From single nucleotide polymorphisms to constant immunosuppression: Mesenchymal stem cell therapy for autoimmune diseases

BioMed Research International

Volumn 2013, Issue , 2013, Pages

  Chinnadurai, Raghavan ^a   Waller, Edmund K ^a   Galipeau, Jacques ^a   Nooka, Ajay K ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA DEFENSIN; BORTEZOMIB; CHEMOKINE RECEPTOR CCR6; DEXTRAN SULFATE; INDOLEAMINE 2,3 DIOXYGENASE; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; KYNURENINE; MYELIN; PROSTAGLANDIN E2; T LYMPHOCYTE RECEPTOR; TRYPTOPHAN;

ALLELE; ALLERGIC ENCEPHALOMYELITIS; APOPTOSIS; ARTHRITIS; AUTOCRINE EFFECT; AUTOIMMUNE DISEASE; AUTOPHAGOSOME; AUTOPHAGY; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL FUNCTION; CELLULAR IMMUNITY; COLITIS; CROHN DISEASE; CYTOKINE RELEASE; DISEASE ACTIVITY; DISEASE PREDISPOSITION; ENZYME ACTIVITY; GENE LOCUS; GENETIC ASSOCIATION; GRAVES DISEASE; HELPER CELL; HUMAN; HUMORAL IMMUNITY; HYPERGLYCEMIA; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; IN VITRO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE EPITHELIUM; LIVER REGENERATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMA CELL; MONOCYTE; MULTIPLE SCLEROSIS; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; OUTCOME ASSESSMENT; PANETH CELL; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIMARY BILIARY CIRRHOSIS; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; SCLERODERMA; SENESCENCE; SINGLE NUCLEOTIDE POLYMORPHISM; SJOEGREN SYNDROME; STROMAL CELL FUNCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC SCLEROSIS; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH17 CELL; THERAPY EFFECT; TUMOR MICROENVIRONMENT; UPREGULATION; WHOLE BODY RADIATION; ANIMAL; GENE THERAPY; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; METABOLISM; METHODOLOGY;

ANIMALS; AUTOIMMUNE DISEASES; GENETIC PREDISPOSITION TO DISEASE; GENETIC THERAPY; HUMANS; IMMUNOSUPPRESSION; MESENCHYMAL STROMAL CELLS; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84890070174     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2013/929842     Document Type: Review

References (105)

1. Pittenger M. F., Mackay M. A., Beck S. C., Multilineage potential of adult human mesenchymal stem cells. Science 1999 284 5411 143 147 (Pubitemid 29282067)
2. Francois M., Galipeau J., New insights on translational development of mesenchymal stromal cells for suppressor therapy. Journal of Cell Physiology 2012 227 11 3535 3538 10.1002/jcp.24081
3. Dominici M., Le Blanc K., Mueller I., Slaper-Cortenbach I., Marini F. C., Krause D. S., Deans R. J., Keating A., Prockop D. J., Horwitz E. M., Minimal criteria for defining multipotent mesenchymal stromal cells. the international society for cellular therapy position statement. Cytotherapy 2006 8 4 315 317 2-s2.0-33747713246 10.1080/14653240600855905 (Pubitemid 44269669)
4. Ren G., Chen X., Dong F., Li W., Ren X., Zhang Y., Shi Y., Concise review: mesenchymal stem cells and translational medicine: emerging issues. Stem Cells Translational Medicine 2012 1 1 51 58
5. Uccelli A., Moretta L., Pistoia V., Mesenchymal stem cells in health and disease. Nature Reviews Immunology 2008 8 9 726 736 2-s2.0-50249158511 10.1038/nri2395
6. Abumaree M., Al Jumah M., Pace R. A., Kalionis B., Immunosuppressive properties of mesenchymal stem cells. Stem Cell Reviews 2012 8 2 375 392 10.1007/s12015-011-9312-0
7. Stagg J., Galipeau J., Mechanisms of immune modulation by mesenchymal stromal cells and clinical translation. Current Molecular Medicine 2013 13 5 856 867 10.2174/1566524011313050016
8. English K., Mechanisms of mesenchymal stromal cell immunomodulation. Immunology&Cell Biology 2013 91 1 19 26 10.1038/icb.2012.56
