Therapeutic effects of human mesenchymal stem cells in ex vivo human lungs injured with live bacteria

American Journal of Respiratory and Critical Care Medicine

Volumn 187, Issue 7, 2013, Pages 751-760

  Lee, Jae W ^a   Krasnodembskaya, Anna ^b   McKenna, David H ^c   Song, Yuanlin ^a   Abbott, Jason ^a   Matthay, Michael A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Acute lung injury; Bacterial pneumonia; Cell based therapy; Keratinocyte growth factor

Indexed keywords

KERATINOCYTE GROWTH FACTOR; NEUTRALIZING ANTIBODY; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEREMIA; BACTERIAL CLEARANCE; BACTERIAL PNEUMONIA; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; ESCHERICHIA COLI; EX VIVO STUDY; FLUID BALANCE; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG ALVEOLUS MACROPHAGE; LUNG FLUID; LUNG INJURY; MESENCHYMAL STEM CELL; MONOCYTE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ACUTE LUNG INJURY; ANALYSIS OF VARIANCE; CELLS, CULTURED; ESCHERICHIA COLI INFECTIONS; FIBROBLAST GROWTH FACTOR 7; HUMANS; INFLAMMATION; MACROPHAGES, ALVEOLAR; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; PHAGOCYTOSIS; PNEUMONIA, BACTERIAL; PULMONARY ALVEOLI; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2;

EID: 84872522183     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201206-0990OC     Document Type: Article

References (47)

