Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice

Journal of Immunology

Volumn 179, Issue 3, 2007, Pages 1855-1863

  Gupta, Naveen ^a   Su, Xiao ^a   Popov, Boris ^b   Jae, Woo Lee ^a   Serikov, Vladimir ^b   Matthay, Michael A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTOXIN; INTERLEUKIN 10; MACROPHAGE INFLAMMATORY PROTEIN 2; TUMOR NECROSIS FACTOR ALPHA; AUTACOID; CYTOKINE; LIPOPOLYSACCHARIDE;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HISTOPATHOLOGY; IMMUNE RESPONSE; LUNG ALVEOLUS MACROPHAGE; LUNG EDEMA; LUNG LAVAGE; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SURVIVAL RATE; ANIMAL; BIOSYNTHESIS; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL STRAIN 3T3; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; ENDOTRACHEAL INTUBATION; IMMUNOLOGY; LUNG; MESENCHYMAL STEM CELL; METABOLISM; MORTALITY; PATHOLOGY;

3T3 CELLS; ANIMALS; BONE MARROW TRANSPLANTATION; BRONCHOALVEOLAR LAVAGE FLUID; CELL DIFFERENTIATION; CELLS, CULTURED; CYTOKINES; INFLAMMATION MEDIATORS; INTUBATION, INTRATRACHEAL; LIPOPOLYSACCHARIDES; LUNG; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL;

EID: 34548610480     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.179.3.1855     Document Type: Article

References (35)

