44 2 281 292 2-s2.0-39149089319 10.1016/j.yjmcc.2007.11.010
130. Cheng Z., Ou L., Zhou X., Li F., Jia X., Zhang Y., Liu X., Li Y., Ward C. A., Melo L. G., Kong D., Targeted migration of mesenchymal stem cells modified with CXCR4 gene to infarcted myocardium improves cardiac performance. Molecular Therapy 2008 16 3 571 579 2-s2.0-39849097361 10.1038/sj.mt.6300374 (Pubitemid 351314998)
131. Bobis-Wozowicz S., Miekus K., Wybieralska E., Jarocha D., Zawisz A., Madeja Z., Majka M., Genetically modified adipose tissue-derived mesenchymal stem cells overexpressing CXCR4 display increased motility, invasiveness, and homing to bone marrow of NOD/SCID mice. Experimental Hematology 2011 39 6 686 e4 2-s2.0-79956279508 10.1016/j.exphem.2011.03.004
132. Wiehe J. M., Kaya Z., Homann J. M., GMP-adapted overexpression of CXCR4 in human mesenchymal stem cells for cardiac repair. International Journal of Cardiology 2012 167 5 2073 2081 10.1016/j.ijcard.2012.05.065
133. Da Silva C. L., Madeira C., Mendes R. D., Ribeiro S. C., Boura J. S., Aires-Barros M. R., Cabral J. M. S., Nonviral gene delivery to mesenchymal stem cells using cationic liposomes for gene and cell therapy. Journal of Biomedicine and Biotechnology 2010 2010 12 2-s2.0-77955411071 10.1155/2010/735349 735349
134. Gul-Uludag H., Xu P., Marquez-Curtis L. A., Xing J., Janowska-Wieczorek A., Chen J., Cationic liposome-mediated CXCR4 gene delivery into hematopoietic stem/progenitor cells: implications for clinical transplantation and gene therapy. Stem Cells and Development 2012 2 10 1587 1596
135. Marquez-Curtis L. A., Gul-Uludag H., Xu P., Chen J., Janowska-Wieczorek A., CXCR4 transfection of cord blood mesenchymal stromal cells with the use of cationic liposome enhances their migration toward stromal cell-derived factor-1. Cytotherapy 2013 15 7 840 849
136. Murphy J. W., Cho Y., Sachpatzidis A., Fan C., Hodsdon M. E., Lolis E., Structural and functional basis of CXCL12 (stromal cell-derived factor-1 α) binding to heparin. The Journal of Biological Chemistry 2007 282 13 10018 10027 2-s2.0-34248168879 10.1074/jbc.M608796200 (Pubitemid 47104591)
137. Ma J., Ge J., Zhang S., Sun A., Shen J., Chen L., Wang K., Zou Y., Time course of myocardial stromal cell-derived factor 1 expression and beneficial effects of intravenously administered bone marrow stem cells in rats with experimental myocardial infarction. Basic Research in Cardiology 2005 100 3 217 223 2-s2.0-25144491290 10.1007/s00395-005-0521-z (Pubitemid 41348812)
138. Segers V. F. M., Tokunou T., Higgins L. J., MacGillivray C., Gannon J., Lee R. T., Local delivery of protease-resistant stromal cell derived factor-1 for stem cell recruitment after myocardial infarction. Circulation 2007 116 15 1683 1692 2-s2.0-35148820656 10.1161/CIRCULATIONAHA.107.718718 (Pubitemid 47537842)
139. Christopherson K. W. II, Hangoc G., Broxmeyer H. E., Cell surface peptidase CD26/dipeptidylpeptidase IV regulates CXCL12/stromal cell-derived factor-1 α -mediated chemotaxis of human cord blood CD34+ progenitor cells. Journal of Immunology 2002 169 12 7000 7008 2-s2.0-0037114177 (Pubitemid 36899288)
140. Sadir R., Imberty A., Baleux F., Lortat-Jacob H., Heparan sulfate/heparin oligosaccharides protect stromal cell-derived factor-1 (SDF-1)/CXCL12 against proteolysis induced by CD26/dipeptidyl peptidase IV. The Journal of Biological Chemistry 2004 279 42 43854 43860 2-s2.0-6344284808 10.1074/jbc.M405392200 (Pubitemid 39390692)
141. McQuibban G. A., Butler G. S., Gong J.-H., Bendall L., Power C., Clark-Lewis I., Overall C. M., Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived Factor-1. The Journal of Biological Chemistry 2001 276 47 43503 43508 2-s2.0-0035941359 10.1074/jbc.M107736200
142. Tsai L.-K., Leng Y., Wang Z., Leeds P., Chuang D.-M., The mood stabilizers valproic acid and lithium enhance mesenchymal stem cell migration via distinct mechanisms. Neuropsychopharmacology 2010 35 11 2225 2237 2-s2.0-78651280399 10.1038/npp.2010.97
143. Zhang Y., Foudi A., Geay J.-F., Berthebaud M., Buet D., Jarrier P., Jalil A., Vainchenker W., Louache F., Intracellular localization and constitutive endocytosis of CXCR4 in human CD34+ hematopoietic progenitor cells. Stem Cells 2004 22 6 1015 1029 2-s2.0-8644249116 (Pubitemid 39507088)
144. Levoye A., Balabanian K., Baleux F., Bachelerie F., Lagane B., CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 2009 113 24 6085 6093 2-s2.0-67650349084 10.1182/blood-2008-12-196618
