Podoplanin negatively regulates CD4+ effector T cell responses

Journal of Clinical Investigation

Volumn 125, Issue 1, 2015, Pages 129-140

  Peters, Anneli ^a   Burkett, Patrick R ^a,b   Sobel, Raymond A ^c   Buckley, Christopher D ^d   Watson, Steve P ^e   Bettelli, Estelle ^f   Kuchroo, Vijay K ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d QUEEN ELIZABETH HOSPITAL   (United Kingdom)

^e UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^f BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; IMMUNOGLOBULIN; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; INTERLEUKIN 7; MUCIN; PODOPLANIN; PROGRAMMED DEATH 1 RECEPTOR; T CELL IMMUNOGLOBULIN AND MUCIN DOMAIN CONTAINING MOLECULE 3 RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; GP38 PROTEIN, MOUSE; MEMBRANE PROTEIN;

ADAPTIVE IMMUNITY; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL COUNT; CELL INFILTRATION; CELL POPULATION; CELL SURVIVAL; CONTROLLED STUDY; EFFECTOR CELL; GENE EXPRESSION PROFILING; GENETIC SUSCEPTIBILITY; HISTOPATHOLOGY; IMMUNE RESPONSE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL EXPANSION; TH17 CELL; 129 MOUSE; ANIMAL; C57BL MOUSE; CELL CULTURE; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTOPENIA; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL SURVIVAL; CELLS, CULTURED; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; LYMPHOPENIA; MEMBRANE GLYCOPROTEINS; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 84920453478     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI74685     Document Type: Article

References (36)

1. Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 cells. Annu Rev Immunol. 2009;27:485-517.
2. Joller N, Peters A, Anderson AC, Kuchroo VK. Immune checkpoints in central nervous system autoimmunity. Immunol Rev. 2012;248(1):122-139.
3. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252-264.
4. Sakuishi K, Apetoh L, Sullivan JM, Blazar BR, Kuchroo VK, Anderson AC. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med. 2010;207(10):2187-2194.
5. Peters A, et al. Th17 cells induce ectopic lymphoid follicles in central nervous system tissue inflammation. Immunity. 2011;35(6):986-996.
6. Schacht V, Dadras SS, Johnson LA, Jackson DG, Hong YK, Detmar M. Up-regulation of the lymphatic marker podoplanin, a mucin-type transmembrane glycoprotein, in human squa-mous cell carcinomas and germ cell tumors. Am J Pathol. 2005;166(3):913-921.
7. Astarita JL, Acton SE, Turley SJ. Podoplanin: emerging functions in development, the immune system, and cancer. Front Immunol. 2012;3:283.
8. Ramirez MI, Millien G, Hinds A, Cao Y, Seldin DC, Williams MC. T1alpha, a lung type I cell differentiation gene, is required for normal lung cell proliferation and alveolus formation at birth. Dev Biol. 2003;256(1):61-72.
9. Schacht V, et al. T1α/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J. 2003;22(14):3546-3556.
10. Waterhouse P, et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science. 1995;270(5238):985-988.
11. Nishimura H, Minato N, Nakano T, Honjo T. Immunological studies on PD-1 deficient mice: implication of PD-1 as a negative regulator for B cell responses. Int Immunol. 1998;10(10):1563-1572.
12. Bettelli E, Pagany M, Weiner HL, Linington C, Sobel RA, Kuchroo VK. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J Exp Med. 2003;197(9):1073-1081.
13. Ma A, Koka R, Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol. 2006;24:657-679.
14. Li J, Huston G, Swain SL. IL-7 promotes the transition of CD4 effectors to persistent memory cells. J Exp Med. 2003;198(12):1807-1815.
15. Christou CM, et al. Renal cells activate the platelet receptor CLEC-2 through podoplanin. Biochem J. 2008;411(1):133-140.
16. Suzuki-Inoue K, et al. Essential in vivo roles of the C-type lectin receptor CLEC-2: embryonic/neonatal lethality of CLEC-2-deficient mice by blood/lymphatic misconnections and impaired thrombus formation of CLEC-2-deficient platelets. J Biol Chem. 2010;285(32):24494-24507.
17. Peters A, Lee Y, Kuchroo VK. The many faces of Th17 cells. Curr Opin Immunol. 2011;23(6):702-706.
18. Joller N, et al. Cutting edge: TIGIT has T cell-intrinsic inhibitory functions. J Immunol. 2011;186(3):1338-1342.
19. Dardalhon V, et al. Tim-3/galectin-9 pathway: regulation of Th1 immunity through promotion of CD11b+Ly-6G+ myeloid cells. J Immunol. 2010;185(3):1383-1392.
20. Engelhardt JJ, Sullivan TJ, Allison JP. CTLA-4 overexpression inhibits T cell responses through a CD28-B7-dependent mechanism. J Immunol. 2006;177(2):1052-1061.
21. Jäger A, Dardalhon V, Sobel RA, Bettelli E, Kuch-roo VK. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J Immunol. 2009;183(11):7169-7177.
22. Suzuki-Inoue K, et al. Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. J Biol Chem. 2007;282(36):25993-26001.
23. Cueni LN, Detmar M. Galectin-8 interacts with podoplanin and modulates lymphatic endothelial cell functions. Exp Cell Res. 2009;315(10):1715-1723.
24. Kerjaschki D, et al. Lymphatic neoangiogenesis in human kidney transplants is associated with immunologically active lymphocytic infiltrates. J Am Soc Nephrol. 2004;15(3):603-612.
25. Colonna M, Samaridis J, Angman L. Molecular characterization of two novel C-type lectin-like receptors, one of which is selectively expressed in human dendritic cells. Eur J Immunol. 2000;30(2):697-704.
26. Mourao-Sa D, et al. CLEC-2 signaling via Syk in myeloid cells can regulate inflammatory responses. Eur J Immunol. 2011;41(10):3040-3053.
27. Liu FT, Rabinovich GA. Galectins: regulators of acute and chronic inflammation. Ann N Y Acad Sci. 2010;1183:158-182.
28. Turley SJ, Fletcher AL, Elpek KG. The stromal and haematopoietic antigen-presenting cells that reside in secondary lymphoid organs. Nat Rev Immunol. 2010;10(12):813-825.
29. Weyand CM, Kurtin PJ, Goronzy JJ. Ectopic lym-phoid organogenesis: a fast track for autoimmu-nity. Am J Pathol. 2001;159(3):787-793.
30. Francisco LM, Sage PT, Sharpe AH. The PD-1 pathway in tolerance and autoimmunity. Immunol Rev. 2010;236:219-242.
31. Good-Jacobson KL, Szumilas CG, Chen L, Sharpe AH, Tomayko MM, Shlomchik MJ. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat Immunol. 2010;11(6):535-542.
32. Hirota K, et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat Immunol. 2011;12(3):255-263.
33. Liu X, et al. Crucial role of interleukin-7 in T helper type 17 survival and expansion in autoimmune disease. Nat Med. 2010;16(2):191-197.
34. Lee Y, et al. Induction and molecular signature of pathogenic TH17 cells. Nat Immunol. 2012;13(10):991-999.
35. Bettelli E, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 2006;441(7090):235-238.
36. Lang G, et al. The structure of the human CD2 gene and its expression in transgenic mice. EMBO J. 1988;7(6):1675-1682.