Traumatic brain injury: Mesenchymal stem cells regulate blood-brain barrier integrity through TIMP3 release after traumatic brain injury

Science Translational Medicine

Volumn 4, Issue 161, 2012, Pages

  Menge, Tyler ^a   Zhao, Yuhai ^b   Zhao, Jing ^b   Wataha, Kathryn ^a   Gerber, Michael ^b   Zhang, Jianhu ^c   Letourneau, Phillip ^b   Redell, John ^b   Shen, Li ^c   Wang, Jing ^c   Peng, Zhalong ^b   Xue, Hasen ^b   Kozar, Rosemary ^b   Cox, Charles S ^b   Khakoo, Aarif Y ^d   Holcomb, John B ^b   Dash, Pramod K ^b   Pati, Shibani ^a,e  

^a BLOOD SYSTEMS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d AMGEN INC   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; ENZYME INHIBITOR; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; RECOMBINANT ENZYME; RECOMBINANT TISSUE INHIBITOR OF METALLOPROTEINASE 3; SMALL INTERFERING RNA; TISSUE INHIBITOR OF METALLOPROTEINASE 3; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 2;

ADHERENT CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CORTEX; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; CELL SELECTION; CELL SEPARATION; COCULTURE; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME SYNTHESIS; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIVER; LUNG; MESENCHYMAL STEM CELL; MICROARRAY ANALYSIS; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; SPLEEN; TRAUMATIC BRAIN INJURY; WESTERN BLOTTING;

EID: 84869749821     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3004660     Document Type: Article

References (27)

