Real-time immune cell interactions in target tissue during autoimmune-induced damage and graft tolerance

Journal of Experimental Medicine

Volumn 211, Issue 3, 2014, Pages 441-456

  Miska, Jason ^a   Abdulreda, Midhat H ^a   Devarajan, Priyadharshini ^a   Lui, Jen Bon ^a   Suzuki, Jun ^a,c   Pileggi, Antonello ^a,b   Berggren, Per Olof ^a   Chen, Zhibin ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b University of Miami College of Engineering   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN P 15095; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DAMAGE; CELL DIVISION; CELL FUNCTION; CELL GROWTH; CELL INTERACTION; CELL PROTECTION; CONTROLLED STUDY; CYTOLOGY; DENDRITIC CELL; EFFECTOR CELL; GROWTH INHIBITION; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; MOLECULAR IMAGING; MOUSE; MOUSE MODEL; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TARGET CELL; TARGET ORGAN; TISSUE GRAFT;

ADOPTIVE TRANSFER; ANALYSIS OF VARIANCE; ANIMALS; AUTOANTIGENS; AUTOIMMUNITY; BROMODEOXYURIDINE; CELL COMMUNICATION; CROSSES, GENETIC; FLUORESCENCE; IMAGE PROCESSING, COMPUTER-ASSISTED; ISLETS OF LANGERHANS TRANSPLANTATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RNA INTERFERENCE; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION TOLERANCE;

EID: 84896860062     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20130785     Document Type: Article

References (66)

1. Abdulreda, M.H., G. Faleo, R.D. Molano, M. Lopez-Cabezas, J. Molina, Y. Tan, O.A. Echeverria, E. Zahr-Akrawi, R. Rodriguez-Diaz, P.K. Edlund, et al. 2011. High-resolution, noninvasive longitudinal live imaging of immune responses. Proc. Natl. Acad. Sci. USA. 108:12863-12868. http://dx.doi.org/10.1073/pnas.1105002108
2. Baecher-Allan, C., E. Wolf, and D.A. Hafler. 2006. MHC class II expression identifies functionally distinct human regulatory T cells. J. Immunol. 176:4622-4631.
3. Benhar, I., A. London, and M. Schwartz. 2012. The privileged immunity of immune privileged organs: the case of the eye. Front Immunol. 3:296. http://dx.doi.org/10.3389/fimmu.2012.00296
4. Berney, T., R.D. Molano, P. Cattan, A. Pileggi, C. Vizzardelli, R. Oliver, C. Ricordi, and L. Inverardi. 2001. Endotoxin-mediated delayed islet graft function is associated with increased intra-islet cytokine production and islet cell apoptosis. Transplantation. 71:125-132. http://dx.doi.org/10.1097/00007890-200101150-00020
5. Cano, D.A., I.C. Rulifson, P.W. Heiser, L.B. Swigart, S. Pelengaris, M. German, G.I. Evan, J.A. Bluestone, and M. Hebrok. 2008. Regulated beta-cell regeneration in the adult mouse pancreas. Diabetes. 57:958-966. http://dx.doi.org/10.2337/db07-0913
6. Chatenoud, L. 2011. Diabetes: type 1 diabetes mellitus-a door opening to a real therapy? Nat Rev Endocrinol. 7:564-566. http://dx.doi.org/10.1038/nrendo.2011.148
7. Chen, Z., A.E. Herman, M. Matos, D. Mathis, and C. Benoist. 2005. Where CD4+CD25+ T reg cells impinge on autoimmune diabetes. J. Exp. Med. 202:1387-1397. http://dx.doi.org/10.1084/jem.20051409
8. Chen, Z., J. Stockton, D. Mathis, and C. Benoist. 2006. Modeling CTLA4- linked autoimmunity with RNA interference in mice. Proc. Natl. Acad. Sci. USA. 103:16400-16405. http://dx.doi.org/10.1073/pnas.0607854103
9. Dissanayake, D., H. Hall, N. Berg-Brown, A.R. Elford, S.R. Hamilton, K. Murakami, L.S. Deluca, J.L. Gommerman, and P.S. Ohashi. 2011. Nuclear factor-kB1 controls the functional maturation of dendritic cells and prevents the activation of autoreactive T cells. Nat. Med. 17:1663-1667. http://dx.doi.org/10.1038/nm.2556
10. Dor, Y., J. Brown, O.I. Martinez, and D.A. Melton. 2004. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature. 429:41-46. http://dx.doi.org/10.1038/nature02520
11. Driver, J.P., F. Scheuplein, Y.G. Chen, A.E. Grier, S.B. Wilson, and D.V. Serreze. 2010. Invariant natural killer T-cell control of type 1 diabetes: a dendritic cell genetic decision of a silver bullet or Russian roulette. Diabetes. 59:423-432. http://dx.doi.org/10.2337/db09-1116
12. Ermann, J., V. Szanya, G.S. Ford, V. Paragas, C.G. Fathman, and K. Lejon. 2001. CD4(+)CD25(+) T cells facilitate the induction of T cell anergy. J. Immunol. 167:4271-4275.
