Effects of modified FOLFOX-6 chemotherapy on cellular immune function in patients with gastric cancer

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1 ONCOLOGY LETTERS 15: , 2018 Effects of modified FOLFOX-6 chemotherpy on cellulr immune function in ptients with gstric cncer LIANG WANG 1, DONGER ZHOU 1, HAITAO REN 2 nd YAN CHEN 3 Deprtments of 1 Heptobiliry Pncretic Surgery nd 2 Burns nd Wound Center, The Second Affilited Hospitl, School of Medicine, Zhejing University, Hngzhou, Zhejing ; 3 Emergency Deprtment, The Second Affilited Hospitl of Dlin Medicl University, Dlin, Lioning , P.R. Chin Received June 19, 2016; Accepted Februry 12, 2018 DOI: /ol Abstrct. Tumor immunosuppression serves n importnt role in the occurrence nd development of gstric cncer. However, the effect of chemotherpy on the immune function of ptients remins uncler. The present study imed to investigte chnges in cellulr immune function nd regultory T cells (T regs ) in ptients with gstric cncer prior to nd following chemotherpy. In the peripherl blood of ptients with gstric cncer, the percentge of CD4 + T cells ws substntilly decresed compred with tht of helthy controls (11.39±5.91 vs ±3.37%, respectively; P<0.05). High frequencies of CD8 + T cells nd T regs were lso observed in the peripherl blood of ptients. Although the number of T cells decresed following chemotherpy (the proportions of CD4 + nd CD8 + cells were 8.99±7.31 nd 16.00±4.51%, respectively), the rtio of CD4 + /CD8 + T cells incresed (0.31±0.17 vs. 0.56±0.22; P<0.05). Furthermore, the level of C C motif chemokine lignd 20 (CCL20) ws incresed in ptients prior to chemotherpy compred with helthy controls. As the sole receptor for CCL20, high level of expression of C C motif chemokine receptor 6 on circulting T regs ws lso identified in the ptients, which decresed following chemotherpy. These results suggest tht chemotherpy my efficiently promote cellulr immune function nd inhibit immunosuppression in ptients with gstric cncer. Correspondence to: Dr Hito Ren, Deprtment of Burns nd Wound Center, The Second Affilited Hospitl, School of Medicine, Zhejing University, 88 Jiefng Street, Hngzhou, Zhejing , P.R. Chin E mil: rht@zju.edu.cn Dr Yn Chen, Emergency Deprtment, The Second Affilited Hospitl of Dlin Medicl University, 467 Zhongshn Rod, Dlin, Lioning , P.R. Chin E mil: chenymet@163.com Key words: gstric cncer, chemotherpy, regultory T cells, chemokine receptor type 6 Introduction Gstric cncer is the second leding cuse of cncer ssocited mortlity in Chin (1). Due to lck of screening protocols, the mjority of ptients often present with loclly dvnced disese or even metstsis t initil dignosis. As surgery lone is not sufficient to gurntee curtive tretment in ptients with dvnced disese, djuvnt therpies must be considered in order to increse the possibility of cure in surgiclly treted ptients with high risk of recurrence (2,3). While chemotherpy hs been widely used in the clinicl tretment of gstric cncer, its effects on the immune sttus of ptients remin unknown. Tumor immune tolernce serves n importnt role in contributing to the occurrence nd development of gstric cncer (4). Previous studies hve indicted tht the outcome of n immune response towrds tumor is primrily determined by the type of immune response elicited (5,6). Regultory T cells (T regs ) hve been demonstrted to induce tumor immunosuppression nd therefore hve prominent role in the development of cncer (7 9). Previous studies hve demonstrted tht the level of T regs, which re usully evluted by immunohistochemicl quntifiction of Forkhed box protein P3 (FoxP3) positive T cells, re ssocited with poor outcome (10 13). The present study explored the effect of folinic cid (FA)/fluorourcil (5 FU)/oxlipltin (FOLFOX 6) chemotherpy on T regs nd the immune function of ptients with