1. M. A. Matthay, A. Goolaerts, J. P. Howard, J. W. Lee, Mesenchymal stem cells for acute lung injury: Preclinical evidence. Crit. Care Med. 38, S569-S573 (2010).
2. S. Pati, M. H. Gerber, T. D. Menge, K. A. Wataha, Y. Zhao, J. A. Baumgartner, J. Zhao, P. A. Letourneau, M. P. Huby, L. A. Baer, J. R. Salsbury, R. A. Kozar, C. E. Wade, P. A. Walker, P. K. Dash, C. S. Cox Jr., M. F. Doursout, J. B. Holcomb, Bone marrow derived mesenchymal stem cells inhibit inflammation and preserve vascular endothelial integrity in the lungs after hemorrhagic shock. PLoS One 6, e25171 (2011).
3. S. Pati, A. Y. Khakoo, J. Zhao, F. Jimenez, M. H. Gerber, M. Harting, J. B. Redell, R. Grill, Y. Matsuo, S. Guha, C. S. Cox, M. S. Reitz, J. B. Holcomb, P. K. Dash, Human mesenchymal stem cells inhibit vascular permeability by modulating vascular endothelial cadherin/b-catenin signaling. Stem Cells Dev. 20, 89-101 (2011).
4. S. C. Picinich, P. J. Mishra, J. Glod, D. Banerjee, The therapeutic potential of mesenchymal stem cells. Cell- & tissue-based therapy. Expert Opin. Biol. Ther. 7, 965-973 (2007).
5. U. M. Fischer, M. T. Harting, F. Jimenez, W. O. Monzon-Posadas, H. Xue, S. I. Savitz, G. A. Laine, C. S. Cox Jr., Pulmonary passage is a major obstacle for intravenous stem cell delivery: The pulmonary first-pass effect. Stem Cells Dev. 18, 683-692 (2009).
6. A. Y. Khakoo, S. Pati, S. A. Anderson, W. Reid, M. F. Elshal, I. I. Rovira, A. T. Nguyen, D. Malide, C. A. Combs, G. Hall, J. Zhang, M. Raffeld, T. B. Rogers, W. Stetler-Stevenson, J. A. Frank, M. Reitz, T. Finkel, Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J. Exp. Med. 203, 1235-1247 (2006).
7. R. A. Black, TIMP3 checks inflammation. Nat. Genet. 36, 934-935 (2004).
8. S. E. Gill, I. Huizar, E. M. Bench, S. W. Sussman, Y. Wang, R. Khokha, W. C. Parks, Tissue inhibitor of metalloproteinases 3 regulates resolution of inflammation following acute lung injury. Am. J. Pathol. 176, 64-73 (2010).
9. N. S. Kishnani, P. W. Staskus, T. T. Yang, F. R. Masiarz, S. P. Hawkes, Identification and characterization of human tissue inhibitor of metalloproteinase-3 and detection of three additional metalloproteinase inhibitor activities in extracellular matrix. Matrix Biol. 14, 479-488 (1995).
10. H. I. Kwak, E. A. Mendoza, K. J. Bayless, ADAM17 co-purifies with TIMP-3 and modulates endothelial invasion responses in three-dimensional collagen matrices. Matrix Biol. 28, 470-479 (2009).
11. A. Amour, P. M. Slocombe, A. Webster, M. Butler, C. G. Knight, B. J. Smith, P. E. Stephens, C. Shelley, M. Hutton, V. Knäuper, A. J. Docherty, G. Murphy, TNF-a converting enzyme (TACE) is inhibited by TIMP-3. FEBS Lett. 435, 39-44 (1998).
12. J. H. Qi, Q. Ebrahem, N. Moore, G. Murphy, L. Claesson-Welsh, M. Bond, A. Baker, B. Anand-Apte, A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): Inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat. Med. 9, 407-415 (2003).
13. R. H. Lee, A. A. Pulin, M. J. Seo, D. J. Kota, J. Ylostalo, B. L. Larson, L. Semprun-Prieto, P. Delafontaine, D. J. Prockop, 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 5, 54-63 (2009).
14. A. Marmarou, A review of progress in understanding the pathophysiology and treatment of brain edema. Neurosurg. Focus 22, E1 (2007).
15. S. M. Weis, D. A. Cheresh, Pathophysiological consequences of VEGF-induced vascular permeability. Nature 437, 497-504 (2005).
16. J. Koyama, S. Miyake, T. Sasayama, T. Kondoh, E. Kohmura, Effect of VEGF receptor antagonist (VGA1155) on brain edema in the rat cold injury model. Kobe J. Med. Sci. 53, 199-207 (2007).
17. M. Garofalo, G. Di Leva, G. Romano, G. Nuovo, S. S. Suh, A. Ngankeu, C. Taccioli, F. Pichiorri, H. Alder, P. Secchiero, P. Gasparini, A. Gonelli, S. Costinean, M. Acunzo, G. Condorelli, C. M. Croce, miR-221&222 regulate TRAIL resistance and enhance tumorigenicity through PTEN and TIMP3 downregulation. Cancer Cell 16, 498-509 (2009).
18. J. B. Redell, Y. Liu, P. K. Dash, Traumatic brain injury alters expression of hippocampal microRNAs: Potential regulators of multiple pathophysiological processes. J. Neurosci. Res. 87, 1435-1448 (2009).
19. J. K. Lee, J. H. Shin, J. Suh, I. S. Choi, K. S. Ryu, B. J. Gwag, Tissue inhibitor ofmetalloproteinases-3 (TIMP-3) expression is increased during serum deprivation-induced neuronal apoptosis in vitro and in the G93A mouse model of amyotrophic lateral sclerosis: A potential modulator of Fas-mediated apoptosis. Neurobiol. Dis. 30, 174-185 (2008).
20. I. Kaur, S. Rathi, S. Chakrabarti, Variations in TIMP3 are associated with age-related macular degeneration. Proc. Natl. Acad. Sci. U.S.A. 107, E112-E113 (2010).
21. S. G. Jacobson, A. V. Cideciyan, J. Bennett, R. M. Kingsley, V. C. Sheffield, E. M. Stone, Novel mutation in the TIMP3 gene causes Sorsby fundus dystrophy. Arch. Ophthalmol. 120, 376-379 (2002).
22. G. J. Block, S. Ohkouchi, F. Fung, J. Frenkel, C. Gregory, R. Pochampally, G. DiMattia, D. E. Sullivan, D. J. Prockop, Multipotent stromal cells are activated to reduce apoptosis in part by upregulation and secretion of stanniocalcin-1. Stem Cells 27, 670-681 (2009).
23. X. Fang, A. P. Neyrinck, M. A. Matthay, J. W. Lee, Allogeneic human mesenchymal stem cells restore epithelial protein permeability in cultured human alveolar type II cells by secretion of angiopoietin-1. J. Biol. Chem. 285, 26211-26222 (2010).
24. C. E. Dixon, G. L. Clifton, J. W. Lighthall, A. A. Yaghmai, R. L. Hayes, A controlled cortical impact model of traumatic brain injury in the rat. J. Neurosci. Methods 39, 253-262 (1991).
25. J. Zhao, S. Pati, J. B. Redell, M. Zhang, A. N. Moore, P. K. Dash, Caffeic acid phenethyl ester protects blood-brain barrier integrity and reduces contusion volume in rodent models of traumatic brain injury. J. Neurotrauma 29, 1209-1218 (2012).
26. R. A. Irizarry, B. M. Bolstad, F. Collin, L. M. Cope, B. Hobbs, T. P. Speed, Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15 (2003).
27. S. Pounds, S. W. Morris, Estimating the occurrence of false positives and false negatives in microarray studies by approximating and partitioning the empirical distribution of p-values. Bioinformatics 19, 1236-1242 (2003).