Mesenchymal stem cells express serine protease inhibitor to evade the host immune response

Blood

Volumn 117, Issue 4, 2011, Pages 1176-1183

  El Haddad, Najib ^a   Heathcote, Dean ^b   Moore, Robert ^a   Yang, Sunmi ^a   Azzi, Jamil ^a   Mfarrej, Bechara ^a   Atkinson, Mark ^c   Sayegh, Mohamed H ^a   Lee, Jeng Shin ^a   Ashton Rickardt, Philip G ^b   Abdi, Reza ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANZYME B; SERINE PROTEINASE INHIBITOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ENZYME INHIBITION; IMMUNE RESPONSE; IMMUNOSURVEILLANCE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; WILD TYPE;

EID: 79251590238     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-06-287979     Document Type: Article

References (40)

1. Granero-Molto F, Weis JA, Longobardi L, Spagnoli A. Role of mesenchymal stem cells in regenerative medicine: application to bone and cartilage repair. Expert Opin Biol Ther. 2008;8(3):255-268. (Pubitemid 351428415)
2. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease. Nat Rev Immunol. 2008;8(9):726-736.
3. Augello A, Tasso R, Negrini SM, Cancedda R, Pennesi G. Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis Rheum. 2007;56(4):1175-1186. (Pubitemid 46608642)
4. Fiorina P, Jurewicz M, Augello A, et al. Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes. J Immunol. 2009;183(2):993-1004.
5. Tyndall A, Houssiau FA. Mesenchymal stem cells in the treatment of autoimmune diseases. Ann Rheum Dis. 2010;69(8):1413-1414.
6. Ryan JM, Barry FP, Murphy JM, Mahon BP. Mesenchymal stem cells avoid allogeneic rejection. J Inflamm (Lond). 2005;2:8.
7. Rasmusson I, Uhlin M, Le Blanc K, Levitsky V. Mesenchymal stem cells fail to trigger effector functions of cytotoxic T lymphocytes. J Leukoc Biol. 2007;82(4):887-893. (Pubitemid 47511049)
8. Abdi R, Fiorina P, Adra CN, Atkinson M, Sayegh MH. Immunomodulation by mesenchymal stem cells: a potential therapeutic strategy for type 1 diabetes. Diabetes. 2008;57(7):1759-1767.
9. 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(8):1208-1213. (Pubitemid 37339646)
10. Nauta AJ, Westerhuis G, Kruisselbrink AB, Lurvink EG, Willemze R, Fibbe WE. Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood. 2006;108(6):2114-2120. (Pubitemid 44395028)
11. Le Blanc K, Pittenger M. Mesenchymal stem cells: progress toward promise. Cytotherapy. 2005;7(1):36-45.
12. Rasmusson I. Immune modulation by mesenchymal stem cells. Exp Cell Res. 2006;312(12):2169-2179.
13. Parekkadan B, Milwid JM. Mesenchymal stem cells as therapeutics. Annu Rev Biomed Eng. 2010;12:87-117.
14. Shresta S, Heusel JW, Macivor DM, Wesselschmidt RL, Russell JH, Ley TJ. Granzyme B plays a critical role in cytotoxic lymphocyte-induced apoptosis. Immunol Rev. 1995;146:211-221.
15. Cullen SP, Martin SJ. Mechanisms of granule-dependent killing. Cell Death Differ. 2008;15(2):251-262.
16. Adrain C, Murphy BM, Martin SJ. Molecular ordering of the caspase activation cascade initiated by the cytotoxic T lymphocyte/natural killer (CTL/NK) protease granzyme B. J Biol Chem. 2005;280(6):4663-4673.
17. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 1998;94(4):481-490. (Pubitemid 28391864)
18. Hirst CE, Buzza MS, Bird CH, et al. The intracellular granzyme B inhibitor, proteinase inhibitor 9, is up-regulated during accessory cell maturation and effector cell degranulation, and its overexpression enhances CTL potency. J Immunol. 2003;170(2):805-815.
19. Stout-Delgado HW, Getachew Y, Rogers TE, Miller BC, Thiele DL. The role of serpinb9/serine protease inhibitor 6 in preventing granzyme B-dependent hepatotoxicity. Hepatology. 2007;46(5):1530-1540.