9. Dazzi F., Lopes L., Weng L., Mesenchymal stromal cells: a key player in 'innate tolerance'? Immunology 2012 137 3 206 213
10. Yi T., Song S. U., Immunomodulatory properties of mesenchymal stem cells and their therapeutic applications. Archives of Pharmacal Research 2012 35 2 213 221 10.1007/s12272-012-0202-z
11. De Miguel M. P., Fuentes-Julián S., Blázquez- Martínez A., Immunosuppressive properties of mesenchymal stem cells: advances and applications. Current Molecular Medicine 2012 12 5 574 591
12. Duffy M. M., Ritter T., Ceredig R., Griffin M. D., Mesenchymal stem cell effects on T-cell effector pathways. Stem Cell Research and Therapy 2011 2 4, article 34 2-s2.0-80052451886 10.1186/scrt75
13. Charbord P., Bone marrow mesenchymal stem cells: historical overview and concepts. Human Gene Therapy 2010 21 9 1045 1056 2-s2.0-77957845081 10.1089/hum.2010.115
14. Yagi H., Soto-Gutierrez A., Parekkadan B., Kitagawa Y., Tompkins R. G., Kobayashi N., Yarmush M. L., Mesenchymal stem cells: mechanisms of immunomodulation and homing. Cell Transplantation 2010 19 6 667 679 2-s2.0-77958572322 10.3727/096368910X508762
15. Le Blanc K., Mougiakakos D., Multipotent mesenchymal stromal cells and the innate immune system. Nature Reviews Immunology 2012 12 5 383 396 2-s2.0-84860238652 10.1038/nri3209
16. Visscher P. M., Brown M. A., McCarthy M. I., Yang J., Five years of GWAS discovery. American Journal of Human Genetics 2012 90 1 7 24 2-s2.0-84855861504 10.1016/j.ajhg.2011.11.029
17. Keegan B. M., Noseworthy J. H., Multiple sclerosis. Annual Review of Medicine 2002 53 285 302 2-s2.0-0036187060 10.1146/annurev.med.53.082901.103909 (Pubitemid 34182821)
18. Zappia E., Casazza S., Pedemonte E., Benvenuto F., Bonanni I., Gerdoni E., Giunti D., Ceravolo A., Cazzanti F., Frassoni F., Mancardi G., Uccelli A., Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005 106 5 1755 1761 2-s2.0-23944519424 10.1182/blood-2005-04-1496 (Pubitemid 41208591)
19. Zhang J., Li Y., Chen J., Cui Y., Lu M., Elias S. B., Mitchell J. B., Hammill L., Vanguri P., Chopp M., Human bone marrow stromal cell treatment improves neurological functional recovery in EAE mice. Experimental Neurology 2005 195 1 16 26 2-s2.0-23644458723 10.1016/j.expneurol.2005.03.018 (Pubitemid 41116810)
20. Rafei M., Campeau P. M., Aguilar-Mahecha A., Buchanan M., Williams P., Birman E., Yuan S., Young Y. K., Boivin M.-N., Forner K., Basik M., Galipeau J., Mesenchymal stromal cells ameliorate experimental autoimmune encephalomyelitis by inhibiting CD4 Th17 T cells in a CC chemokine ligand 2-dependent manner. Journal of Immunology 2009 182 10 5994 6002 2-s2.0-70349881103 10.4049/jimmunol.0803962
21. Mallam E., Kemp K., Wilkins A., Rice C., Scolding N., Characterization of in vitro expanded bone marrow-derived mesenchymal stem cells from patients with multiple sclerosis. Multiple Sclerosis 2010 16 8 909 918 2-s2.0-77955159550 10.1177/1352458510371959
22. Mazzanti B., Aldinucci A., Biagioli T., Barilaro A., Urbani S., Dal Pozzo S., Amato M. P., Siracusa G., Crescioli C., Manuelli C., Bosi A., Saccardi R., Massacesi L., Ballerini C., Differences in mesenchymal stem cell cytokine profiles between MS patients and healthy donors: implication for assessment of disease activity and treatment. Journal of Neuroimmunology 2008 199 1-2 142 150 2-s2.0-47549110548 10.1016/j.jneuroim.2008.05.006
