Multipotent adult progenitor cells decrease cold ischemic injury in ex vivo perfused human lungs: An initial pilot and feasibility study

Transplantation Research

Volumn 3, Issue 1, 2014, Pages

  La Francesca, Saverio ^a,f   Ting, Anthony E ^b   Sakamoto, Jason ^c   Rhudy, Jessica ^c   Bonenfant, Nicholas R ^d   Borg, Zachary D ^d   Cruz, Fernanda F ^e   Goodwin, Meagan ^d   Lehman, Nicholas A ^b   Taggart, Jennifer M ^b   Deans, Robert ^b   Weiss, Daniel J ^d  

^a Methodist DeBakey Heart and Vascular Center   (United States)

^b ATHERSYS INC   (United States)

^c HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^e FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^f Harvard Apparatus Regenerative Technology Inc   (United States)

Author keywords

Cell therapy; Ischemia reperfusion injury; Lung transplantation; Mesenchymal stromal cell

Indexed keywords

ADULT; ARTICLE; ARTIFICIAL VENTILATION; BRONCHOALVEOLAR LAVAGE FLUID; BRONCHOSCOPY; CASE REPORT; CLINICAL ASSESSMENT; COLD ISCHEMIA; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG PERFUSION; MALE; MIDDLE AGED; MULTIPOTENT STEM CELL; POSITIVE END EXPIRATORY PRESSURE; PRIORITY JOURNAL;

EID: 84930189104     PISSN: None     EISSN: 20471440     Source Type: Journal    
DOI: 10.1186/2047-1440-3-19     Document Type: Article

References (41)

