Lung cancer-derived galectin-1 contributes to cancer associated fibroblast-mediated cancer progression and immune suppression through TDO2/kynurenine axis

Oncotarget

Volumn 7, Issue 19, 2016, Pages 27584-27598

  Hsu, Ya Ling ^a   Hung, Jen Yu ^b,c   Chiang, Shin Yi ^a   Jian, Shu Fang ^a   Wu, Cheng Ying ^a   Lin, Yi Shiuan ^a   Tsai, Ying Ming ^a,b   Chou, Shah Hwa ^b   Tsai, Ming Ju ^a,b   Kuo, Po Lin ^a,d  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

Author keywords

Cancer associated fibroblasts; Galectin 1; Kynurenine; Lung cancer

Indexed keywords

680C91; ENZYME INHIBITOR; GALECTIN 1; KYNURENINE; PROTEIN KINASE B; PROTEIN KINASE WNK1; TRYPTOPHAN; TRYPTOPHAN 2,3 DIOXYGENASE; TRYPTOPHAN 2,3 DIOXYGENASE INHIBITOR; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CELL; CANCER GROWTH; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DENDRITIC CELL; FEEDBACK SYSTEM; FIBROBLAST; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LEWIS CARCINOMA; LUNG CANCER; METASTASIS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; T LYMPHOCYTE; TUMOR INVASION; UPREGULATION; A-549 CELL LINE; ANIMAL; CANCER ASSOCIATED FIBROBLAST; COCULTURE; DEFICIENCY; DISEASE EXACERBATION; GENE KNOCKDOWN; GENETICS; IMMUNOLOGY; LUNG TUMOR; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

A549 CELLS; ANIMALS; CANCER-ASSOCIATED FIBROBLASTS; CARCINOMA, LEWIS LUNG; CELL LINE, TUMOR; COCULTURE TECHNIQUES; DISEASE PROGRESSION; GALECTIN 1; GENE KNOCKDOWN TECHNIQUES; HUMANS; KYNURENINE; LUNG NEOPLASMS; MICE; NEOPLASM METASTASIS; SIGNAL TRANSDUCTION; TRYPTOPHAN OXYGENASE; UP-REGULATION;

EID: 84968846665     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8488     Document Type: Article

References (38)

