Expression of immune checkpoint molecules of T cell immunoglobulin and mucin protein 3/galectin-9 for NK cell suppression in human gastrointestinal stromal tumors

Oncology Reports

Volumn 34, Issue 4, 2015, Pages 2099-2105

  Komita, Hideo ^a   Koido, Shigeo ^a,b   Hayashi, Kazumi ^b   Kan, Shin ^b   Ito, Masaki ^b   Kamata, Yuko ^b   Suzuki, Masafumi ^b   Homma, Sadamu ^b  

^a Division of Gastroenterology and Hepatology   (Japan)

^b JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Galectin 9; Gastrointestinal stromal tumor; Immune checkpoint; Natural killer cell; T cell immunoglobulin and mucin protein 3

Indexed keywords

CD56 ANTIGEN; ECALECTIN; PEPTIDES AND PROTEINS; PROGRAMMED DEATH 1 RECEPTOR; T CELL IMMUNOGLOBULIN AND MUCIN PROTEIN 3; UNCLASSIFIED DRUG; CD69 ANTIGEN; GALECTIN; HAVCR2 PROTEIN, HUMAN; LECTIN; LEUKOCYTE ANTIGEN; LGALS9 PROTEIN, HUMAN; MEMBRANE PROTEIN; NCAM1 PROTEIN, HUMAN; T LYMPHOCYTE ANTIGEN;

ADULT; AGED; ARTICLE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GASTROINTESTINAL STROMAL TUMOR; HUMAN; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; LYMPHOCYTIC INFILTRATION; MALE; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR IMMUNITY; IMMUNOLOGY; METABOLISM; MIDDLE AGED; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD; ANTIGENS, CD56; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; GALECTINS; GASTROINTESTINAL STROMAL TUMORS; HUMANS; KILLER CELLS, NATURAL; LECTINS, C-TYPE; MALE; MEMBRANE PROTEINS; MIDDLE AGED;

EID: 84939188238     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2015.4149     Document Type: Article

References (46)