gstric cncer prior to nd following chemotherpy. It ws indicted tht chemotherpy my inhibit the secretion of C C motif chemokine lignd 20 (CCL20) to prevent the migrtion of T regs, thereby ssisting in enhncing the ntitumor immune response. Mterils nd methods Ptients nd specimens. The clinicl records of 38 ptients with gstric cncer who underwent curtive surgicl intervention of primry tumors between June 2011 nd September 2014 t the Second Affilited Hospitl, Zhejing University School of Medicine (Hngzhou, Chin) were collected. Written informed consent ws obtined from the ptients nd the study ws pproved by the Ethics Committee of the Second Affilited Hospitl. Tumor stges were clssified ccording to the 7th edition of the Americn Joint Committee on Cncer Tumor Node Metstsis Clssifiction (14). Ptients treted

2 8636 WANG et l: FOLFOX-6 AND CELLULAR IMMUNE FUNCTION IN GASTRIC CANCER with neodjuvnt chemotherpy were excluded. Blood ws obtined from ptients before nd fter chemotherpy nd helthy control. Chemotherpy. Venous blood (3 ml) ws obtined from ptients with gstric cncer (n=38) nd from helthy individuls (n=31), using n EDTA K2 nticogulnt mining vessel (BD Biosciences, Frnklin Lkes, NJ, USA). Blood ws obtined from the gstric cncer ptients 1 dy prior to chemotherpy nd 1 month following chemotherpy. Chemotherpy consisted of 65 mg/m 2 intrvenously (IV) oxlipltin on dy 1, 200 mg/m 2 FA IV s 2 h infusion, followed by 400 mg/m 2 bolus 5 FU IV nd 22 h infusion of 5,600 mg/m 2 5 FU IV on dys 1 nd 2, every 2 weeks (15). All ptients who were included in the present study completed t lest three cycles of chemotherpy. Flow cytometry. Peripherl blood mononucler cells (PBMCs) were isolted by Ficoll density grdient (GE Helthcre, ct. no ) centrifugtion (400 x g for 30 min t 18 C). Antibodies specific for mouse FITC conjugted nti cluster of differentition (CD)4 (clone RM4 5, ct. no ), mouse PE conjugted nti CD25 (clone BC96, ct. no ), mouse APC conjugted nti interleukin receptor 7 (CD127; clone A019D5, ct. no ), mouse APC/CY7 conjugted nti CC motif chemokine receptor 6 (CCR6; clone G034E3, ct. no ) nd mouse PE/CY7 conjugted nti IFN γ (clone B27, ct. no ) were purchsed from BioLegend, Inc., (Sn Diego, CA, USA). A totl of 5 µl ntibody ws dded per million cells in 100 µl stining Buffer (BioLegend, Inc.; ct. no ). IFN γ ws detected by the Intrcellulr Cytokine Stining kit from BD Phrmingen (BD Biosciences), ccording to the mnufcturer's protocol, nd ws quntified by flow cytometry. PBMCs were blocked with Fc Receptor Blocking Solution t room temperture for 5 min (BioLegend, Inc.; ct. no ). After 10 min, red cells were removed by lysis buffer (BioLegend, Inc.; ct. no ). Then, cells were incubted with ntibody t 4 C for 30 min, wshed once with PBS. The cells were resuspended in 0.5 ml PBS. Flow cytometric nlysis ws performed on BD FACSCnto II instrument (BD Biosciences). The dt ws nlyzed by FlowJo V10 (FlowJo LLC, Ashlnd, OR, USA). ELISA. CCL20 ws detected by CCL20 ELISA kit (ct. no. DM3A00; R&D Systems, Inc., Minnepolis, MN, USA), following the mnufcturer's protocol. Sttisticl nlysis. The dt were nlyzed using the Prism 5 softwre (GrphPd Softwre, Inc., Sn Diego, CA, USA). Continuous vribles re presented s the men ± stndrd devition, nd compred using the unpired Student's t test between two groups or one wy nlysis of vrince between multiple groups followed by Tukey's post hoc test. Dichotomous vribles were compred using χ 2 test or Fisher's exct test. P<0.05 ws considered to indicte sttisticlly significnt difference. Results Distribution of T cell subsets in the peripherl blood of ptients with gstric cncer. A totl of 38 ptients Tble I. Clinicl dt of the 38 ptients with gstric cncer. Chrcteristics Vlue Age, yers; medin (rnge) 64 (43 78) Sex, n Mle 23 Femle 16 AJCC stge, n 0 1 I 7 II 11 III 