Indomethacin enhances anti-tumor efficacy of a MUC1 peptide vaccine against breast cancer in MUC1 transgenic mice
Autoři:
Jennifer M. Curry aff001; Dahlia M. Besmer aff001; Timothy K. Erick aff001; Nury Steuerwald aff002; Lopamudra Das Roy aff001; Priyanka Grover aff001; Shanti Rao aff001; Sritama Nath aff001; Jacob W. Ferrier aff003; Robert W. Reid aff003; Pinku Mukherjee aff001
Působiště autorů:
Department of Biological Sciences, University of North Carolina at Charlotte, Charlotte, NC, United States of America
aff001; Molecular Biology and Genomics Laboratory, Carolinas Medical Center, Charlotte, NC, United States of America
aff002; Department of Bioinformatics and Genomics, University of North Carolina at Charlotte, Charlotte, NC, United States of America
aff003; OncoTAb, Inc., Charlotte, NC, United States of America
aff004
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0224309
Souhrn
In recent years, vaccines against tumor antigens have shown potential for combating invasive cancers, including primary tumors and metastatic lesions. This is particularly pertinent for breast cancer, which is the second-leading cause of cancer-related death in women. MUC1 is a glycoprotein that is normally expressed on glandular epithelium, but is overexpressed and under-glycosylated in most human cancers, including the majority of breast cancers. This under-glycosylation exposes the MUC1 protein core on the tumor-associated form of the protein. We have previously shown that a vaccine consisting of MUC1 core peptides stimulates a tumor-specific immune response. However, this immune response is dampened by the immunosuppressive microenvironment within breast tumors. Thus, in the present study, we investigated the effectiveness of MUC1 vaccination in combination with four different drugs that inhibit different components of the COX pathway: indomethacin (COX-1 and COX-2 inhibitor), celecoxib (COX-2 inhibitor), 1-methyl tryptophan (indoleamine 2,3 dioxygenase inhibitor), and AH6809 (prostaglandin E2 receptor antagonist). These treatment regimens were explored for the treatment of orthotopic MUC1-expressing breast tumors in mice transgenic for human MUC1. We found that the combination of vaccine and indomethacin resulted in a significant reduction in tumor burden. Indomethacin did not increase tumor-specific immune responses over vaccine alone, but rather appeared to reduce the proliferation and increase apoptosis of tumor cells, thus rendering them susceptible to immune cell killing.
Klíčová slova:
Apoptosis – Breast cancer – Breast tumors – Cancer treatment – Cancer vaccines – Enzyme-linked immunoassays – Mouse models – Vaccines
Zdroje
1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30. Epub 2018/01/10. doi: 10.3322/caac.21442 29313949.
2. Clarke M, Collins R, Darby S, Davies C, Elphinstone P, Evans V, et al. Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: an overview of the randomised trials. Lancet. 2005;366(9503):2087–106. doi: 10.1016/S0140-6736(05)67887-7 16360786.
3. Redig AJ, McAllister SS. Breast cancer as a systemic disease: a view of metastasis. J Intern Med. 2013;274(2):113–26. doi: 10.1111/joim.12084 23844915; PubMed Central PMCID: PMC3711134.
4. Monnot GC, Romero P. Rationale for immunological approaches to breast cancer therapy. Breast. 2017. doi: 10.1016/j.breast.2017.06.009 28629632.
5. Antonia S, Mule JJ, Weber JS. Current developments of immunotherapy in the clinic. Curr Opin Immunol. 2004;16(2):130–6. doi: 10.1016/j.coi.2004.01.012 15023403.
6. Avigan D, Vasir B, Gong J, Borges V, Wu Z, Uhl L, et al. Fusion cell vaccination of patients with metastatic breast and renal cancer induces immunological and clinical responses. Clin Cancer Res. 2004;10(14):4699–708. doi: 10.1158/1078-0432.CCR-04-0347 15269142.
