Review
. 2018 Sep; 24(32):3583-3616.
doi: 10.3748/wjg.v24.i32.3583.

Prognostic significance of tumor immune microenvironment and immunotherapy: Novel insights and future perspectives in gastric cancer

Daniela Cornelia Lazăr 1 Mihaela Flavia Avram 2 Ioan Romoșan 3 Mărioara Cornianu 4 Sorina Tăban 4 Adrian Goldiș 5 
Affiliations
  • PMID: 30166856
  •     224 References
  •     58 citations

Abstract

Despite a decrease in gastric cancer incidence, the development of novel biologic agents and combined therapeutic strategies, the prognosis of gastric cancer remains poor. Recently, the introduction of modern immunotherapy, especially using immune checkpoint inhibitors, led to an improved prognosis in many cancers. The use of immunotherapy was also associated with manageable adverse event profiles and promising results in the treatment of patients with gastric cancer, especially in heavily pretreated patients. These data have led to an accelerated approval of some checkpoint inhibitors in this setting. Understanding the complex relationship between the host immune microenvironment and tumor and the immune escape phenomenon leading to cancer occurrence and progression will subsequently lead to the identification of prognostic immune markers. Furthermore, this understanding will result in the discovery of both new mechanisms for blocking tumor immunosuppressive signals and pathways to stimulate the local immune response by targeting and modulating different subsets of immune cells. Due to the molecular heterogeneity of gastric cancers associated with different clinico-biologic parameters, immune markers expression and prognosis, novel immunotherapy algorithms should be personalized and addressed to selected subsets of gastric tumors, which have been proven to elicit the best clinical responses. Future perspectives in the treatment of gastric cancer include tailored dual immunotherapies or a combination of immunotherapy with other targeted agents with synergistic antitumor effects.

Keywords: Gastric cancer; Immune checkpoint inhibitors; Immunotherapy; Prognostic significance; Tumor immune microenvironment.