1. Miettinen M and Lasota J: Gastrointestinal stromal tumors-definition, clinical, histological, immunohistochemical, and molecular genetic features and differential diagnosis. Virchows Arch 438: 1-12, 2001.
2. Hirota S, Isozaki K, Moriyama Y, Hashimoto K, Nishida T, Ishiguro S, Kawano K, Hanada M, Kurata A, Takeda M, et al: Gain-of-function mutations of c-kit in human gastrointestinal stromal tumors. Science 279: 577-580, 1998.
3. Rubin BP, Singer S, Tsao C, Duensing A, Lux ML, Ruiz R, Hibbard MK, Chen CJ, Xiao S, Tuveson DA, et al: KIT activation is a ubiquitous feature of gastrointestinal stromal tumors. Cancer Res 61: 8118-8121, 2001.
4. Corless CL, Fletcher JA and Heinrich MC: Biology of gastrointestinal stromal tumors. J Clin Oncol 22: 3813-3825, 2004.
5. Demetri GD, von Mehren M, Blanke CD, Van den Abbeele AD, Eisenberg B, Roberts PJ, Heinrich MC, Tuveson DA, Singer S, Janicek M, et al: Efficacy and safety of imatinib mesylate in advanced gastrointestinal stromal tumors. N Engl J Med 347: 472-480, 2002.
6. Le Cesne A, Ray-Coquard I, Bui BN, Adenis A, Rios M, Bertucci F, Duffaud F, Chevreau C, Cupissol D, Cioffi A, et al; French Sarcoma Group: Discontinuation of imatinib in patients with advanced gastrointestinal stromal tumours after 3 years of treatment: An open-label multicentre randomised phase 3 trial. Lancet Oncol 11: 942-949, 2010.
7. Rusakiewicz S, Semeraro M, Sarabi M, Desbois M, Locher C, Mendez R, Vimond N, Concha A, Garrido F, Isambert N, et al: Immune infiltrates are prognostic factors in localized gastrointestinal stromal tumors. Cancer Res 73: 3499-3510, 2013.
8. Rubin BP, Heinrich MC and Corless CL: Gastrointestinal stromal tumour. Lancet 369: 1731-1741, 2007.
9. Ménard C, Blay JY, Borg C, Michiels S, Ghiringhelli F, Robert C, Nonn C, Chaput N, Taïeb J, Delahaye NF, et al: Natural killer cell IFN-gamma levels predict long-term survival with imatinib mesylate therapy in gastrointestinal stromal tumor-bearing patients. Cancer Res 69: 3563-3569, 2009.
10. Borg C, Terme M, Taïeb J, Ménard C, Flament C, Robert C, Maruyama K, Wakasugi H, Angevin E, Thielemans K, et al: Novel mode of action of c-kit tyrosine kinase inhibitors leading to NK cell-dependent antitumor effects. J Clin Invest 114: 379-388, 2004.
11. Perez D, Herrmann T, Jungbluth AA, Samartzis P, Spagnoli G, Demartines N, Clavien PA, Marino S, Seifert B and Jaeger D: Cancer testis antigen expression in gastrointestinal stromal tumors: New markers for early recurrence. Int J Cancer 123: 1551-1555, 2008.
12. Perez D, Hauswirth F, Jäger D, Metzger U, Samartzis EP, Went P and Jungbluth A: Protein expression of cancer testis antigens predicts tumor recurrence and treatment response to imatinib in gastrointestinal stromal tumors. Int J Cancer 128: 2947-2952, 2011.
13. Ghadban T, Perez DR, Vashist YK, Bockhorn M, Koenig AM, El Gammal AT, Izbicki JR, Metzger U, Hauswirth F, Frosina D, et al: Expression of cancer testis antigens CT10 (MAGE-C2) and GAGE in gastrointestinal stromal tumors. Eur J Surg Oncol 40: 1307-1312, 2014.
14. Kang GH, Kim KM, Noh JH, Sohn TS, Kim S, Park CK, Lee CS and Kang DY: WT-1 expression in gastrointestinal stromal tumours. Pathology 42: 54-57, 2010.
15. Pardoll DM: The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 12: 252-264, 2012.
16. Ramsay AG: Immune checkpoint blockade immunotherapy to activate anti-tumour T-cell immunity. Br J Haematol 162: 313-325, 2013.
17. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, et al: Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 363: 711-723, 2010.
18. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K, et al: Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 369: 122-133, 2013.
19. Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, Walsh LA, Postow MA, Wong P, Ho TS, et al: Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 371: 2189-2199, 2014.
20. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al: Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 366: 2443-2454, 2012.
21. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, et al: Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 366: 2455-2465, 2012.
22. da Silva IP, Gallois A, Jimenez-Baranda S, Khan S, Anderson AC, Kuchroo VK, Osman I and Bhardwaj N: Reversal of NK-cell exhaustion in advanced melanoma by Tim-3 blockade. Cancer Immunol Res 2: 410-422, 2014.
23. Fujihara S, Mori H, Kobara H, Rafiq K, Niki T, Hirashima M and Masaki T: Galectin-9 in cancer therapy. Recent Pat Endocr Metab Immune Drug Discov 7: 130-137, 2013.
24. Leffler H, Carlsson S, Hedlund M, Qian Y and Poirier F: Introduction to galectins. Glycoconj J 19: 433-440, 2004.
