A proinflammatory secretome mediates the impaired immunopotency of human mesenchymal stromal cells in elderly patients with atherosclerosis

Stem Cells Translational Medicine

Volumn 6, Issue 4, 2017, Pages 1132-1140

  Mancini, Özge Kizilay ^a,b   Lora, Maximilien ^a,b   Shum Tim, Dominique ^b   Nadeau, Stephanie ^c,d   Rodier, Francis ^c,d   Colmegna, Inés ^a,b  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c Institut du Cancer de Montreal   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Aging; Atherosclerosis; Immunopotency; Mesenchymal stromal cells

Indexed keywords

INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; MACROPHAGE MIGRATION INHIBITION FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE;

ADULT; AGED; AGING; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL ISOLATION; CELL VIABILITY; CONTROLLED STUDY; CORONARY ARTERY BYPASS GRAFT; CYTOKINE PRODUCTION; DNA DAMAGE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOMODULATION; IMMUNOPHENOTYPING; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; LYMPHOCYTE PROLIFERATION; MESENCHYMAL STROMA CELL; PERICARDIAL FAT; PERIPHERAL BLOOD MONONUCLEAR CELL; SUBCUTANEOUS FAT; T LYMPHOCYTE ACTIVATION; CELL CULTURE; COCULTURE; CYTOLOGY; IMMUNOLOGY; MESENCHYMAL STEM CELL; METABOLISM; MIDDLE AGED;

ADULT; AGED; ATHEROSCLEROSIS; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CHEMOKINE CCL2; COCULTURE TECHNIQUES; HUMANS; INTERLEUKIN-6; INTERLEUKIN-8; MESENCHYMAL STEM CELLS; MIDDLE AGED;

EID: 85017554643     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.1002/sctm.16-0221     Document Type: Article

References (50)