23. Connick P., Kolappan M., Crawley C., Webber D. J., Patani R., Michell A. W., Du M.-Q., Luan S.-L., Altmann D. R., Thompson A. J., Compston A., Scott M. A., Miller D. H., Chandran S., Autologous mesenchymal stem cells for the treatment of secondary progressive multiple sclerosis: an open-label phase 2a proof-of-concept study. The Lancet Neurology 2012 11 2 150 156 2-s2.0-84855982886 10.1016/S1474-4422(11)70305-2
24. Karussis D., Karageorgiou C., Vaknin-Dembinsky A., Gowda-Kurkalli B., Gomori J. M., Kassis I., Bulte J. W. M., Petrou P., Ben-Hur T., Abramsky O., Slavin S., Safety and immunological effects of mesenchymal stem cell transplantation in patients with multiple sclerosis and amyotrophic lateral sclerosis. Archives of Neurology 2010 67 10 1187 1194 2-s2.0-77957964299 10.1001/archneurol.2010.248
25. Pravica V., Popadic D., Savic E., Markovic M., Drulovic J., Mostarica-Stojkovic M., Single nucleotide polymorphisms in multiple sclerosis: disease susceptibility and treatment response biomarkers. Immunologic Research 2012 52 1-2 42 52 2-s2.0-84859913275 10.1007/s12026-012-8273-y
26. Ryan J. M., Barry F. P., Murphy J. M., Mahon B. P., Mesenchymal stem cells avoid allogeneic rejection. Journal of Inflammation 2005 2 article 8
27. Romieu-Mourez R., François M., Boivin M.-N., Stagg J., Galipeau J., Regulation of MHC class II expression and antigen processing in murine and human mesenchymal stromal cells by IFN-gamma, TGF-beta, and cell density. Journal of Immunology 2007 179 3 1549 1558 2-s2.0-34548630221
28. Najar M., Raicevic G., Id Boufker H., Stamatopoulos B., De Bruyn C., Meuleman N., Bron D., Toungouz M., Lagneaux L., Modulated expression of adhesion molecules and galectin-1: role during mesenchymal stromal cell immunoregulatory functions. Experimental Hematology 2010 38 10 922 932 2-s2.0-77956617456 10.1016/j.exphem.2010.05.007
29. Kang S. K., Shin I. S., Ko M. S., Jo J. Y., Ra J. C., Journey of mesenchymal stem cells for homing: strategies to enhance efficacy and safety of stem cell therapy. Stem Cells International 2012 2012 11 342968 10.1155/2012/342968
30. Djouad F., Fritz V., Apparailly F., Louis-Plence P., Bony C., Sany J., Jorgensen C., Noël D., Reversal of the immunosuppressive properties of mesenchymal stem cells by tumor necrosis factor alpha in collagen-induced arthritis. Arthritis and Rheumatism 2005 52 5 1595 1603 2-s2.0-18644370435 10.1002/art.21012 (Pubitemid 40663952)
31. Bouffi C., Bony C., Courties G., Jorgensen C., Noël D., IL-6-dependent PGE2 secretion by mesenchymal stem cells inhibits local inflammation in experimental arthritis. PLoS One 2010 5 12 2-s2.0-78650085746 10.1371/journal.pone.0014247 e14247
32. Augello A., Tasso R., Negrini S. M., Cancedda R., Pennesi G., Cell therapy using allogeneic bone marrow mesenchymal stem cells prevents tissue damage in collagen-induced arthritis. Arthritis and Rheumatism 2007 56 4 1175 1186 2-s2.0-34247231682 10.1002/art.22511 (Pubitemid 46608642)
33. Papadopoulou A., Yiangou M., Athanasiou E., Mesenchymal stem cells are conditionally therapeutic in preclinical models of rheumatoid arthritis. Annals of the Rheumatic Diseases 2012 71 10 1733 1740
34. Papadaki H. A., Kritikos H. D., Cemetzi C., Bone marrow progenitor cell reserve and function and stromal cell function are defective in rheumatoid arthritis: evidence for a tumor necrosis factor alpha-mediated effect. Blood 2002 99 5 1610 1619 (Pubitemid 34533033)
35. Bocelli-Tyndall C., Bracci L., Spagnoli G., Braccini A., Bouchenaki M., Ceredig R., Pistoia V., Martin I., Tyndall A., Bone marrow mesenchymal stromal cells (BM-MSCs) from healthy donors and auto-immune disease patients reduce the proliferation of autologous- and allogeneic-stimulated lymphocytes in vitro. Rheumatology 2007 46 3 403 408 2-s2.0-33847386693 10.1093/rheumatology/kel267 (Pubitemid 46344649)