19 IV 0 Performnce sttus, n ECOG ECOG 2 7 Histopthologicl type, n Intestinl 24 Diffuse 12 Unknown 2 UICC, Union for Interntionl Cncer Control; ECOG, Estern Coopertive Oncology Group. Tble II. T cell subsets in PBMCs from ptients nd controls. Ptients Helthy controls Group (n=38) (n=31) P vlue CD4 + /PBMC (%) 11.39± ± CD8 + /PBMC (%) 36.81± ± CD4 + /CD ± ± Sttisticlly significnt (P<0.05). PBMCs, peripherl blood mononucler cells; CD, cluster of differentition. were enrolled in the present study, including 23 mles nd 16 femles. The ge of the ptients rnged from 43 to 78 yers, with medin ge of 64 yers. A totl of 31 ptients hd grde 0 1 ECOG performnce sttus; the other 7 ptients hd grde 2 ECOG performnce sttus (16) (Tble I). The proportions of CD4 + nd CD8 + T cells in the peripherl blood of ptients with gstric cncer nd norml control individuls were compred. The percentge of CD4 + T cells ws significntly decresed compred with tht of the norml controls (22.34±3.37 vs ±5.91%; P=0.03). However, the percentge of CD8 + T cells ws incresed in the ptients with gstric cncer compred with the controls (36.81±5.33 vs ±2.01%, respectively; P=0.01; Fig. 1; Tble II). In ddition, the rtio of CD4 + T cells to CD8 + T cells ws significntly decresed in the ptient group compred with the helthy control group (P=0.005; Tble II). These results indicted tht the ptients with gstric cncer exhibited impired cellulr immune function compred with the

3 ONCOLOGY LETTERS 15: , Figure 1. Proportion of CD4 + nd CD8 + T cells in the peripherl blood from ptients with gstric cncer (prior to nd following chemotherpy), nd from the control group. CD, cluster of differentition. Tble III. T cell subsets in PBMCs between ptients prior to nd following chemotherpy. Prior to Following Group chemotherpy chemotherpy P vlue CD4 + /PBMC, % 11.39± ± CD8 + /PBMC, % 36.81± ± CD4 + /CD8 + rtio 0.31± ± Sttisticlly significnt (P<0.05). PBMCs, peripherl blood mononucler cells; CD, cluster of differentition. Tble V. Distribution of CD4 + T cell subsets in peripherl blood mononucler cells between ptients prior to nd following chemotherpy. Prior to Following Group chemotherpy chemotherpy P vlue IFN γ + /CD4 + (%) 13.15± ± T reg /CD4 + (%) 18.33± ± Sttisticlly significnt (P<0.05). IFN γ, interferon γ; CD, cluster of differentition; T reg, T regultory cells. Tble IV. Distribution of CD4 + T cell subsets in peripherl blood mononucler cells between ptients nd controls. Ptients Helthy Group (n=38) controls (n=31) P vlue IFN γ + /CD4 + (%) 13.15± ± T reg /CD4 + (%) 18.33± ± Sttisticlly significnt (P<0.05). IFN γ, interferon γ; CD, cluster of differentition; T reg, T regultory cells. helthy controls. The proportions of CD4 + T cells nd CD8 + T cells in the PBMCs of ptients with gstric cncer prior to nd following chemotherpy were dditionlly ssessed by flow cytometric nlysis (Fig. 1). Prior to chemotherpy, the CD4 + nd CD8 + T cells ccounted for 11.39±5.91% nd 36.81±5.33%, respectively, in the ptient group. Although the number of T cells decresed following chemotherpy (the proportions of CD4 + nd CD8 + cells were 8.99±7.31% nd 16.00±4.51%, respectively), the rtio of CD4 + /CD8 + T cells ws incresed compred with the rtio prior to chemotherpy [0.56±0.22 vs. 0.31±0.17, respectively (P<0.05); Tble III]. Effect of chemotherpy on T cell subsets. To evlute the effect of chemotherpy on the function of the T cells, the production of interferon (IFN) γ by CD4 + T cells in ptients ws investigted. It ws identified tht the percentge of IFN γ + T cells from the CD4 + T cells ws decresed in the ptient cohort compred with helthy controls (Tble IV), but ws incresed following chemotherpy compred with prior to chemotherpy (Fig. 2; Tble V). Furthermore, whether the chemotherpy ffected immunosuppressive T regs cells ws exmined. Liu et l (17) suggested