TIM-4 promotes the growth of non-small-cell lung cancer in a RGD motif-dependent manner

British Journal of Cancer

Volumn 113, Issue 10, 2015, Pages 1484-1492

  Zhang, Qianqian ^a,b   Wang, Hongxing ^a   Wu, Xiaodong ^a,c   Liu, Bing ^a   Liu, Wen ^a   Wang, Rong ^a   Liang, Xiaohong ^a   Ma, Chunhong ^a   Gao, Lifen ^a  

^a SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b General Hospital of Ji'nan Military Region   (China)

^c Jinan Blood Centre   (China)

Author keywords

integrin v 3; non small cell lung cancer; RGD motif; TIM 4

Indexed keywords

CELL SURFACE PROTEIN; CYCLIN A; CYCLIN B1; CYCLIN D1; MESSENGER RNA; OSTEOPONTIN; T CELL IMMUNOGLOBULIN DOMAIN AND MUCIN DOMAIN 4 PROTEIN; UNCLASSIFIED DRUG; VITRONECTIN RECEPTOR; CYCLINE; KI 67 ANTIGEN; MEMBRANE PROTEIN; TIMD4 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARGININE GLYCINE ASPARTIC ACID MOTIF; ARTICLE; CANCER PROGNOSIS; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SQUAMOUS CELL LUNG CARCINOMA; TUMOR DIFFERENTIATION; TUMOR GROWTH; UPREGULATION; ADULT; AGED; ANIMAL; BINDING SITE; CANCER TRANSPLANTATION; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; METABOLISM; MIDDLE AGED; NON SMALL CELL LUNG CANCER; PATHOLOGY; TUMOR CELL LINE;

ADULT; AGED; ANIMALS; BINDING SITES; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTEGRIN ALPHAVBETA3; KI-67 ANTIGEN; LUNG NEOPLASMS; MALE; MEMBRANE PROTEINS; MICE; MIDDLE AGED; NEOPLASM TRANSPLANTATION; PROLIFERATING CELL NUCLEAR ANTIGEN;

EID: 84947494362     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2015.323     Document Type: Article

References (46)