1. Rubenfeld, G. D., E. Caldwell, E. Peabody, J. Weaver, D. P. Martin, M. Neff, E. J. Stern, and L. D. Hudson. 2005. Incidence and outcomes of acute lung injury. N. Engl. J. Med. 353: 1685-1693.
2. Ware, L. B., and M. A. Matthay. 2000. The acute respiratory distress syndrome. N. Engl. J. Med. 342: 1334-1349.
3. Ortiz, L., F. Gambelli, C. McBride, D. Gaupp, M. Baddoo, N. Kaminski, and D. G. Phinney. 2003. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc. Natl. Acad. Sci. USA 100: 8407-8411.
4. Rojas, M., X. Jianguo, C. R. Woods, A. L. Mora, W. Spears, J. Roman, and K. L. Brigham. 2005. Bone marrow derived mesenchymal stem cells in repair of the injured lung. Am. J. Resp. Cell Mol. Biol. 33: 145-152.
5. Prockop, D. J. 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276: 71-74.
6. Pittenger, M. F., A. M. Mackay, S. C. Beck, R. K. Jaiswal, R. Douglas, J. D. Mosca, M. A. Moorman, D. W. Simonetti, S. Craig, and D. R. Marshak. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
7. Krause, D. S., N. D. Theise, M. I. Collector, O. Henegariu, S. Hwang, R. Gardner, S. Neutzel, and S. Sharkis. 2001. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105: 369-377.
8. Kotton, D. N., B. Y. Ma, and W. Y. Cardoso. 2001. Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development 128: 5181-5188.
9. Aggarwal, S., and M. F. Pittenger. 2005. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105: 1815-1822.
10. Corcione, A., F. Benvenuto, E. Ferretti, D. Giunti, V. Cappiello, F. Cazzanti, M. Risso, F. Gualandi, G. L. Mancardi, V. Pistoia, and A. Uccelli. 2006. Human mesenchymal stem cells modulate B-cell functions. Blood 107: 367-372.
11. Glennie, S., I. Soeiro, P. J. Dyson, W.-F. E. Lam, and F. Dazzi. 2005. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 105: 2821-2827.
12. Krampera, M., A. Pasini, G. Pizzolo, L. Cosmi, S. Romagnani, and F. Annunziato. 2006. Regenerative and immunomodulatory potential of mesenchymal stem cells. Curr. Opin. Pharmacol. 6: 1-7.
13. Barbash, I. M., P. Chouraqui, J. Baron, M. S. Feinberg, S. Etzion, A. Tessone, L. Miller, E. Guetta, D. Zipori, L. H. Kedes, et al. 2003. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: feasibility, cell migration, and body distribution. Circulation 108: 863-868.
14. Li, T. S., M. Hayashi, H. Ito, A. Furutani, T. Murata, M. Matsuzaki, and K. Hamano. 2005. Regeneration of infarcted myocardium by intramyocardial implantation of ex vivo transforming growth factor-β-preprogrammed bone marrow stem cells. Circulation 111: 2438-2445.
15. Strauer, B. E., M. Brehm, T. Zeus, M. Kostering, A. Hernandez, R. V. Sorg, G. Kogler, and P. Wernet. 2002. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation 106: 1913-1918.
16. Su, X., M. R. Looney, L. Robriquet, X. Fang, and M. A. Matthay. 2004. Direct visual instillation as a method for efficient delivery of fluid into the distal airspaces of anesthesized mice. Exp. Lung Res. 30: 479-493.
17. Modelska, K., J. F. Pittet, H. G. Fokesson, V. C. Broaddus, and M. A. Matthay. 1999. Acid-induced lung injury: protective effect of anti-interleukin-8 pretreatment on alveolar epithelial barrier function in rabbits. Am. J. Respir. Crit. Care Med. 160: 1450-1456.
18. Ma, T., N. Fukuda, Y. Song, M. A. Matthay, and A. S. Verkman. 2000. Lung fluid transport in aquaporin-5 knockout mice. J. Clin. Invest. 105: 93-100.
19. Looney, M. R., X. Su, J. A. Van Ziffle, C. A. Lowell, and M. A. Matthay. 2006. Neutrophils and their Fcγ receptors are essential in a mouse model of transfusion-related acute lung injury. J. Clin. Invest. 116: 1615-1623.
20. Mrozek, J. D., K. M. Smith, D. R. Bing, P. A. Meyers, S. C. Simonton, J. E. Connett, and M. C. Mammel. 1997. Exogenous surfactant and partial liquid ventilation: physiologic and pathologic effects. Am. J. Respir. Crit. Care Med. 156: 1058-1065.
21. Lefort, J., M. Singer, D. Leduc, P. Renesto, M. A. Nahori, M. Huerre, C. Creminon, M. Chignard, and B. B. Vargaftig. 1998. Systemic administration of endotoxin induces bronchopulmonary hyperreactivity dissociated from TNF-α formation and neutrophil sequestration into the murine lungs. J. Immunol. 161: 474-480.
22. 51Cr-labeled lipopolysaccharide in tissue culture cells and livers of normal mice. Infect. Immun. 14: 100-105.
23. Shimada, H., N. Hasegawa, H. Koh, S. Tasaka, M. Shimizu, W. Yamada, T. Nishimura, K. Amakawa, M. Kohno, M. Sawafuji, et al. 2006. Effects of initial passage of endotoxin through the liver on the extent of acute lung injury in a rat model. Shock 26: 311-315.
24. Cho, H. H., Y. C. Bae, and J. S. Jung. 2006. Role of Toll-like receptors on human adipose-derived stromal cells. Stem Cells 24: 2744-2752.
25. Nagai, Y., K. P. Garrett, S. Ohta, U. Bahrun, T. Kouro, S. Akira, K. Takatsu, and P. W. Kincade. 2006. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24: 801-812.
26. Pevsner-Fischer, M., V. Morad, M. Cohen-Sfady, L. Rousso-Noori, A. Zanin-Zhorov, S. Cohen, I. R. Cohen, and D. Zipori. 2007. Toll-like receptors and their ligands control mesenchymal stem cell functions. Blood 109: 1422-1432.
27. Beyth, S., Z. Borovsky, D. Mevorach, M. Liebergall, Z. Gazit, H. Aslan, E. Galun, and J. Rachmilewitz. 2005. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 105: 2214-2219.
28. Shanley, T. P., N. Vasi, and A. Denenberg. 2000. Regulation of chemokine expression by IL-10 in lung inflammation. Cytokine 12: 1054-1064.
29. Spight, D., B. Zhao, M. Haas, S. Wert, A. Denenberg, and T. P. Shanley. 2005. Immunoregulatory effects of regulated, lung-targeted expression of IL-10 in vivo. Am. J. Physiol. 288: L251-L265.
30. + T-cell subsets expressing a regulatory/ suppressive phenotype. Haematologica 90: 516-525.
31. Batten, P., P. Sarathchandra, J. Antoniw, S. S. Tay, M. W. Lowdell, P. M. Taylor, and M. H. Yacoub. 2006. Human mesenchymal stem cells induce T cell anergy and downregulate T cell allo-responses via the TH2 pathway: relevance to tissue engineering human heart valves. Tissue Eng. 12: 2263-2273.
32. Gomez, C. R., S. Hirano, B. T. Cutro, S. Birjandi, H. Baila, V. Nomellini, and E. J. Kovacs. 2007. Advanced age exacerbates the pulmonary inflammatory response after lipopolysaccharide exposure. Crit. Care Med. 35: 246-251.
33. Chu, S. J., W. C. Perng, C. M. Hung, D. M. Chang, S. H. Lin, and K. L. Huang. 2005. Effects of various body temperatures after lipopolysaccharide- induced lung injury in rats. Chest 128: 327-336.
34. Koay, M. A., X. Gao, M. K. Washington, K. S. Parman, R. T. Sadikot, T. S. Blackwell, and J. W. Christman. 2002. Macrophages are necessary for maximal nuclear factor-κB activation in response to endotoxin. Am. J. Respir. Cell Mol. Biol. 26: 572-578.
35. Miyahara, Y., N. Nagaya, M. Kataoka, B. Yanagawa, K. Tanaka, H. Hao, K. Ishino, H. Ishida, T. Shimizu, K. Kangawa, et al. 2006. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat. Med. 12: 459-465.