7. Kwilas AR, Ardiani A, Dirmeier U, Wottawah C, Schlom J, Hodge JW. A poxviral-based cancer vaccine the transcription factor twist inhibits primary tumor growth and metastases in a model of metastatic breast cancer and improves survival in a spontaneous prostate cancer model. Oncotarget. 2015;6(29):28194–210. doi: 10.18632/oncotarget.4442 26317648; PubMed Central PMCID: PMC4695054.
8. Guo C, Manjili MH, Subjeck JR, Sarkar D, Fisher PB, Wang XY. Therapeutic cancer vaccines: past, present, and future. Adv Cancer Res. 2013;119:421–75. doi: 10.1016/B978-0-12-407190-2.00007-1 23870514; PubMed Central PMCID: PMC3721379.
9. Hattrup CL, Gendler SJ. Structure and function of the cell surface (tethered) mucins. Annu Rev Physiol. 2008;70:431–57. doi: 10.1146/annurev.physiol.70.113006.100659 17850209.
10. Nath S, Mukherjee P. MUC1: a multifaceted oncoprotein with a key role in cancer progression. Trends Mol Med. 2014;20(6):332–42. doi: 10.1016/j.molmed.2014.02.007 24667139; PubMed Central PMCID: PMC5500204.
11. Gendler SJ, Lancaster CA, Taylor-Papadimitriou J, Duhig T, Peat N, Burchell J, et al. Molecular cloning and expression of human tumor-associated polymorphic epithelial mucin. J Biol Chem. 1990;265(25):15286–93. 1697589.
12. Mukherjee P, Madsen CS, Ginardi AR, Tinder TL, Jacobs F, Parker J, et al. Mucin 1-specific immunotherapy in a mouse model of spontaneous breast cancer. J Immunother. 2003;26(1):47–62. 12514429.
13. Ghosh SK, Pantazopoulos P, Medarova Z, Moore A. Expression of underglycosylated MUC1 antigen in cancerous and adjacent normal breast tissues. Clin Breast Cancer. 2013;13(2):109–18. doi: 10.1016/j.clbc.2012.09.016 23122537; PubMed Central PMCID: PMC3578066.
14. Siroy A, Abdul-Karim FW, Miedler J, Fong N, Fu P, Gilmore H, et al. MUC1 is expressed at high frequency in early-stage basal-like triple-negative breast cancer. Hum Pathol. 2013;44(10):2159–66. doi: 10.1016/j.humpath.2013.04.010 23845471; PubMed Central PMCID: PMC4167755.
15. Croce MV, Isla-Larrain MT, Rua CE, Rabassa ME, Gendler SJ, Segal-Eiras A. Patterns of MUC1 tissue expression defined by an anti-MUC1 cytoplasmic tail monoclonal antibody in breast cancer. J Histochem Cytochem. 2003;51(6):781–8. doi: 10.1177/002215540305100609 12754289.
16. Zaretsky JZ, Barnea I, Aylon Y, Gorivodsky M, Wreschner DH, Keydar I. MUC1 gene overexpressed in breast cancer: structure and transcriptional activity of the MUC1 promoter and role of estrogen receptor alpha (ERalpha) in regulation of the MUC1 gene expression. Mol Cancer. 2006;5:57. doi: 10.1186/1476-4598-5-57 17083744; PubMed Central PMCID: PMC1636664.
17. Cheever MA, Allison JP, Ferris AS, Finn OJ, Hastings BM, Hecht TT, et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res. 2009;15(17):5323–37. doi: 10.1158/1078-0432.CCR-09-0737 19723653.
18. Mukherjee P, Pathangey LB, Bradley JB, Tinder TL, Basu GD, Akporiaye ET, et al. MUC1-specific immune therapy generates a strong anti-tumor response in a MUC1-tolerant colon cancer model. Vaccine. 2007;25(9):1607–18. doi: 10.1016/j.vaccine.2006.11.007 17166639; PubMed Central PMCID: PMC1810513.
