In Vivo Interleukin-13-Primed Macrophages Contribute to Reduced Alloantigen-Specific T Cell Activation and Prolong Immunological Survival of Allogeneic Mesenchymal Stem Cell Implants

Stem Cells

Volumn 34, Issue 7, 2016, Pages 1971-1984

  Hoornaert, Chloé J ^a   Luyckx, Evi ^a   Reekmans, Kristien ^a   Dhainaut, Maxime ^b   Guglielmetti, Caroline ^a   Le Blon, Debbie ^a   Dooley, Dearbhaile ^c   Fransen, Erik ^a   Daans, Jasmijn ^a   Verbeeck, Louca ^a   Quarta, Alessandra ^a   De Vocht, Nathalie ^a   Lemmens, Evi ^c   Goossens, Herman ^a   Van der Linden, Annemie ^a   Roobrouck, Valerie D ^d   Verfaillie, Catherine ^d   Hendrix, Sven ^c   Moser, Muriel ^b   Berneman, Zwi N ^a   Ponsaerts, Peter ^a   more..

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c HASSELT UNIVERSITY   (Belgium)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Allogeneic transplantation; Alternative activation; Graft survival; Interleukin 13; Macrophages; Mesenchymal stem cells; T cell activation

Indexed keywords

ALLOANTIGEN; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 2; LENTIVIRUS VECTOR;

ADAPTIVE IMMUNITY; ALLOGENEIC STEM CELL TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ARTICLE; CD8+ T LYMPHOCYTE; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; GRAFT REJECTION; GRAFT SURVIVAL; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOSTIMULATION; IN VIVO STUDY; INNATE IMMUNITY; MACROPHAGE; MACROPHAGE ACTIVATION; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NONHUMAN; PHENOTYPE; T LYMPHOCYTE ACTIVATION;

EID: 84978962365     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2360     Document Type: Article

References (72)

1. Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 1976;4:267–274.
2. Horwitz EM, Prockop DJ, Fitzpatrick LA et al. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 1999;5:309–313.
3. Arinzeh TL, Peter SJ, Archambault MP et al. Allogeneic mesenchymal stem cells regenerate bone in a critical-sized canine segmental defect. J Bone Joint Surg Am 2003;85:1927–1935.
4. Quevedo HC, Hatzistergos KE, Oskouei BN et al. Allogeneic mesenchymal stem cells restore cardiac function in chronic ischemic cardiomyopathy via trilineage differentiating capacity. Proc Natl Acad Sci USA 2009;106:14022–14027.
5. Sun L, Akiyama K, Zhang H et al. Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells 2009;27:1421–1432.
6. Chen FH, Rousche KT, Tuan RS. Technology Insight: Adult stem cells in cartilage regeneration and tissue engineering. Nat Clin Pract Rheum 2006;2:373–382.
7. Cristofanilli M, Harris VK, Zigelbaum A et al. Mesenchymal stem cells enhance the engraftment and myelinating ability of allogeneic oligodendrocyte progenitors in dysmyelinated mice. Stem Cells Dev 2011;20:2065–2076.
8. Uccelli A, Moretta L, Pistoia V. Immunoregulatory function of mesenchymal stem cells. Eur J Immunol 2006;36:2566–2573.
9. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007;110:3499–3506.
10. Casiraghi F, Azzollini N, Cassis P et al. Pretransplant infusion of mesenchymal stem cells prolongs the survival of a semiallogeneic heart transplant through the generation of regulatory T cells. J Immunol 2008;181:3933–3946.
11. Jiang X, Liu C, Hao J et al. CD4+CD25 + regulatory T cells are not required for mesenchymal stem cell function in fully MHC-mismatched mouse cardiac transplantation. Cell Tissue Res 2014;358:503–514.
12. Tan J, Wu W, Xu X et al. Induction therapy with autologous mesenchymal stem cells in living-related kidney transplants: A randomized controlled trial. JAMA 2012;307:1169–1177.
13. Le Blanc K, Frassoni F, Ball L et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: A phase II study. Lancet 2008;371:1579–1586.
14. Connick P, Kolappan M, Crawley C et al. Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: An open-label phase 2a proof-of-concept study. Lancet Neurol 2012;11:150–156.
15. Schwarz EJ, Alexander GM, Prockop DJ et al. Multipotential marrow stromal cells transduced to produce L-DOPA: Engraftment in a rat model of Parkinson disease. Hum Gene Ther 1999;10:2539–2549.
16. Li Y, Chen J, Zhang CL et al. Gliosis and brain remodeling after treatment of stroke in rats with marrow stromal cells. Glia 2005;49:407–417.
17. Ronsyn MW, Daans J, Spaepen G et al. Plasmid-based genetic modification of human bone marrow-derived stromal cells: Analysis of cell survival and transgene expression after transplantation in rat spinal cord. BMC Biotechnol 2007;7:1–17.
18. Caplan AI, Dennis JE. Mesenchymal stem cells as trophic mediators. J Cell Biochem 2006;98:1076–1084.
19. Wu Y, Chen L, Scott PG et al. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 2007;25:2648–2659.
20. Eliopoulos N, Al-Khaldi A, Crosato M et al. A neovascularized organoid derived from retrovirally engineered bone marrow stroma leads to prolonged in vivo systemic delivery of erythropoietin in nonmyeloablated, immunocompetent mice. Gene Ther 2003;10:478–489.
21. Van Damme A, Chuah MK, Dell'accio F et al. Bone marrow mesenchymal cells for haemophilia A gene therapy using retroviral vectors with modified long-terminal repeats. Haemophilia 2003;9:94–103.
22. Lee RH, Pulin AA, Seo MJ et al. Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009;5:54–63.
23. Figueroa FE, Carrión F, Villanueva S et al. Mesenchymal stem cell treatment for autoimmune diseases: A critical review. Biol Res 2012;45:269–277.
24. Ankrum J, Karp JM. Mesenchymal stem cell therapy: Two steps forward, one step back. Trends Mol Med 2010;16:203–209.
25. Ankrum JA, Ong JF, Karp JM. Mesenchymal stem cells: Immune evasive, not immune privileged. Nat Biotechnol 2014;32:252–260.
26. Caplan AI. Why are MSCs therapeutic?. New data: New insight. J Pathol 2009;217:318–324.
27. Shen J, Tsai YT, Dimarco NM et al. Transplantation of mesenchymal stem cells from young donors delays aging in mice. Sci Rep 2011;1:67.
28. Di Nicola M, Carlo-Stella C, Magni M et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002;99:3838–3843.
29. Krampera M, Glennie S, Dyson J et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 2003;101:3722–3729.
30. Beyth S, Borovsky Z, Mevorach D et al. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 2005;105:2214–2219.
31. Djouad F, Plence P, Bony C et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 2003;102:3837–3844.
32. De Vocht N, Praet J, Reekmans K et al. Tackling the physiological barriers for successful mesenchymal stem cell transplantation into the central nervous system. Stem Cell Res Ther 2013;4:101.
33. Zangi L, Margalit R, Reich-Zeliger S et al. Direct imaging of immune rejection and memory induction by allogeneic mesenchymal stromal cells. Stem Cells 2009;27:2865–2874.
34. Eggenhofer E, Benseler V, Kroemer A et al. Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion. Front Immunol 2012;3:297.
35. Harting MT, Jimenez F, Xue H et al. Intravenous mesenchymal stem cell therapy for traumatic brain injury. J Neurosurg 2009;110:1189–1197.
36. Ezquer FE, Ezquer ME, Parrau DB et al. Systemic administration of multipotent mesenchymal stromal cells reverts hyperglycemia and prevents nephropathy in type 1 diabetic mice. Biol Blood Marrow Transplant 2008;14:631–640.
37. Gutierrez-Fernandez M, Rodriguez-Frutos B, Ramos-Cejudo J et al. Effects of intravenous administration of allogenic bone marrow- and adipose tissue-derived mesenchymal stem cells on functional recovery and brain repair markers in experimental ischemic stroke. Stem Cell Res Ther 2013;4:11.
38. Everaert BR, Bergwerf I, De Vocht N et al. Multimodal in vivo imaging reveals limited allograft survival, intrapulmonary cell trapping and minimal evidence for ischemia-directed BMSC homing. BMC Biotechnol 2012;12:93.