tht CD127 expression is inversely correlted with FoxP3 in T regs cells; thus, CD127 ws exmined insted of FoxP3 in the present study (Fig. 3). It ws identified tht the proportion of T regs ws significntly incresed in the ptients vs. helthy controls (Tble IV), but decresed following chemotherpy compred with prior to chemotherpy (Tble V). These results suggest tht chemotherpy my promote ntitumor immunity nd prtilly restore cellulr immune function in ptients with gstric cncer. CCL20 is required for the recruitment of CCR6 + T regs in ptients with gstric cncer. It hs been estblished tht the CCL20/CCR6 signl medites the migrtion of T regs to the tumor microenvironment in humn liver cncer (11,18). To identify whether this occurred in gstric cncer, the concentrtion of CCL20 in 30 ptients nd 30 helthy controls from the originl cohort ws detected. The results indicted tht the level of CCL20 ws significntly incresed prior to

4 8638 WANG et l: FOLFOX-6 AND CELLULAR IMMUNE FUNCTION IN GASTRIC CANCER Figure 2. IFN γ production in CD4 + T cells in the peripherl blood of ptients with gstric cncer (prior to nd following chemotherpy) nd the control group. CD, cluster of differentition; IFN γ, interferon γ. Figure 3. Percentge of CD25 + /CD127 /CD4 + T cells in the peripherl blood of ptients with gstric cncer (prior to nd following chemotherpy) nd the control group. CD, cluster of differentition. Figure 4. Expression levels of (A) CCL20 nd (B) CCR6 in the peripherl blood of ptients with gstric cncer (prior to nd following chemotherpy) nd the control group. CCL20, C C motif chemokine lignd 20; CCR6, C C motif chemokine receptor 6. Dt re compred using the unpired t test ( *** P<0.001).

5 ONCOLOGY LETTERS 15: , chemotherpy in ptients compred with the helthy controls (Fig. 4A). After chemotherpy, the expression of CCL20 significntly decresed. CCR6 hs been estblished s the sole receptor for the chemokine CCL20 (11). As expected, it ws identified tht the expression of CCR6 on T regs ws significntly decresed following chemotherpy (P<0.01; Fig. 4B). These dt suggested tht CCL20 ws required for the recruitment of CCR6 + T regs in ptients with gstric cncer. Discussion Due to the low chemotherpeutic sensitivity of gstric cncer, surgery nd chemotherpy is the primry course of tretment, nd gstric cncer hs 5 yer overll survivl rte of 30 60% in surgiclly curble cses (19,20). The survivl benefits of chemotherpy re well recognized, but the effect of chemotherpy on immune cells remins unknown. Tumors re believed to be controlled by the immune system through process termed immunosurveillnce, which includes n equilibrium phse nd eventul immune escpe. The results from previous study using mouse model indicted tht chemotherpy my selectively inhibit T regs, while spring effector T cells (21). Of the compounds included in the chemotherpy regimens of the present study, oxlipltin nd 5 FU re hypothesized to induce immunogenic cell deth nd prtilly deplete or trnsiently inctivte inhibitory immune cells (22). Therefore, we hypothesized tht chemotherpy my result in immunomodultion in ptients, suppressing the inhibitory immune cell function. Cellulr immunity serves key role in the ntitumor immune response (23). T cells re criticl in the immune regultion nd surveillnce involved in cellulr immunity, nd re divided into two mjor subsets: CD4 + nd CD8 +. The rtio of CD4 + /CD8 + cells significntly ffects the host immune function; decresed CD4 + /CD8 + rtio impirs the immune systems of ptients nd promotes the development of tumors (24). A previous study indicted tht chemotherpy my selectively decrese nïve CD4 + T cells, but preserved the ctivted CD4 + or CD8 + nd memory T cells (25). However, this prticulr study compred the frction of CD4 + cells mong the totl mononucler cells in the bone mrrow of ptients