IL-18 is involved in eosinophil-mediated tumoricidal activity against a colon carcinoma cell line by upregulating LFA-1 and ICAM-1

Journal of Immunology

Volumn 195, Issue 5, 2015, Pages 2483-2492

  Gatault, Solène ^a   Delbeke, Marie ^a   Driss, Virginie ^a   Sarazin, Aurore ^a   Dendooven, Arnaud ^a   Kahn, Jean Emmanuel ^b,c   Lefèvre, Guillaume ^c,d   Capron, Monique ^a  

^a UNIVERSITÉ DE LILLE   (France)

^b LABORATOIRE DES SCIENCES DU CLIMAT ET DE L ENVIRONNEMENT   (France)

^c UNIV LILLE   (France)

^d LILLE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD18 ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 8; JUNCTIONAL ADHESION MOLECULE A; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MESSENGER RNA; INTERLEUKIN 18; RECOMBINANT PROTEIN;

ADAPTIVE IMMUNITY; ANTIGEN BINDING; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CARCINOMA CELL LINE; CELL ADHESION; CELL CONTACT; CELL INTERACTION; CELL MEDIATED CYTOTOXICITY; COLO 205 CELL LINE; COLON CARCINOMA; CONTROLLED STUDY; EOSINOPHIL; GAMMA DELTA T LYMPHOCYTE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IL 18 GENE; INNATE IMMUNITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; CACO 2 CELL LINE; CELL CULTURE; COLON TUMOR; CYTOTOXICITY; DRUG EFFECTS; FLOW CYTOMETRY; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ANTIGENS, CD11A; APOPTOSIS; BLOTTING, WESTERN; CACO-2 CELLS; CELL ADHESION; CELL LINE, TUMOR; CELLS, CULTURED; COLONIC NEOPLASMS; CYTOTOXICITY, IMMUNOLOGIC; EOSINOPHILS; FLOW CYTOMETRY; GENE EXPRESSION; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; INTERLEUKIN-18; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; RECOMBINANT PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UP-REGULATION;

EID: 84940121985     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402914     Document Type: Article

References (59)