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Oncotarget, 2015 May 27; 6(24). PMID: 26008981    Free PMC article.
Efficient eradication of subcutaneous but not of autochthonous gastric tumors by adoptive T cell transfer in an SV40 T antigen mouse model.
Carole Bourquin, Philip von der Borch, +8 authors, Stefan Endres.
J Immunol, 2010 Jul 21; 185(4). PMID: 20644173
Analysis of promoter methylation, polymorphism and expression profile of cytotoxic T-lymphocyte-associated antigen-4 in patients with gastric cancer.
Dor Mohammad Kordi-Tamandani, Shahrbbanou Karimi Davani, Taybeh Baranzehi, Simin Hemati.
J Gastrointestin Liver Dis, 2014 Oct 01; 23(3). PMID: 25267951
The toxins of William B. Coley and the treatment of bone and soft-tissue sarcomas.
Edward F McCarthy.
Iowa Orthop J, 2006 Jun 23; 26. PMID: 16789469    Free PMC article.
Highly Cited.
The peripheral immune status of granulocytic myeloid-derived suppressor cells correlates the survival in advanced gastric cancer patients receiving cisplatin-based chemotherapy.
Hirokazu Shoji, Kohei Tada, +14 authors, Tetsuya Hamaguchi.
Oncotarget, 2017 Dec 10; 8(56). PMID: 29221113    Free PMC article.
Medical management of gastric cancer: a 2017 update.
Nikolaos Charalampakis, Panagiota Economopoulou, +6 authors, Amanda Psyrri.
Cancer Med, 2017 Dec 15; 7(1). PMID: 29239137    Free PMC article.
Review.
Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma.
Andrew T Parsa, James S Waldron, +10 authors, Russell O Pieper.
Nat Med, 2006 Dec 13; 13(1). PMID: 17159987
Highly Cited.
The blockade of immune checkpoints in cancer immunotherapy.
Drew M Pardoll.
Nat Rev Cancer, 2012 Mar 23; 12(4). PMID: 22437870    Free PMC article.
Highly Cited. Review.
Tumor infiltration by Tbet+ effector T cells and CD20+ B cells is associated with survival in gastric cancer patients.
Audrey Hennequin, Valentin Derangère, +10 authors, Sylvain Ladoire.
Oncoimmunology, 2016 Apr 09; 5(2). PMID: 27057426    Free PMC article.
The clinicopathological and prognostic significance of PD-L1 expression in gastric cancer: a meta-analysis of 10 studies with 1,901 patients.
Minghui Zhang, Yuandi Dong, +5 authors, Qingyuan Zhang.
Sci Rep, 2016 Nov 29; 6. PMID: 27892511    Free PMC article.
Improved survival with ipilimumab in patients with metastatic melanoma.
F Stephen Hodi, Steven J O'Day, +26 authors, Walter J Urba.
N Engl J Med, 2010 Jun 08; 363(8). PMID: 20525992    Free PMC article.
Highly Cited.
The prognostic effects of tumor infiltrating regulatory T cells and myeloid derived suppressor cells assessed by multicolor flow cytometry in gastric cancer patients.
Han Sol Choi, Sang Yun Ha, +9 authors, Eun-Suk Kang.
Oncotarget, 2016 Jan 23; 7(7). PMID: 26799288    Free PMC article.
Immune response against frameshift-induced neopeptides in HNPCC patients and healthy HNPCC mutation carriers.
Yvette Schwitalle, Matthias Kloor, +6 authors, Magnus von Knebel Doeberitz.
Gastroenterology, 2008 Apr 09; 134(4). PMID: 18395080
Highly Cited.
The biology of VEGF and its receptors.
Napoleone Ferrara, Hans-Peter Gerber, Jennifer LeCouter.
Nat Med, 2003 Jun 05; 9(6). PMID: 12778165
Highly Cited. Review.
Comprehensive molecular characterization of gastric adenocarcinoma.
Cancer Genome Atlas Research Network.
Nature, 2014 Aug 01; 513(7517). PMID: 25079317    Free PMC article.
Highly Cited.
Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients.
Mark E Dudley, John R Wunderlich, +2 authors, Steven A Rosenberg.
J Immunother, 2003 Jul 05; 26(4). PMID: 12843795    Free PMC article.
Highly Cited.
Chromosome 9p copy number gains involving PD-L1 are associated with a specific proliferation and immune-modulating gene expression program active across major cancer types.
Jan Budczies, Carsten Denkert, +2 authors, Albrecht Stenzinger.
BMC Med Genomics, 2017 Dec 08; 10(1). PMID: 29212506    Free PMC article.
The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma.
S Coca, J Perez-Piqueras, +5 authors, M Moreno.
Cancer, 1997 Jun 15; 79(12). PMID: 9191519
Highly Cited.
Fulminant Myocarditis with Combination Immune Checkpoint Blockade.
Douglas B Johnson, Justin M Balko, +29 authors, Javid J Moslehi.
N Engl J Med, 2016 Nov 03; 375(18). PMID: 27806233    Free PMC article.
Highly Cited.
Ex-vivo expanded human NK cells express activating receptors that mediate cytotoxicity of allogeneic and autologous cancer cell lines by direct recognition and antibody directed cellular cytotoxicity.
Caroline J Voskens, Ryuko Watanabe, +3 authors, Dean L Mann.
J Exp Clin Cancer Res, 2010 Oct 13; 29. PMID: 20937115    Free PMC article.
Microsatellite instability and survival in gastric cancer: A systematic review and meta-analysis.
Lin Zhu, Zhi Li, +3 authors, Xiujuan Qu.
Mol Clin Oncol, 2015 Jul 03; 3(3). PMID: 26137290    Free PMC article.
PD-1 and PD-L1 as emerging therapeutic targets in gastric cancer: current evidence.
Phu N Tran, Sarmen Sarkissian, Joseph Chao, Samuel J Klempner.
Gastrointest Cancer, 2017 Aug 02; 7. PMID: 28757801    Free PMC article.
Meta-analysis shows that prevalence of Epstein-Barr virus-positive gastric cancer differs based on sex and anatomic location.
Gwen Murphy, Ruth Pfeiffer, M Constanza Camargo, Charles S Rabkin.
Gastroenterology, 2009 May 19; 137(3). PMID: 19445939    Free PMC article.
Highly Cited.
Elevated neutrophil-to-lymphocyte ratio is associated with nutritional impairment, immune suppression, resistance to S-1 plus cisplatin, and poor prognosis in patients with stage IV gastric cancer.
