MSC microvesicles for the treatment of lung disease: A new paradigm for cell-free therapy

Antioxidants and Redox Signaling

Volumn 21, Issue 13, 2014, Pages 1905-1915

  Sdrimas, Konstantinos ^a,b   Kourembanas, Stella ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE LUNG INJURY; CELL THERAPY; HUMAN; HYPEROXIA; LUNG BLOOD VESSEL; LUNG DISEASE; LUNG DYSPLASIA; LUNG FIBROSIS; LUNG INJURY; LUNG VASCULAR DISEASE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PULMONARY HYPERTENSION; REVIEW; VASCULAR DISEASE; ANIMAL; BIOLOGICAL THERAPY; CYTOLOGY; CYTOPLASM VESICLE; LUNG DISEASES; MESENCHYMAL STROMA CELL; PATHOPHYSIOLOGY; PROCEDURES; TRANSPLANTATION;

ANIMALS; CELL- AND TISSUE-BASED THERAPY; CYTOPLASMIC VESICLES; HUMANS; LUNG DISEASES; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS;

EID: 84910119440     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5784     Document Type: Review

References (83)

1. Amsalem Y, Mardor Y, Feinberg MS, Landa N, Miller L, Daniels D, Ocherashvilli A, Holbova R, Yosef O, Barbash IM, et al. Iron-oxide labeling and outcome of transplanted mesenchymal stem cells in the infarcted myocardium. Circulation 116(11 Suppl): 138-145, 2007.
2. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, and Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967, 1997.
3. Aslam M, Baveja R, Liang OD, Fernandez-Gonzalez A, Lee C, Mitsialis SA, and Kourembanas S. Bone marrow stromal cells attenuate lung injury in a murine model of neonatal chronic lung disease. Am J Respir Crit Care Med 180: 1122-1130, 2009.
4. Baber SR, Deng W, Master RG, Bunnell BA, Taylor BK, Murthy SN, Hyman AL, and Kadowitz PJ. Intratracheal mesenchymal stem cell administration attenuates monocrotaline-induced pulmonary hypertension and endothelial dysfunction. Am J Physiol Heart Circ Physiol 292: H1120-H1128, 2007.
5. Baglio SR, Pegtel DM, and Baldini N. Mesenchymal stem cell secreted vesicles provide novel opportunities in (stem) cell-free therapy. Front Physiol 3: 359, 2012.
6. Balasubramaniam V, Ryan SL, Seedorf GJ, Roth EV, Heumann TR, Yoder MC, Ingram DA, Hogan CJ, Markham NE, and Abman SH. Bone marrow-derived angiogenic cells restore lung alveolar and vascular structure after neonatal hyperoxia in infant mice. Am J Physiol Lung Cell Mol Physiol 298: L315-L323, 2010.
7. Banerjee M, Kumar A, and Bhonde RR. Reversal of experimental diabetes by multiple bone marrow transplantation. Biochem Biophys Res Commun 328: 318-325, 2005.
8. Beyth S, Borovsky Z, Mevorach D, Liebergall M, Gazit Z, Aslan H, Galun E, and Rachmilewitz J. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 105: 2214-2219, 2005.
9. Binato R, de Souza Fernandez T, Lazzarotto-Silva C, Du Rocher B, Mencalha A, Pizzatti L, Bouzas LF, and Abdelhay E. Stability of human mesenchymal stem cells during in vitro culture: considerations for cell therapy. Cell Prolif 46: 10-22, 2013.
10. Bruno S, Grange C, Deregibus MC, Calogero RA, Saviozzi S, Collino F, Morando L, Busca A, Falda M, Bussolati B, et al. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol 20: 1053-1067, 2009.
11. Budoni M, Fierabracci A, Luciano R, Petrini S, Di Ciommo V, and Muraca M. The immunosuppressive effect of mesenchymal stromal cells on B lymphocytes is mediated by membrane vesicles. Cell Transplant 22: 369-379, 2013.
12. Caplan AI and Correa D. The MSC: an injury drugstore. Cell Stem Cell 9: 11-15, 2011.
13. Chang JC, Summer R, Sun X, Fitzsimmons K, and Fine A. Evidence that bone marrow cells do not contribute to the alveolar epithelium. Am J Respir Cell Mol Biol 33: 335-342, 2005.
14. Chhabra P and Brayman KL. Stem cell therapy to cure type 1 diabetes: from hype to hope. Stem Cells Transl Med 2: 328-336, 2013.
