CD43 functions as an E-selectin ligand for Th17 cells in vitro and is required for rolling on the vascular endothelium and Th17 cell recruitment during inflammation in vivo

Journal of Immunology

Volumn 196, Issue 3, 2016, Pages 1305-1316

  Velazquez, Francisco ^a,b   Grodecki Pena, Anna ^a   Knapp, Andrew ^a   Salvador, Ane M ^a   Nevers, Tania ^a   Croce, Kevin J ^c   Alcaide, Pilar ^a,b  

^a TUFTS MEDICAL CENTER   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; HERMES ANTIGEN; LEUKOSIALIN; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; P SELECTIN GLYCOPROTEIN LIGAND 1; TUMOR NECROSIS FACTOR ALPHA; LIGAND;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CELL ADHESION; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LEUKOCYTE ROLLING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TH17 CELL; VASCULAR ENDOTHELIUM; ANIMAL; C57BL MOUSE; CELL SEPARATION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FLOW CYTOMETRY; IMMUNOLOGY; IMMUNOPRECIPITATION; KNOCKOUT MOUSE; WESTERN BLOTTING;

ANIMALS; ANTIGENS, CD43; BLOTTING, WESTERN; CELL SEPARATION; E-SELECTIN; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENDOTHELIUM, VASCULAR; FLOW CYTOMETRY; IMMUNOPRECIPITATION; INFLAMMATION; LEUKOCYTE ROLLING; LIGANDS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; TH17 CELLS;

EID: 84957694579     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501171     Document Type: Article

References (50)

