Myeloid-derived suppressor cells down-regulate L-selectin expression on CD4+ and CD8+ T cells

Journal of Immunology

Volumn 183, Issue 2, 2009, Pages 937-944

  Hanson, Erica M ^a   Clements, Virginia K ^a   Sinha, Pratima ^a   Ilkovitch, Dan ^b   Ostrand Rosenberg, Suzanne ^a  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEIN; L SELECTIN; PROTEIN ADAM17; PROUROKINASE; UNCLASSIFIED DRUG; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE; UROKINASE;

AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MEMBRANE; COMPETITIVE INHIBITION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SUPPRESSOR CELL; TUMOR IMMUNITY; AGING; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL MOTION; CELLULAR IMMUNITY; CHEMISTRY; COCULTURE; CYTOLOGY; EXPERIMENTAL NEOPLASM; IMMUNOLOGY; METABOLISM; PARACRINE SIGNALING; PHYSIOLOGY; TUMOR CELL LINE;

ADAM PROTEINS; AGING; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELL MOVEMENT; COCULTURE TECHNIQUES; DOWN-REGULATION; IMMUNITY, CELLULAR; L-SELECTIN; MICE; MICE, INBRED BALB C; MYELOID CELLS; NEOPLASMS, EXPERIMENTAL; PARACRINE COMMUNICATION; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 70249140303     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0804253     Document Type: Article

References (75)