15. Chimenti L, Luque T, Bonsignore MR, Ramirez J, Navajas D, and Farre R. Pre-treatment with mesenchymal stem cells reduces ventilator-induced lung injury. Eur Respir J 40: 939-948, 2012.
16. Chow K, Fessel JP, Kaoriihida S, Schmidt EP, Gaskill C, Alvarez D, Graham B, Harrison DG, Wagner DH Jr., Nozik-Grayck E, et al. Dysfunctional resident lung mesenchymal stem cells contribute to pulmonary microvascular remodeling. Pulm Circ 3: 31-49, 2013.
17. Chugh AR, Beache GM, Loughran JH, Mewton N, Elmore JB, Kajstura J, Pappas P, Tatooles A, Stoddard MF, Lima JA, et al. Administration of cardiac stem cells in patients with ischemic cardiomyopathy: the SCIPIO trial: surgical aspects and interim analysis of myocardial function and viability by magnetic resonance. Circulation 126(11 Suppl 1): S54-S64, 2012.
18. Collino F, Deregibus MC, Bruno S, Sterpone L, Aghemo G, Viltono L, Tetta C, and Camussi G. Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS One 5: e11803, 2010.
19. Curley GF, Hayes M, Ansari B, Shaw G, Ryan A, Barry F, O'Brien T, O'Toole D, and Laffey JG. Mesenchymal stem cells enhance recovery and repair following ventilatorinduced lung injury in the rat. Thorax 67: 496-501, 2012.
20. de Sa Silva F, Almeida PN, Rettore JV, Maranduba CP, de Souza CM, de Souza GT, Zanette Rde S, Miyagi SP, Santos Mde O, Marques MM, et al. Toward personalized cell therapies by using stem cells: seven relevant topics for safety and success in stem cell therapy. J Biomed Biotechnol 2012: 758102, 2012
21. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, and Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8: 315-317, 2006.
22. Dorronsoro A and Robbins PD. Regenerating the injured kidney with human umbilical cord mesenchymal stem cellderived exosomes. Stem Cell Res Ther 4: 39, 2013.
23. Duffy MM, Ritter T, Ceredig R, and Griffin MD. Mesenchymal stem cell effects on T-cell effector pathways. Stem Cell Res Ther 2: 34, 2011.
24. Eggenhofer E, Benseler V, Kroemer A, Popp FC, Geissler EK, Schlitt HJ, Baan CC, Dahlke MH, and Hoogduijn MJ. Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion. Front Immunol 3: 297, 2012.
25. Escudier B, Dorval T, Chaput N, Andre F, Caby MP, Novault S, Flament C, Leboulaire C, Borg C, Amigorena S, et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J Transl Med 3: 10, 2005.
26. Ezquer FE, Ezquer ME, Parrau DB, Carpio D, Yanez AJ, and Conget PA. Systemic administration of multipotent mesenchymal stromal cells reverts hyperglycemia and prevents nephropathy in type 1 diabetic mice. Biol Blood Marrow Transplant 14: 631-640, 2008.
27. Foronjy RF and Majka SM. The potential for resident lung mesenchymal stem cells to promote functional tissue regeneration: understanding microenvironmental cues. Cells 1: 874, 2012.
28. Foudah D, Redaelli S, Donzelli E, Bentivegna A, Miloso M, Dalpra L, and Tredici G. Monitoring the genomic stability of in vitro cultured rat bone-marrow-derived mesenchymal stem cells. Chromosome Res 17: 1025-1039, 2009.
29. Gnecchi M, He H, Liang OD, Melo LG, Morello F, Mu H, Noiseux N, Zhang L, Pratt RE, Ingwall JS, et al. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 11: 367-368, 2005.
30. Hansmann G, Fernandez-Gonzalez A, Aslam M, Vitali SH, Martin T, Mitsialis SA, and Kourembanas S. Mesenchymal stem cell-mediated reversal of bronchopulmonary dysplasia and associated pulmonary hypertension. Pulm Circ 2: 170-181, 2012.
31. Hare JM, Traverse JH, Henry TD, Dib N, Strumpf RK, Schulman SP, Gerstenblith G, DeMaria AN, Denktas AE, Gammon RS, et al. A randomized, double-blind, placebocontrolled, dose-escalation study of intravenous adult human mesenchymal stem cells (prochymal) after acute myocardial infarction. J Am Coll Cardiol 54: 2277-2286, 2009.
32. Hodges RJ, Jenkin G, Hooper SB, Allison B, Lim R, Dickinson H, Miller SL, Vosdoganes P, and Wallace EM. Human amnion epithelial cells reduce ventilation-induced preterm lung injury in fetal sheep. Am J Obstet Gynecol 206: 448.e8-e15, 2012.