1. Murphy, C. A., C. L. Langrish, Y. Chen, W. Blumenschein, T. McClanahan, R. A. Kastelein, J. D. Sedgwick, and D. J. Cua. 2003. Divergent pro - And antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198: 1951-1957.
2. 7 suppresses lymphocyte migration to the gut. J. Clin. Invest. 117: 2526-2538.
3. Iwakura, Y., and H. Ishigame. 2006. The IL-23/IL-17 axis in inflammation. J. Clin. Invest. 116: 1218-1222.
4. Weaver, C. T., R. D. Hatton, P. R. Mangan, and L. E. Harrington. 2007. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25: 821-852.
5. Ley, K., and G. S. Kansas. 2004. Selectins in T-cell recruitment to non-lymphoid tissues and sites of inflammation. Nat. Rev. Immunol. 4: 325-335.
6. 2 (naive) T cells roll efficiently on E - And P-selectin and vascular cell adhesion molecule-1 under flow. J. Immunol. 158: 3640-3650.
7. Zarbock, A., K. Ley, R. P. McEver, and A. Hidalgo. 2011. Leukocyte ligands for endothelial selectins: specialized glycoconjugates that mediate rolling and signaling under flow. Blood 118: 6743-6751.
8. Alcaide, P., E. Maganto-Garcia, G. Newton, R. Travers, K. J. Croce, D. X. Bu, F. W. Luscinskas, and A. H. Lichtman. 2012. Difference in Th1 and Th17 lymphocyte adhesion to endothelium. J. Immunol. 188: 1421-1430.
9. Griffin, G. K., G. Newton, M. L. Tarrio, D. X. Bu, E. Maganto-Garcia, V. Azcutia, P. Alcaide, N. Grabie, F. W. Luscinskas, K. J. Croce, and A. H. Lichtman. 2012. IL-17 and TNF - A sustain neutrophil recruitment during inflammation through syner-gistic effects on endothelial activation. J. Immunol. 188: 6287-6299.
10. Hirata, T., G. Merrill-Skoloff, M. Aab, J. Yang, B. C. Furie, and B. Furie. 2000. P-selectin glycoprotein ligand 1 (PSGL-1) is a physiological ligand for E-selectin in mediating T helper 1 lymphocyte migration. J. Exp. Med. 192: 1669-1676.
11. Xia, L., M. Sperandio, T. Yago, J. M. McDaniel, R. D. Cummings, S. Pearson-White, K. Ley, and R. P. McEver. 2002. P-selectin glycoprotein ligand-1-deficient mice have impaired leukocyte tethering to E-selectin under flow. J. Clin. Invest. 109: 939-950.
12. Matsumoto, M., A. Shigeta, Y. Furukawa, T. Tanaka, M. Miyasaka, and T. Hirata. 2007. CD43 collaborates with P-selectin glycoprotein ligand-1 to mediate E-selectin-dependent T cell migration into inflamed skin. J. Immunol. 178: 2499-2506.
13. Nácher, M., A. B. Blázquez, B. Shao, A. Matesanz, C. Prophete, M. C. Berin, P. S. Frenette, and A. Hidalgo. 2011. Physiological contribution of CD44 as a ligand for E-selectin during inflammatory T-cell recruitment. Am. J. Pathol. 178: 2437-2446.
14. Alcaide, P., S. L. King, C. J. Dimitroff, Y. C. Lim, R. C. Fuhlbrigge, and F. W. Luscinskas. 2007. The 130-kDa glycoform of CD43 functions as an E-selectin ligand for activated Th1 cells in vitro and in delayed-type hypersensi-tivity reactions in vivo. J. Invest. Dermatol. 127: 1964-1972.
15. + human T cells. Blood 107: 1421-1426.
16. + T lymphocytes in graft-versus-host disease. Glycobiology 4: 885-893.
17. Cannon, J. L., A. Collins, P. D. Mody, D. Balachandran, K. J. Henriksen, C. E. Smith, J. Tong, B. S. Clay, S. D. Miller, and A. I. Sperling. 2008. CD43 regulates Th2 differentiation and inflammation. J. Immunol. 180: 7385-7393.
18. Rosenstein, Y., A. Santana, and G. Pedraza-Alva. 1999. CD43, a molecule with multiple functions. Immunol. Res. 20: 89-99.
19. Pedraza-Alva, G., and Y. Rosenstein. 2007. CD43-one molecule, many tales to recount. Signal Transduction 7: 372-385.
20. Ford, M. L., T. M. Onami, A. I. Sperling, R. Ahmed, and B. D. Evavold. 2003. CD43 modulates severity and onset of experimental autoimmune encephalo-myelitis. J. Immunol. 171: 6527-6533.
21. Flynn, K. M., M. Michaud, and J. A. Madri. 2013. CD44 deficiency contributes to enhanced experimental autoimmune encephalomyelitis: a role in immune cells and vascular cells of the blood-brain barrier. Am. J. Pathol. 182: 1322-1336.
22. Osmers, I., D. C. Bullard, and S. R. Barnum. 2005. PSGL-1 is not required for development of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 166: 193-196.
23. Yago, T., J. Fu, J. M. McDaniel, J. J. Miner, R. P. McEver, and L. Xia. 2010. Core 1-derived O-glycans are essential E-selectin ligands on neutrophils. Proc. Natl. Acad. Sci. USA 107: 9204-9209.
24. Yamazaki, T., X. O. Yang, Y. Chung, A. Fukunaga, R. Nurieva, B. Pappu, N. Martin-Orozco, H. S. Kang, L. Ma, A. D. Panopoulos, et al. 2008. CCR6 regulates the migration of inflammatory and regulatory T cells. J. Immunol. 181: 8391-8401.
25. Fuhlbrigge, R. C., S. L. King, C. J. Dimitroff, T. S. Kupper, and R. Sackstein. 2002. Direct real-time observation of E - And P-selectin-mediated rolling on cutaneous lymphocyte - Associated antigen immobilized on Western blots. J. Immunol. 168: 5645-5651.
26. Edwards, J. C., A. D. Sedgwick, and D. A. Willoughby. 1981. The formation of a structure with the features of synovial lining by subcutaneous injection of air: an in vivo tissue culture system. J. Pathol. 134: 147-156.