1. Lee JC, Christie JD: Primary graft dysfunction. Proc Am Thorac Soc 2009, 6(1):39-46.
2. de Perrot M, Liu M, Waddell TK, Keshavjee S: Ischemia-reperfusion-induced lung injury. Am J Respir Crit Care Med 2003, 167(4):490-511.
3. den Hengst WA, Gielis JF, Lin JY, Van Schil PE, De Windt LJ, Moens AL: Lung ischemia-reperfusion injury: a molecular and clinical view on a complex pathophysiological process. Am J Physiol Heart Circ Physiol 2010, 299(5):H1283-H1299.
4. Weyker PD, Webb CAJ, Kiamanesh D, Flynn BC: Lung ischemia reperfusion injury: a bench-to-bedside review. Semin Cardiothorac Vasc Anesth 2013, 17:28.
5. Hall DJ, Baz M, Daniels MJ, Staples ED, Klodell CT, Moldawer LL, Beaver TM: Immediate postoperative inflammatory response predicts long-term outcome in lung-transplant recipients. Interact Cardiovasc Thorac Surg 2012, 15(4):603-607.
6. Huang HJ, Yusen RD, Meyers BF, Walter MJ, Mohanakumar T, Patterson GA, Trulock EP, Hachem RR: Late primary graft dysfunction after lung transplantation and bronchiolitis obliterans syndrome. Am J Transplant 2008, 8(11):2454-2462.
7. Bharat A, Kuo E, Steward N, Aloush A, Hachem R, Trulock EP, Patterson GA, Meyers BF, Mohanakumar T: Immunological link between primary graft dysfunction and chronic lung allograft rejection. Ann Thorac Surg 2008, 86(1):189-195.
8. Whitson BA, Prekker ME, Herrington CS, Whelan TP, Radosevich DM, Hertz MI, Dahlberg PS: Primary graft dysfunction and long-term pulmonary function after lung transplantation. J Heart Lung Transplant 2007, 26(10):1004-1011.
9. Carter YM, Gelman AE, Kreisel D: Pathogenesis, management, and consequences of primary graft dysfunction. Semin Thorac Cardiovasc Surg 2008, 20(2):165-172.
10. Warneckea G, Haverich A: Lung re-transplantation: review. Curr Opin Organ Transplant 2012, 17:485-489.
11. Snell GI, Westall GP: The contribution of airway ischemia and vascular remodelling to the pathophysiology of bronchiolitis obliterans syndrome and chronic lung allograft dysfunction. Curr Opin Organ Transplant 2010, 15(5):558-562.
12. Diamond JM, Christie JD: The contribution of airway and lung tissue ischemia to primary graft dysfunction. Curr Opin Organ Transplant 2010, 15(5):552-557.
13. Pettersson GB, Budev M: The role of ischemia in postlung transplantation complications. Curr Opin Organ Transplant 2010, 15(5):549-551.
14. Machuca TN, Cypel M, Keshavjee S: Advances in lung preservation. Surg Clin North Am 2013, 93(6):1373-1394.
15. Keating A: Mesenchymal stromal cells: new directions. Cell Stem Cell 2012, 10(6):709-716.
16. Prockop DJ, Oh JY: Medical therapies with adult stem/progenitor cells (MSCs): a backward journey from dramatic results in vivo to the cellular and molecular explanations. J Cell Biochem 2012, 113(5):1460-1469.
17. Bianco P, Cao X, Frenette PS, Mao JJ, Robey PG, Simmons PJ, Wang CY: The meaning, the sense, and the significance: translating the science of mesenchymal stem cells into medicine. Nat Med 2013, 19:35-42.
18. Weiss DJ: Stem cells, cell therapies and bioengineering in lung biology and diseases: comprehensive review of the literature. Ann Am Thorac Soc 2013, 10(5):S45-S97.
19. Matthay MA, Anversa P, Bhattacharya J, Burnett BK, Chapman HA, Hare JM, Hei DJ, Hoffman AM, Kourembanas S, McKenna DH, Ortiz LA, Ott HC, Tente W, Thebaud B, Trapnell BC, Weiss DJ, Yuan XJ, Blaisdell CJ: Cell therapy for lung diseases. Report from an NIH-NHLBI workshop, November 13-14, 2012 Am J of Resp and Critl Care Med 2013, 188(3):370-375.
20. Bedi SS, Hetz R, Thomas C, Smith P, Olsen AB, Williams S, Xue H, Aroom K, Uray K, Hamilton J, Mays RW, Cox CS Jr: Intravenous multipotent adult progenitor cell therapy attenuates activated microglial/macrophage response and improves spatial learning after traumatic brain injury. Stem Cells Transl Med 2013, 2:953-960.
21. Eggenhofer E, Popp FC, Mendicino M, Silber P, Van't Hof W, Renner P, Hoogduijn MJ, Pinxteren J, van Rooijen N, Geissler EK, Deans R, Schlitt HJ, Dahlke MH: Heart grafts tolerized through third-party multipotent adult progenitor cells can be retransplanted to secondary hosts with no immunosuppression. Stem Cell Trans Med 2013, 2(8):595-606.
22. Obermajer N, Popp FC, Johnson CL, Benseler V, Dahlke MH: Rationale and prospects of mesenchymal stem cell therapy for liver transplantation. Curr Opin Organ Trans 2014, 19(1):60-422.