33. Jang MJ, Kim HS, Lee HG, Kim GJ, Jeon HG, Shin HS, Chang SK, Hur GH, Chong SY, Oh D, et al. Placentaderived mesenchymal stem cells have an immunomodulatory effect that can control acute graft-versus-host disease in mice. Acta Haematol 129: 197-206, 2013.
34. Jansen BJ, Gilissen C, Roelofs H, Schaap-Oziemlak A, Veltman JA, Raymakers RA, Jansen JH, Kogler G, Figdor CG, Torensma R, et al. Functional differences between mesenchymal stem cell populations are reflected by their transcriptome. Stem Cells Dev 19: 481-490, 2010.
35. Jarvinen L, Badri L, Wettlaufer S, Ohtsuka T, Standiford TJ, Toews GB, Pinsky DJ, Peters-Golden M, and Lama VN. Lung resident mesenchymal stem cells isolated from human lung allografts inhibit T cell proliferation via a soluble mediator. J Immunol 181: 4389-4396, 2008.
36. Jun D, Garat C, West J, Thorn N, Chow K, Cleaver T, Sullivan T, Torchia EC, Childs C, Shade T, et al. The pathology of bleomycin-induced fibrosis is associated with loss of resident lung mesenchymal stem cells that regulate effector T-cell proliferation. Stem Cells 29: 725-735, 2011.
37. Kajstura J, Rota M, Hall SR, Hosoda T, D'Amario D, Sanada F, Zheng H, Ogorek B, Rondon-Clavo C, Ferreira-Martins J, et al. Evidence for human lung stem cells. N Engl J Med 364: 1795-1806, 2011.
38. Kanki-Horimoto S, Horimoto H, Mieno S, Kishida K, Watanabe F, Furuya E, and Katsumata T. Implantation of mesenchymal stem cells overexpressing endothelial nitric oxide synthase improves right ventricular impairments caused by pulmonary hypertension. Circulation 114(1 Suppl): I181-I185, 2006.
39. Kebriaei P, Isola L, Bahceci E, Holland K, Rowley S, McGuirk J, Devetten M, Jansen J, Herzig R, Schuster M, et al. Adult human mesenchymal stem cells added to corticosteroid therapy for the treatment of acute graft-versushost disease. Biol Blood Marrow Transplant 15: 804-811, 2009.
40. Khemani E, McElhinney DB, Rhein L, Andrade O, Lacro RV, Thomas KC, and Mullen MP. Pulmonary artery hypertension in formerly premature infants with bronchopulmonary dysplasia: clinical features and outcomes in the surfactant era. Pediatrics 120: 1260-1269, 2007.
41. Kitazawa Y, Li XK, Xie L, Zhu P, Kimura H, and Takahara S. Bone marrow-derived conventional, but not cloned, mesenchymal stem cells suppress lymphocyte proliferation and prevent graft-versus-host disease in rats. Cell Transplant 21: 581-590, 2012.
42. Kotton DN, Ma BY, Cardoso WV, Sanderson EA, Summer RS, Williams MC, and Fine A. Bone marrow-derived cells as progenitors of lung alveolar epithelium. Development 128: 5181-5188, 2001.
43. Kuang PP, Lucey E, Rishikof DC, Humphries DE, Bronsnick D, and Goldstein RH. Engraftment of neonatal lung fibroblasts into the normal and elastase-injured lung. Am J Respir Cell Mol Biol 33: 371-377, 2005.
44. Lai RC, Arslan F, Lee MM, Sze NS, Choo A, Chen TS, Salto-Tellez M, Timmers L, Lee CN, El Oakley RM, et al. Exosome secreted by MSC reduces myocardial ischemia/ reperfusion injury. Stem Cell Res 4: 214-222, 2010.
45. Lamparski HG, Metha-Damani A, Yao JY, Patel S, Hsu DH, Ruegg C, and Le Pecq JB. Production and characterization of clinical grade exosomes derived from dendritic cells. J Immunol Methods 270: 211-226, 2002.
46. Le Blanc K and Ringden O. Immunobiology of human mesenchymal stem cells and future use in hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 11: 321-334, 2005.
47. Leblond AL, Naud P, Forest V, Gourden C, Sagan C, Romefort B, Mathieu E, Delorme B, Collin C, Pages JC, et al. Developing cell therapy techniques for respiratory disease: intratracheal delivery of genetically engineered stem cells in a murine model of airway injury. Hum Gene Ther 20: 1329-1343, 2009.