27. Yang, J., T. Hirata, K. Croce, G. Merrill-Skoloff, B. Tchernychev, E. Williams, R. Flaumenhaft, B. C. Furie, and B. Furie. 1999. Targeted gene disruption demonstrates that P-selectin glycoprotein ligand 1 (PSGL-1) is required for P-selectin-mediated but not E-selectin-mediated neutrophil rolling and migration. J. Exp. Med. 190: 1769-1782.
28. + T-cell trafficking. Blood 106: 3432-3439.
29. Grabie, N., M. W. Delfs, Y. C. Lim, J. R. Westrich, F. W. Luscinskas, and A. H. Lichtman. 2002. b-Galactoside a2, 3-sialyltransferase-I gene expression during Th2 but not Th1 differentiation: implications for core2-glycan formation on cell surface proteins. Eur. J. Immunol. 32: 2766-2772.
30. 2-mediated slow leukocyte rolling. Blood 116: 485-494.
31. Katayama, Y., A. Hidalgo, J. Chang, A. Peired, and P. S. Frenette. 2005. CD44 is a physiological E-selectin ligand on neutrophils. J. Exp. Med. 201: 1183-1189.
32. Ritonja, A., A. D. Rowan, D. J. Buttle, N. D. Rawlings, V. Turk, and A. J. Barrett. 1989. Stem bromelain: amino acid sequence and implications for weak binding of cystatin. FEBS Lett. 247: 419-424.
33. Alon, R., T. Feizi, C. T. Yuen, R. C. Fuhlbrigge, and T. A. Springer. 1995. Glycolipid ligands for selectins support leukocyte tethering and rolling under physiologic flow conditions. J. Immunol. 154: 5356-5366.
34. Wang, C., S. G. Kang, J. Lee, Z. Sun, and C. H. Kim. 2009. The roles of CCR6 in migration of Th17 cells and regulation of effector T-cell balance in the gut. Mucosal Immunol. 2: 173-183.
35. Manjunath, N., M. Correa, M. Ardman, and B. Ardman. 1995. Negative regulation of T-cell adhesion and activation by CD43. Nature 377: 535-538.
36. Ding, Z. M., J. E. Babensee, S. I. Simon, H. Lu, J. L. Perrard, D. C. Bullard, X. Y. Dai, S. K. Bromley, M. L. Dustin, M. L. Entman, et al. 1999. Relative contribution of LFA-1 and Mac-1 to neutrophil adhesion and migration. J. Immunol. 163: 5029-5038.
37. Hafezi-Moghadam, A., and K. Ley. 1999. Relevance of L-selectin shedding for leukocyte rolling in vivo. J. Exp. Med. 189: 939-948.
38. H17 cells. Nat. Immunol. 13: 991-999.
39. Tuccillo, F. M., A. de Laurentiis, C. Palmieri, G. Fiume, P. Bonelli, A. Borrelli, P. Tassone, I. Scala, F. M. Buonaguro, I. Quinto, and G. Scala. 2014. Aberrant gly-cosylation as biomarker for cancer: focus on CD43. BioMed Res. Int. 2014: 742831.
40. Huang, M. C., A. Laskowska, D. Vestweber, and M. K. Wild. 2002. The a(1, 3)-fucosyltransferase Fuc-TIV, but not Fuc-TVII, generates sialyl Lewis X-like epitopes preferentially on glycolipids. J. Biol. Chem. 277: 47786-47795.
41. Nimrichter, L., M. M. Burdick, K. Aoki, W. Laroy, M. A. Fierro, S. A. Hudson, C. E. Von Seggern, R. J. Cotter, B. S. Bochner, M. Tiemeyer, et al. 2008. E-selectin receptors on human leukocytes. Blood 112: 3744-3752.
42. Tessier, P. A., P. H. Naccache, I. Clark-Lewis, R. P. Gladue, K. S. Neote, and S. R. McColl. 1997. Chemokine networks in vivo: involvement of C-X-C and C-C chemokines in neutrophil extravasation in vivo in response to TNF - A. J. Immunol. 159: 3595-3602.
43. Yoshizaki, A., K. Yanaba, Y. Iwata, K. Komura, A. Ogawa, Y. Akiyama, E. Muroi, T. Hara, F. Ogawa, M. Takenaka, et al. 2010. Cell adhesion molecules regulate fibrotic process via Th1/Th2/Th17 cell balance in a bleomycin-induced scleroderma model. J. Immunol. 185: 2502-2515.
44. Labow, M. A., C. R. Norton, J. M. Rumberger, K. M. Lombard-Gillooly, D. J. Shuster, J. Hubbard, R. Bertko, P. A. Knaack, R. W. Terry, M. L. Harbison, et al. 1994. Characterization of E-selectin-deficient mice: demonstration of overlapping function of the endothelial selectins. Immunity 1: 709-720.
45. Ley, K., M. Allietta, D. C. Bullard, and S. Morgan. 1998. Importance of E-selectin for firm leukocyte adhesion in vivo. Circ. Res. 83: 287-294.
46. Austrup, F., D. Vestweber, E. Borges, M. Löhning, R. Bräuer, U. Herz, H. Renz, R. Hallmann, A. Scheffold, A. Radbruch, and A. Hamann. 1997. P - And E-selectin mediate recruitment of T-helper-1 but not T-helper-2 cells into inflam-med tissues. Nature 385: 81-83.
47. Staite, N. D., J. M. Justen, L. M. Sly, A. L. Beaudet, and D. C. Bullard. 1996. Inhibition of delayed-type contact hypersensitivity in mice deficient in both E-selectin and P-selectin. Blood 88: 2973-2979.
48. Rosenstein, Y., J. K. Park, W. C. Hahn, F. S. Rosen, B. E. Bierer, and S. J. Burakoff. 1991. CD43, a molecule defective in Wiskott-Aldrich syndrome, binds ICAM-1. Nature 354: 233-235.
49. Woodman, R. C., B. Johnston, M. J. Hickey, D. Teoh, P. Reinhardt, B. Y. Poon, and P. Kubes. 1998. The functional paradox of CD43 in leukocyte recruitment: a study using CD43-deficient mice. J. Exp. Med. 188: 2181-2186.
50. Carlow, D. A., and H. J. Ziltener. 2006. CD43 deficiency has no impact in competitive in vivo assays of neutrophil or activated T cell recruitment efficiency. J. Immunol. 177: 6450-6459.