13. Faleo, G., C. Fotino, N. Bocca, R.D. Molano, E. Zahr-Akrawi, J. Molina, S. Villate, O. Umland, J.S. Skyler, A.L. Bayer, et al. 2012. Prevention of autoimmune diabetes and induction of β-cell proliferation in NOD mice by hyperbaric oxygen therapy. Diabetes. 61:1769-1778. http://dx.doi.org/10.2337/db11-0516
14. Feuerer, M., Y. Shen, D.R. Littman, C. Benoist, and D. Mathis. 2009. How punctual ablation of regulatory T cells unleashes an autoimmune lesion within the pancreatic islets. Immunity. 31:654-664. http://dx.doi.org/10.1016/j.immuni.2009.08.023
15. Fife, B.T., K.E. Pauken, T.N. Eagar, T. Obu, J. Wu, Q. Tang, M. Azuma, M.F. Krummel, and J.A. Bluestone. 2009. Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat. Immunol. 10:1185-1192. http://dx.doi.org/10.1038/ni.1790
16. Germain, R.N., E.A. Robey, and M.D. Cahalan. 2012. A decade of imaging cellular motility and interaction dynamics in the immune system. Science. 336:1676-1681. http://dx.doi.org/10.1126/science.1221063
17. Hadjantonakis, A.K., S. Macmaster, and A. Nagy. 2002. Embryonic stem cells and mice expressing different GFP variants for multiple non-invasive reporter usage within a single animal. BMC Biotechnol. 2:11. http://dx.doi.org/10.1186/1472-6750-2-11
18. Hagness, M., K. Henjum, J. Landskron, K.W. Brudvik, B.A. Bjørnbeth, A. Foss, K. Taskén, and E.M. Aandahl. 2012. Kinetics and activation requirements of contact-dependent immune suppression by human regulatory T cells. J. Immunol. 188:5459-5466. http://dx.doi.org/10.4049/jimmunol.1101367
19. Hahn, S., R. Gehri, and P. Erb. 1995. Mechanism and biological significance of CD4-mediated cytotoxicity. Immunol. Rev. 146:57-79. http://dx.doi.org/10.1111/j.1600-065X.1995.tb00684.x
20. Han, D., X. Cai, J. Wen, N.S. Kenyon, and Z. Chen. 2012. From biomarkers to a clue of biology: a computation-aided perspective of immune gene expression profiles in human type 1 diabetes. Front Immunol. 3:320.