48. Lee C, Mitsialis SA, Aslam M, Vitali SH, Vergadi E, Konstantinou G, Sdrimas K, Fernandez-Gonzalez A, and Kourembanas S. Exosomes mediate the cytoprotective action of mesenchymal stromal cells on hypoxia-induced pulmonary hypertension. Circulation 126: 2601-2611, 2012.
49. Lee JW, Fang X, Gupta N, Serikov V, and 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 U S A 106: 16357-16362, 2009.
50. Liang OD, Mitsialis SA, Chang MS, Vergadi E, Lee C, Aslam M, Fernandez-Gonzalez A, Liu X, Baveja R, and Kourembanas S. Mesenchymal stromal cells expressing heme oxygenase-1 reverse pulmonary hypertension. Stem Cells 29: 99-107, 2011.
51. Luan Y, Zhang X, Kong F, Cheng GH, Qi TG, and Zhang ZH. Mesenchymal stem cell prevention of vascular remodeling in high flow-induced pulmonary hypertension through a paracrine mechanism. Int Immunopharmacol 14: 432-437, 2012.
52. Luan Y, Zhang ZH, Wei DE, Zhao JJ, Kong F, Cheng GH, and Wang YB. Implantation of mesenchymal stem cells improves right ventricular impairments caused by experimental pulmonary hypertension. Am J Med Sci 343: 402-406, 2012.
53. Mac Sweeney R and McAuley DF. Mesenchymal stem cell therapy in acute lung injury: is it time for a clinical trial? Thorax 67: 475-476, 2012.
54. Mathivanan S, Ji H, and Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics 73: 1907-1920, 2010.
55. Mathivanan S and Simpson RJ. ExoCarta: A compendium of exosomal proteins and RNA. Proteomics 9: 4997-5000, 2009.
56. Matthay MA, Anversa P, Bhattacharya J, Burnett BK, Chapman HA, Hare JM, Hei DJ, Hoffman AM, Kourembanas S, McKenna DH, et al. Cell Therapy for Lung Diseases: Report from an NIH-NHLBI Workshop November 13-14, 2012. Am J Respir Crit CareMed 188: 370, 2013.
57. Morse MA, Garst J, Osada T, Khan S, Hobeika A, Clay TM, Valente N, Shreeniwas R, Sutton MA, Delcayre A, et al. A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 3: 9, 2005.
58. Musina RA, Bekchanova ES, and Sukhikh GT. Comparison of mesenchymal stem cells obtained from different human tissues. Bull Exp Biol Med 139: 504-509, 2005.
59. Parekkadan B, van Poll D, Suganuma K, Carter EA, Berthiaume F, Tilles AW, and Yarmush ML. Mesenchymal stem cell-derived molecules reverse fulminant hepatic failure. PLoS One 2: e941, 2007.
60. Patel KM, Crisostomo P, Lahm T, Markel T, Herring C, Wang M, Meldrum KK, Lillemoe KD, and Meldrum DR. Mesenchymal stem cells attenuate hypoxic pulmonary vasoconstriction by a paracrine mechanism. J Surg Res 143: 281-285, 2007.
61. Peng L, Jia Z, Yin X, Zhang X, Liu Y, Chen P, Ma K, and Zhou C. Comparative analysis of mesenchymal stem cells from bone marrow, cartilage, and adipose tissue. Stem Cells Dev 17: 761-773, 2008. 61a.
62. Pierro M, Ionescu L, Montemurro T, Vadivel A, Weissmann G, Oudit G, Emery D, Bodiga S, Eaton F, Péault B, Mosca F, Lazzari L, and Thébaud B. Short-term, long-term and paracrine effect of human umbilical cord-derived stem cells in lung injury prevention and repair in experimental bronchopulmonary dysplasia. Thorax 68:475-484, 2013.
63. Popova AP, Bentley JK, Anyanwu AC, Richardson MN, Linn MJ, Lei J, Wong EJ, Goldsmith AM, Pryhuber GS, and Hershenson MB. Glycogen synthase kinase-3beta/betacatenin signaling regulates neonatal lung mesenchymal stromal cell myofibroblastic differentiation. Am J Physiol Lung Cell Mol Physiol 303: L439-L448, 2012.
64. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276: 71-74, 1997.
65. Ranganath SH, Levy O, Inamdar MS, and Karp JM. Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 10: 244-258, 2012.