23. Penn MS, Ellis S, Gandhi S, Greenbaum A, Hodes Z, Mendelsohn FO, Strasser D, Ting AE, Sherman W: Adventitial delivery of an allogeneic bone marrowderived adherent stem cell in acute myocardial infarction: phase I clinical study. Circ Res 2012, 110(2):304-311.
24. Maziarz RT, Devos T, Bachier C, Goldstein SC, Leis J, Cooke KR, Perry R, Deans RJ, Van't Hof WJ, Lazarus HM: Prophylaxis of acute GVHD using Multistem® stromal cell therapy: preliminary results after administration of single or multiple doses in a phase 1 trial. Biol Blood Marrow Transplant 2012, 18(2 Sup):S264-S265.
25. #NCT01436487 (Study to examine the effects of MultiStem in ischemic stroke). [clinicaltrials.gov].
26. NCT01240915 (A study to investigate the safety and possible clinical benefit of Multistem(r) in patients with moderate to severe ulcerative colitis). [clinicaltrials.gov].
27. #NCT01841632 (Safety study of multipotent progenitor cells for immunomodulation therapy after liver transplantation). [clinicaltrials.gov].
28. Boozer S, Lehman N, Lakshmipathy U, Love B, Raber A, Maitra A, Deans R, Rao MS, Ting AE: Global characterization and genomic stability of human MAPC, a multipotent adult progenitor cell. J Stem Cells 2009, 4:17-28.
29. Rojas M, Cárdenes N, Kocyildirim E, Tedrow JR, Cáceres E, Deans R, Ting A, Bermúdez C: Human adult bone marrow-derived stem cells decrease severity of lipopolysaccharide-induced acute respiratory distress syndrome in sheep. Stem Cell Res Ther 2014, 5(2):42.
30. Lathrop MJ, Brooks EM, Bonenfant NR, Sokocevic D, Borg ZD, Goodwin M, Loi R, Cruz FF, Dunaway CW, Steele C, Weiss DJ: Mesenchymal stromal cells mediate Aspergillus hyphal extract-induced allergic airways inflammation by inhibition of the Th17 signaling pathway. Stem Cell Trans Med 2014.
31. Goodwin M, Sueblinvong V, Eisenhauer P, Ziats NP, Leclair L, Poynter ME, Steele C, Rincon M, Weiss DJ: Bone marrow derived mesenchymal stromal cells inhibit Th2-mediated allergic airways inflammation in mice. Stem Cells 2011, 29(7):1137-1148.
32. Cypel M, Liu M, Rubacha M, Yeung JC, Hirayama S, Anraku M, Sato M, Medin J, Davidson BL, de Perrot M, Waddell TK, Slutsky AS, Keshavjee S: Functional repair of human donor lungs by IL-10 gene therapy. Sci Transl Med 2009, 1(4):4-9.
33. Fernandez LG, Sharma AK, LaPar DJ, Kron IL, Laubach VE: Adenosine A1 receptor activation attenuates lung ischemia-reperfusion injury. J Thorac Cardiovasc Surg 2013, 145(6):1654-1659.
34. Mulloy DP, Sharma AK, Fernandez LG, Zhao Y, Lau CL, Kron IL, Laubach VE: Adenosine A3 receptor activation attenuates lung ischemia-reperfusion injury. Ann Thorac Surg 2013, 95(5):1762-1767.
35. Menasche P: Cardiac cell therapy: lessons from clinical trials. J Mol Cell Cardiol 2011, 50(2):258-265.
36. Hare JM, Fishman JE, Gerstenblith G, DiFede Velazquez DL, Zambrano JP, Suncion VY, Tracy M, Ghersin E, Johnston PV, Brinker JA, Breton E, Davis-Sproul J, Schulman IH, Byrnes J,Mendizabal AM, LoweryMH, Rouy D, Altman P,Wong Po Foo C, Ruiz P, Amador A, Da Silva J, McNiece IK, Heldman AW, George R, Lardo A: Comparison of allogeneic vs autologous bone marrow-derived mesenchymal stem cells delivered by transendocardial injection in patients with ischemic cardiomyopathy: the POSEIDON randomized trial. JAMA 2012, 308(22):2369-2379.
37. Weiss DJ, Casaburi R, Flannery R, LeRoux-Williams M, Tashkin DP: A placebocontrolled, randomized trial of mesenchymal stem cells in COPD. Chest 2013, 143(6):1590-1598.
38. Wierup P, Haraldsson A, Nilsson F, Pierre L, Scherstén H, Silverborn M, Sjöberg T, Westfeldt U, Steen S: Ex vivo evaluation of nonacceptable donor lungs. Ann Thorac Surg 2006, 81(2):460-466.
39. Ingemansson R, Eyjolfsson A, Mared L, Pierre L, Algotsson L, Ekmehag B, Gustafsson R, Johnsson P, Koul B, Lindstedt S, Lührs C, Sjöberg T, Steen S: Clinical transplantation of initially rejected donor lungs after reconditioning ex vivo. Ann Thorac Surg 2009, 87(1):255-260.
40. Cypel M, Yeung JC, Liu M, Anraku M, Chen F, Karolak W, Sato M, Laratta J, Azad S, Madonik M, Chow CW, Chaparro C, Hutcheon M, Singer LG, Slutsky AS, Yasufuku K, de Perrot M, Pierre AF, Waddell TK, Keshavjee S: Normothermic ex vivo lung perfusion in clinical lung transplantation. N Engl J Med 2011, 364(15):1431-1440.
41. McAuley DF, Curley GF, Hamid UI, Laffey JG, Abbott J, McKenna DH, Fang X, Matthay MA, Lee JW: Clinical grade allogeneic human mesenchymal stem cells restore alveolar fluid clearance in human lungs rejected for transplantation. Am J Physiol Lung Cell Mol Physiol 2014, 306(9):L809-L815.