1. Rothenberg, M. E., and S. P. Hogan. 2006. The eosinophil. Annu. Rev. Immunol. 24: 147-174.
2. Costello, R., T. O'Callaghan, and G. Sébahoun. 2005. [Eosinophils and antitumour response]. Rev. Med. Interne 26: 479-484.
3. Gatault, S., F. Legrand, M. Delbeke, S. Loiseau, and M. Capron. 2012. Involvement of eosinophils in the anti-tumor response. Cancer Immunol. Immunother. 61: 1527-1534.
4. Pretlow, T. P., E. F. Keith, A. K. Cryar, A. A. Bartolucci, A. M. Pitts, T. G. Pretlow, II, P. M. Kimball, and E. A. Boohaker. 1983. Eosinophil infiltration of human colonic carcinomas as a prognostic indicator. Cancer Res. 43: 2997-3000.
5. Fernández-Aceñero, M. J., M. Galindo-Gallego, J. Sanz, and A. Aljama. 2000. Prognostic influence of tumor-associated eosinophilic infiltrate in colorectal carcinoma. Cancer 88: 1544-1548.
6. Nielsen, H. J., U. Hansen, I. J. Christensen, C. M. Reimert, N. Brünner, and F. Moesgaard. 1999. Independent prognostic value of eosinophil and mast cell infiltration in colorectal cancer tissue. J. Pathol. 189: 487-495.
7. Harbaum, L., M. J. Pollheimer, P. Kornprat, R. A. Lindtner, C. Bokemeyer, and C. Langner. 2014. Peritumoral eosinophils predict recurrence in colorectal cancer. Mod. Pathol. 28: 403-413.
8. Legrand, F., V. Driss, G. Woerly, S. Loiseau, E. Hermann, J.-J. Fournié, L. Héliot, V. Mattot, F. Soncin, M.-L. Gougeon, et al. 2009. A functional gammadeltaTCR/CD3 complex distinct from gammadeltaT cells is expressed by human eosinophils. PLoS One 4: e5926.
9. Legrand, F., V. Driss, M. Delbeke, S. Loiseau, E. Hermann, D. Dombrowicz, and M. Capron. 2010. Human eosinophils exert TNF-α and granzyme A-mediated tumoricidal activity toward colon carcinoma cells. J. Immunol. 185: 7443-7451.
10. Munitz, A., I. Bachelet, S. Fraenkel, G. Katz, O. Mandelboim, H.-U. Simon, L. Moretta, M. Colonna, and F. Levi-Schaffer. 2005. 2B4 (CD244) is expressed and functional on human eosinophils. J. Immunol. 174: 110-118.
11. Fantuzzi, G., and C. A. Dinarello. 1999. Interleukin-18 and interleukin-1 beta: two cytokine substrates for ICE (caspase-1). J. Clin. Immunol. 19: 1-11.
12. Okamura, H., H. Tsutsi, T. Komatsu, M. Yutsudo, A. Hakura, T. Tanimoto, K. Torigoe, T. Okura, Y. Nukada, K. Hattori, et al. 1995. Cloning of a new cytokine that induces IFN-γ production by T cells. Nature 378: 88-91.
13. Sawada, M., T. Kawayama, H. Imaoka, Y. Sakazaki, H. Oda, S. Takenaka, Y. Kaku, K. Azuma, M. Tajiri, N. Edakuni, et al. 2013. IL-18 induces airway hyperresponsiveness and pulmonary inflammation via CD4+ T cell and IL-13. PLoS One 8: e54623.
14. Freeman, C. M., M. K. Han, F. J. Martinez, S. Murray, L. X. Liu, S. W. Chensue, T. J. Polak, J. Sonstein, J. C. Todt, T. M. Ames, et al. 2010. Cytotoxic potential oflung CD8(+) T cells increases with chronic obstructive pulmonary disease severity and with in vitro stimulation by IL-18 or IL-15. J. Immunol. 184: 6504-6513.
15. Tanaka, F., W. Hashimoto, H. Okamura, P. D. Robbins, M. T. Lotze, and H. Tahara. 2000. Rapid generation of potent and tumor-specific cytotoxic T lymphocytes by interleukin 18 using dendritic cells and natural killer cells. Cancer Res. 60: 4838-4844.
16. Sugie, T., K. Murata-Hirai, M. Iwasaki, C. T. Morita, W. Li, H. Okamura, N. Minato, M. Toi, and Y. Tanaka. 2013. Zoledronic acid-induced expansion of gd T cells from early-stage breast cancer patients: effect of IL-18 on helper NK cells. Cancer Immunol. Immunother. 62: 677-687.