36. Ruyssen-Witrand A., Constantin A., Cambon-Thomsen A., Thomsen M., New insights into the genetics of immune responses in rheumatoid arthritis. Tissue Antigens 2012 80 2 105 118
37. Pricola K. L., Kuhn N. Z., Haleem-Smith H., Song Y., Tuan R. S., Interleukin-6 maintains bone marrow-derived mesenchymal stem cell stemness by an ERK1/2-dependent mechanism. Journal of Cellular Biochemistry 2009 108 3 577 588 2-s2.0-70350150677 10.1002/jcb.22289
38. Francois M., Birman E., Forner K. A., Gaboury L., Galipeau J., Adoptive transfer of mesenchymal stromal cells accelerates intestinal epithelium recovery of irradiated mice in an interleukin-6-dependent manner. Cytotherapy 2012 14 10 1164 1170
39. Ghannam S., Pène J., Torcy-Moquet G., Jorgensen C., Yssel H., Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. Journal of Immunology 2010 185 1 302 312 2-s2.0-77956215701 10.4049/jimmunol.0902007
40. Sun L. Y., Zhang H. Y., Feng X. B., Hou Y. Y., Lu L. W., Fan L. M., Abnormality of bone marrow-derived mesenchymal stem cells in patients with systemic lupus erythematosus. Lupus 2007 16 2 121 128 2-s2.0-33847374613 10.1177/0961203306075793 (Pubitemid 46347934)
41. Nie Y., Lau C. S., Lie A. K. W., Chan G. C. F., Mok M. Y., Defective phenotype of mesenchymal stem cells in patients with systemic lupus erythematosus. Lupus 2010 19 7 850 859 2-s2.0-77952921223 10.1177/ 0961203309361482
42. Carrion F., Nova E., Ruiz C., Autologous mesenchymal stem cell treatment increased T regulatory cells with no effect on disease activity in two systemic erythematosus patients. Lupus 2010 19 3 317 322
43. Pontillo A., Girardelli M., Kamada A. J., Pancotto J. A. T., Donadi E. A., Crovella S., Sandrin-Garcia P., Polimorphisms in inflammasome genes are involved in the predisposition to systemic lupus erythematosus. Autoimmunity 2012 45 4 271 278 2-s2.0-84859861944 10.3109/08916934.2011.637532
44. Xu J., Wang D., Liu D., Allogeneic mesenchymal stem cell treatment alleviates experimental and clinical Sjogren syndrome. Blood 2012 120 15 3142 3151
45. Ice J. A., Li H., Adrianto I., Genetics of Sjogren's syndrome in the genome-wide association era. Journal of Autoimmunity 2012 39 1-2 57 63
46. Cipriani P., Di Benedetto P., Liakouli V., Mesenchymal stem cells (MSCs) from scleroderma patients (SSc) preserve their immunomodulatory properties although senescent and normally induce T regulatory cells (Tregs) with a functional phenotype: implications for cellular-based therapy. Clinical&Experimental Immunology 2013 173 2 195 206
47. Romano E., Manetti M., Guiducci S., Ceccarelli C., Allanore Y., Matucci-Cerinic M., The genetics of systemic sclerosis: an update. Clinical and Experimental Rheumatology 2011 29 2, supplement 65 S75 S86
48. Akiyama K., Chen C., Wang D., Xu X., Qu C., Yamaza T., Cai T., Chen W., Sun L., Shi S., Mesenchymal-stem-cell-induced immunoregulation involves FAS-ligand-/FAS-mediated T cell apoptosis. Cell Stem Cell 2012 10 5 544 555 2-s2.0-84860636948 10.1016/j.stem.2012.03.007
49. Baumgart D. C., Sandborn W. J., Crohn's disease. Lancet 2012 380 9853 1590 1605 10.1016/S0140-6736(12)60026-9
50. Copland I. B., Galipeau J., Death and inflammation following somatic cell transplantation. Seminars in Immunopathology 2011 33 6 535 550 2-s2.0-81855182158 10.1007/s00281-011-0274-8
51. Duijvestein M., Vos A. C. W., Roelofs H., Wildenberg M. E., Wendrich B. B., Verspaget H. W., Kooy-Winkelaar E. M. C., Koning F., Zwaginga J. J., Fidder H. H., Verhaar A. P., Fibbe W. E., Van Den Brink G. R., Hommes D. W., Autologous bone marrow-derived mesenchymal stromal cell treatment for refractory luminal Crohn's disease: results of a phase I study. Gut 2010 59 12 1662 1669 2-s2.0-78649895490 10.1136/gut.2010.215152