1. Abe Y, Kamachi F, Kawamoto T, Makino F, Ito J, Kojima Y, Moustapha Ael D, Usui Y, Yagita H, Takasaki Y, Okumura K, Akiba H (2013) TIM-4 has dual function in the induction and effector phases of murine arthritis. J Immunol 191(9): 4562-4572.
2. Albacker LA, Karisola P, Chang YJ, Umetsu SE, Zhou M, Akbari O, Kobayashi N, Baumgarth N, Freeman GJ, Umetsu DT, DeKruyff RH (2010) TIM-4, a receptor for phosphatidylserine, controls adaptive immunity by regulating the removal of antigen-specific T cells. J Immunol 185(11): 6839-6849.
3. Albacker LA, Yu S, Bedoret D, Lee WL, Umetsu SE, Monahan S, Freeman GJ, Umetsu DT, DeKruyff RH (2013) TIM-4, expressed by medullary macrophages, regulates respiratory tolerance by mediating phagocytosis of antigen-specific T cells. Mucosal Immunol 6(3): 580-590.
4. Aoka Y, Johnson FL, Penta K, Hirata KiK, Hidai C, Schatzman R, Varner JA, Quertermous T (2002) The embryonic angiogenic factor Del1 accelerates tumor growth by enhancing vascular formation. Microvasc Res 64(1): 148-161.
5. Baghdadi M, Nagao H, Yoshiyama H, Akiba H, Yagita H, Dosaka-Akita H, Jinushi M (2013) Combined blockade of TIM-3 and TIM-4 augments cancer vaccine efficacy against established melanomas. Cancer Immunol Immunother 62(4): 629-637.
6. Baghdadi M, Yoneda A, Yamashina T, Nagao H, Komohara Y, Nagai S, Akiba H, Foretz M, Yoshiyama H, Kinoshita I, Dosaka-Akita H, Takeya M, Viollet B, Yagita H, Jinushi M (2013) TIM-4 glycoprotein-mediated degradation of dying tumor cells by autophagy leads to reduced antigen presentation and increased immune tolerance. Immunity 39(6): 1070-1081.
7. Boland JM, Kwon ED, Harrington SM, Wampfler JA, Tang H, Yang P, Aubry MC (2013) Tumor B7-H1 and B7-H3 expression in squamous cell carcinoma of the lung. Clin Lung Cancer 14(2): 157-163.
8. Cam A, de Mejia EG (2012) RGD-peptide lunasin inhibits Akt-mediated NFkB activation in human macrophages through interaction with the aVb3 integrin. Mol Nutr Food Res 56(10): 1569-1581.
9. Cao Y, Zhou X, Huang X, Li Q, Gao L, Jiang L, Huang M, Zhou J (2013) Tim-3 expression in cervical cancer promotes tumor metastasis. PLoS One 8(1): e53834.
10. Carrascosa C, Obula RG, Missiaglia E, Lehr HA, Delorenzi M, Frattini M, Rüegg C, Mariotti A (2012) MFG-E8/lactadherin regulates cyclins D1/D3 expression and enhances the tumorigenic potential of mammary epithelial cells. Oncogene 31(12): 1521-1532.
11. Chen C, Qu QX, Shen Y, Mu CY, Zhu YB, Zhang XG, Huang JA (2012) Induced expression of B7-H4 on the surface of lung cancer cell by the tumor-associated macrophages: A potential mechanism of immune escape. Cancer Lett 317(1): 99-105.
12. Cui R, Takahashi F, Ohashi R, Gu T, YoshiokaM, Nishio K, Ohe Y, Tominaga S, Takagi Y, Sasaki S, Fukuchi Y, Takahashi K (2007) Abrogation of the interaction between osteopontin and alphavbeta3 integrin reduces tumor growth of human lung cancer cells in mice. Lung Cancer 57(3): 302-310.
13. Danhier F, Le Breton A, Préat V (2012) RGD-based strategies to target alpha(v) beta(3) integrin in cancer therapy and diagnosis. Mol Pharm 9(11): 2961-2973.
14. Dorfman DM, Hornick JL, Shahsafaei A, Freeman GJ (2010) The phosphatidylserine receptors, T cell immunoglobulin mucin proteins 3 and 4, are markers of histiocytic sarcoma and other histiocytic and dendritic cell neoplasms. Hum Pathol 41(10): 1486-1494.
15. Flannagan RS, Canton J, Furuya W, Glogauer M, Grinstein S (2014) The phosphatidylserine receptor TIM4 utilizes integrins as coreceptors to effect phagocytosis. Mol Biol Cell 25(9): 1511-1522.
16. Gargalovic PS, Erbilgin A, Kohannim O, Pagnon J, Wang X, Castellani L, LeBoeuf R, Peterson ML, Spear BT, Lusis AJ (2010) Quantitative trait locus mapping and identification of ZHX2 as a novel regulator of plasma lipid metabolism. Circ Cardiovasc Genet 3(1): 60-67.
17. Goc A, Liu J, Byzova TV, Somanath PR (2012) Akt1 mediates prostate cancer cell microinvasion and chemotaxis to metastatic stimuli via integrin b3 affinity modulation. Br J Cancer 107(4): 713-723.
18. Han CP, Kok LF, Wang PH, Wu TS, Tyan YS, Cheng YW, Lee MY, Yang SF (2009) Scoring of p16(INK4a) immunohistochemistry based on independent nuclear staining alone can sufficiently distinguish between endocervical and endometrial adenocarcinomas in a tissue microarray study. Mod Pathol 22(6): 797-806.
19. Kim HS, Kim HS, Lee CW, Chung DH (2010) T cell Ig domain and mucin domain 1 engagement on invariant NKT cells in the presence of TCR stimulation enhances IL-4 production but inhibits IFN-gamma production. J Immunol 184(8): 4095-4106.
20. Li H, Zhou X, Ran Q, Wang L (2013a) Parapharyngeal liposarcoma: A case report. Diagn Pathol 8: 42.
21. Li J, Cao D, Guo G, Wu Y, Chen Y (2013b) Expression and anatomical distribution of TIM-containing molecules in Langerhans cell sarcoma. J Mol Histol 44(2): 213-220.
