Allo-reactivity of mesenchymal stem cells in rhesus macaques is dose and haplotype dependent and limits durable cell engraftment in vivo

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Isakova, Iryna A ^a   Lanclos, Calvin ^b   Bruhn, Julie ^b   Kuroda, Marcelo J ^b   Baker, Kate C ^b   Krishnappa, Veena ^c   Phinney, Donald G ^c  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ALLOGENEIC STEM CELL TRANSPLANTATION; ALLOIMMUNITY; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOLOGOUS STEM CELL TRANSPLANTATION; B LYMPHOCYTE; CELL EXPANSION; CONTROLLED STUDY; DONOR SELECTION; FEMALE; HAPLOTYPE; IMMUNE RESPONSE; IN VIVO STUDY; LYMPHOCYTE COUNT; MOTOR PERFORMANCE; NEUTROPHIL COUNT; NONHUMAN; OUTCOME ASSESSMENT; POSTOPERATIVE PERIOD; REAL TIME POLYMERASE CHAIN REACTION; RHESUS MONKEY; SOCIAL INTERACTION; T LYMPHOCYTE; TEMPERAMENT;

ANIMALS; B-LYMPHOCYTES; CELL PROLIFERATION; FEMALE; GRAFT SURVIVAL; HAPLOTYPES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; KILLER CELLS, NATURAL; LYMPH NODES; LYMPHOCYTE COUNT; MACACA MULATTA; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; NATURAL KILLER T-CELLS; NEUTROPHILS; TRANSPLANTATION, HOMOLOGOUS;

EID: 84900335160     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087238     Document Type: Article

References (54)