17. Leung, B. P., S. Culshaw, J. A. Gracie, D. Hunter, C. A. Canetti, C. Campbell, F. Cunha, F. Y. Liew, and I. B. McInnes. 2001. A role for IL-18 in neutrophil activation. J. Immunol. 167: 2879-2886.
18. Chow, J. Y., C. K. Wong, P. F. Cheung, and C. W. Lam. 2010. Intracellular signaling mechanisms regulating the activation of human eosinophils by the novel Th2 cytokine IL-33: implications for allergic inflammation. Cell. Mol. Immunol. 7: 26-34.
19. Palma, G., A. Barbieri, S. Bimonte, M. Palla, S. Zappavigna, M. Caraglia, P. A. Ascierto, G. Ciliberto, and C. Arra. 2013. Interleukin 18: friend or foe in cancer. Biochim. Biophys. Acta 1836: 296-303.
20. Nakamori, M., M. Iwahashi, M. Nakamura, K. Ueda, X. Zhang, and H. Yamaue. 2003. Intensification of antitumor effect by T helper 1-dominant adoptive immunogene therapy for advanced orthotopic colon cancer. Clin. Cancer Res. 9: 2357-2365.
21. Hashimoto, W., T. Osaki, H. Okamura, P. D. Robbins, M. Kurimoto, S. Nagata, M. T. Lotze, and H. Tahara. 1999. Differential antitumor effects of administration of recombinant IL-18 or recombinant IL-12 are mediated primarily by Fas-Fas ligandand perforin-induced tumor apoptosis, respectively. J. Immunol. 163: 583-589.
22. Osaki, T., J.-M. Péron, Q. Cai, H. Okamura, P. D. Robbins, M. Kurimoto, M. T. Lotze, and H. Tahara. 1998. IFN-γ-inducing factor/IL-18 administration mediates IFN-γ-and IL-12-independent antitumor effects. J. Immunol. 160: 1742-1749.
23. Tian, H., G. Shi, G. Yang, J. Zhang, Y. Li, T. Du, J. Wang, F. Xu, L. Cheng, X. Zhang, et al. 2014. Cellular immunotherapy using irradiated lung cancer cell vaccine co-expressing GM-CSF and IL-18 can induce significant antitumor effects. BMC Cancer 14: 48.
24. Zhang, B., K.-F. Wu, Y.-M. Lin, X.-T. Ma, Q. Rao, G.-G. Zheng, Z.-Y. Cao, G. Li, and Y.-H. Song. 2004. Gene transfer of pro-IL-18 and IL-1β converting enzyme cDNA induces potent antitumor effects in L1210 cells. Leukemia 18: 817-825.
25. Zaki, M. H., M. Lamkanfi, and T.-D. Kanneganti. 2011. The Nlrp3 inflammasome: contributions to intestinal homeostasis. Trends Immunol. 32: 171-179.
26. Salcedo, R., A. Worschech, M. Cardone, Y. Jones, Z. Gyulai, R.-M. Dai, E. Wang, W. Ma, D. Haines, C. O'hUigin, et al. 2010. MyD88-mediated signaling prevents development of adenocarcinomas of the colon: role of interleukin 18. J. Exp. Med. 207: 1625-1636.
27. Zaki, M. H., P. Vogel, M. Body-Malapel, M. Lamkanfi, and T.-D. Kanneganti. 2010. IL-18 production downstream of the Nlrp3 inflammasome confers protection against colorectal tumor formation. J. Immunol. 185: 4912-4920.
28. Allen, I. C., E. M. TeKippe, R.-M. T. Woodford, J. M. Uronis, E. K. Holl, A. B. Rogers, H. H. Herfarth, C. Jobin, and J. P.-Y. Ting. 2010. The NLRP3 inflammasome functions as a negative regulator of tumorigenesis during colitisassociated cancer. J. Exp. Med. 207: 1045-1056.
29. Higashi, K., S. Hazama, A. Araki, K. Yoshimura, N. Iizuka, S. Yoshino, T. Noma, and M. Oka. 2014. A novel cancer vaccine strategy with combined IL-18 and HSV-TK gene therapy driven by the hTERT promoter in a murine colorectal cancer model. Int. J. Oncol. 45: 1412-1420.
30. Hoffmann, D., W. Bayer, T. Grunwald, and O. Wildner. 2007. Intratumoral expression of respiratory syncytial virus fusion protein in combination with cytokines encoded by adenoviral vectors as in situ tumor vaccine for colorectal cancer. Mol. Cancer Ther. 6: 1942-1950.