52. Ciccocioppo R., Bernardo M. E., Sgarella A., Maccario R., Avanzini M. A., Ubezio C., Minelli A., Alvisi C., Vanoli A., Calliada F., Dionigi P., Perotti C., Locatelli F., Corazza G. R., Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising crohn's disease. Gut 2011 60 6 788 798 2-s2.0-79955853222 10.1136/gut.2010.214841
53. Panés J., Ords I., Ricart E., Stem cell treatment for crohns disease. Expert Review of Clinical Immunology 2010 6 4 597 605 2-s2.0-77954401909 10.1586/eci.10.27
54. Peterson N., Guthery S., Denson L., Lee J., Saeed S., Prahalad S., Biank V., Ehlert R., Tomer G., Greed R., Rudolph C., Kugathasan S., Genetic variants in the autophagy pathway contribute to paediatric crohn's disease. Gut 2008 57 9 1336 1337 2-s2.0-50249133280 10.1136/gut.2008.152207
55. Hampe J., Franke A., Rosenstiel P., Till A., Teuber M., Huse K., Albrecht M., Mayr G., De La Vega F. M., Briggs J., Günther S., Prescott N. J., Onnie C. M., Häsler R., Sipos B., Fölsch U. R., Lengauer T., Platzer M., Mathew C. G., Krawczak M., Schreiber S., A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for crohn disease in ATG16L1. Nature Genetics 2007 39 2 207 211 2-s2.0-33846627302 10.1038/ng1954 (Pubitemid 46184351)
56. Levine B., Mizushima N., Virgin H. W., Autophagy in immunity and inflammation. Nature 2011 469 7330 323 335 2-s2.0-78751672975 10.1038/nature09782
57. Lapaquette P., Brest P., Hofman P., Darfeuille-Michaud A., Etiology of crohn's disease: many roads lead to autophagy. Journal of Molecular Medicine 2012 90 9 987 996
58. Stappenbeck T. S., Rioux J. D., Mizoguchi A., Saitoh T., Huett A., Darfeuille-Michaud A., Wileman T., Mizushima N., Carding S., Akira S., Parkes M., Xavier R. J., Crohn disease: a current perspective on genetics, autophagy and immunity. Autophagy 2011 7 4 355 374 2-s2.0-78650430453 10.4161/auto.7.4. 13074
59. Xavier R. J., Huett A., Rioux J. D., Autophagy as an important process in gut homeostasis and crohn's disease pathogenesis. Gut 2008 57 6 717 720 2-s2.0-44149123849 10.1136/gut.2007.134254 (Pubitemid 351716957)
60. Deretic V., Links between autophagy, innate immunity, inflammation and crohn's disease. Digestive Diseases 2009 27 3 246 251 2-s2.0-70349924078 10.1159/000228557
61. Saitoh T., Fujita N., Jang M. H., Uematsu S., Yang B.-G., Satoh T., Omori H., Noda T., Yamamoto N., Komatsu M., Tanaka K., Kawai T., Tsujimura T., Takeuchi O., Yoshimori T., Akira S., Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 2008 456 7219 264 268 2-s2.0-56249090667 10.1038/nature07383
62. Cadwell K., Liu J. Y., Brown S. L., Miyoshi H., Loh J., Lennerz J. K., Kishi C., Kc W., Carrero J. A., Hunt S., Stone C. D., Brunt E. M., Xavier R. J., Sleckman B. P., Li E., Mizushima N., Stappenbeck T. S., Virgin H. W. IV, A key role for autophagy and the autophagy gene Atg16l1 in mouse and human intestinal paneth cells. Nature 2008 456 7219 259 263 2-s2.0-56249135538 10.1038/nature07416
63. Plantinga T. S., Crisan T. O., Oosting M., Van De Veerdonk F. L., De Jong D. J., Philpott D. J., Van Der Meer J. W. M., Girardin S. E., Joosten L. A. B., Netea M. G., Crohn's disease-associated ATG16L1 polymorphism modulates pro-inflammatory cytokine responses selectively upon activation of NOD2. Gut 2011 60 9 1229 1235 2-s2.0-80051550866 10.1136/gut.2010.228908
64. Sanchez C. G., Penfornis P., Oskowitz A. Z., Boonjindasup A. G., Cai D. Z., Dhule S. S., Rowan B. G., Kelekar A., Krause D. S., Pochampally R. R., Activation of autophagy in mesenchymal stem cells provides tumor stromal support. Carcinogenesis 2011 32 7 964 972 2-s2.0-79960046702 10.1093/carcin/bgr029