1. Phinney DG, Prockop DJ (2007) Concise review: mesenchymal stem/multipotent stromal cells: the state of transdifferentiation and modes of tissue repair - current views. Stem Cells 25: 2896-2902 (Pubitemid 350127874)
2. Tolar J, Le Blanc K, Keating A, Blazar BR (2010) Concise review: hitting the right spot with mesenchymal stromal cells. Stem Cells 28: 1446-1455.
3. Ren G, Zhang L, Zhao X, Xu G, Zhang Y, et al. (2008) Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2: 141-150. (Pubitemid 351181031)
4. Giuliani M., Fleury M, Vernochet A, Ketroussi F, Clay D, et al. (2011) Long-lasting inhibitory effects of fetal liver mesenchymal stem cells on T-lymphocyte proliferation. PLoS One 6: e19988.
5. Selmani Z, Naji A, Zidi I, Favier B, Gaiffe E, et al. (2008) Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+CD25high-FOXP3+ regulatory T cells. Stem Cells 26: 212-222.
6. Ghannam S, Pene J, Torcy-Moquet G, Jorgensen C, Yssel H (2010) Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. J Immunol 185: 302-312.
7. Chiesa S, Morbelli S, Morando S, Massollo M, Marini C, et al. (2011) Mesenchymal stem cells impair in vivo T-cell priming by dendritic cells. Proc Natl Acad Sci USA 108: 17384-17389.
8. Brandau S, Jakob M, Hemeda H, Bruderek K, Janeschik S, et al. (2010) Tissue-resident mesenchymal stem cells attract peripheral blood neutrophils and enhance their inflammatory activity in response to microbial challenge. J Leukoc Biol 88: 1005-1015.
9. Spaggiari GM, Capobianco A, Abdelrazik H, Becchetti F, Mingari MC, et al. (2008) Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood 111: 1327-1333. (Pubitemid 351213419)
10. Eliopoulos N, Stagg J, Lejeune L, Pommey S, Galipeau J. (2005) Allogeneic marrow stromal cells are immune rejected by MHC class I-and class II-mismatched recipient mice. Blood 106: 4057-4065. (Pubitemid 41775910)
11. Sudres M, Norol F, Trenado A, Gregoire S, Charlotte F, et al. (2006) Bone marrow mesenchymal stem cells suppress lymphocyte proliferation in vitro but fail to prevent graft-versus-host disease in mice. J Immunol 176: 7761-7767. (Pubitemid 43849077)
12. Camp D, Loeffler D, Farrah D, Boreneman JN, LeWitt PA (2009) Cellular immune response to intrastriatally implanted allogeneic bone marrow stromal cells in a rat model of Parkinson's disease. J Neuroinflammation 6: 17.
13. Rossignol J, Boyer C, Thinard R, Remy S, Dugast AS, et al. (2009) Mesenchymal stem cells induce a weak immune response in the rat striatum after allo or xeno-transplantation. J Cell Mol Med 13: 2547-5458.
14. Poncelet AJ, Vercruysse J, Saliez A, Gianello P (2007) Although pig allogeneic mesenchymal stem cells are not immunogenic in vitro, intra-cardiac injection elicits an immune response in vivo. Transplantation 83: 783-790. (Pubitemid 46569198)
15. Beggs KJ, Lyubimov A, Borneman JN, Bartholomew A, Moseley A, et al. (2006) Immunologic consequences of multiple, high-dose administration of allogeneic mesenchymal stem cells to baboons. Cell Transplant 15: 711-721. (Pubitemid 46095254)
16. Isakova IA, Dufour J, Lanclos C, Bruhn J, Phinney DG (2010) Cell dose dependent increases in circulating levels of immune effector cells in rhesus macaques following intra-cranial injection of allogeneic MSCs. Expt Hematol 38: 957-967.
17. Zangi L, Margalit R, Reich-Zeliger S, Bachar-Lusting E, Beilhack A, et al. (2009) Direct imaging of immune rejection and memory induction by allogeneic mesenchymal stromal cells. Stem Cells 27: 2865-2874.
18. Renner P, Eggenhofer E, Rosenauer A, Popp FC, Steinmann JF, et al. (2009) Mesenchymal stem cells require a sufficient, ongoing immune response to exert their immunosuppressive function. Transplant Proc 41: 2607-2611.
19. Seifert M, Stolk M, Polenz D, Volk HD (2010) Detrimental effects of rat mesenchymal stromal cell pretreatment in a model of acute kidney rejection. Front Immunol 3: 202.
20. Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O (2003) Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 57: 11-20. (Pubitemid 38019084)
21. Najar M, Rouas R, Raicevic G, Boufker HI, Lewalle P, et al. (2009) Mesenchymal stromal cells promote or suppress the proliferation of T lymphocytes from cord blood and peripheral blood: the importance of low cell ratio and role of interleukin-6. Cytotherapy 11: 570-583.
22. Le Blanc K, Frassoni F, Ball L, Locatelli F, Roelofs H, et al. (2008) Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371: 1579-1586. (Pubitemid 351626841)
23. von Bahr L, Sundberg B, Lonnies L, Sander B, Karbach H, et al. (2012) Long-term complications, immunological effects, and role of passage for outcome in mesenchymal stromal cell therapy. Biol Blood Marrow Transplant 18: 557-564.
24. Isakova IA, Baker K, Dufour J, Gaupp D, Phinney DG (2006) Preclinical evaluation of adult stem cell engraftment and toxicity in the CNS of rhesus macaques. Mol Ther 13: 1173-1184. (Pubitemid 43796155)
25. Isakova IA, Baker K, Dutreil M, Dufour J, Gaupp D, et al. (2007) Age- and dose-related effects on MSC engraftment levels and anatomical distribution in the central nervous system of non-human primates: identification of novel MSC subpopulations that respond to guidance cues in the brain. Stem Cells 25: 3261-3270. (Pubitemid 350294452)
26. Gabriel C, Danzer M, Hackl C, Kopal G, Hufnagl P, et al. (2009) Rapid high-throughput human leukocyte antigen typing by massively parallel pyrosequencing for high-resolution allele identification. Hum Immunol 70: 960-964.