with tht of helthy controls (13.7±5.0 vs. 22.9±6.6, respectively), which my not tke into ccount the complex cell composition of the bone mrrow. Furthermore, from the sme dt set, n increse of the rtio of CD4 + /CD8 + (1.63 vs. 1.55) ws identified in the ptients received chemotherpy, compred with the helthy control (25). We hypothesize tht the percentge of CD4 in peripherl blood my better reflect the immune sttus of ptients, s there re numerous cell types existing in BM, including progenitors nd nïve T cells. Consistent with this previous study, to the best of our knowledge, the present study demonstrted for the first time the effects of systemic tretment on the peripherl immune cell popultions of ptients with gstric cncer. Although totl counts were reduced following chemotherpy, the proportion of CD4 + /CD8 + cells incresed compred with before chemotherpy, suggesting tht chemotherpy my enhnce the cellulr immune function in ptients with gstric cncer. T regs serve criticl role in the mintennce of self tolernce nd suppression of utoimmune disese (26,27). T regs re lso essentil for the immunopthogenesis of cncer, in which they my prevent the nti tumor immune response in non ntigen specific mnner (28). There is emerging evidence suggesting tht higher frequencies of T regs in tumors microenvironment re ssocited with poor outcome (29,30). However, the role of T regs remins controversil in gstric cncer, prticulrly in the peripherl blood: Previous studies hve demonstrted tht CD4 + CD25 + (T regs ) cells comprise 5 10% of peripherl CD4 + T cells in helthy controls (11); however, this is inccurte for the T regs definition. The most specific cell mrker of T regs identified is the nucler trnscription fctor FoxP3 (31). As Liu et l (17) demonstrted, CD127 expression ws inversely correlted with FoxP3 expression. In the present study, the combined expression of CD4, CD25 nd CD127 ws used to clculte the popultion of T reg cells out of the totl CD4 + popultion; this proportion ws 1.5±0.31% in helthy controls, but ws significntly incresed in ptients with gstric cncer (18.33±2.51%). Furthermore, the function of CD4 + T cells ws lso investigted in ptients with gstric cncer. Incresed IFN γ production following chemotherpy ws identified, which is predominntly medited by CD4 + T cells subsequent to the development of ntigen specific immunity. Tken together, the dt from the present study indicted tht chemotherpy my effectively suppress the quntity nd function of T regs. The high frction of T regs in the peripherl blood rises the question how these cells migrte to the tumor. It hs been reveled tht CCL20 is importnt in recruiting circulting T regs into tumor tissue in the liver cncer (11,18). In the present study, n increse in the level of CCL20 ws lso observed in the ptient group compred with helthy controls. Furthermore, s the only known receptor for CCL20 (32), the level of CCR6 ws significntly higher in the T regs of ptients. Therefore, the elevtion of T regs is due to, t lest in prt, their selective migrtion in response to CCL20. In conclusion, the present study suggested tht chemotherpy my promote cellulr immune function nd inhibit immunosuppression in ptients with gstric cncer. These results provide dditionl understnding of the mechnism of FOLFOX 6 chemotherpy on gstric cncer, nd provide importnt insights into the immune sttus of ptients with gstric cncer. Acknowledgements Not pplicble. Funding The present study ws supported by grnts from the Scientific Reserch Foundtion of the Helth Deprtment of Zhejing Province (grnt no., 2011KYA069) nd the Nturl Science Foundtion of Zhejing Province, Chin (grnt nos., LY15H150004, LY17H nd LQ15H160010). Avilbility of dt nd mterils The dtsets used nd/or nlyzed during the current study re vilble from the corresponding uthor on resonble request.