65. 4 -injured rat liver model via increased autophagic mechanism. Stem Cells 2013 31 8 1584 1596
66. Dominguez-Bendala J., Lanzoni G., Inverardi L., Ricordi C., Concise review: mesenchymal stem cells for diabetes. Stem Cells Translational Medicine 2012 1 1 59 63
67. Ezquer F. E., Ezquer M. E., Parrau D. B., Carpio D., Yañez A. J., Conget P. A., Systemic administration of multipotent mesenchymal stromal cells reverts hyperglycemia and prevents nephropathy in type 1 diabetic mice. Biology of Blood and Marrow Transplantation 2008 14 6 631 640 2-s2.0-43449112935 10.1016/j.bbmt.2008.01.006
68. Madec A. M., Mallone R., Afonso G., Abou Mrad E., Mesnier A., Eljaafari A., Thivolet C., Mesenchymal stem cells protect NOD mice from diabetes by inducing regulatory T cells. Diabetologia 2009 52 7 1391 1399 2-s2.0-67349224622 10.1007/s00125-009-1374-z
69. Fiorina P., Jurewicz M., Augello A., Vergani A., Dada S., La Rosa S., Selig M., Godwin J., Law K., Placidi C., Smith R. N., Capella C., Rodig S., Adra C. N., Atkinson M., Sayegh M. H., Abdi R., Immunomodulatory function of bone marrow-derived mesenchymal stem cells in experimental autoimmune type 1 diabetes. Journal of Immunology 2009 183 2 993 1004 2-s2.0-70249122431 10.4049/jimmunol.0900803
70. Jurewicz M., Yang S., Augello A., Godwin J. G., Moore R. F., Azzi J., Fiorina P., Atkinson M., Sayegh M. H., Abdi R., Congenic mesenchymal stem cell therapy reverses hyperglycemia in experimental type 1 diabetes. Diabetes 2010 59 12 3139 3147 2-s2.0-78650071907 10.2337/db10-0542
71. Concannon P., Rich S. S., Nepom G. T., Genetics of type 1A diabetes. The New England Journal of Medicine 2009 360 16 1646 1654 2-s2.0-64749116743 10.1056/NEJMra0808284
72. Krampera M., Cosmi L., Angeli R., Pasini A., Liotta F., Andreini A., Santarlasci V., Mazzinghi B., Pizzolo G., Vinante F., Romagnani P., Maggi E., Romagnani S., Annunziato F., Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 2006 24 2 386 398 2-s2.0-33746889097 10.1634/stemcells.2005-0008 (Pubitemid 44464808)
73. Munn D. H., Mellor A. L., Indoleamine 2,3-dioxygenase and tumor-induced tolerance. Journal of Clinical Investigation 2007 117 5 1147 1154 2-s2.0-34248173331 10.1172/JCI31178 (Pubitemid 46718399)
74. François M., Romieu-Mourez R., Li M., Galipeau J., Human MSC suppression correlates with cytokine induction of indoleamine 2,3-dioxygenase and bystander M2 macrophage differentiation. Molecular Therapy 2012 20 1 187 195 2-s2.0-84856960632 10.1038/mt.2011.189
75. Krampera M., Galipeau J., Shi Y., Tarte K., Sensebe L., Immunological characterization of multipotent mesenchymal stromal cells-The International Society for Cellular Therapy (ISCT) working proposal. Cytotherapy 2013 15 9 1054 1061
76. Oertelt-Prigione S., Mao T. K., Selmi C., Tsuneyama K., Ansari A. A., Coppel R. L., Invernizzi P., Podda M., Gershwin M. E., Impaired indoleamine 2,3-dioxygenase production contributes to the development of autoimmunity in primary biliary cirrhosis. Autoimmunity 2008 41 1 92 99 2-s2.0-38049033923 10.1080/08916930701619730
77. Arefayene M., Philips S., Cao D., Mamidipalli S., Desta Z., Flockhart D. A., Wilkes D. S., Skaar T. C., Identification of genetic variants in the human indoleamine 2,3-dioxygenase (IDO1) gene, which have altered enzyme activity. Pharmacogenetics and Genomics 2009 19 6 464 476 2-s2.0-70149116670 10.1097/FPC.0b013e32832c005a
78. + Treg impairment in systemic sclerosis. Human Immunology 2013 74 2 166 169
79. Francisco L. M., Sage P. T., Sharpe A. H., The PD-1 pathway in tolerance and autoimmunity. Immunological Reviews 2010 236 1 219 242 2-s2.0-77953747963 10.1111/j.1600-065X.2010.00923.x