145. Tondreau T., Meuleman N., Stamatopoulos B., De Bruyn C., Delforge A., Dejeneffe M., Martiat P., Bron D., Lagneaux L., In vitro study of matrix metalloproteinase/tissue inhibitor of metalloproteinase production by mesenchymal stromal cells in response to inflammatory cytokines: the role of their migration in injured tissues. Cytotherapy 2009 11 5 559 569 2-s2.0-70849093289 10.1080/14653240903051541
146. De Becker A., van Hummelen P., Bakkus M., Broek I. V., 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 2-s2.0-34547650992 10.3324/haematol.10475 (Pubitemid 350144289)
147. Tsai L.-K., Wang Z., Munasinghe J., Leng Y., Leeds P., Chuang D.-M., 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 2-s2.0-80053309997 10.1161/STROKEAHA.110.612788
148. Lu J., Teh B. K., Wang L., Wang Y., Tan Y. S., Lai M. C., Reid K. B. M., The classical and regulatory functions of C1q in immunity and autoimmunity. Cellular and Molecular Immunology 2008 5 1 9 21 2-s2.0-47049116653 10.1038/cmi.2008.2
149. Jalili A., Marquez-Curtis L., Shirvaikar N., Wysoczynski M., Ratajczak M., Janowska-Wieczorek A., Complement C1q enhances homing-related responses of hematopoietic stem/progenitor cells. Transfusion 2010 50 9 2002 2010 2-s2.0-77956313117 10.1111/j.1537-2995.2010.02664.x
150. Hung S.-C., Pochampally R. R., Hsu S.-C., Sanchez C. C., Chen S.-C., Spees J., Prockop D. J., Short-term exposure of multipotent stromal cells to low oxygen increases their expression of CX3CR1 and CXCR4 and their engraftment in vivo. PLoS ONE 2007 2 5, article e416 2-s2.0-34548739439 10.1371/journal.pone. 0000416
151. Li L., Jiang J., Regulatory factors of mesenchymal stem cell migration into injured tissues and their signal transduction mechanisms. Frontiers of Medicine in China 2011 5 1 33 39 2-s2.0-80055078628 10.1007/s11684-011-0114-1
152. Chen J., Crawford R., Chen C., Xiao Y., The key regulatory roles of the PI3K/Akt signaling pathway in the functionalities of mesenchymal stem cells and applications in tissue regeneration. Tissue Engineering B 2013 19 6 516 528 10.1089/ten.TEB.2012.0672
153. Liu H., Xue W., Ge G., Luo X., Li Y., Xiang H., Ding X., Tian P., Tian X., Hypoxic preconditioning advances CXCR4 and CXCR7 expression by activating HIF-1 α in MSCs. Biochemical and Biophysical Research Communications 2010 401 4 509 515 2-s2.0-77958480787 10.1016/j.bbrc.2010.09.076
154. Ryu C. H., Park S. A., Kim S. M., Lim J. Y., Jeong C. H., Jun J. A., Oh J. H., Park S. H., Oh W.-I., Jeun S.-S., 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. Biochemical and Biophysical Research Communications 2010 398 1 105 110 2-s2.0-77954763320 10.1016/j.bbrc.2010.06.043
155. Lin M. N., Shang D. S., Sun W., Involvement of PI3K and ROCK signaling pathways in migration of bone marrow-derived mesenchymal stem cells through human brain microvascular endothelial cell monolayers. Brain Research 2013 1513 1 8 10.1016/j.brainres.2013.03.035
156. Bulj Z., Duchi S., Bevilacqua A., Protein kinase B/AKT isoform 2 drives migration of human mesenchymal stem cells. International Journal of Oncology 2013 42 1 118 126
157. Xie J., Wang W., Si J. W., Notch signaling regulates CXCR4 expression and the migration of mesenchymal stem cells. Cellular Immunology 2013 281 1 68 75
158. Krampera M., Galipeau J., Shi Y., Tarte K., Sensebe L., MSC Committee of the International Society for Cellular Therapy (ISCT), Immunological characterization of multipotent mesenchymal stromal cells-the international society for cellular therapy (ISCT) working proposal. Cytotherapy 2013 15 9 1054 1061
159. Dimarino A. M., Caplan A. I., Bonfield T. L., Mesenchymal stem cells in tissue repair. Frontiers in Immunology 2013 4, article 201
160. Lalu M. M., McIntyre L., Pugliese C., Safety of cell therapy with mesenchymal stromal cells (SafeCell): a systematic review and meta-analysis of clinical trials. PLoS One 2012 7 10 e47559
161. Wang Y., Han Z.-b., Song Y.-p., Han Z. C., Safety of mesenchymal stem cells for clinical application. Stem Cells International 2012 2012 4 652034 10.1155/2012/652034
162. von Bahr L., Batsis I., Moll G., Analysis of tissues following mesenchymal stromal cell therapy in humans indicates limited long-term engraftment and no ectopic tissue formation. Stem Cells 2012 30 7 1575 1578
163. François M., Copland I. B., Yuan S., Romieu-Mourez R., Waller E. K., Galipeau J., Cryopreserved mesenchymal stromal cells display impaired immunosuppressive properties as a result of heat-shock response and impaired interferon- γ licensing. Cytotherapy 2012 14 2 147 152 2-s2.0-84855890176 10.3109/14653249.2011.623691