19. Mukherjee P, Basu GD, Tinder TL, Subramani DB, Bradley JM, Arefayene M, et al. Progression of pancreatic adenocarcinoma is significantly impeded with a combination of vaccine and COX-2 inhibition. J Immunol. 2009;182(1):216–24. 19109152; PubMed Central PMCID: PMC3838792.
20. Mukherjee P, Ginardi AR, Madsen CS, Tinder TL, Jacobs F, Parker J, et al. MUC1-specific CTLs are non-functional within a pancreatic tumor microenvironment. Glycoconj J. 2001;18(11–12):931–42. doi: 10.1023/a:1022260711583 12820727.
21. Mukherjee P, Tinder TL, Basu GD, Pathangey LB, Chen L, Gendler SJ. Therapeutic efficacy of MUC1-specific cytotoxic T lymphocytes and CD137 co-stimulation in a spontaneous breast cancer model. Breast Dis. 2004;20:53–63. 15687707.
22. Zarghi A, Arfaei S. Selective COX-2 Inhibitors: A Review of Their Structure-Activity Relationships. Iran J Pharm Res. 2011;10(4):655–83. 24250402; PubMed Central PMCID: PMC3813081.
23. Zha S, Yegnasubramanian V, Nelson WG, Isaacs WB, De Marzo AM. Cyclooxygenases in cancer: progress and perspective. Cancer Lett. 2004;215(1):1–20. doi: 10.1016/j.canlet.2004.06.014 15374627.
24. Dannenberg AJ, Subbaramaiah K. Targeting cyclooxygenase-2 in human neoplasia: rationale and promise. Cancer Cell. 2003;4(6):431–6. 14706335.
25. Rodriguez PC, Hernandez CP, Quiceno D, Dubinett SM, Zabaleta J, Ochoa JB, et al. Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J Exp Med. 2005;202(7):931–9. doi: 10.1084/jem.20050715 16186186; PubMed Central PMCID: PMC2213169.
26. Liu B, Qu L, Yan S. Cyclooxygenase-2 promotes tumor growth and suppresses tumor immunity. Cancer Cell Int. 2015;15:106. doi: 10.1186/s12935-015-0260-7 26549987; PubMed Central PMCID: PMC4635545.
27. Shim JY, An HJ, Lee YH, Kim SK, Lee KP, Lee KS. Overexpression of cyclooxygenase-2 is associated with breast carcinoma and its poor prognostic factors. Mod Pathol. 2003;16(12):1199–204. doi: 10.1097/01.MP.0000097372.73582.CB 14681319.
28. Pockaj BA, Basu GD, Pathangey LB, Gray RJ, Hernandez JL, Gendler SJ, et al. Reduced T-cell and dendritic cell function is related to cyclooxygenase-2 overexpression and prostaglandin E2 secretion in patients with breast cancer. Ann Surg Oncol. 2004;11(3):328–39. doi: 10.1245/aso.2004.05.027 14993030.
29. Gupta RA, DuBois RN. Translational studies on Cox-2 inhibitors in the prevention and treatment of colon cancer. Ann N Y Acad Sci. 2000;910:196–204; discussion -6. doi: 10.1111/j.1749-6632.2000.tb06709.x 10911914.
30. Gupta RA, Dubois RN. Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2. Nat Rev Cancer. 2001;1(1):11–21. doi: 10.1038/35094017 11900248.
31. Basu GD, Pathangey LB, Tinder TL, LaGioia M, Gendler SJ, Mukherjee P. COX-2 inhibitor induces apoptosis in breast cancer cells in an in vivo model of spontaneous metastatic breast cancer. Molecular Cancer Research. 2004;2:632–42. 15561779
32. Basu GD, Pathangey LB, Tinder TL, Gendler SJ, Mukherjee P. Mechanisms underlying the growth inhibitory effects of the cyclo-oxygenase-2 inhibitor celecoxib in human breast cancer cells. Breast Cancer Res. 2005;7(4):R422–35. doi: 10.1186/bcr1019 15987447; PubMed Central PMCID: PMC1175053.