25. Heusschen R, Griffioen AW and Thijssen VL: Galectin-9 in tumor biology: A jack of multiple trades. Biochim Biophys Acta 1836: 177-185, 2013.
26. Irie A, Yamauchi A, Kontani K, Kihara M, Liu D, Shirato Y, Seki M, Nishi N, Nakamura T, Yokomise H, et al: Galectin-9 as a prognostic factor with antimetastatic potential in breast cancer. Clin Cancer Res 11: 2962-2968, 2005.
27. van den Brûle F, Califice S and Castronovo V: Expression of galectins in cancer: A critical review. Glycoconj J 19: 537-542, 2004.
28. Yang RY and Liu FT: Galectins in cell growth and apoptosis. Cell Mol Life Sci 60: 267-276, 2003.
29. Liu FT, Yang RY, Saegusa J, Chen HY and Hsu DK: Galectins in regulation of apoptosis. Adv Exp Med Biol 705: 431-442, 2011.
30. Kageshita T, Kashio Y, Yamauchi A, Seki M, Abedin MJ, Nishi N, Shoji H, Nakamura T, Ono T and Hirashima M: Possible role of galectin-9 in cell aggregation and apoptosis of human melanoma cell lines and its clinical significance. Int J Cancer 99: 809-816, 2002.
31. Kobayashi T, Kuroda J, Ashihara E, Oomizu S, Terui Y, Taniyama A, Adachi S, Takagi T, Yamamoto M, Sasaki N, et al: Galectin-9 exhibits anti-myeloma activity through JNK and p38 MAP kinase pathways. Leukemia 24: 843-850, 2010.
32. Nobumoto A, Nagahara K, Oomizu S, Katoh S, Nishi N, Takeshita K, Niki T, Tominaga A, Yamauchi A and Hirashima M: Galectin-9 suppresses tumor metastasis by blocking adhesion to endothelium and extracellular matrices. Glycobiology 18: 735-744, 2008.
33. van Dongen M, Savage ND, Jordanova ES, Briaire-de Bruijn IH, Walburg KV, Ottenhoff TH, Hogendoorn PC, van der Burg SH, Gelderblom H and van Hall T: Anti-inflammatory M2 type macrophages characterize metastasized and tyrosine kinase inhibitor-treated gastrointestinal stromal tumors. Int J Cancer 127: 899-909, 2010.
34. Cameron S, Haller F, Dudas J, Moriconi F, Gunawan B, Armbrust T, Langer C, Füzesi L and Ramadori G: Immune cells in primary gastrointestinal stromal tumors. Eur J Gastroenterol Hepatol 20: 327-334, 2008.
35. Z hu C, Anderson AC, Schubart A, Xiong H, Imitola J, Khoury SJ, Zheng XX, Strom TB and Kuchroo VK: The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 6: 1245-1252, 2005.
36. Li H, Wu K, Tao K, Chen L, Zheng Q, Lu X, Liu J, Shi L, Liu C, Wang G, et al: Tim-3/galectin-9 signaling pathway mediates T-cell dysfunction and predicts poor prognosis in patients with hepatitis B virus-associated hepatocellular carcinoma. Hepatology 56: 1342-1351, 2012.
37. Ju Y, Hou N, Meng J, Wang X, Zhang X, Zhao D, Liu Y, Zhu F, Zhang L, Sun W, et al: T cell immunoglobulin-and mucin-domain-containing molecule-3 (Tim-3) mediates natural killer cell suppression in chronic hepatitis B. J Hepatol 52: 322-329, 2010.
38. Han G, Chen G, Shen B and Li Y: Tim-3: An activation marker and activation limiter of innate immune cells. Front Immunol 4: 449, 2013.
39. Hou H, Liu W, Wu S, Lu Y, Peng J, Zhu Y, Lu Y, Wang F and Sun Z: Tim-3 negatively mediates natural killer cell function in LPS-induced endotoxic shock. PLoS One 9: e110585, 2014.
40. Golden-Mason L, McMahan RH, Strong M, Reisdorph R, Mahaffey S, Palmer BE, Cheng L, Kulesza C, Hirashima M, Niki T, et al: Galectin-9 functionally impairs natural killer cells in humans and mice. J Virol 87: 4835-4845, 2013.
41. Gleason MK, Lenvik TR, McCullar V, Felices M, O'Brien MS, Cooley SA, Verneris MR, Cichocki F, Holman CJ, Panoskaltsis? Mortari A, et al: Tim-3 is an inducible human natural killer cell receptor that enhances interferon gamma production in response to galectin-9. Blood 119: 3064-3072, 2012.
42. Ferris RL, Lu B and Kane LP: Too much of a good thing Tim-3 and TCR signaling in T cell exhaustion. J Immunol 193: 1525-1530, 2014.
43. Ndhlovu LC, Lopez-Vergès S, Barbour JD, Jones RB, Jha AR, Long BR, Schoeffler EC, Fujita T, Nixon DF and Lanier LL: Tim-3 marks human natural killer cell maturation and suppresses cell-mediated cytotoxicity. Blood 119: 3734-3743, 2012.
44. Campbell KS and Hasegawa J: Natural killer cell biology: An update and future directions. J Allergy Clin Immunol 132: 536-544, 2013.
45. Lee KM, Bhawan S, Majima T, Wei H, Nishimura MI, Yagita H and Kumar V: Cutting edge: The NK cell receptor 2B4 augments antigen-specific T cell cytotoxicity through CD48 ligation on neighboring T cells. J Immunol 170: 4881-4885, 2003.
46. Mocikat R, Braumüller H, Gumy A, Egeter O, Ziegler H, Reusch U, Bubeck A, Louis J, Mailhammer R, Riethmüller G, et al: Natural killer cells activated by MHC class I(low) targets prime dendritic cells to induce protective CD8 T cell responses. Immunity 19: 561-569, 2003.