80. Sharpe A. H., Wherry E. J., Ahmed R., Freeman G. J., The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nature Immunology 2007 8 3 239 245 2-s2.0-34247884612 10.1038/ni1443 (Pubitemid 46745373)
81. Greenwald R. J., Freeman G. J., Sharpe A. H., The B7 family revisited. Annual Review of Immunology 2005 23 515 548 2-s2.0-17644425689 10.1146/annurev.immunol.23.021704.115611 (Pubitemid 40563179)
82. Najar M., Raicevic G., Kazan H. F., Immune-related antigens, surface molecules and regulatory factors in human-derived mesenchymal stromal cells: the expression and impact of inflammatory priming. Stem Cell Reviews 2012 8 4 1188 1198
83. Sheng H., Wang Y., Jin Y., Zhang Q., Zhang Y., Wang L., Shen B., Yin S., Liu W., Cui L., Li N., A critical role of IFNgamma in priming MSC-mediated suppression of T cell proliferation through up-regulation of B7-H1. Cell Research 2008 18 8 846 857 2-s2.0-49149120713 10.1038/cr.2008.80
84. Tipnis S., Viswanathan C., Majumdar A. S., Immunosuppressive properties of human umbilical cord-derived mesenchymal stem cells: role of B7-H1 and IDO. Immunology and Cell Biology 2010 88 8 795 806 2-s2.0-78649333063 10.1038/icb.2010.47
85. Ni R., Ihara K., Miyako K., Kuromaru R., Inuo M., Kohno H., Hara T., PD-1 gene haplotype is associated with the development of type 1 diabetes mellitus in Japanese children. Human Genetics 2007 121 2 223 232 2-s2.0-33947097389 10.1007/s00439-006-0309-8 (Pubitemid 46404456)
86. Hayashi M., Kouki T., Takasu N., Sunagawa S., Komiya I., Association of an A/C single nucleotide polymorphism in programmed cell death-ligand 1 gene with graves' disease in Japanese patients. European Journal of Endocrinology 2008 158 6 817 822 2-s2.0-44949142100 10.1530/EJE-07-0649 (Pubitemid 351837370)
87. Gianchecchi E., Delfino D. V., Fierabracci A., Recent insights into the role of the PD-1/PD-L1 pathway in immunological tolerance and autoimmunity. Autoimmunity Reviews 2013 12 11 1091 1100
88. Wang S. C., Lin C. H., Ou T. T., Ligands for programmed cell death 1 gene in patients with systemic lupus erythematosus. The Journal of Rheumatology 2007 34 4 721 725
89. Prokunina L., Castillejo-López C., Öberg F., Gunnarsson I., Berg L., Magnusson V., Brookes A. J., Tentler D., Kristjansdóttir H., Gróndal G., Isine Bolstad A., Svenungsson E., Lundberg I., Sturfelt G., Jönssen A., Truedsson L., Lima G., Alcocer-Varela J., Jonsson R., Gyllensten U. B., Harley J. B., Alarcón-Segovia D., Steinsson K., Alarcón-Riquelme M. E., A regulatory polymorphism in PDCD1 is associated with susceptibility to systemic lupus erythematosus in humans. Nature Genetics 2002 32 4 666 669 2-s2.0-13244277850 10.1038/ng1020 (Pubitemid 35435182)
90. Nielsen C., Laustrup H., Voss A., Junker P., Husby S., Lillevang S. T., A putative regulatory polymorphism in PD-1 is associated with nephropathy in a population-based cohort of systemic lupus erythematosus patients. Lupus 2004 13 7 510 516 2-s2.0-4043135770 (Pubitemid 39071204)
91. Nielsen C., Hansen D., Husby S., Jacobsen B. B., Lillevang S. T., Association of a putative regulatory polymorphism in the PD-1 gene with susceptibility to type 1 diabetes. Tissue Antigens 2003 62 6 492 497 2-s2.0-0344099132 10.1046/j.1399-0039.2003.00136.x (Pubitemid 37479307)
92. Lin S. C., Yen J. H., Tsai J. J., Tsai W. C., Ou T. T., Liu H. W., Chen C. J., Association of a programmed death 1 gene polymorphism with the development of rheumatoid arthritis, but not systemic lupus erythematosus. Arthritis and Rheumatism 2004 50 3 770 775 2-s2.0-1542343979 10.1002/art.20040 (Pubitemid 38326176)