1. + myeloid cells suppress T cell sensitization in tumor-draining lymph nodes. J. Immunol. 181: 3291-3300.
2. Rosen, S. D. 2004. Ligands for L-selectin: homing, inflammation, and beyond. Annu. Rev. Immunol. 22: 129-156.
3. Khan, A. I., R. C. Landis, and R. Malhotra. 2003. L-selectin ligands in lymphoid tissues and models of inflammation. Inflammation 27: 265-280.
4. Xu, J., I. S. Grewal, G. P. Geba, and R. A. Flavell. 1996. Impaired primary T cell responses in L-selectin-deficient mice. J. Exp. Med. 183: 589-598.
5. Gallatin, W. M., I. L. Weissman, and E. C. Butcher. 1983. A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature 304: 30-34.
6. Bradley, L. M., S. R. Watson, and S. L. Swain. 1994. Entry of naive CD4 T cells into peripheral lymph nodes requires L-selectin. J. Exp. Med. 180: 2401-2406.
7. Lepault, F., M. C. Gagnerault, C. Faveeuw, and C. Boitard. 1994. Recirculation, phenotype and functions of lymphocytes in mice treated with monoclonal antibody MEL-14. Eur. J. Immunol. 24: 3106-3112.
8. Stremmel, C., W. Sienel, S. Eggeling, B. Passlick, and A. Slavin. 2006. Inhibition of T cell homing by down-regulation of CD62L and the induction of a Th-2 response as a method to prevent acute allograft rejection in mice. Eur. J. Cardiothorac. Surg. 30: 362-369.
9. Tedder, T. F., D. A. Steeber, and P. Pizcueta. 1995. L-selectin-deficient mice have impaired leukocyte recruitment into inflammatory sites. J. Exp. Med. 181: 2259-2264.
10. Ley, K., C. Laudanna, M. I. Cybulsky, and S. Nourshargh. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7: 678-689.
11. Hafezi-Moghadam, A., K. L. Thomas, A. J. Prorock, Y. Huo, and K. Ley. 2001. L-selectin shedding regulates leukocyte recruitment. J. Exp. Med. 193: 863-872.
12. Tang, M. L., L. P. Hale, D. A. Steeber, and T. F. Tedder. 1997. L-selectin is involved in lymphocyte migration to sites of inflammation in the skin: delayed rejection of allografts in L-selectin-deficient mice. J. Immunol. 158: 5191-5199.
13. Arbones, M. L., D. C. Ord, K. Ley, H. Ratech, C. Maynard-Curry, G. Otten, D. J. Capon, and T. F. Tedder. 1994. Lymphocyte homing and leukocyte rolling and migration are impaired in L-selectin-deficient mice. Immunity 1: 247-260.
14. Steeber, D. A., M. L. Tang, N. E. Green, X. Q. Zhang, J. E. Sloane, and T. F. Tedder. 1999. Leukocyte entry into sites of inflammation requires overlapping interactions between the L-selectin and ICAM-1 pathways. J. Immunol. 163: 2176-2186.
15. Yamada, M., K. Yanaba, M. Hasegawa, Y. Matsushita, M. Horikawa, K. Komura, T. Matsushita, A. Kawasuji, T. Fujita, K. Takehara, et al. 2006. Regulation of local and metastatic host-mediated anti-tumour mechanisms by L-selectin and intercellular adhesion molecule-1. Clin. Exp. Immunol. 143: 216-227.
16. Finn, O. J. 2003. Cancer vaccines: between the idea and the reality. Nat. Rev. Immunol. 3: 630-641.
17. + myeloid cells derived from tumor-bearing mice inhibit primary T cell activation induced through CD3/CD28 costimulation. J. Immunol. 165: 779-785.
18. + myeloid cells. J. Immunol. 166: 5398-5406.
19. Almand, B., J. I. Clark, E. Nikitina, J. van Beynen, N. R. English, S. C. Knight, D. P. Carbone, and D. I. Gabrilovich. 2001. Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J. Immunol. 166: 678-689.
20. Bronte, V., P. Serafini, E. Apolloni, and P. Zanovello. 2001. Tumor-induced immune dysfunctions caused by myeloid suppressor cells. J. Immunother. 24: 431-446.
21. Kusmartsev, S., and D. I. Gabrilovich. 2002. Immature myeloid cells and cancer-associated immune suppression. Cancer Immunol. Immunother. 51: 293-298.
22. Serafini, P., C. De Santo, I. Marigo, S. Cingarlini, L. Dolcetti, G. Gallina, P. Zanovello, and V. Bronte. 2004. Derangement of immune responses by myeloid suppressor cells. Cancer Immunol. Immunother. 53: 64-72.
23. Gabrilovich, D. I., V. Bronte, S. H. Chen, M. P. Colombo, A. Ochoa, S. Ostrand-Rosenberg, and H. Schreiber. 2007. The terminology issue for myeloid-derived suppressor cells. Cancer Res. 67: 425; author reply 426.
24. Sinha, P., C. Okoro, D. Foell, H. H. Freeze, S. Ostrand-Rosenberg, and G. Srikrishna. 2008. Proinflammatory s100 proteins regulate the accumulation of myeloid-derived suppressor cells. J. Immunol. 181: 4666-4675.
25. + T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J. Immunol. 172: 989-999.
26. Bunt, S. K., P. Sinha, V. K. Clements, J. Leips, and S. Ostrand-Rosenberg. 2006. Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J. Immunol. 176: 284-290.
27. Rodriguez, P. C., C. P. Hernandez, D. Quiceno, S. M. Dubinett, J. Zabaleta, J. B. Ochoa, J. Gilbert, and A. C. Ochoa. 2005. Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J. Exp. Med. 202: 931-939.