33. Jendrossek V. Targeting apoptosis pathways by Celecoxib in cancer. Cancer Lett. 2013;332(2):313–24. doi: 10.1016/j.canlet.2011.01.012 21345578.
34. Basu GD, Tinder TL, Bradley JM, Tu T, Hattrup CL, Pockaj BA, et al. Cyclooxygenase-2 inhibitor enhances the efficacy of a breast cancer vaccine: role of IDO. J Immunol. 2006;177(4):2391–402. doi: 10.4049/jimmunol.177.4.2391 16888001.
35. Hwu P, Du MX, Lapointe R, Do M, Taylor MW, Young HA. Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J Immunol. 2000;164(7):3596–9. doi: 10.4049/jimmunol.164.7.3596 10725715.
36. Godin-Ethier J, Hanafi LA, Piccirillo CA, Lapointe R. Indoleamine 2,3-dioxygenase expression in human cancers: clinical and immunologic perspectives. Clin Cancer Res. 2011;17(22):6985–91. doi: 10.1158/1078-0432.CCR-11-1331 22068654.
37. Moon YW, Hajjar J, Hwu P, Naing A. Targeting the indoleamine 2,3-dioxygenase pathway in cancer. J Immunother Cancer. 2015;3:51. doi: 10.1186/s40425-015-0094-9 26674411; PubMed Central PMCID: PMC4678703.
38. Takikawa O, Yoshida R, Kido R, Hayaishi O. Tryptophan degradation in mice initiated by indoleamine 2,3-dioxygenase. J Biol Chem. 1986;261(8):3648–53. 2419335.
39. Muller AJ, Malachowski WP, Prendergast GC. Indoleamine 2,3-dioxygenase in cancer: targeting pathological immune tolerance with small-molecule inhibitors. Expert Opin Ther Targets. 2005;9(4):831–49. doi: 10.1517/14728222.9.4.831 16083346.
40. Muller AJ, DuHadaway JB, Donover PS, Sutanto-Ward E, Prendergast GC. Inhibition of indoleamine 2,3-dioxygenase, an immunoregulatory target of the cancer suppression gene Bin1, potentiates cancer chemotherapy. Nat Med. 2005;11(3):312–9. doi: 10.1038/nm1196 15711557.
41. Muller AJ, Prendergast GC. Indoleamine 2,3-dioxygenase in immune suppression and cancer. Curr Cancer Drug Targets. 2007;7(1):31–40. doi: 10.2174/156800907780006896 17305476.
42. Uyttenhove C, Pilotte L, Theate I, Stroobant V, Colau D, Parmentier N, et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat Med. 2003;9(10):1269–74. doi: 10.1038/nm934 14502282.
43. Wobser M, Voigt H, Houben R, Eggert AO, Freiwald M, Kaemmerer U, et al. Dendritic cell based antitumor vaccination: impact of functional indoleamine 2,3-dioxygenase expression. Cancer Immunol Immunother. 2007;56(7):1017–24. doi: 10.1007/s00262-006-0256-1 17195079.
44. Nakanishi M, Rosenberg DW. Multifaceted roles of PGE2 in inflammation and cancer. Semin Immunopathol. 2013;35(2):123–37. doi: 10.1007/s00281-012-0342-8 22996682; PubMed Central PMCID: PMC3568185.
45. Woodward DF, Pepperl DJ, Burkey TH, Regan JW. 6-Isopropoxy-9-oxoxanthene-2-carboxylic acid (AH 6809), a human EP2 receptor antagonist. Biochem Pharmacol. 1995;50(10):1731–3. doi: 10.1016/0006-2952(95)02035-7 7503778.
46. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol. 1992;12(3):954–61. doi: 10.1128/mcb.12.3.954 1312220; PubMed Central PMCID: PMC369527.
47. Rowse GJ, Tempero RM, VanLith ML, Hollingsworth MA, Gendler SJ. Tolerance and immunity to MUC1 in a human MUC1 transgenic murine model. Cancer Res. 1998;58(2):315–21. 9443411.
48. Simpson-Herren L, Lloyd HH. Kinetic parameters and growth curves for experimental tumor systems. Cancer Chemother Rep. 1970;54(3):143–74. Epub 1970/06/01. 5527016.
49. Gendler SJ, Spicer AP. Epithelial mucin genes. Annu Rev Physiol. 1995;57:607–34. Epub 1995/01/01. doi: 10.1146/annurev.ph.57.030195.003135 7778880.
50. Roy LD, Dillon LM, Zhou R, Moore LJ, Livasy C, El-Khoury JM, et al. A tumor specific antibody to aid breast cancer screening in women with dense breast tissue. Genes Cancer. 2017;8(3–4):536–49. doi: 10.18632/genesandcancer.134 28680538; PubMed Central PMCID: PMC5489651.
51. Roy LD, Sahraei M, Subramani DB, Besmer D, Nath S, Tinder TL, et al. MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene. 2011;30(12):1449–59. doi: 10.1038/onc.2010.526 21102519; PubMed Central PMCID: PMC3063863.
52. Nath S, Roy LD, Grover P, Rao S, Mukherjee P. Mucin 1 Regulates Cox-2 Gene in Pancreatic Cancer. Pancreas. 2015;44(6):909–17. doi: 10.1097/MPA.0000000000000371 26035123; PubMed Central PMCID: PMC4500655.
53. Moore LJ, Roy LD, Zhou R, Grover P, Wu ST, Curry JM, et al. Antibody-Guided In Vivo Imaging for Early Detection of Mammary Gland Tumors. Transl Oncol. 2016;9(4):295–305. doi: 10.1016/j.tranon.2016.05.001 27567952; PubMed Central PMCID: PMC5006816.
54. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 2003;19(2):185–93. doi: 10.1093/bioinformatics/19.2.185 12538238.
55. Roy LD, Curry JM, Sahraei M, Besmer DM, Kidiyoor A, Gruber HE, et al. Arthritis augments breast cancer metastasis: role of mast cells and SCF/c-Kit signaling. Breast Cancer Res. 2013;15(2):R32. doi: 10.1186/bcr3412 23577751; PubMed Central PMCID: PMC3672823.
56. Roy LD, Ghosh S, Pathangey LB, Tinder TL, Gruber HE, Mukherjee P. Collagen induced arthritis increases secondary metastasis in MMTV-PyV MT mouse model of mammary cancer. BMC Cancer. 2011;11:365. doi: 10.1186/1471-2407-11-365 21859454; PubMed Central PMCID: PMC3224388.
57. Coelho AL, Schaller MA, Benjamim CF, Orlofsky AZ, Hogaboam CM, Kunkel SL. The chemokine CCL6 promotes innate immunity via immune cell activation and recruitment. J Immunol. 2007;179(8):5474–82. doi: 10.4049/jimmunol.179.8.5474 17911634.
58. Hao NB, Lu MH, Fan YH, Cao YL, Zhang ZR, Yang SM. Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol. 2012;2012:948098. doi: 10.1155/2012/948098 22778768; PubMed Central PMCID: PMC3385963.
59. Munder M. Arginase: an emerging key player in the mammalian immune system. Br J Pharmacol. 2009;158(3):638–51. doi: 10.1111/j.1476-5381.2009.00291.x 19764983; PubMed Central PMCID: PMC2765586.
60. Bengtsson AK, Ryan EJ. Immune function of the decoy receptor osteoprotegerin. Crit Rev Immunol. 2002;22(3):201–15. 12498383.