93. Prokunina L., Padyukov L., Bennet A., De Faire U., Wiman B., Prince J., Alfredsson L., Klareskog L., Alarcón-Riquelme M., Association of the PD-1.3A allele of the PDCD1 gene in patients with rheumatoid arthritis negative for rheumatoid factor and the shared epitope. Arthritis and Rheumatism 2004 50 6 1770 1773 2-s2.0-2642575164 10.1002/art.20280 (Pubitemid 38725088)
94. Kroner A., Mehling M., Hemmer B., Rieckmann P., Toyka K. V., Mäurer M., Wiendl H., A PD-1 polymorphism is associated with disease progression in multiple sclerosis. Annals of Neurology 2005 58 1 50 57 2-s2.0-21844451620 10.1002/ana.20514 (Pubitemid 40962460)
95. Newby P. R., Roberts-Davies E. L., Brand O. J., Heward J. M., Franklyn J. A., Gough S. C. L., Simmonds M. J., Tag SNP screening of the PDCD1 gene for association with graves' disease. Clinical Endocrinology 2007 67 1 125 128 2-s2.0-34250763243 10.1111/j.1365-2265.2007.02848.x (Pubitemid 46955451)
96. Nagafuchi S., The role of B cells in regulating the magnitude of immune response. Microbiology and Immunology 2010 54 8 487 490 2-s2.0-77955001099 10.1111/j.1348-0421.2010.00235.x
97. Corcione A., Benvenuto F., Ferretti E., Giunti D., Cappiello V., Cazzanti F., Risso M., Gualandi F., Mancardi G. L., Pistoia V., Uccelli A., Human mesenchymal stem cells modulate B-cell functions. Blood 2006 107 1 367 372 2-s2.0-30144440925 10.1182/blood-2005-07-2657 (Pubitemid 43053565)
98. Tabera S., Pérez-Simón J. A., Díez-Campelo M., Sánchez-Abarca L. I., Blanco B., López A., Benito A., Ocio E., Sánchez-Guijo F. M., Cañizo C., San Miguel J. F., The effect of mesenchymal stem cells on the viability, proliferation and differentiation of B-lymphocytes. Haematologica 2008 93 9 1301 1309 2-s2.0-50849088328 10.3324/haematol.12857
99. Asari S., Itakura S., Ferreri K., Liu C.-P., Kuroda Y., Kandeel F., Mullen Y., Mesenchymal stem cells suppress B-cell terminal differentiation. Experimental Hematology 2009 37 5 604 615 2-s2.0-64249129065 10.1016/j.exphem.2009.01.005
100. Franquesa M., Hoogduijin M. J., Bestard O., Grinyó J. M., Immunomodulatory effect of mesenchymal stem cells on B cells. Frontiers Immunology 2012 3 article 212
101. Rafei M., Hsieh J., Fortier S., Li M., Yuan S., Birman E., Forner K., Boivin M.-N., Doody K., Tremblay M., Annabi B., Galipeau J., Mesenchymal stromal cell derived CCL2 suppresses plasma cell immunoglobulin production via STAT3 inactivation and PAX5 induction. Blood 2008 112 13 4991 4998 2-s2.0-58149388233 10.1182/blood-2008-07-166892
102. Schena F., Gambini C., Gregorio A., Mosconi M., Reverberi D., Gattorno M., Casazza S., Uccelli A., Moretta L., Martini A., Traggiai E., Interferon- γ -dependent inhibition of B cell activation by bone marrow-derived mesenchymal stem cells in a murine model of systemic lupus erythematosus. Arthritis and Rheumatism 2010 62 9 2776 2786 2-s2.0-77956371047 10.1002/art.27560
103. Liu O., Xu J., Gang D., Periodontal ligament stem cells regulate B lymphocyte function via programmed cell death protein 1. Stem Cells 2013 31 7 1371 1382
104. Agata Y., Kawasaki A., Nishimura H., Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. International Immunology 1996 8 5 765 772 (Pubitemid 26148299)
105. Bertsias G. K., Nakou M., Choulaki C., Raptopoulou A., Papadimitraki E., Goulielmos G., Kritikos H., Sidiropoulos P., Tzardi M., Kardassis D., Mamalaki C., Boumpas D. T., Genetic, immunologic, and immunohistochemical analysis of the programmed death 1/programmed death ligand 1 pathway in human systemic lupus erythematosus. Arthritis and Rheumatism 2009 60 1 207 218 2-s2.0-58249094864 10.1002/art.24227