20. Sun J, Bird CH, Sutton V, et al. A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. J Biol Chem. 1996;271(44):27802-27809.
21. Bladergroen BA, Strik MC, Bovenschen N, et al. The granzyme B inhibitor, protease inhibitor 9, is mainly expressed by dendritic cells and at immune-privileged sites. J Immunol. 2001;166(5):3218-3225. (Pubitemid 33117320)
22. Zhang M, Park SM, Wang Y, et al. Serine protease inhibitor 6 protects cytotoxic T cells from self-inflicted injury by ensuring the integrity of cytotoxic granules. Immunity. 2006;24(4):451-461.
23. Medema JP, de Jong J, Peltenburg LT, et al. Blockade of the granzyme B/perforin pathway through overexpression of the serine protease inhibitor PI-9/SPI-6 constitutes a mechanism for immune escape by tumors. Proc Natl Acad Sci U S A. 2001;98(20):11515-11520.
24. Wang XM, Terasaki PI, Rankin GW Jr, Chia D, Zhong HP, Hardy S. A new microcellular cytotoxicity test based on calcein AM release. Hum Immunol. 1993;37(4):264-270.
25. Bernardo ME, Locatelli F, Fibbe WE. Mesenchymal stromal cells. Ann N Y Acad Sci. 1176:101-117.
26. Charbord P. Bone marrow mesenchymal stem cells: historical overview and concepts. Hum Gene Ther. 2010;21(9):1045-1056.
27. Sun S, Guo Z, Xiao X, et al. Isolation of mouse marrow mesenchymal progenitors by a novel and reliable method. Stem Cells. 2003;21(5):527-535.
28. Ohishi M, Schipani E. Bone marrow mesenchymal cells. J Cell Biochem. 2010;109(2):277-282.
29. Papadopoulos NG, Dedoussis GV, Spanakos G, Gritzapis AD, Baxevanis CN, Papamichail M. An improved fluorescence assay for the determination of lymphocyte-mediated cytotoxicity using flow cytometry. J Immunol Methods. 1994;177(1-2):101-111.
30. Phillips T, Opferman JT, Shah R, Liu N, Froelich CJ, Ashton-Rickardt PG. A role for the granzyme B inhibitor serine protease inhibitor 6 in CD8+ memory cell homeostasis. J Immunol. 2004;173(6):3801-3809. (Pubitemid 39280742)
31. Greiner DL, Hesselton RA, Shultz LD. SCID mouse models of human stem cell engraftment. Stem Cells. 1998;16(3):166-177.
32. Christianson GJ, Brooks W, Vekasi S, et al. Beta 2-microglobulin- deficient mice are protected from hypergammaglobulinemia and have defective antibody responses because of increased IgG catabolism. J Immunol. 1997;159(10):4781-4792.
33. Sadan O, Melamed E, Offen D. Bone-marrow-derived mesenchymal stem cell therapy for neurodegenerative diseases. Expert Opin Biol Ther. 2009;9(12):1487-1497.
34. Paczesny S, Choi SW, Ferrara JL. Acute graft-versus-host disease: new treatment strategies. Curr Opin Hematol. 2009;16(6):427-436.
35. De Bari C, Dell'accio F. Mesenchymal stem cells in rheumatology: a regenerative approach to joint repair. Clin Sci (Lond). 2007;113(8):339-348. (Pubitemid 47572274)
36. Jones BJ, McTaggart SJ. Immunosuppression by mesenchymal stromal cells: from culture to clinic. Exp Hematol. 2008;36(6):733-741.
37. Sayegh MH, Turka LA. The role of T-cell costimulatory activation pathways in transplant rejection. N Engl J Med. 1998;338(25):1813-1821.
38. Pistoia V, Raffaghello L. Potential of mesenchymal stem cells for the therapy of autoimmune diseases. Expert Rev Clin Immunol. 2010;6(2):211-218.
39. Sun J, Ooms L, Bird CH, Sutton VR, Trapani JA, Bird PI. A new family of 10 murine ovalbumin serpins includes two homologs of proteinase inhibitor 8 and two homologs of the granzyme B inhibitor (proteinase inhibitor 9). J Biol Chem. 1997;272(24):15434-15441.
40. Tseng HC, Arasteh A, Paranjpe A, et al. Increased lysis of stem cells but not their differentiated cells by natural killer cells: de-differentiation or reprogramming activates NK cells. PLoS One. 2010;5(7):e11590.