61. Emery JG, McDonnell P, Burke MB, Deen KC, Lyn S, Silverman C, et al. Osteoprotegerin is a receptor for the cytotoxic ligand TRAIL. J Biol Chem. 1998;273(23):14363–7. doi: 10.1074/jbc.273.23.14363 9603945.
62. O'Kelly J, Chung A, Lemp N, Chumakova K, Yin D, Wang HJ, et al. Functional domains of CCN1 (Cyr61) regulate breast cancer progression. Int J Oncol. 2008;33(1):59–67. 18575751.
63. Espinoza I, Menendez JA, Kvp CM, Lupu R. CCN1 promotes vascular endothelial growth factor secretion through alphavbeta 3 integrin receptors in breast cancer. J Cell Commun Signal. 2014;8(1):23–7. doi: 10.1007/s12079-013-0214-6 24338441; PubMed Central PMCID: PMC3972397.
64. Burger AM, Leyland-Jones B, Banerjee K, Spyropoulos DD, Seth AK. Essential roles of IGFBP-3 and IGFBP-rP1 in breast cancer. Eur J Cancer. 2005;41(11):1515–27. Epub 2005/06/28. doi: 10.1016/j.ejca.2005.04.023 15979304.
65. Stergiou N, Gaidzik N, Heimes AS, Dietzen S, Besenius P, Jakel J, et al. Reduced Breast Tumor Growth after Immunization with a Tumor-Restricted MUC1 Glycopeptide Conjugated to Tetanus Toxoid. Cancer Immunol Res. 2019;7(1):113–22. Epub 2018/11/11. doi: 10.1158/2326-6066.CIR-18-0256 30413430.
66. Zhang H, Jia E, Xia W, Lv T, Lu C, Xu Z, et al. Utilizing VEGF165b mutant as an effective immunization adjunct to augment antitumor immune response. Vaccine. 2019;37(15):2090–8. Epub 2019/03/07. doi: 10.1016/j.vaccine.2019.02.055 30837171.
67. Apostolopoulos V, Pietersz GA, Tsibanis A, Tsikkinis A, Drakaki H, Loveland BE, et al. Pilot phase III immunotherapy study in early-stage breast cancer patients using oxidized mannan-MUC1 [ISRCTN71711835]. Breast Cancer Res. 2006;8(3):R27. Epub 2006/06/17. doi: 10.1186/bcr1505 16776849; PubMed Central PMCID: PMC1557739.
68. Vassilaros S, Tsibanis A, Tsikkinis A, Pietersz GA, McKenzie IF, Apostolopoulos V. Up to 15-year clinical follow-up of a pilot Phase III immunotherapy study in stage II breast cancer patients using oxidized mannan-MUC1. Immunotherapy. 2013;5(11):1177–82. Epub 2013/11/06. doi: 10.2217/imt.13.126 24188672.
69. Miles D, Roche H, Martin M, Perren TJ, Cameron DA, Glaspy J, et al. Phase III multicenter clinical trial of the sialyl-TN (STn)-keyhole limpet hemocyanin (KLH) vaccine for metastatic breast cancer. Oncologist. 2011;16(8):1092–100. Epub 2011/05/17. doi: 10.1634/theoncologist.2010-0307 21572124; PubMed Central PMCID: PMC3228158.
70. Mirandola P, Ponti C, Gobbi G, Sponzilli I, Vaccarezza M, Cocco L, et al. Activated human NK and CD8+ T cells express both TNF-related apoptosis-inducing ligand (TRAIL) and TRAIL receptors but are resistant to TRAIL-mediated cytotoxicity. Blood. 2004;104(8):2418–24. doi: 10.1182/blood-2004-04-1294 15205263.
71. Falschlehner C, Schaefer U, Walczak H. Following TRAIL's path in the immune system. Immunology. 2009;127(2):145–54. doi: 10.1111/j.1365-2567.2009.03058.x 19476510; PubMed Central PMCID: PMC2691779.