1. Ware LB, Matthay MA. The acute respiratory distress syndrome. N Engl J Med 2000;342:1334-1349.
2. Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, Neff M, Stern EJ, Hudson LD. Incidence and outcomes of acute lung injury. N Engl J Med 2005;353:1685-1693.
3. Matthay MA, Zimmerman GA. Acute lung injury and the acute respiratory distress syndrome: four decades of inquiry into pathogenesis and rational management. Am J Respir Cell Mol Biol 2005;33:319-327.
4. The Acute Respiratory Distress Syndrome Network. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome. The Acute Respiratory Distress Syndrome Network. N Engl J Med 2000;342:1301-1308.
5. Wiedemann HP, Wheeler AP, Bernard GR, Thompson BT, Hayden D, deBoisblanc B, Connors AF Jr, Hite RD, Harabin AL. Comparison of two fluid-management strategies in acute lung injury. N Engl J Med 2006;354:2564-2575.
6. Weiss DJ, Kolls JK, Ortiz LA, Panoskaltsis-Mortari A, Prockop DJ. Stem cells and cell therapies in lung biology and lung diseases. Proc Am Thorac Soc 2008;5:637-667.
7. Prockop DJ, Olson SD. Clinical trials with adult stem/progenitor cells for tissue repair: let's not overlook some essential precautions. Blood 2007;109:3147-3151.
8. Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, Phinney DG. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA 2003;100:8407-8411.
9. Ortiz LA, Dutreil M, Fattman C, Pandey AC, Torres G, Go K, Phinney DG. Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci USA 2007;104:11002-11007.
10. Yamada M, Kubo H, Kobayashi S, Ishizawa K, Numasaki M, Ueda S, Suzuki T, Sasaki H. Bone marrow-derived progenitor cells are important for lung repair after lipopolysaccharide-induced lung injury. J Immunol 2004;172:1266-1272.
11. Rojas M, Xu J, Woods CR, Mora AL, Spears W, Roman J, Brigham KL. Bone marrow-derived mesenchymal stem cells in repair of the injured lung. Am J Respir Cell Mol Biol 2005;33:145-152.
12. Xu J, Woods CR, Mora AL, Joodi R, Brigham KL, Iyer S, Rojas M. Prevention of endotoxin-induced systemic response by bone marrowderived mesenchymal stem cells in mice. Am J Physiol Lung Cell Mol Physiol 2007;293:L131-L141.
13. Gupta N, Su X, Popov B, Lee JW, Serikov V, Matthay MA. Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice. J Immunol 2007;179:1855-1863.
14. Mei SH, McCarter SD, Deng Y, Parker CH, Liles WC, Stewart DJ. Prevention of LPS-induced acute lung injury in mice by mesenchymal stem cells overexpressing angiopoietin 1. PLoS Med 2007;4:e269.
15. Zhen G, Liu H, Gu N, Zhang H, Xu Y, Zhang Z. Mesenchymal stem cells transplantation protects against rat pulmonary emphysema. Front Biosci 2008;13:3415-3422.
16. Xu J, Qu J, Cao L, Sai Y, Chen C, He L, Yu L. Mesenchymal stem cellbased angiopoietin-1 gene therapy for acute lung injury induced by lipopolysaccharide in mice. J Pathol 2008;214:472-481.
17. Nemeth K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, Robey PG, Leelahavanichkul K, Koller BH, Brown JM, et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)- dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 2009;15:42-49.
18. Krause DS, Theise ND, Collector MI, Henegariu O, Hwang S, Gardner R, Neutzel S, Sharkis SJ. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 2001;105:369-377.
19. Wang G, Bunnell BA, Painter RG, Quiniones BC, Tom S, Lanson NA Jr, Spees JL, Bertucci D, Peister A, Weiss DJ, et al. Adult stem cells from bone marrow stroma differentiate into airway epithelial cells: potential therapy for cystic fibrosis. Proc Natl Acad Sci USA 2005;102: 186-191.
20. Spees JL, Pociask DA, Sullivan DE, Whitney MJ, Lasky JA, Prockop DJ, Brody AR. Engraftment of bone marrow progenitor cells in a rat model of asbestos-induced pulmonary fibrosis. Am J Respir Crit Care Med 2007;176:385-394.
21. Hung SC, Pochampally RR, Hsu SC, Sanchez C, Chen SC, Spees J, Prockop DJ. 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:e416.
22. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 2003;31:890-896.
23. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005;105:1815-1822.
24. Glennie S, Soeiro I, Dyson PJ, Lam EW, Dazzi F. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 2005;105:2821-2827.
25. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002;99:3838-3843.
26. Klyushnenkova E, Mosca JD, Zernetkina V, Majumdar MK, Beggs KJ, Simonetti DW, Deans RJ, McIntosh KR. T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. J Biomed Sci 2005;12:47-57.
27. Rasmusson I, Ringden O, Sundberg B, Le Blanc K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 2003;76:1208-1213.
28. Chen L, Tredget EE, Wu PY, Wu Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PloS One 2008;3:e1886.
29. Mei SH, Haitsma JJ, Dos Santos CC, Deng Y, Lai PF, Slutsky AS, Liles WC, Stewart DJ. Mesenchymal stem cells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis. Am J Respir Crit Care Med 2010;182:1047-1057.
30. Lee JW, Fang X, Gupta N, Serikov V, Matthay MA. Allogeneic human mesenchymal stem cells for treatment of E. coli endotoxin-induced acute lung injury in the ex vivo perfused human lung. Proc Natl Acad Sci USA 2009;106:16357-16362.
31. Wu H, Suzuki T, Carey B, Trapnell BC, McCormack FX. Keratinocyte growth factor augments pulmonary innate immunity through epithelium-driven, GM-CSF-dependent paracrine activation of alveolar macrophages. J Biol Chem 2011;286:14932-14940.
32. Lee JW, Krasnodembskaya A, Fang X, McKenna DH, Read EJ, Matthay MA. Allogeneic human mesenchymal stem cells inhibit bacterial growth and restore normal alveolar fluid transport in an ex vivo perfused human lung injured by live E. coli. Am J Respir Crit Care Med 2011;183:A1247.
33. Krasnodembskaya A, Song Y, Fang X, Gupta N, Serikov V, Lee JW, Matthay MA. Antibacterial effect of human mesenchymal stem cells is mediated in part from secretion of the antimicrobial peptide LL-37. Stem Cells 2010;28:2229-2238.
34. Gupta N, Krasnodembskaya A, Kapetanaki M, Mouded M, Tan X, Serikov V, Matthay MA. Mesenchymal stem cells enhance survival and bacterial clearance in murine Escherichia coli pneumonia. Thorax 2012;67:533-539.
35. Gonzalez-Rey E, Anderson P, Gonzalez MA, Rico L, Buscher D, Delgado M. Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis. Gut 2009;58:929-939.
36. Kim J, Hematti P. Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages. Exp Hematol 2009;37:1445-1453.
37. Krasnodembskaya A, Samarani G, Song Y, Zhuo H, Su X, Lee JW, Gupta N, Petrini M, Matthay MA. Human mesenchymal stem cells reduce mortality and bacteremia in gram negative sepsis in mice in part by enhancing the phagocytic activity of blood monocytes. Am J Physiol Lung Cell Mol Physiol 2012;302:L1003-L1013.
38. Nemeth K, Mayer B, Mezey E. Modulation of bone marrow stromal cell functions in infectious diseases by toll-like receptor ligands. J Mol Med (Berl) 2010;88:5-10.
39. Rubin JS, Osada H, Finch PW, Taylor WG, Rudikoff S, Aaronson SA. Purification and characterization of a newly identified growth factor specific for epithelial cells. Proc Natl Acad Sci USA 1989;86:802-806.
40. Nemzek JA, Ebong SJ, Kim J, Bolgos GL, Remick DG. Keratinocyte growth factor pretreatment is associated with decreased macrophage inflammatory protein-2alpha concentrations and reduced neutrophil recruitment in acid aspiration lung injury. Shock 2002;18:501-506.
41. Yano T, Deterding RR, Simonet WS, Shannon JM, Mason RJ. Keratinocyte growth factor reduces lung damage due to acid instillation in rats. Am J Respir Cell Mol Biol 1996;15:433-442.
42. Sugahara K, Iyama K, Kuroda MJ, Sano K. Double intratracheal instillation of keratinocyte growth factor prevents bleomycin-induced lung fibrosis in rats. J Pathol 1998;186:90-98.
43. Yi ES, Salgado M, Williams S, Kim SJ, Masliah E, Yin S, Ulich TR. Keratinocyte growth factor decreases pulmonary edema, transforming growth factor-beta and platelet-derived growth factor-BB expression, and alveolar type II cell loss in bleomycin-induced lung injury. Inflammation 1998;22:315-325.
44. Barazzone C, Donati YR, Rochat AF, Vesin C, Kan CD, Pache JC, Piguet PF. Keratinocyte growth factor protects alveolar epithelium and endothelium from oxygen-induced injury in mice. Am J Pathol 1999;154:1479-1487.
45. Panos RJ, Bak PM, Simonet WS, Rubin JS, Smith LJ. Intratracheal instillation of keratinocyte growth factor decreases hyperoxia-induced mortality in rats. J Clin Invest 1995;96:2026-2033.
46. Viget NB, Guery BP, Ader F, Neviere R, Alfandari S, Creuzy C, Roussel-Delvallez M, Foucher C, Mason CM, Beaucaire G, et al. Keratinocyte growth factor protects against Pseudomonas aeruginosainduced lung injury. Am J Physiol Lung Cell Mol Physiol 2000;279: L1199-L1209.
47. Islam MN, Das SR, Emin MT, Wei M, Sun L, Westphalen K, Rowlands DJ, Quadri SK, Bhattacharya S, Bhattacharya J. Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat Med 2012;18:759-765.