21. Hara, M., R.F. Dizon, B.S. Glick, C.S. Lee, K.H. Kaestner, D.W. Piston, and V.P. Bindokas. 2006. Imaging pancreatic beta-cells in the intact pancreas. Am. J. Physiol. Endocrinol. Metab. 290:E1041-E1047. http://dx.doi.org/10.1152/ajpendo.00365.2005
22. Hogquist, K.A., S.C. Jameson, W.R. Heath, J.L. Howard, M.J. Bevan, and F.R. Carbone. 1994. T cell receptor antagonist peptides induce positive selection. Cell. 76:17-27. http://dx.doi.org/10.1016/0092-8674(94)90169-4
23. Huang, Y.H., D.K. Sojka, and D.J. Fowell. 2012. Cutting edge: Regulatory T cells selectively attenuate, not terminate, T cell signaling by disrupting NF-kB nuclear accumulation in CD4 T cells. J. Immunol. 188:947-951. http://dx.doi.org/10.4049/jimmunol.1101027
24. Josefowicz, S.Z., L.F. Lu, and A.Y. Rudensky. 2012. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30:531-564. http://dx.doi.org/10.1146/annurev.immunol.25.022106.141623
25. Katz, J.D., B. Wang, K. Haskins, C. Benoist, and D. Mathis. 1993. Following a diabetogenic T cell from genesis through pathogenesis. Cell. 74:1089- 1100. http://dx.doi.org/10.1016/0092-8674(93)90730-E
26. Kurts, C., W.R. Heath, F.R. Carbone, J. Allison, J.F. Miller, and H. Kosaka. 1996. Constitutive class I-restricted exogenous presentation of self antigens in vivo. J. Exp. Med. 184:923-930. http://dx.doi.org/10.1084/jem.184.3.923
27. Lu, Y., J. Suzuki, M. Guillioli, O. Umland, and Z. Chen. 2011. Induction of selfantigen- specific Foxp3+ regulatory T cells in the periphery by lymphodepletion treatment with anti-mouse thymocyte globulin in mice. Immunology. 134:50-59. http://dx.doi.org/10.1111/j.1365-2567.2011.03466.x
28. Lu, Y., H. Schneider, and C.E. Rudd. 2012. Murine regulatory T cells differ from conventional T cells in resisting the CTLA-4 reversal of TCR stop-signal. Blood. 120:4560-4570. http://dx.doi.org/10.1182/blood-2012-04-421420
29. Mandl, J.N., R. Liou, F. Klauschen, N. Vrisekoop, J.P. Monteiro, A.J. Yates, A.Y. Huang, and R.N. Germain. 2012. Quantification of lymph node transit times reveals differences in antigen surveillance strategies of naive CD4+ and CD8+ T cells. Proc. Natl. Acad. Sci. USA. 109:18036-18041. http://dx.doi.org/10.1073/pnas.1211717109
30. Mathis, D., and C. Benoist. 2004. Back to central tolerance. Immunity. 20:509- 516. http://dx.doi.org/10.1016/S1074-7613(04)00111-6
31. Mempel, T.R., M.J. Pittet, K. Khazaie, W. Weninger, R. Weissleder, H. von Boehmer, and U.H. von Andrian. 2006. Regulatory T cells reversibly suppress cytotoxic T cell function independent of effector differentiation. Immunity. 25:129-141. http://dx.doi.org/10.1016/j.immuni.2006.04.015
32. Miska, J., E. Bas, P. Devarajan, and Z. Chen. 2012. Autoimmunity-mediated antitumor immunity: tumor as an immunoprivileged self. Eur. J. Immunol. 42:2584-2596. http://dx.doi.org/10.1002/eji.201242590
33. Mukhopadhaya, A., T. Hanafusa, I. Jarchum, Y.G. Chen, Y. Iwai, D.V. Serreze, R.M. Steinman, K.V. Tarbell, and T.P. DiLorenzo. 2008. Selective delivery of beta cell antigen to dendritic cells in vivo leads to deletion and tolerance of autoreactive CD8+ T cells in NOD mice. Proc. Natl. Acad. Sci. USA. 105:6374-6379. http://dx.doi.org/10.1073/pnas.0802644105
34. Nakamura, K., A. Kitani, and W. Strober. 2001. Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J. Exp. Med. 194:629-644. http://dx.doi.org/10.1084/jem.194.5.629
35. Onishi, Y., Z. Fehervari, T. Yamaguchi, and S. Sakaguchi. 2008. Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc. Natl. Acad. Sci. USA. 105:10113-10118. http://dx.doi.org/10.1073/pnas.0711106105
36. Paust, S., L. Lu, N. McCarty, and H. Cantor. 2004. Engagement of B7 on effector T cells by regulatory T cells prevents autoimmune disease. Proc. Natl. Acad. Sci. USA. 101:10398-10403. http://dx.doi.org/10.1073/pnas.0403342101
37. Piccirillo, C.A., and E.M. Shevach. 2001. Cutting edge: control of CD8+ T cell activation by CD4+CD25+ immunoregulatory cells. J. Immunol. 167:1137-1140.