39. Quertainmont R, Cantinieaux D, Botman O et al. Mesenchymal stem cell graft improves recovery after spinal cord injury in adult rats through neurotrophic and pro-angiogenic actions. PloS One 2012;7:e39500.
40. Ishikane S, Ohnishi S, Yamahara K et al. Allogeneic injection of fetal membrane-derived mesenchymal stem cells induces therapeutic angiogenesis in a rat model of hind limb ischemia. Stem Cells 2008;26:2625–2633.
41. Chen J, Li Y, Wang L et al. Therapeutic benefit of intravenous administration of bone marrow stromal cells after cerebral ischemia in rats. Stroke 2001;32:1005–1011.
42. Eliopoulos N, Stagg J, Lejeune L et al. Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Blood 2005;106:4057–4065.
43. Nauta AJ, Westerhuis G, Kruisselbrink AB et al. Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting. Blood 2006;108:2114–2120.
44. Sbano P, Cuccia A, Mazzanti B et al. Use of donor bone marrow mesenchymal stem cells for treatment of skin allograft rejection in a preclinical rat model. Arch Dermatol Res 2008;300:115–124.
45. Tambuyzer BR, Bergwerf I, De Vocht N et al. Allogeneic stromal cell implantation in brain tissue leads to robust microglial activation. Immunol Cell Biol 2009;87:267–273.
46. Van Dyken SJ, Locksley RM. Interleukin-4- and interleukin-13-mediated alternatively activated macrophages: Roles in homeostasis and disease. Annu Rev Immunol 2013;31:317–343.
47. Graber P, Gretener D, Herren S et al. The distribution of IL-13 receptor α1 expression on B cells, T cells and monocytes and its regulation by IL-13 and IL-4. Eur J Immunol 1998;28:4286–4298.
48. de Vries JE. The role of IL-13 and its receptor in allergy and inflammatory responses. J Allergy Clin Immunol 102:165–169.
49. Bergwerf I, De Vocht N, Tambuyzer B et al. Reporter gene-expressing bone marrow-derived stromal cells are immune-tolerated following implantation in the central nervous system of syngeneic immunocompetent mice. BMC Biotechnol 2009;9:1.
50. Ibrahimi A, Vande Velde G, Reumers V et al. Highly efficient multicistronic lentiviral vectors with peptide 2A sequences. Hum Gene Ther 2009;20:845–860.
51. Baekelandt V, Eggermont K, Michiels M et al. Optimized lentiviral vector production and purification procedure prevents immune response after transduction of mouse brain. Gene Ther 2003;10:1933–1940.
52. Geraerts M, Michiels M, Baekelandt V et al. Upscaling of lentiviral vector production by tangential flow filtration. J Gene Med 2005;7:1299–1310.
53. Praet J, Santermans E, Reekmans K et al. Histological characterization and quantification of cellular events following neural and fibroblast(-like) stem cell grafting in healthy and demyelinated CNS tissue. In: Christ B, Oerlecke J, Stock P, eds. Animal Models for Stem Cell Therapy. New York: Springer; 2014:265–283.
54. De Vocht N, Lin D, Praet J et al. Quantitative and phenotypic analysis of mesenchymal stromal cell graft survival and recognition by microglia and astrocytes in mouse brain. Immunobiology 2013;218:696–705.
55. Le Blon D, Hoornaert C, Daans J et al. Distinct spatial distribution of microglia and macrophages following mesenchymal stem cell implantation in mouse brain. Immunol Cell Biol 2014;92:650–658.
56. Guglielmetti C, Praet J, Rangarajan JR et al. Multimodal imaging of subventricular zone neural stem/progenitor cells in the cuprizone mouse model reveals increased neurogenic potential for the olfactory bulb pathway, but no contribution to remyelination of the corpus callosum. NeuroImage 2014;86:99–110.
57. Orije J, Kara F, Guglielmetti C et al. Longitudinal monitoring of metabolic alterations in cuprizone mouse model of multiple sclerosis using 1H-magnetic resonance spectroscopy. NeuroImage 2015;114:128–135.
58. Praet J, Orije J, Kara F et al. Cuprizone-induced demyelination and demyelination-associated inflammation result in different proton magnetic resonance metabolite spectra. NMR Biomed 2015;28:505–513.
59. Praet J, Reekmans K, Lin D et al. Cell type-associated differences in migration, survival, and immunogenicity following grafting in CNS tissue. Cell Transplant 2012;21:1867–1881.
60. Mantovani A, Sica A, Sozzani S et al. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 2004;25:677–686.
61. Praet J, Guglielmetti C, Berneman Z et al. Cellular and molecular neuropathology of the cuprizone mouse model: Clinical relevance for multiple sclerosis. Neurosci Biobehav R 2014;47:485–505.
62. Herrera OB, Golshayan D, Tibbott R et al. A novel pathway of alloantigen presentation by dendritic cells. J Immunol 2004;173:4828–4837.
63. Sivanathan KN, Gronthos S, Rojas-Canales D et al. Interferon-gamma modification of mesenchymal stem cells: Implications of autologous and allogeneic mesenchymal stem cell therapy in allotransplantation. Stem Cell Rev 2014;10:351–375.
64. Chan JL, Tang KC, Patel AP et al. Antigen-presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-gamma. Blood 2006;107:4817–4824.
65. Benichou G, Valujskikh A, Heeger PS. Contributions of direct and indirect T cell alloreactivity during allograft rejection in mice. J Immunol 1999;162:352–358.
66. Lee RS, Grusby MJ, Glimcher LH et al. Indirect recognition by helper cells can induce donor-specific cytotoxic T lymphocytes in vivo. J Exp Med 1994;179:865–872.
67. Zecher D, van Rooijen N, Rothstein DM et al. An innate response to allogeneic nonself mediated by monocytes. J Immunol 2009;183:7810–7816.
68. Liu W, Xiao X, Demirci G et al. Innate NK cells and macrophages recognize and reject allogeneic nonself in vivo via different mechanisms. J Immunol 2012;188:2703–2711.
69. Rodriguez PC, Zea AH, DeSalvo J et al. L-arginine consumption by macrophages modulates the expression of CD3 zeta chain in T lymphocytes. J Immunol 2003;171:1232–1239.
70. Bronte V, Serafini P, Mazzoni A et al. L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol 2003;24:301–305.
71. Campeau PM, Rafei M, Francois M et al. Mesenchymal stromal cells engineered to express erythropoietin induce anti-erythropoietin antibodies and anemia in allorecipients. Mol Ther 2009;17:369–372.
72. Lillicrap D, VandenDriessche T, High K. Cellular and genetic therapies for haemophilia. Haemophilia 2006;12 (Suppl 3):36–41.