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin 2015; 65: 87-108.
2. D'Addario G, Früh M, Reck M, Baumann P, Klepetko W, Felip E; ESMO Guidelines Working Group. Metastatic nonsmall-cell lung cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2010; 21 Suppl 5: v116-119.
3. Quail DF, Joyce JA. Microenvi ronmental regulation of tumor progression and metastasis. Nat Med 2013; 19: 1423-1437.
4. Ohshio Y, Teramoto K, Hanaoka J, Tezuka N, Itoh Y, Asai T, Daigo Y, Ogasawara K. Cancer-associated fibroblast-targeted strategy enhances antitumor immune responses in dendritic cell-based vaccine. Cancer Sci 2015; 106: 134-142.
5. Jiang L, Xiao L, Sugiura H, Huang X, Ali A, Kuro-o M, Deberardinis RJ, Boothman DA. Metabolic reprogramming during TGFbeta1-induced epithelial-to-mesenchymal transition. Oncogene 2015; 34: 3908-3916.
6. Chen JY, Li CF, Kuo CC, Tsai K, Hou MF, Hung WC. Cancer/stroma interplay via cyclooxygenase-2 and indoleamine 2,3-dioxygenase promotes breast cancer progression. Breast Cancer Res 2014; 16: 410.
7. Creelan BC, Antonia S, Bepler G, Garrett TJ, Simon GR, Soliman HH. Indoleamine 2,3-dioxygenase activity and clinical outcome following induction chemotherapy and concurrent chemoradiation in Stage III non-small cell lung cancer. Oncoimmunology 2013; 2: e23428.
8. Platten M, Wick W, Van den Eynde BJ. Tryptophan Catabolism in Cancer: Beyond IDO and Tryptophan Depletion. Cancer Res 2012; 72: 5435-5440.
9. Chuang SC, Fanidi A, Ueland PM, Relton C, Midttun O, Vollset SE, Gunter MJ, Seckl MJ, Travis RC, Wareham N, Trichopoulou A, Lagiou P, Trichopoulos D, Peeters PH, Bueno-de-Mesquita HB, Boeing H, Wientzek A, Kuehn T, Kaaks R, Tumino R, Agnoli C, Palli D, Naccarati A, Aicua EA, Sánchez MJ, Quirós JR, Chirlaque MD, Agudo A, Johansson M, Grankvist K, Boutron-Ruault MC, Clavel-Chapelon F, Fagherazzi G, Weiderpass E, Riboli E, Brennan PJ, Vineis P, Johansson M. Circulating Biomarkers of Tryptophan and the Kynurenine Pathway and Lung Cancer Risk. Cancer Epidemiol Biomarkers Prev 2014; 23: 461-468.
10. Creelan BC, Antonia S, Bepler G, Garrett TJ, Simon GR, Soliman HH. Indoleamine 2,3-dioxygenase activity and clinical outcome following induction chemotherapy and concurrent chemoradiation in Stage III non-small cell lung cancer. Oncoimmunology 2013; 2: e23428.
11. Suzuki Y, Suda T, Furuhashi K, Suzuki M, Fujie M, Hahimoto D, Nakamura Y, Inui N, Nakamura H, Chida K. Increased serum kynurenine/tryptophan ratio correlates with disease progression in lung cancer. Lung Cancer 2010; 67: 361-365.
12. Wang W, Guo H, Geng J, Zheng X, Wei H, Sun R, Tian Z. Tumor-released Galectin-3, a soluble inhibitory ligand of human NKp30, plays an important role in tumor escape from NK cell attack. J Biol Chem. 2014; 289: 33311-33319.
13. Kouo T, Huang L, Pucsek AB, Cao M, Solt S, Armstrong T, Jaffee E. Galectin-3 Shapes Antitumor Immune Responses by Suppressing CD8+ T Cells via LAG-3 and Inhibiting Expansion of Plasmacytoid Dendritic Cells. Cancer Immunol Res 2015; 3: 412-423.
14. Kuo PL, Hung JY, Huang SK, Chou SH, Cheng DE, Jong YJ, Hung CH, Yang CJ, Tsai YM, Hsu YL, Huang MS. Lung Cancer-Derived Galectin-1 Mediates Dendritic Cell Anergy through Inhibitor of DNA Binding 3/IL-10 Signaling Pathway. J Immunol 2011; 186: 1521-1530.
15. Wu MH, Hong HC, Hong TM, Chiang WF, Jin YT, Chen YL. Targeting galectin-1 in carcinoma-associated fibroblasts inhibits oral squamous cell carcinoma metastasis by downregulating MCP-1/CCL2 expression. Clin Cancer Res 2011; 17: 1306-1316.
16. Bergot AS, Ford N, Leggatt GR, Wells JW, Frazer IH, Grimbaldeston MA. HPV16-E7 expression in squamous epithelium creates a local immune suppressive environment via CCL2-and CCL5-mediated recruitment of mast cells. PLoS Pathog 2014; 10: e1004466.
17. Mi Z, Bhattacharya SD, Kim VM, Guo H, Talbot LJ, Kuo PC. Osteopontin promotes CCL5-mesenchymal stromal cell-mediated breast cancer metastasis. Carcinogenesis 2011; 32: 477-487.
18. Ling W, Zhang J, Yuan Z, Ren G, Zhang L, Chen X, Rabson AB, Roberts AI, Wang Y, Shi Y. Mesenchymal stem cells use IDO to regulate immunity in tumor microenvironment. Cancer Res 2014; 74: 1576-1587.
19. Wang Y, Yang BH, Li H, Cao S, Ren XB, Yu JP. IDO(+) DCs and signalling pathways. Curr Cancer Drug Targets 2013; 13: 278-288.