72. Smyth MJ, Cretney E, Takeda K, Wiltrout RH, Sedger LM, Kayagaki N, et al. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) contributes to interferon gamma-dependent natural killer cell protection from tumor metastasis. J Exp Med. 2001;193(6):661–70. doi: 10.1084/jem.193.6.661 11257133; PubMed Central PMCID: PMC2193421.
73. Takeda K, Hayakawa Y, Smyth MJ, Kayagaki N, Yamaguchi N, Kakuta S, et al. Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells. Nat Med. 2001;7(1):94–100. doi: 10.1038/83416 11135622.
74. Renema N, Navet B, Heymann MF, Lezot F, Heymann D. RANK-RANKL signalling in cancer. Biosci Rep. 2016;36(4). doi: 10.1042/BSR20160150 27279652; PubMed Central PMCID: PMC4974605.
75. Holen I, Croucher PI, Hamdy FC, Eaton CL. Osteoprotegerin (OPG) is a survival factor for human prostate cancer cells. Cancer Res. 2002;62(6):1619–23. 11912131.
76. Popovic PJ, Zeh HJ 3rd, Ochoa JB. Arginine and immunity. J Nutr. 2007;137(6 Suppl 2):1681S–6S. doi: 10.1093/jn/137.6.1681S 17513447.
77. Fletcher M, Ramirez ME, Sierra RA, Raber P, Thevenot P, Al-Khami AA, et al. l-Arginine depletion blunts antitumor T-cell responses by inducing myeloid-derived suppressor cells. Cancer Res. 2015;75(2):275–83. doi: 10.1158/0008-5472.CAN-14-1491 25406192; PubMed Central PMCID: PMC4297565.
78. Bronte V, Serafini P, Mazzoni A, Segal DM, Zanovello P. L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol. 2003;24(6):302–6. 12810105.
79. Gun FD, Ozturk OG, Polat A, Polat G. HLA class-II allele frequencies in Turkish breast cancer patients. Med Oncol. 2012;29(2):466–71. Epub 2011/03/05. doi: 10.1007/s12032-011-9873-4 21373933.
80. Mahmoodi M, Nahvi H, Mahmoudi M, Kasaian A, Mohagheghi MA, Divsalar K, et al. HLA-DRB1,-DQA1 and -DQB1 allele and haplotype frequencies in female patients with early onset breast cancer. Pathol Oncol Res. 2012;18(1):49–55. Epub 2011/07/02. doi: 10.1007/s12253-011-9415-6 21720852.
81. Farmaki E, Chatzistamou I, Kaza V, Kiaris H. A CCL8 gradient drives breast cancer cell dissemination. Oncogene. 2016;35(49):6309–18. Epub 2016/05/18. doi: 10.1038/onc.2016.161 27181207; PubMed Central PMCID: PMC5112152.
82. Wang ZQ, Milne K, Webb JR, Watson PH. CD74 and intratumoral immune response in breast cancer. Oncotarget. 2017;8(8):12664–74. Epub 2016/04/09. doi: 10.18632/oncotarget.8610 27058619; PubMed Central PMCID: PMC5355043.
83. Taylor PR, Brown GD, Reid DM, Willment JA, Martinez-Pomares L, Gordon S, et al. The beta-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J Immunol. 2002;169(7):3876–82. Epub 2002/09/24. doi: 10.4049/jimmunol.169.7.3876 12244185.
84. Chiba S, Ikushima H, Ueki H, Yanai H, Kimura Y, Hangai S, et al. Recognition of tumor cells by Dectin-1 orchestrates innate immune cells for anti-tumor responses. Elife. 2014;3:e04177. Epub 2014/08/26. doi: 10.7554/eLife.04177 25149452; PubMed Central PMCID: PMC4161974.
85. Tsai MS, Bogart DF, Castaneda JM, Li P, Lupu R. Cyr61 promotes breast tumorigenesis and cancer progression. Oncogene. 2002;21(53):8178–85. Epub 2002/11/22. doi: 10.1038/sj.onc.1205682 12444554.