27. Brazelton TB (1973) Neonatal behavioral assessment scale. Clinics in Developmental Medicine, No. 50. Philadelphia: William Heinemann Medical Books.
28. Giavedoni LD, Velasquillo MC, Parodi LM, Hubbard GB, Hodara VL (2000) Cytokine expression, natural killer cell activation, and phenotypic changes in lymphoid cells from rhesus macaques during acute infection with pathogenic simian immunodeficiency virus. J Virol 74: 1648-1657. (Pubitemid 30434020)
29. Webster RL, Johnson RP (2005) Delineation of multiple subpopulations of natural killer cells in rhesus macaques. Immunology 115: 206-214. (Pubitemid 40733406)
30. - natural killer cells: enrichment in mucosal and secondary lymphoid tissues and altered function during chronic SIV infection. Blood 115: 4439-4446.
31. Autissier P, Soulas C, Burdo TH, Williams KC (2010) Immuno-phenotyping of lymphocyte, monocyte, and dendritic cell subsets in normal rhesus macaques by 12-color flow cytometry: clarification on DC heterogeneity. J Immunol Methods 360: 119-128.
32. Liang J, Zhang H, Hua B, Wang H, Lu L, et al. (2010) Allogenic mesenchymal stem cells transplantation in refractory systemic lupus erythematosus: a pilot clinical study. Ann Rheum Dis 69: 1423-1429.
33. Hare JM, Fishman JE, Gerstenblith G, DeFede Velazquez DL, Zambrano JP, et al. (2012) 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 308: 2369-2379.
34. Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, et al. (2000) The neutrophil as a cellular source of chemokines. Immunol Rev 177: 195-203.
35. Ibata M, Takahashi T, Shimizu T, Inoue Y, Maeda S, et al. (2011) Spontaneous rejection of intradermally transplanted non-engineered tumor cells by neutrophils and macrophages from syngenic strains of mice. Microbiol Immunol 55: 726-735.
36. Carbone E, Ruggiero G, Terrazzano G, Palomba C, Manzo C, et al. (1997) A new mechanism of NK cell cytotoxicity activation: the CD40-CD40 ligand interaction. J Exp Med 185: 2053-2060. (Pubitemid 27265988)
37. Nolan CR, Saenz KP, Thomas CA 3rd, Murphy KD (1995) Role of eosinophils in chronic vascular rejection of renal allografts. Am J Kidney Dis 26: 634-642.
38. Llano M, Lee N, Navarro F, Garcia P, Albar JP, et al. (1998) HLA-E bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G derived nonamer. Eur J Immunol 28: 2854-2863. (Pubitemid 28425243)
39. Bryceson YT, March ME, Ljunggren HG, Long EO (2005) Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 107: 159-166.
40. Spaggiari GM, Capobianco A, Becchetti F, Mingari MC, Moretta L (2006) Mesenchymal stem cells-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 107: 1484-1490. (Pubitemid 43242385)
41. Boyiadzis M, Memon S, Carson J, Allen K, Szczepanski MJ, et al. (2008) Upregulation of NK cell activating receptors following allogeneic hematopoietic stem cell transplantation under a lymphodepleting reduced intensity regimen is associated with elevated IL-15 levels. Biol Blood Marrow Transplant 14: 290-300. (Pubitemid 351218196)
42. Otting N, Heijmans CM, Noort RC, de Groot NG, Doxiadis GG, et al. (2005) Unparalleled complexity of the MHC class I region in rhesus macaques. Proc Natl Acad Sci USA 102: 1626-1631. (Pubitemid 40209218)
43. Zehr KJ, Herskowitz A, Lee PC, Poston RS, Gillinov AM, et al. (1993) Neutrophil adhesion inhibition prolongs survival of cardiac allografts with hyperacute rejection. J Heart Lung Transplant 12: 837-844.
44. El-Sawy T, Fairchild R (2005) Inhibition of polymorphonuclear leukocyte-mediated graft damage synergizes with short-term co-stimulatory blockade to prevent cardiac allograft rejection. Circulation 112: 320-331. (Pubitemid 41022072)
45. Grabie N, Hsieh DT, Buono C, Westrich JR, Allen JA, et al. (2003) Neutrophils sustain pathogenic CD8+ T cell responses in heart. Am J Pathol 163: 2413-2420. (Pubitemid 37466482)
46. Hirayama S, Shiraishi T, Shirakusa T, Higuchi T, Miller EJ (2006) Prevention of neutrophil migration ameliorates rat lung allograft rejection. Mol Med 12: 208-213. (Pubitemid 44925019)
47. Kreisel D, Sugimoto S, Zhu J, Nava R, Li W, et al. (2011) Emergency granulopioesis promotes neutrophil-dendritic cell encounters that prevent mouse lung allograft acceptance. Blood 118: 6172-6182.
48. Kirsner RS, Marston WA, Snyder RJ, Lee TD, Cargill DI, et al. (2012) Spray-applied cell therapy with human allogeneic fibroblasts and keratinocytes for the treatment of chronic venous leg ulcers: a phase 2, multicentre, double-blind, randomized, placebo-controlled trial. Lancet 380: 977-985.
49. Liang J, Li X, Zhang H, Wang D, Feng X, et al. (2012) Allogeneic mesenchymal stem cells transplantation in patients with refractory RA. Clin Rheumatol 31: 157-161.
50. Huang XP, Sun Z, Miyagi Y, McDonald Kinkaid H, Zhang L, et al. (2010) Differentiation of allogeneic mesenchymal stem cells induces immunogenicity and limits their long-term benefits for myocardial repair. Circulation 122: 2419-2429.
51. Steinbrink K, Mahnke K, Grabbe S, Enk AH, Jonuleit H (2009) Myeloid dendritic cell: From sentinel of immunity to key player of peripheral tolerance? Human Immunology 70: 289-293.
52. Hickey WF (2001) Basic principles of immunological surveillance of the normal central nervous system. Glia 36: 118-124.
53. Engelhardt B (2008) The blood-central nervous system barriers actively control immune cell entry into the central nervous system. Curr Pharm Des 14: 1555-1565.
54. Becher B, Prat A, Antel JP (2000) Brain-Immune Connection: immunoregulatory properties of CNS-resident cells. Glia 29: 293-304. (Pubitemid 30121420)