38. Pierson, W., B. Cauwe, A. Policheni, S.M. Schlenner, D. Franckaert, J. Berges, S. Humblet-Baron, S. Schönefeldt, M.J. Herold, D. Hildeman, et al. 2013. Antiapoptotic Mcl-1 is critical for the survival and niche-filling capacity of Foxp3+ regulatory T cells. Nat. Immunol. 14:959-965. http://dx.doi.org/10.1038/ni.2649
39. Read, S., V. Malmström, and F. Powrie. 2000. Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J. Exp. Med. 192:295- 302. http://dx.doi.org/10.1084/jem.192.2.295
40. Ricordi, C., P.E. Lacy, K. Sterbenz, and J.M. Davie. 1987. Low-temperature culture of human islets or in vivo treatment with L3T4 antibody produces a marked prolongation of islet human-to-mouse xenograft survival. Proc. Natl. Acad. Sci. USA. 84:8080-8084. http://dx.doi.org/10.1073/pnas.84.22.8080
41. Rodriguez-Diaz, R., M.H. Abdulreda, A.L. Formoso, I. Gans, C. Ricordi, P.O. Berggren, and A. Caicedo. 2011. Innervation patterns of autonomic axons in the human endocrine pancreas. Cell Metab. 14:45-54. http://dx.doi.org/10.1016/j.cmet.2011.05.008
42. Ruocco, M.G., K.A. Pilones, N. Kawashima, M. Cammer, J. Huang, J.S. Babb, M. Liu, S.C. Formenti, M.L. Dustin, and S. Demaria. 2012. Suppressing T cell motility induced by anti-CTLA-4 monotherapy improves antitumor effects. J. Clin. Invest. 122:3718-3730. http://dx.doi.org/10.1172/JCI61931
43. Samy, E.T., L.A. Parker, C.P. Sharp, and K.S. Tung. 2005. Continuous control of autoimmune disease by antigen-dependent polyclonal CD4+CD25+ regulatory T cells in the regional lymph node. J. Exp. Med. 202:771-781. http://dx.doi.org/10.1084/jem.20041033
44. Schneider, H., J. Downey, A. Smith, B.H. Zinselmeyer, C. Rush, J.M. Brewer, B. Wei, N. Hogg, P. Garside, and C.E. Rudd. 2006. Reversal of the TCR stop signal by CTLA-4. Science. 313:1972-1975. http://dx.doi.org/10.1126/science.1131078
45. Sherry, N.A., J.A. Kushner, M. Glandt, T. Kitamura, A.M. Brillantes, and K.C. Herold. 2006. Effects of autoimmunity and immune therapy on beta-cell turnover in type 1 diabetes. Diabetes. 55:3238-3245. http://dx.doi.org/10.2337/db05-1034
46. Shevach, E.M. 2006. From vanilla to 28 flavors: multiple varieties of T regulatory cells. Immunity. 25:195-201. http://dx.doi.org/10.1016/j.immuni.2006.08.003
47. Shevach, E.M. 2008. Immunology. Regulating suppression. Science. 322:202-203. http://dx.doi.org/10.1126/science.1164872
48. Shevach, E.M. 2011. Biological functions of regulatory T cells. Adv. Immunol. 112:137-176. http://dx.doi.org/10.1016/B978-0-12-387827-4.00004-8
49. Speier, S., D. Nyqvist, O. Cabrera, J. Yu, R.D. Molano, A. Pileggi, T. Moede, M. Köhler, J. Wilbertz, B. Leibiger, et al. 2008a. Noninvasive in vivo imaging of pancreatic islet cell biology. Nat. Med. 14:574-578. http://dx.doi.org/10.1038/nm1701
50. Speier, S., D. Nyqvist, M. Köhler, A. Caicedo, I.B. Leibiger, and P.O. Berggren. 2008b. Noninvasive high-resolution in vivo imaging of cell biology in the anterior chamber of the mouse eye. Nat. Protoc. 3:1278-1286. http://dx.doi.org/10.1038/nprot.2008.118
51. Stadinski, B.D., T. Delong, N. Reisdorph, R. Reisdorph, R.L. Powell, M. Armstrong, J.D. Piganelli, G. Barbour, B. Bradley, F. Crawford, et al. 2010. Chromogranin A is an autoantigen in type 1 diabetes. Nat. Immunol. 11:225-231. http://dx.doi.org/10.1038/ni.1844
52. Surh, C.D., and J. Sprent. 2008. Homeostasis of naive and memory T cells. Immunity. 29:848-862. http://dx.doi.org/10.1016/j.immuni.2008.11.002