20. Marsh T, Pietras K, McAllister SS. Fibroblasts as architects of cancer pathogenesis. Biochim Biophys Acta 2013; 1832: 1070-1078.
21. Opitz CA, Litzenburger UM, Sahm F, Ott M, Tritschler I, Trump S, Schumacher T, Jestaedt L, Schrenk D, Weller M, Jugold M, Guillemin GJ, Miller CL, Lutz C, Radlwimmer B, Lehmann I, von Deimling A, Wick W, Platten M. An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 2011; 478: 197-203.
22. Shimba S, Komiyama K, Moro I, Tezuka M. Overexpression of the aryl hydrocarbon receptor (AhR) accelerates the cell proliferation of A549 cells. J Biochem 2002; 132: 795-802.
23. Daniel P, Filiz G, Brown DV, Hollande F, Gonzales M, D'Abaco G, Papalexis N, Phillips WA, Malaterre J, Ramsay RG, Mantamadiotis T. Selective CREB-dependent cyclin expression mediated by the PI3K and MAPK pathways supports glioma cell proliferation. Oncogenesis 2014; 3: e108.
24. Du K, Montminy M. CREB Is a Regulatory Target for the Protein Kinase Akt/PKB. J Biol Chem 1998; 273: 32377-32379.
25. Casaburi I, Avena P, Lanzino M, Sisci D, Giordano F, Maris P, Catalano S, Morelli C, Andò S. Chenodeoxycholic acid through a TGR5-dependent CREB signaling activation enhances cyclin D1 expression and promotes human endometrial cancer cell proliferation. Cell Cycle 2012; 11: 2699-26710.
26. Zhang T, Zhang J, You X, Liu Q, Du Y, Gao Y, Shan C, Kong G, Wang Y, Yang X, Ye L, Zhang X. Hepatitis B virus X protein modulates oncogene Yes-associated protein by CREB to promote growth of hepatoma cells. Hepatology 2012; 56: 2051-2059. www.impactjournals.com/oncotarget 27598 Oncotarget
27. Garzon-Muvdi T, Schiapparelli P, Ap Rhys C, Guerrero-Cazares H, Smith C, Kim DH, Kone L, Farber H, Lee DY, An SS, Levchenko A, Quiñones-Hinojosa A. Regulation of brain tumor dispersal by NKCC1 through a novel role in focal adhesion regulation. PLoS Biol 2012; 10: e1001320.
28. Moniz S, Jordan P. Emerging roles for WNK kinases in cancer. Cell Mol Life Sci 2010; 67: 1265-1276.
29. Dbouk HA, Weil LM, Perera GK, Dellinger MT, Pearson G, Brekken RA, Cobb MH. Actions of the protein kinase WNK1 on endothelial cells are differentially mediated by its substrate kinases OSR1 and SPAK. Proc Natl Acad Sci U S A 2014; 111: 15999-16004.
30. Xu BE, Stippec S, Lazrak A, Huang CL, Cobb MH. WNK1 activates SGK1 by a phosphatidylinositol 3-kinasedependent and non-catalytic mechanism. J Biol Chem 2005; 280: 34218-34223.
31. McCormick JA, Ellison DH. The WNKs: Atypical Protein Kinases With Pleiotropic Actions. Physiol Rev 2011; 91: 177-219.
32. Wu Y, Liu M, Li Z, Wu XB, Wang Y, Wang Y, Nie M, Huang F, Ju J, Ma C, Tan R, Zen K, Zhang CY, Fu K, Chen YG, Wang MR, Zhao Q. LYAR promotes colorectal cancer cell mobility by activating galectin-1 expression. Oncotarget 2015; 6: 32890-32901. doi: 10.18632/oncotarget.5335.
33. Cimmino F, Schulte JH, Zollo M, Koster J, Versteeg R, Iolascon A, Eggert A, Schramm A. Galectin-1 is a major effector of TrkB-mediated neuroblastoma aggressiveness. Oncogene 2009; 28: 2015-2023.
34. Tang D, Gao J, Wang S, Yuan Z, Ye N, Chong Y, Xu C, Jiang X, Li B, Yin W, Miao Y, Wang D, Jiang K. Apoptosis and anergy of T cell induced by pancreatic stellate cellsderived galectin-1 in pancreatic cancer. Tumour Biol 2015; 36: 5617-5626.
35. Verschuere T, Toelen J, Maes W, Poirier F, Boon L, Tousseyn T, Mathivet T, Gerhardt H, Mathieu V, Kiss R, Lefranc F, Van Gool SW, De Vleeschouwer S. Gliomaderived galectin-1 regulates innate and adaptive antitumor immunity. Int J Cancer 2014; 134: 873-884.
36. He XJ, Tao HQ, Hu ZM, Ma YY, Xu J, Wang HJ, Xia YJ, Li L, Fei BY, Li YQ, Chen JZ. Expression of galectin-1 in carcinoma-associated fibroblasts promotes gastric cancer cell invasion through upregulation of integrin beta1. Cancer Sci 2014; 105: 1402-1410.
37. Ogasawara N, Oguro T, Sakabe T, Matsushima M, Takikawa O, Isobe K, Nagase F. Hemoglobin induces the expression of indoleamine 2,3-dioxygenase in dendritic cells through the activation of PI3K, PKC, and NF-kappaB and the generation of reactive oxygen species. J Cell Biochem 2009; 108: 716-725.
38. Koorella C, Nair JR, Murray ME, Carlson LM, Watkins SK, Lee KP. Novel regulation of CD80/CD86-induced phosphatidylinositol 3-kinase signaling by NOTCH1