1. Herrington W, Lacey B, Sherliker P et al. Epidemiology of atherosclerosis and the potential to reduce the global burden of athe-rothrombotic disease. Circ Res 2016;118: 535–546.
2. Schaftenaar F, Frodermann V, Kuiper J et al. Atherosclerosis: The interplay between lipids and immune cells. Curr Opin Lipidol 2016;27:209– 215.
3. Liuzzo G, Goronzy JJ, Yang H et al. Monoclonal T-cell proliferation and plaque instability in acute coronary syndromes. Circulation 2000;101:2883–2888.
4. Kita T, Yamashita T, Sasaki N et al. Regression of atherosclerosis with anti-CD3 antibody via augmenting a regulatory T-cell response in mice. Cardiovasc Res 2014;102:107–117.
5. Emeson EE, Shen ML, Bell CG et al. Inhibition of atherosclerosis in CD4 T-cell-ablated and nude (nu/nu) C57BL/6 hyperlipidemic mice. Am J Pathol 1996;149:675–685.
6. Zhao N, Dong Q, Qian C et al. Lovastatin blocks Kv1.3 channel in human T cells: a new mechanism to explain its immunomodulatory properties. Sci Rep 2015;5:17381
7. Rodriguez-Perea AL, Montoya CJ, Olek S et al. Statins increase the frequency of circulating CD41 FOXP31 regulatory T cells in healthy individuals. J Immunol Res 2015;2015: 762506.
8. Moreira DM, da Silva RL, Vieira JL et al. Role of vascular inflammation in coronary artery disease: Potential of anti-inflammatory drugs in the prevention of atherothrombosis. Inflammation and anti-inflammatory drugs in coronary artery disease. Am J Cardiovasc Drugs 2015;15:1–11.
9. Everett BM, Pradhan AD, Solomon DH et al. Rationale and design of the Cardiovascular Inflammation Reduction Trial: A test of the inflammatory hypothesis of atherothrombosis. Am Heart J 2013;166:199–207 e115.
10. Mangi AA, Noiseux N, Kong D et al. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med 2003;9:1195–1201.
11. Atsma DE, Fibbe WE, Rabelink TJ. Opportunities and challenges for mesenchymal stem cell-mediated heart repair. Curr Opin Lipidol 2007;18:645–649.
12. Barbash IM, Chouraqui P, Baron J et al. Systemic delivery of bone marrow-derived mesenchymal stem cells to the infarcted myocardium: Feasibility, cell migration, and body distribution. Circulation 2003;108:863–868.
13. Amado LC, Saliaris AP, Schuleri KH et al. Cardiac repair with intramyocardial injection of allogeneic mesenchymal stem cells after myocardial infarction. Proc Natl Acad Sci USA 2005; 102:11474–11479.
14. Bartholomew A, Sturgeon C, Siatskas M et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 2002;30: 42–48.
15. Reinders ME, de Fijter JW, Roelofs H et al. Autologous bone marrow-derived mesenchymal stromal cells for the treatment of allograft rejection after renal transplantation: Results of a phase I study. STEM CELLS TRANSL MED 2013;2:107–111.
16. Zappia E, Casazza S, Pedemonte E et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005;106:1755–1761.
17. Augello A, Tasso R, Negrini SM et al. Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis Rheum 2007;56:1175–1186.
18. Fan H, Zhao G, Liu L et al. Pre-treatment with IL-1beta enhances the efficacy of MSC transplantation in DSS-induced colitis. Cell Mol Immunol 2012;9:473–481.
19. Frodermann V, van Duijn J, van Pel M et al. Mesenchymal stem cells reduce murine atherosclerosis development. Sci Rep 2015;5: 15559.
20. Kizilay Mancini O, Shum-Tim D, Stochaj U et al. Age, atherosclerosis and type 2 diabetes reduce human mesenchymal stromal cell-mediated T-cell suppression. Stem Cell Res Ther 2015;6:140.
21. Wu LW, Wang YL, Christensen JM et al. Donor age negatively affects the immunoregu-latory properties of both adipose and bone marrow derived mesenchymal stem cells. Transpl Immunol 2014;30:122–127.
22. Ankrum JA, Ong JF, Karp JM. Mesenchymal stem cells: Immune evasive, not immune privileged. Nat Biotechnol 2014;32:252–260.
23. Bernacki SH, Wall ME, Loboa EG. Isolation of human mesenchymal stem cells from bone and adipose tissue. Methods Cell Biol 2008;86:257–278.
24. Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006;8:315–317.
25. Trickett A, and Kwan YL. T cell stimulation and expansion using anti-CD3/CD28 beads. J Immunol Methods 2003;275:251– 255.
26. Kronsteiner B, Wolbank S, Peterbauer A et al. Human mesenchymal stem cells from adipose tissue and amnion influence T-cells depending on stimulation method and presence of other immune cells. Stem Cells Dev 2011;20:2115–2126.
27. Roederer M. Interpretation of cellular proliferation data: Avoid the panglossian. Cytometry A 2011;79:95–101.
28. Klopp AH, Spaeth EL, Dembinski JL et al. Tumor irradiation increases the recruitment of circulating mesenchymal stem cells into the tumor microenvironment. Cancer Res 2007;67:11687–11695.
29. Fischer-Valuck BW, Barrilleaux BL, Phinney DG et al. Migratory response of mesenchymal stem cells to macrophage migration inhibitory factor and its antagonist as a function of colony-forming efficiency. Biotechnol Lett 2010;32:19–27.
30. Garcia J, Wright K, Roberts S et al. Characterisation of synovial fluid and infrapatellar fat pad derived mesenchymal stromal cells: The influence of tissue source and inflammatory stimulus. Sci Rep 2016;6:24295.
31. Mattar P, Bieback K. Comparing the immunomodulatory properties of bone marrow, adipose tissue, and birth-associated tissue mesenchymal stromal cells. Front Immunol 2015;6:560.
32. Houtgraaf JH, den Dekker WK, van Dalen BM et al. First experience in humans using adipose tissue-derived regenerative cells in the treatment of patients with ST-segment elevation myocardial infarction. J Am Coll Cardiol 2012;59:539–540.
33. Perin EC, Sanz-Ruiz R, Sanchez PL et al. Adipose-derived regenerative cells in patients with ischemic cardiomyopathy: The PRECISE Trial. Am Heart J 2014;168:88–95 e82.
34. O’Hagan-Wong K, Nadeau S, Carrier-Leclerc A et al. Increased IL-6 secretion by aged human mesenchymal stromal cells disrupts hematopoietic stem and progenitor cells’ homeostasis. Oncotarget 2016;7:13285– 13296.
35. Rodier F, Coppe JP, Patil CK et al. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol 2009;11:973–979.
36. Akiyama K, Chen C, Wang D et al. Mes-enchymal-stem-cell-induced immunoregulation involves FAS-ligand-/FAS-mediated T cell apoptosis. Cell Stem Cell 2012;10:544–555.
37. Bernadotte A, Mikhelson VM, Spivak IM. Markers of cellular senescence. Telomere shortening as a marker of cellular senescence. Aging (Albany NY) 2016;8:3–11.
38. Coppe JP, Patil CK, Rodier F et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 2008;6:2853–2868.
39. Rogakou EP, Pilch DR, Orr AH et al. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998;273:5858–5868.
40. Ranganath SH, Levy O, Inamdar MS et al. Harnessing the mesenchymal stem cell secretome for the treatment of cardiovascular disease. Cell Stem Cell 2012;10:244–258.
41. Arendt, B.K., A. Velazquez-Dones, R.C. Tschumper, et al., Interleukin 6 induces monocyte chemoattractant protein-1 expression in myeloma cells. Leukemia 2002; 16(10): 2142–2147.
42. Galipeau J. The mesenchymal stromal cells dilemma--does a negative phase III trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road? Cytotherapy, 2013;15:2–8.
43. Rossini A, Frati C, Lagrasta C et al. Human cardiac and bone marrow stromal cells exhibit distinctive properties related to their origin. Cardiovasc Res 2011;89:650–660.
44. Bloom DD, Centanni JM, Bhatia N et al. A reproducible immunopotency assay to measure mesenchymal stromal cell-mediated T-cell suppression. Cytotherapy 2015;17:140–151.
45. Maiellaro K, Taylor WR. The role of the adventitia in vascular inflammation. Cardiovasc Res 2007;75:640–648.
46. Psaltis PJ, Simari RD. Vascular wall progenitor cells in health and disease. Circ Res 2015;116:1392–1412.
47. Hansson GK, Libby P. The immune response in atherosclerosis: A double-edged sword. Nat Rev Immunol 2006; 6:508–519.
48. Ortlepp JR, Vesper K, Mevissen V et al. Chemokine receptor (CCR2) genotype is associated with myocardial infarction and heart failure in patients under 65 years of age. J Mol Med (Berl) 2003;81:363–367.
49. Apostolakis S., Vogiatzi K, Amanatidou V et al. Interleukin 8 and cardiovascular disease. Cardiovasc Res 2009;84:353–360.
50. Danesh J, Kaptoge S, Mann AG et al. Long-term interleukin-6 levels and subsequent risk of coronary heart disease: Two new prospective studies and a systematic review. PLoS Med 2008;5:e78.