28. Sinha, P., V. K. Clements, and S. Ostrand-Rosenberg. 2005. Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J. Immunol. 174: 636-645. (Pubitemid 40094255)
29. Sinha, P., V. K. Clements, and S. Ostrand-Rosenberg. 2005. Interleukin-13-regulated M2 macrophages in combination with myeloid suppressor cells block immune surveillance against metastasis. Cancer Res. 65: 11743-11751.
30. Bronte, V., P. Serafini, A. Mazzoni, D. M. Segal, and P. Zanovello. 2003. L-Arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol. 24: 302-306.
31. + T cell tolerance in cancer. Nat. Med. 13: 828-835.
32. Sinha, P., V. K. Clements, S. K. Bunt, S. M. Albelda, and S. Ostrand-Rosenberg. 2007. Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J. Immunol. 179: 977-983.
33. + myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin. Cancer Res. 11: 6713-6721.
34. + T cell-mediated spontaneous diabetes in neonatal mice. J. Immunol. 157: 978-983.
35. + single positive cells with a class II major histocompatibility complex-restricted receptor. J. Exp. Med. 180: 25-34.
36. Pulaski, B. A., and S. Ostrand-Rosenberg. 1998. Reduction of established spontaneous mammary carcinoma metastases following immunotherapy with major histocompatibility complex class II and B7.1 cell-based tumor vaccines. Cancer Res. 58: 1486-1493.
37. Ilkovitch, D., M. E. Handel-Fernandez, L. M. Herbert, and D. M. Lopez. 2008. Antitumor effects of mucin 1/sec involves the modulation of urokinase-type plasminogen activator and signal transducer and activator of transcription 1 expression in tumor cells. Cancer Res. 68: 2427-2435.
38. Pulaski, B. A., D. S. Terman, S. Khan, E. Muller, and S. Ostrand-Rosenberg. 2000. Cooperativity of Staphylococcal aureus enterotoxin B superantigen, major histocompatibility complex class II, and CD80 for immunotherapy of advanced spontaneous metastases in a clinically relevant postoperative mouse breast cancer model. Cancer Res. 60: 2710-2715.
39. Pulaski, B. A., and S. Ostrand-Rosenberg. 2000. Mouse 4T1 breast Tumor Model. J. E. Coligan, A. M. Kruisbeek, D. H. Margulies, E. M. Shevach, W. Strober, eds. In Current Protocols in Immunology, 4: 20.2.1.
40. + tumor cells with interleukin-12 reduces established metastatic disease and stimulates immune effectors and monokine induced by interferon γ. Cancer Immunol. Immunother. 49: 34-45.
41. Armstrong, T. D., V. K. Clements, B. K. Martin, J. P. Ting, and S. Ostrand-Rosenberg. 1997. Major histocompatibility complex class II-transfected tumor cells present endogenous antigen and are potent inducers of tumorspecific immunity. Proc. Natl. Acad. Sci. USA 94: 6886-6891.
42. Ilkovitch, D., and D. M. Lopez. 2009. Urokinase-mediated recruitment of myeloid-derived suppressor cells and their suppressive mechanisms are blocked by MUC1/sec. Blood 113: 4729-4739.
43. Grizzle, W. E., X. Xu, S. Zhang, C. R. Stockard, C. Liu, S. Yu, J. Wang, J. D. Mountz, and H. G. Zhang. 2007. Age-related increase of tumor susceptibility is associated with myeloid-derived suppressor cell mediated suppression of T cell cytotoxicity in recombinant inbred BXD12 mice. Mech. Ageing Dev. 128: 672-680.
44. Heithoff, D. M., E. Y. Enioutina, D. Bareyan, R. A. Daynes, and M. J. Mahan. 2008. Conditions that diminish myeloid derived suppressor cell activities stimulate cross-protective immunity. Infect. Immun. 76: 5191-5199.
45. Wang, Y., A. H. Herrera, Y. Li, K. K. Belani, and B. Walcheck. 2009. Regulation of mature ADAM17 by redox agents for L-selectin shedding. J. Immunol. 182: 2449-2457.
46. Li, X., L. Perez, Z. Pan, and H. Fan. 2007. The transmembrane domain of TACE regulates protein ectodomain shedding. Cell Res. 17: 985-998.
47. Lee, D., J. B. Schultz, P. A. Knauf, and M. R. King. 2007. Mechanical shedding of L-selectin from the neutrophil surface during rolling on sialyl Lewis X under flow. J. Biol. Chem. 282: 4812-4820.
48. Li, Y., J. Brazzell, A. Herrera, and B. Walcheck. 2006. ADAM17 deficiency by mature neutrophils has differential effects on L-selectin shedding. Blood 108: 2275-2279.
49. Smalley, D. M., and K. Ley. 2005. L-selectin: mechanisms and physiological significance of ectodomain cleavage. J. Cell. Mol. Med. 9: 255-266.
50. Charbonneau, M., K. Harper, F. Grondin, M. Pelmus, P. P. McDonald, and C. M. Dubois. 2007. Hypoxia-inducible factor mediates hypoxic and tumor necrosis factor α-induced increases in tumor necrosis factor-α converting enzyme/ADAM17 expression by synovial cells. J. Biol. Chem. 282: 33714-33724.
51. + T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res. 58: 3491-3494.
52. + T-lymphocytes. Lab. Invest. 75: 67-76.