66. Schreml S, Babilas P, Fruth S, Orso E, Schmitz G, Mueller MB, Nerlich M, and Prantl L. Harvesting human adipose tissue-derived adult stem cells: resection versus liposuction. Cytotherapy 11: 947-957, 2009.
67. Simons M and Raposo G. Exosomes - vesicular carriers for intercellular communication. Curr Opin Cell Biol 21: 575-581, 2009.
68. Spaggiari GM, Capobianco A, Becchetti S, Mingari MC, and Moretta L. Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NKcell proliferation. Blood 107: 1484-1490, 2006.
69. Theise ND, Henegariu O, Grove J, Jagirdar J, Kao PN, Crawford JM, Badve S, Saxena R, and Krause DS. Radiation pneumonitis in mice: a severe injury model for pneumocyte engraftment from bone marrow. Exp Hematol 30: 1333-1338, 2002.
70. Thery C, Ostrowski M, and Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9: 581-593, 2009.
71. Thery C, Zitvogel L, and Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2: 569-579, 2002.
72. Tsai MS, Hwang SM, Chen KD, Lee YS, Hsu LW, Chang YJ, Wang CN, Peng HH, Chang YL, Chao AS, et al. Functional network analysis of the transcriptomes of mesenchymal stem cells derived from amniotic fluid, amniotic membrane, cord blood, and bone marrow. Stem Cells 25: 2511-2523, 2007.
73. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, and Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654-659, 2007.
74. van Haaften T, Byrne R, Bonnet S, Rochefort GY, Akabutu J, Bouchentouf M, Rey-Parra GJ, Galipeau J, Haromy A, Eaton F, et al. Airway delivery of mesenchymal stem cells prevents arrested alveolar growth in neonatal lung injury in rats. Am J Respir Crit Care Med 180: 1131-1142, 2009.
75. van Koppen A, Joles JA, van Balkom BW, Lim SK, de Kleijn D, Giles RH, and Verhaar MC. Human embryonic mesenchymal stem cell-derived conditioned medium rescues kidney function in rats with established chronic kidney disease. PLoS One 7: e38746, 2012.
76. Vosdoganes P, Hodges RJ, Lim R, Westover AJ, Acharya RY, Wallace EM, and Moss TJ. Human amnion epithelial cells as a treatment for inflammation-induced fetal lung injury in sheep. Am J Obstet Gynecol 205: 156 e26-e33, 2012.
77. Wang XX, Zhang FR, Shang YP, Zhu JH, Xie XD, Tao QM, and Chen JZ. Transplantation of autologous endothelial progenitor cells may be beneficial in patients with idiopathic pulmonary arterial hypertension: a pilot randomized controlled trial. J Am Coll Cardiol 49: 1566-1571, 2007.
78. Wong PM, Lees AN, Louw J, Lee FY, French N, Gain K, Murray CP, Wilson A, and Chambers DC. Emphysema in young adult survivors of moderate-to-severe bronchopulmonary dysplasia. Eur Respir J 32: 321-328, 2008.
79. Yeo RW, Lai RC, Zhang B, Tan SS, Yin Y, Teh BJ, and Lim SK. Mesenchymal stem cell: an efficient mass producer of exosomes for drug delivery. Adv Drug Deliv Rev 65: 336-341, 2012.
80. Zhang Y, Liao S, Yang M, Liang X, Poon MW, Wong CY, Wang J, Zhou Z, Cheong SK, Lee CN, et al. Improved cell survival and paracrine capacity of human embryonic stem cell-derived mesenchymal stem cells promote therapeutic potential for pulmonary arterial hypertension. Cell Transplant 21: 2225-2239, 2012.
81. Zhou Y, Xu H, Xu W, Wang B, Wu H, Tao Y, Zhang B, Wang M, Mao F, Yan Y, et al. Exosomes released by human umbilical cord mesenchymal stem cells protect against cisplatin-induced renal oxidative stress and apoptosis in vivo and in vitro. Stem Cell Res Ther 4: 34, 2013.
82. Zhou YF, Bosch-Marce M, Okuyama H, Krishnamachary B, Kimura H, Zhang L, Huso DL, and Semenza GL. Spontaneous transformation of cultured mouse bone marrowderived stromal cells. Cancer Res 66: 10849-10854, 2006.
83. Zhu JH, Wang XX, Zhang FR, Shang YP, Tao QM, and Chen JZ. Safety and efficacy of autologous endothelial progenitor cells transplantation in children with idiopathic pulmonary arterial hypertension: open-label pilot study. Pediatr Transplant 12: 650-655, 2008