31. Pages, F., A. Berger, S. Lebel-Binay, F. Zinzindohoue, C. Danel, B. Piqueras, O. Carriere, N. Thiounn, P. H. Cugnenc, and W. H. Fridman. 2000. Proinflammatory and antitumor properties of interleukin-18 in the gastrointestinal tract. Immunol. Lett. 75: 9-14.
32. Woerly, G., N. Roger, S. Loiseau, D. Dombrowicz, A. Capron, and M. Capron. 1999. Expression of CD28 and CD86 by human eosinophils and role in the secretion of type 1 cytokines (interleukin 2 and interferon g): inhibition by immunoglobulin a complexes. J. Exp. Med. 190: 487-495.
33. Driss, V., F. Legrand, E. Hermann, S. Loiseau, Y. Guerardel, L. Kremer, E. Adam, G. Woerly, D. Dombrowicz, and M. Capron. 2009. TLR2-dependent eosinophil interactions with mycobacteria: role of a-defensins. Blood 113: 3235-3244.
34. Dinarello, C. A., D. Novick, S. Kim, and G. Kaplanski. 2013. Interleukin-18 and IL-18 binding protein. Front. Immunol. 4: 289.
35. Tai, P. C., C. J. Spry, D. M. Bakes, and J. R. Barkans. 1985. Eosinophil membrane antigens: phenotypic frequencies in normal individuals and patients with the hypereosinophilic syndrome. Int. Arch. Allergy Appl. Immunol. 77: 249-251.
36. Lantero, S., D. Spallarossa, M. Silvestri, F. Sabatini, L. Scarso, E. Crimi, and G. A. Rossi. 2002. In allergic asthma experimental exposure to allergens is associated with depletion of blood eosinophils overexpressing LFA-1. Allergy 57: 1036-1043.
37. Pernot, S., M. Terme, T. Voron, O. Colussi, E. Marcheteau, E. Tartour, and J. Taieb. 2014. Colorectal cancer and immunity: what we know and perspectives. World J. Gastroenterol. 20: 3738-3750.
38. Decot, V., G. Woerly, M. Loyens, S. Loiseau, B. Quatannens, M. Capron, and D. Dombrowicz. 2005. Heterogeneity of expression of IgA receptors by human, mouse, and rat eosinophils. J. Immunol. 174: 628-635.
39. von Wasielewski, R., S. Seth, J. Franklin, R. Fischer, K. Hübner, M. L. Hansmann, V. Diehl, and A. Georgii. 2000. Tissue eosinophilia correlates strongly with poor prognosis in nodular sclerosing Hodgkin's disease, allowing for known prognostic factors. Blood 95: 1207-1213.
40. Glimelius, I., J. Rubin, K. Rostgaard, R.-M. Amini, M. Simonsson, K. M. Sorensen, K. E. Smedby, P. Venge, H. Hjalgrim, D. Molin, and G. Enblad. 2011. Predictors of histology, tissue eosinophilia and mast cell infiltration in Hodgkin's lymphoma-a population-based study. Eur. J. Haematol. 87: 208-216.
41. Nutten, S., J.-P. Papin, G. Woerly, D. W. Dunne, J. MacGregor, F. Trottein, and M. Capron. 1999. Selectin and Lewis(x) are required as co-receptors in antibodydependent cell-mediated cytotoxicity of human eosinophils to Schistosoma mansoni schistosomula. Eur. J. Immunol. 29: 799-808.
42. Bleijs, D. A., R. de Waal-Malefyt, C. G. Figdor, and Y. van Kooyk. 1999. Costimulation of T cells results in distinct IL-10 and TNF-α cytokine profiles dependent on binding to ICAM-1, ICAM-2 or ICAM-3. Eur. J. Immunol. 29: 2248-2258.
43. Fraemohs, L., R. R. Koenen, G. Ostermann, B. Heinemann, and C. Weber. 2004. The functional interaction of the b 2 integrin lymphocyte function-associated antigen-1 with junctional adhesion molecule-A is mediated by the I domain. J. Immunol. 173: 6259-6264.
44. Laukoetter, M. G., P. Nava, W. Y. Lee, E. A. Severson, C. T. Capaldo, B. A. Babbin, I. R. Williams, M. Koval, E. Peatman, J. A. Campbell, et al. 2007. JAM-A regulates permeability and inflammation in the intestine in vivo. J. Exp. Med. 204: 3067-3076.