86. Huang YT, Lan Q, Lorusso G, Duffey N, Ruegg C. The matricellular protein CYR61 promotes breast cancer lung metastasis by facilitating tumor cell extravasation and suppressing anoikis. Oncotarget. 2017;8(6):9200–15. Epub 2016/12/03. doi: 10.18632/oncotarget.13677 27911269; PubMed Central PMCID: PMC5354725.
87. Marzec KA, Baxter RC, Martin JL. Targeting Insulin-Like Growth Factor Binding Protein-3 Signaling in Triple-Negative Breast Cancer. Biomed Res Int. 2015;2015:638526. Epub 2015/07/30. doi: 10.1155/2015/638526 26221601; PubMed Central PMCID: PMC4499383.
88. Yu H, Levesque MA, Khosravi MJ, Papanastasiou-Diamandi A, Clark GM, Diamandis EP. Associations between insulin-like growth factors and their binding proteins and other prognostic indicators in breast cancer. Br J Cancer. 1996;74(8):1242–7. Epub 1996/10/01. doi: 10.1038/bjc.1996.523 8883411; PubMed Central PMCID: PMC2075943.
89. Sheen-Chen SM, Zhang H, Huang CC, Tang RP. Insulin-like growth factor-binding protein-3 in breast cancer: analysis with tissue microarray. Anticancer Res. 2009;29(4):1131–5. Epub 2009/05/06. 19414355.
90. McCarthy K, Laban C, McVittie CJ, Ogunkolade W, Khalaf S, Bustin S, et al. The expression and function of IGFBP-3 in normal and malignant breast tissue. Anticancer Res. 2009;29(10):3785–90. Epub 2009/10/23. 19846909.
91. Shiff SJ, Rigas B. The role of cyclooxygenase inhibition in the antineoplastic effects of nonsteroidal antiinflammatory drugs (NSAIDs). J Exp Med. 1999;190(4):445–50. Epub 1999/08/17. doi: 10.1084/jem.190.4.445 10449515; PubMed Central PMCID: PMC2195605.
92. Zhang X, Morham SG, Langenbach R, Young DA. Malignant transformation and antineoplastic actions of nonsteroidal antiinflammatory drugs (NSAIDs) on cyclooxygenase-null embryo fibroblasts. J Exp Med. 1999;190(4):451–59. Epub 1999/08/17. doi: 10.1084/jem.190.4.451 10449516; PubMed Central PMCID: PMC2195603.
93. He TC, Chan TA, Vogelstein B, Kinzler KW. PPARdelta is an APC-regulated target of nonsteroidal anti-inflammatory drugs. Cell. 1999;99(3):335–45. Epub 1999/11/11. doi: 10.1016/s0092-8674(00)81664-5 10555149; PubMed Central PMCID: PMC3779681.
94. Liou JY, Ghelani D, Yeh S, Wu KK. Nonsteroidal anti-inflammatory drugs induce colorectal cancer cell apoptosis by suppressing 14-3-3epsilon. Cancer Res. 2007;67(7):3185–91. Epub 2007/04/06. doi: 10.1158/0008-5472.CAN-06-3431 17409426.
95. Gurpinar E, Grizzle WE, Piazza GA. COX-Independent Mechanisms of Cancer Chemoprevention by Anti-Inflammatory Drugs. Front Oncol. 2013;3:181. Epub 2013/07/23. doi: 10.3389/fonc.2013.00181 23875171; PubMed Central PMCID: PMC3708159.
96. Mazhar D, Ang R, Waxman J. COX inhibitors and breast cancer. Br J Cancer. 2006;94(3):346–50. doi: 10.1038/sj.bjc.6602942 16421592; PubMed Central PMCID: PMC2361146.
Článek vyšel v časopise
PLOS One
2019 Číslo 11
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