6 8640 WANG et l: FOLFOX-6 AND CELLULAR IMMUNE FUNCTION IN GASTRIC CANCER Authors' contributions HR nd LW conceived the ide. LW nd DZ performed the experiments. HR nlyzed the dt. HR, LW nd DZ wrote the mnuscript. All uthors red nd pproved the finl mnuscript. Ethics pprovl nd consent to prticipte Informed consent ws obtined from the ptients nd the study ws pproved by the Ethics Committee of the Second Affilited Hospitl. Consent for publiction Not pplicble. Competing interests The uthors declre tht they hve no competing interests. References 1. Chen W, Zheng R, Bde PD, Zhng S, Zeng H, Bry F, Jeml A, Yu XQ nd He J: Cncer sttistics in Chin, CA Cncer J Clin 66: , Kim NK, Prk YS, Heo DS, Suh C, Kim SY, Prk KC, Kng YK, Shin DB, Kim HT, Kim HJ, et l: A phse III rndomized study of 5 fluorourcil nd cispltin versus 5 fluorourcil, doxorubicin, nd mitomycin C versus 5 fluorourcil lone in the tretment of dvnced gstric cncer. Cncer 71: , Wöhrer SS, Rderer M nd Hejn M: Pllitive chemotherpy for dvnced gstric cncer. Ann Oncol 15: , Choi HS, H SY, Kim HM, Ahn SM, Kng MS, Kim KM, Choi MG, Lee JH, Sohn TS, Be JM, et l: The prognostic effects of tumor infiltrting regultory T cells nd myeloid derived suppressor cells ssessed by multicolor flow cytometry in gstric cncer ptients. Oncotrget 7: , Gjewski TF, Schreiber H nd Fu YX: Innte nd dptive immune cells in the tumor microenvironment. Nt Immunol 14: , Goodmn AM, Kto S, Bzhenov L, Ptel SP, Frmpton GM, Miller V, Stephens PJ, Dniels GA nd Kurzrock R: Tumor muttionl burden s n independent predictor of response to immunotherpy in diverse cncers. Mol Cncer Ther 16: , Zou W: Regultory T cells, tumour immunity nd immunotherpy. Nt Rev Immunol 6: , Curiel TJ: Tregs nd rethinking cncer immunotherpy. J Clin Invest 117: , DeNrdo DG nd Coussens LM: Inflmmtion nd brest cncer. Blncing immune response: Crosstlk between dptive nd innte immune cells during brest cncer progression. Brest Cncer Res 9: 212, Crrers J, Lopez Guillermo A, Fox BC, Colomo L, Mrtinez A, Roncdor G, Montserrt E, Cmpo E nd Bnhm AH: High numbers of tumor infiltrting FOXP3 positive regultory T cells re ssocited with improved overll survivl in folliculr lymphom. Blood 108: , Chen KJ, Lin SZ, Zhou L, Xie HY, Zhou WH, Tki Eldin A nd Zheng SS: Selective recruitment of regultory T cell through CCR6 CCL20 in heptocellulr crcinom fosters tumor progression nd predicts poor prognosis. PLoS One 6: e24671, Deng L, Zhng H, Lun Y, Zhng J, Xing Q, Dong S, Wu X, Liu M nd Wng S: Accumultion of foxp3+ T regultory cells in drining lymph nodes correltes with disese progression nd immune suppression in colorectl cncer ptients. Clin Cncer Res 16: , Droeser R, Zlobec I, Kilic E, Güth U, Heberer M, Spgnoli G, Oertli D nd Tpi C: Differentil pttern nd prognostic significnce of CD4+, FOXP3+ nd IL 17+ tumor infiltrting lymphocytes in ductl nd lobulr brest cncers. BMC Cncer 12: 134, Edge SB nd Compton CC: The Americn Joint Committee on Cncer: The 7th edition of the AJCC cncer stging mnul nd the future of TNM. Ann Surg Oncol 17: , Kem B, Im SA, Hn SW, Hm HS, Kim MA, Oh DY, Lee SH, Kim JH, Kim DW, Kim TY, et l: Modified FOLFOX 6 chemotherpy in dvnced gstric cncer: Results of phse II study nd comprehensive nlysis of polymorphisms s predictive nd prognostic mrker. BMC Cncer 8: 148, Oken