45. Wojcikiewicz, E. P., R. R. Koenen, L. Fraemohs, J. Minkiewicz, H. Azad, C. Weber, and V. T. Moy. 2009. LFA-1 binding destabilizes the JAM-A homophilic interaction during leukocyte transmigration. Biophys. J. 96: 285-293.
46. Van Seventer, G. A., Y. Shimizu, K. J. Horgan, and S. Shaw. 1990. The LFA-1 ligand ICAM-1 provides an important costimulatory signal for T cell receptormediated activation of resting T cells. J. Immunol. 144: 4579-4586.
47. Anikeeva, N., M. Steblyanko, S. Fayngerts, N. Kopylova, D. J. Marshall, G. D. Powers, T. Sato, K. S. Campbell, and Y. Sykulev. 2014. Integrin receptors on tumor cells facilitate NK cell-mediated antibody-dependent cytotoxicity. Eur. J. Immunol. 44: 2331-2339.
48. Haustein, M., R. Ramer, M. Linnebacher, K. Manda, and B. Hinz. 2014. Cannabinoids increase lung cancer cell lysis by lymphokine-activated killer cells via upregulation of ICAM-1. Biochem. Pharmacol. 92: 312-325.
49. Ren, Z., W. Kang, L. Wang, B. Sun, J. Ma, C. Zheng, J. Sun, Z. Tian, X. Yang, and W. Xiao. 2014. E2F1 renders prostate cancer cell resistant to ICAM-1 mediated antitumor immunity by NF-κB modulation. Mol. Cancer 13: 84.
50. Tachimori, A., N. Yamada, Y. Sakate, M. Yashiro, K. Maeda, M. Ohira, H. Nishino, and K. Hirakawa. 2005. Up regulation of ICAM-1 gene expression inhibits tumour growth and liver metastasis in colorectal carcinoma. Eur. J. Cancer 41: 1802-1810.
51. Wang, R., J. J. Jaw, N. C. Stutzman, Z. Zou, and P. D. Sun. 2012. Natural killer cell-produced IFN-γ and TNF-α induce target cell cytolysis through upregulation of ICAM-1. J. Leukoc. Biol. 91: 299-309.
52. Kang, J. S., S. Y. Bae, H. R. Kim, Y. S. Kim, D. J. Kim, B. J. Cho, H.-K. Yang, Y.-I. Hwang, K. J. Kim, H. S. Park, et al. 2009. Interleukin-18 increases metastasis and immune escape of stomach cancer via the downregulation of CD70 and maintenance of CD44. Carcinogenesis 30: 1987-1996.
53. Robertson, M. J., J. W. Mier, T. Logan, M. Atkins, H. Koon, K. M. Koch, S. Kathman, L. N. Pandite, C. Oei, L. C. Kirby, et al. 2006. Clinical and biological effects of recombinant human interleukin-18 administered by intravenous infusion to patients with advanced cancer. Clin. Cancer Res. 12: 4265-4273.
54. Wang, W., T. Tanaka, H. Okamura, M. Sugita, S. Higa, T. Kishimoto, and M. Suemura. 2001. Interleukin-18 enhances the production of interleukin-8 by eosinophils. Eur. J. Immunol. 31: 1010-1016.
55. Tomita, Y., H. Watanabe, H. Kobayashi, T. Nishiyama, S. Tsuji, K. Imai, T. Abo, M. Fujiwara, and S. Sato. 1993. Expression of intercellular adhesion molecule-1 on transitional cell cancer. Possible significance in immunity against tumor cells. Am. J. Pathol. 143: 191-198.
56. Stuyt, R. J. L., M. G. Netea, T. B. H. Geijtenbeek, B. J. Kullberg, C. A. Dinarello, and J. W. M. van der Meer. 2003. Selective regulation of intercellular adhesion molecule-1 expression by interleukin-18 and interleukin-12 on human monocytes. Immunology 110: 329-334.
57. Kohka, H., T. Yoshino, H. Iwagaki, I. Sakuma, T. Tanimoto, Y. Matsuo, M. Kurimoto, K. Orita, T. Akagi, and N. Tanaka. 1998. Interleukin-18/interferon-gamma-inducing factor, a novel cytokine, up-regulates ICAM-1 (CD54) expression in KG-1 cells. J. Leukoc. Biol. 64: 519-527.
58. Toomer, K. H., and Z. Chen. 2014. Autoimmunity as a double agent in tumor killing and cancer promotion. Front. Immunol. 5: 116.
59. Zhang, M., R. Guo, Y. Zhai, X.-Y. Fu, and D. Yang. 2003. Light stimulates IFNgamma-mediated intercellular adhesion molecule-1 upregulation of cancer cells. Hum. Immunol. 64: 416-426.