53. + T cells with broad anti-tumor efficacy are naturally sensitized during tumor progression. J. Immunol. 165: 5738-5749.
54. Carriere, V., R. Colisson, C. Jiguet-Jiglaire, E. Bellard, G. Bouche, T. Al Saati, F. Amalric, J. P. Girard, and C. M'Rini. 2005. Cancer cells regulate lymphocyte recruitment and leukocyte-endothelium interactions in the tumor-draining lymph node. Cancer Res. 65: 11639-11648.
55. Jung, T. M., W. M. Gallatin, I. L. Weissman, and M. O. Dailey. 1988. Downregulation of homing receptors after T cell activation. J. Immunol. 141: 4110-4117.
56. Rosato, A., A. Zambon, B. Macino, S. Mandruzzato, V. Bronte, G. Milan, P. Zanovello, and D. Collavo. 1996. Anti-L-selectin monoclonal antibody treatment in mice enhances tumor growth by preventing CTL sensitization in peripheral lymph nodes draining the tumor area. Int. J. Cancer 65: 847-851.
57. Allavena, P., C. Garlanda, M. G. Borrello, A. Sica, and A. Mantovani. 2008. Pathways connecting inflammation and cancer. Curr. Opin. Genet. Dev. 18: 3-10.
58. Coussens, L. M., and Z. Werb. 2002. Inflammation and cancer. Nature 420: 860-867.
59. Ley, K., D. C. Bullard, M. L. Arbones, R. Bosse, D. Vestweber, T. F. Tedder, and A. L. Beaudet. 1995. Sequential contribution of L- and P-selectin to leukocyte rolling in vivo. J. Exp. Med. 181: 669-675.
60. Kishimoto, T. K., M. A. Jutila, E. L. Berg, and E. C. Butcher. 1989. Neutrophil Mac-1 and MEL-14 adhesion proteins inversely regulated by chemotactic factors. Science 245: 1238-1241.
61. Jung, T. M., and M. O. Dailey. 1990. Rapid modulation of homing receptors (gp90MEL-14) induced by activators of protein kinase C: receptor shedding due to accelerated proteolytic cleavage at the cell surface. J. Immunol. 144: 3130-3136.
62. Rizoli, S. B., O. D. Rotstein, and A. Kapus. 1999. Cell volume-dependent regulation of L-selectin shedding in neutrophils: a role for p38 mitogen-activated protein kinase. J. Biol. Chem. 274: 22072-22080.
63. Stibenz, D., C. Buhrer, D. Laufer, and M. Obladen. 1996. CD45 engagement induces L-selectin down-regulation. Scand. J. Immunol. 44: 37-44.
64. Miethke, T., C. Wahl, B. Holzmann, K. Heeg, and H. Wagner. 1993. Bacterial superantigens induce rapid and T cell receptor Vβ-selective down-regulation of L-selectin (gp90Mel-14) in vivo. J. Immunol. 151: 6777-6782. (Pubitemid 24001052)
65. Walev, I., D. Tappe, E. Gulbins, and S. Bhakdi. 2000. Streptolysin O-permeabilized granulocytes shed L-selectin concomitantly with ceramide generation via neutral sphingomyelinase. J. Leukocyte Biol. 68: 865-872.
66. Phong, M. C., P. Gutwein, S. Kadel, K. Hexel, P. Altevogt, O. Linderkamp, and B. Brenner. 2003. Molecular mechanisms of L-selectin-induced co-localization in rafts and shedding [corrected]. Biochem. Biophys. Res. Commun. 300: 563-569.
67. Stoddart, J. H., Jr., R. R. Jasuja, M. A. Sikorski, U. H. von Andrian, and J. W. Mier. 1996. Protease-resistant L-selectin mutants: down-modulation by cross-linking but not cellular activation. J. Immunol. 157: 5653-5659.
68. Palecanda, A., B. Walcheck, D. K. Bishop, and M. A. Jutila. 1992. Rapid activation- independent shedding of leukocyte L-selectin induced by cross-linking of the surface antigen. Eur. J. Immunol. 22: 1279-1286.
69. Galkina, E., K. Tanousis, G. Preece, M. Tolaini, D. Kioussis, O. Florey, D. O. Haskard, T. F. Tedder, and A. Ager. 2003. L-selectin shedding does not regulate constitutive T cell trafficking but controls the migration pathways of antigen-activated T lymphocytes. J. Exp. Med. 198: 1323-1335.
70. Peschon, J. J., J. L. Slack, P. Reddy, K. L. Stocking, S. W. Sunnarborg, D. C. Lee, W. E. Russell, B. J. Castner, R. S. Johnson, J. N. Fitzner, et al. 1998. An essential role for ectodomain shedding in mammalian development. Science 282: 1281-1284.
71. Arribas, J., L. Coodly, P. Vollmer, T. K. Kishimoto, S. Rose-John, and J. Massague. 1996. Diverse cell surface protein ectodomains are shed by a system sensitive to metalloprotease inhibitors. J. Biol. Chem. 271: 11376-11382.
72. Borland, G., G. Murphy, and A. Ager. 1999. Tissue inhibitor of metalloproteinases-3 inhibits shedding of L-selectin from leukocytes. J. Biol. Chem. 274: 2810-2815.
73. Bunt, S. K., L. Yang, P. Sinha, V. K. Clements, J. Leips, and S. Ostrand-Rosenberg. 2007. Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res. 67: 10019-10026.
74. + immature myeloid cells mediate suppression of T cells in mice bearing tumors of IL-1β-secreting cells. J. Immunol. 175: 8200-8208.
75. Cheng, P., C. A. Corzo, N. Luetteke, B. Yu, S. Nagaraj, M. M. Bui, M. Ortiz, W. Nacken, C. Sorg, T. Vogl, et al. 2008. Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J. Exp. Med. 205: 2235-2249.