53. Tadokoro, C.E., G. Shakhar, S. Shen, Y. Ding, A.C. Lino, A. Maraver, J.J. Lafaille, and M.L. Dustin. 2006. Regulatory T cells inhibit stable contacts between CD4+ T cells and dendritic cells in vivo. J. Exp. Med. 203:505-511. http://dx.doi.org/10.1084/jem.20050783
54. Takahashi, T., Y. Kuniyasu, M. Toda, N. Sakaguchi, M. Itoh, M. Iwata, J. Shimizu, and S. Sakaguchi. 1998. Immunologic self-tolerance maintained by CD25+CD4+ naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. Int. Immunol. 10:1969-1980. http://dx.doi.org/10.1093/intimm/10.12.1969
55. Tang, Q., J.Y. Adams, A.J. Tooley, M. Bi, B.T. Fife, P. Serra, P. Santamaria, R.M. Locksley, M.F. Krummel, and J.A. Bluestone. 2006. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat. Immunol. 7:83-92. http://dx.doi.org/10.1038/ni1289
56. Tarbell, K.V., L. Petit, X. Zuo, P. Toy, X. Luo, A. Mqadmi, H. Yang, M. Suthanthiran, S. Mojsov, and R.M. Steinman. 2007. Dendritic cellexpanded, islet-specific CD4+ CD25+ CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice. J. Exp. Med. 204:191-201. http://dx.doi.org/10.1084/jem.20061631
57. Teft, W.A., M.G. Kirchhof, and J. Madrenas. 2006. A molecular perspective of CTLA-4 function. Annu. Rev. Immunol. 24:65-97. http://dx.doi.org/10.1146/annurev.immunol.24.021605.090535
58. Thornton, A.M., and E.M. Shevach. 1998. CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188:287-296. http://dx.doi.org/10.1084/jem.188.2.287
59. Tisch, R., and B. Wang. 2008. Dysrulation of T cell peripheral tolerance in type 1 diabetes. Adv. Immunol. 100:125-149. http://dx.doi.org/10.1016/S0065-2776(08)00805-5
60. Tite, J.P., and C.A. Janeway Jr. 1984. Cloned helper T cells can kill B lymphoma cells in the presence of specific antigen: Ia restriction and cognate vs. noncognate interactions in cytolysis. Eur. J. Immunol. 14:878-886. http://dx.doi.org/10.1002/eji.1830141004
61. Tsai, S., P. Serra, X. Clemente-Casares, R.M. Slattery, and P. Santamaria. 2013. Dendritic cell-dependent in vivo generation of autoregulatory T cells by antidiabetogenic MHC class II. J. Immunol. 191:70-82. http://dx.doi.org/10.4049/jimmunol.1300168
62. Turley, S., L. Poirot, M. Hattori, C. Benoist, and D. Mathis. 2003. Physiological beta cell death triggers priming of self-reactive T cells by dendritic cells in a type-1 diabetes model. J. Exp. Med. 198:1527-1537. http://dx.doi.org/10.1084/jem.20030966
63. Wan, Y.Y., and R.A. Flavell. 2005. Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc. Natl. Acad. Sci. USA. 102:5126- 5131. http://dx.doi.org/10.1073/pnas.0501701102
64. Wing, K., Y. Onishi, P. Prieto-Martin, T. Yamaguchi, M. Miyara, Z. Fehervari, T. Nomura, and S. Sakaguchi. 2008. CTLA-4 control over Foxp3+ regulatory T cell function. Science. 322:271-275. http://dx.doi.org/10.1126/science.1160062
65. Yi, P., J.S. Park, and D.A. Melton. 2013. Betatrophin: a hormone that controls pancreatic β cell proliferation. Cell. 153:747-758. http://dx.doi.org/10.1016/j.cell.2013.04.008
66. Zhang, N., B. Schröppel, G. Lal, C. Jakubzick, X. Mao, D. Chen, N. Yin, R. Jessberger, J.C. Ochando, Y. Ding, and J.S. Bromberg. 2009. Regulatory T cells sequentially migrate from inflamed tissues to draining lymph nodes to suppress the alloimmune response. Immunity. 30:458-469. http://dx.doi.org/10.1016/j.immuni.2008.12.022