MM, Creech RH, Tormey DC, Horton J, Dvis TE, McFdden ET nd Crbone PP: Toxicity nd response criteri of the Estern Coopertive Oncology Group. Am J Clin Oncol 5: , Liu W, Putnm AL, Xu Yu Z, Szot GL, Lee MR, Zhu S, Gottlieb PA, Kprnov P, Gingers TR, Fzeks de St Groth B, et l: CD127 expression inversely correltes with FoxP3 nd suppressive function of humn CD4+ T reg cells. J Exp Med 203: , Ye LY, Chen W, Bi XL, Xu XY, Zhng Q, Xi XF, Sun X, Li GG, Hu QD, Fu QH nd Ling TB: Hypoxi induced epithelil to mesenchyml trnsition in heptocellulr crcinom induces n immunosuppressive tumor microenvironment to promote metstsis. Cncer Res 76: , Kelley JR nd Duggn JM: Gstric cncer epidemiology nd risk fctors. J Clin Epidemiol 56: 1 9, Kmngr F, Dores GM nd Anderson WF: Ptterns of cncer incidence, mortlity, nd prevlence cross five continents: Defining priorities to reduce cncer disprities in different geogrphic regions of the world. J Clin Oncol 24: , Shurin GV, Tourkov IL, Kneno R nd Shurin MR: Chemotherpeutic gents in noncytotoxic concentrtions increse ntigen presenttion by dendritic cells vi n IL 12 dependent mechnism. J Immunol 183: , Vincent J, Mignot G, Chlmin F, Ldoire S, Bruchrd M, Chevriux A, Mrtin F, Apetoh L, Rébé C nd Ghiringhelli F: 5 Fluorourcil selectively kills tumor ssocited myeloid derived suppressor cells resulting in enhnced T cell dependent ntitumor immunity. Cncer Res 70: , Lio J, Xio J, Zhou Y, Liu Z nd Wng C: Effect of trnsctheter rteril chemoemboliztion on cellulr immune function nd regultory T cells in ptients with heptocellulr crcinom. Mol Med Rep 12: , Shh W, Yn X, Jing L, Zhou Y, Chen H nd Wng Y: A reversed CD4/CD8 rtio of tumor infiltrting lymphocytes nd high percentge of CD4(+)FOXP3(+) regultory T cells re significntly ssocited with clinicl outcome in squmous cell crcinom of the cervix. Cell Mol Immunol 8: 59 66, Solomyer EF, Feuerer M, Bi L, Umnsky V, Beckhove P, Meyberg GC, Bstert G, Schirrmcher V nd Diel IJ: Influence of djuvnt hormone therpy nd chemotherpy on the immune system nlysed in the bone mrrow of ptients with brest cncer. Clin Cncer Res 9: , Kono K, Kwid H, Tkhshi A, Sugi H, Mimur K, Miygw N, Omt H nd Fujii H: CD4(+)CD25high regultory T cells increse with tumor stge in ptients with gstric nd esophgel cncers. Cncer Immunol Immunother 55: , Ke X, Wng J, Li L, Chen IH, Wng H nd Yng XF: Roles of CD4+CD25(high) FOXP3+ Tregs in lymphoms nd tumors re complex. Front Biosci 13: , Ldoire S, Mrtin F nd Ghiringhelli F: Prognostic role of FOXP3+ regultory T cells infiltrting humn crcinoms: The prdox of colorectl cncer. Cncer Immunol Immunother 60: , Hs M, Dimmler A, Hohenberger W, Grbenbuer GG, Niedobitek G nd Distel LV: Stroml regultory T cells re ssocited with fvourble prognosis in gstric cncer of the crdi. BMC Gstroenterol 9: 65, Gooden MJ, de Bock GH, Leffers N, Demen T nd Nijmn HW: The prognostic influence of tumour infiltrting lymphocytes in cncer: A systemtic review with met nlysis. Br J Cncer 105: , Mougikkos D, Choudhury A, Lldser A, Kiessling R nd Johnsson CC: Regultory T cells in cncer. Adv Cncer Res 107: , Ghdjr P, Rubie C, Aebersold DM nd Keilholz U: The chemokine CCL20 nd its receptor CCR6 in humn mlignncy with focus on colorectl cncer. Int J Cncer 125: , 2009.

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