22. Li Z, Ju Z, Frieri M (2013c) The T-cell immunoglobulin and mucin domain (Tim) gene family in asthma, allergy, and autoimmunity. Allergy Asthma Proc 34(1): e21-e26.
23. Melkamu T, Qian X, Upadhyaya P, O'Sullivan MG, Kassie F (2013) Lipopolysaccharide enhances mouse lung tumorigenesis: A model for inflammation-driven lung cancer. Vet Pathol 50(5): 895-902.
24. Meyers JH, Chakravarti S, Schlesinger D, Illes Z, Waldner H, Umetsu SE, Kenny J, Zheng XX, Umetsu DT, DeKruyff RH, Strom TB, Kuchroo VK (2005) TIM-4 is the ligand for TIM-1, and the TIM-1-TIM-4 interaction regulates T cell proliferation. Nat Immunol 6(5): 455-464.
25. Mizui M, Shikina T, Arase H, Suzuki K, Yasui T, Rennert PD, Kumanogoh A, Kikutani H (2008) Bimodal regulation of T cell-mediated immune responses by TIM-4. Int Immunol 20(5): 695-708.
26. Nathan C, Ding A (2010) Nonresolving inflammation. Cell 140(6): 871-882.
27. Park D, Hochreiter-Hufford A, Ravichandran KS (2009) The phosphatidylserine receptor TIM-4 does not mediate direct signaling. Curr Biol 19(4): 346-351.
28. Piao YR, Piao LZ, Zhu LH, Jin ZH, Dong XZ (2013) Prognostic value of T cell immunoglobulin mucin-3 in prostate cancer. Asian Pac J Cancer Prev 14(6): 3897-3901.
29. Ramaekers F, Broers J, Rot MK, Oostendorp T, Wagenaar S, Vooijs P (1987) Detection of epithelial-and neural type of intermediate filament proteins in human lung tumors. Acta Histochem Suppl 34: 45-56.
30. Rodriguez-Manzanet R, DeKruyff R, Kuchroo VK, Umetsu DT (2009) The costimulatory role of TIM molecules. Immunol Rev 229(1): 259-270.
31. Rodriguez-Manzanet R, Meyers JH, Balasubramanian S, Slavik J, Kassam N, Dardalhon V, Greenfield EA, Anderson AC, Sobel RA, Hafler DA, Strom TB, Kuchroo VK (2008) TIM-4 expressed on APCs induces T cell expansion and survival. J Immunol 180(7): 4706-4713.
32. Ruoslahti E (1996) RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 12: 697-715.
33. Siegel R, Ma J, Zou Z, Jemal A (2014) Cancer statistics 2014. CA Cancer J Clin 64(1): 9-29.
34. Steri V, Ellison TS, Gontarczyk AM, Weilbaecher K, Schneider JG, Edwards D, Fruttiger M, Hodivala-Dilke KM, Robinson SD (2014) Acute depletion of endothelial b3-integrin transiently inhibits tumor growth and angiogenesis in mice. Circ Res 114(1): 79-91.
35. Sun HW, Wu C, Tan HY, Wang QS (2012) A new development of FG-CC' siRNA blocking interaction of Tim-1 and Tim-4 can enhance DC vaccine against gastric cancer. Hepatogastroenterology 59(120): 2677-2682.
36. Tabata K, Tanaka T, Hayashi T, Hori T, Nunomura S, Yonezawa S, Fukuoka J (2014) Ki-67 is a strong prognostic marker of non-small cell lung cancer when tissue heterogeneity is considered. BMC Clin Pathol 14: 23.
37. Tian M, Neil JR, Schiemann WP (2011) Transforming growth factor-b and the hallmarks of cancer. Cell Signal 23(6): 951-962.
38. Toda S, Hanayama R, Nagata S (2012) Two-step engulfment of apoptotic cells. Mol Cell Biol 32(1): 118-125.
39. Velcheti V, Schalper KA, Carvajal DE, Anagnostou VK, Syrigos KN, Sznol M, Herbst RS, Gettinger SN, Chen L, Rimm DL (2014) Programmed death ligand-1 expression in non-small cell lung cancer. Lab Invest 94(1): 107-116.
40. Wong K, Valdez PA, Tan C, Yeh S, Hongo JA, Ouyang W (2010) Phosphatidylserine receptor Tim-4 is essential for the maintenance of the homeostatic state of resident peritoneal macrophages. Proc Natl Acad Sci USA 107(19): 8712-8717.
41. Xu LY, Qi JN, Liu X, Ma HX, Yuan W, Zhao PQ, Liang XH, Xu Y, Wang HX, Xu XY, Wang W, Ma CH, Gao LF (2015) Tim-4 inhibits NO generation by murine macrophages. PLoS One 10(4): e0124771.
42. Xu L, Qi J, Zhao P, Liang X, Ju Y, Liu P, Liu B, Guo C, Zhang L, Ma C, Gao L (2010) T cell immunoglobulin-and mucin-domain-containing molecule-4 attenuates concanavalin A-induced hepatitis by regulating macrophage. J Leukoc Biol 88(2): 329-336.
43. Xu L, Xiao H, Xu M, Zhou C, Yi L, Liang H (2011) Glioma-derived T cell immunoglobulin-and mucin domain-containing molecule-4 (TIM4) contributes to tumor tolerance. J Biol Chem 286(42): 36694-36699.
44. Yuan J, Jiang B, Zhao H, Huang Q (2014) Prognostic implication of TIM-3 in clear cell renal cell carcinoma. Neoplasma 61(1): 35-40.
45. Zhao P, Xu L, Wang P, Liang X, Qi J, Liu P, Guo C, Zhang L, Ma C, Gao L (2010) Increased expression of human T-cell immunoglobulin-and mucin-domain-containing molecule-4 in peripheral blood mononuclear cells from patients with system lupus erythematosus. Cell Mol Immunol 7(2): 152-156.
46. Zhuang X, Zhang X, Xia X, Zhang C, Liang X, Gao L, Zhang X, Ma C (2012) Ectopic expression of TIM-3 in lung cancers: A potential independent prognostic factor for patients with NSCLC. Am J Clin Pathol 137(6): 978-985.