Kenji Gonda, Masahiko Shibata, +6 authors, Shinich Sakuramoto.
Mol Clin Oncol, 2017 Dec 30; 7(6). PMID: 29285377    Free PMC article.
Enhancement of DC vaccine potency by activating the PI3K/AKT pathway with a small interfering RNA targeting PTEN.
Jin Hee Kim, Tae Heung Kang, +9 authors, Tae Woo Kim.
Immunol Lett, 2010 Aug 24; 134(1). PMID: 20727912
Adoptive immunotherapy of human gastric cancer with ex vivo expanded T cells.
Yeon Jin Kim, Jaeseung Lim, +7 authors, Sang-Bae Han.
Arch Pharm Res, 2010 Dec 01; 33(11). PMID: 21116782
Pembrolizumab versus Chemotherapy for PD-L1-Positive Non-Small-Cell Lung Cancer.
Martin Reck, Delvys Rodríguez-Abreu, +16 authors, KEYNOTE-024 Investigators.
N Engl J Med, 2016 Oct 11; 375(19). PMID: 27718847
Highly Cited.
Ipilimumab plus dacarbazine for previously untreated metastatic melanoma.
Caroline Robert, Luc Thomas, +21 authors, Jedd D Wolchok.
N Engl J Med, 2011 Jun 07; 364(26). PMID: 21639810
Highly Cited.
Molecular mechanisms of T cell co-stimulation and co-inhibition.
Lieping Chen, Dallas B Flies.
Nat Rev Immunol, 2013 Mar 09; 13(4). PMID: 23470321    Free PMC article.
Highly Cited. Review.
Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1).
Michal Marzec, Qian Zhang, +8 authors, Mariusz A Wasik.
Proc Natl Acad Sci U S A, 2008 Dec 18; 105(52). PMID: 19088198    Free PMC article.
Highly Cited.
Increased PD-1 expression on CD4+ and CD8+ T cells is involved in immune evasion in gastric cancer.
Hiroaki Saito, Hirohiko Kuroda, +2 authors, Masahide Ikeguchi.
J Surg Oncol, 2012 Nov 07; 107(5). PMID: 23129549
The novel negative checkpoint regulator VISTA is expressed in gastric carcinoma and associated with PD-L1/PD-1: A future perspective for a combined gastric cancer therapy?
Christine Böger, Hans-Michael Behrens, Sandra Krüger, Christoph Röcken.
Oncoimmunology, 2017 May 17; 6(4). PMID: 28507801    Free PMC article.
Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation.
G J Freeman, A J Long, +16 authors, T Honjo.
J Exp Med, 2000 Oct 04; 192(7). PMID: 11015443    Free PMC article.
Highly Cited.
Efficacy of adjuvant immunotherapy with cytokine-induced killer cells in patients with locally advanced gastric cancer.
Liangrong Shi, Qi Zhou, +4 authors, Changping Wu.
Cancer Immunol Immunother, 2012 Jun 08; 61(12). PMID: 22674056    Free PMC article.
Gastric cancer: ESMO-ESSO-ESTRO Clinical Practice Guidelines for diagnosis, treatment and follow-up.
T Waddell, M Verheij, +6 authors, European Society of Radiotherapy and Oncology (ESTRO).
Ann Oncol, 2013 Oct 23; 24 Suppl 6. PMID: 24078663
Highly Cited.
Carboplatin and pemetrexed with or without pembrolizumab for advanced, non-squamous non-small-cell lung cancer: a randomised, phase 2 cohort of the open-label KEYNOTE-021 study.
Corey J Langer, Shirish M Gadgeel, +17 authors, KEYNOTE-021 investigators.
Lancet Oncol, 2016 Oct 18; 17(11). PMID: 27745820    Free PMC article.
Highly Cited.
Clinicopathological features of programmed death ligand 1 expression with tumor-infiltrating lymphocyte, mismatch repair, and Epstein-Barr virus status in a large cohort of gastric cancer patients.
Akihito Kawazoe, Takeshi Kuwata, +7 authors, Atsushi Ochiai.
Gastric Cancer, 2016 Sep 16; 20(3). PMID: 27629881
Highly Cited.
Interaction of PD-L1 on tumor cells with PD-1 on tumor-specific T cells as a mechanism of immune evasion: implications for tumor immunotherapy.
Christian Blank, Thomas F Gajewski, Andreas Mackensen.
Cancer Immunol Immunother, 2004 Dec 16; 54(4). PMID: 15599732
Highly Cited. Review.
An open-label, multinational, multicenter study of G17DT vaccination combined with cisplatin and 5-fluorouracil in patients with untreated, advanced gastric or gastroesophageal cancer: the GC4 study.
Jaffer A Ajani, J Randolph Hecht, +4 authors, Dov Michaeli.
Cancer, 2006 Mar 29; 106(9). PMID: 16568451
Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells.
Jens Dannull, Zhen Su, +8 authors, Johannes Vieweg.
J Clin Invest, 2005 Nov 26; 115(12). PMID: 16308572    Free PMC article.
Highly Cited.
Higher numbers of T-bet(+) intratumoral lymphoid cells correlate with better survival in gastric cancer.
Lu-jun Chen, Xiao Zheng, +9 authors, Jing-ting Jiang.
Cancer Immunol Immunother, 2012 Oct 24; 62(3). PMID: 23090288
Programmed death-ligand 1 expression in gastric adenocarcinoma is a poor prognostic factor in a high CD8+ tumor infiltrating lymphocytes group.
Hyeyoon Chang, Woon Yong Jung, +5 authors, Baek-Hui Kim.
Oncotarget, 2016 Oct 16; 7(49). PMID: 27741514    Free PMC article.
Concordance of immune checkpoints within tumor immune contexture and their prognostic significance in gastric cancer.
Congqi Dai, Ruixuan Geng, +6 authors, Jin Li.
Mol Oncol, 2016 Oct 11; 10(10). PMID: 27720576    Free PMC article.
Decreased density of CD3+ tumor-infiltrating lymphocytes during gastric cancer progression.
Takaaki Arigami, Yoshikazu Uenosono, +8 authors, Shoji Natsugoe.
J Gastroenterol Hepatol, 2015 Jan 15; 29(7). PMID: 25587614
Clinical studies applying cytokine-induced killer cells for the treatment of gastrointestinal tumors.
Clara E Jäkel, Annabelle Vogt, Maria A Gonzalez-Carmona, Ingo G H Schmidt-Wolf.
J Immunol Res, 2014 Apr 18; 2014. PMID: 24741629    Free PMC article.
Review.
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A Galetto, M Contarini, +7 authors, L Matera.
J Surg Res, 2001 Aug 23; 100(1). PMID: 11516202
Programmed death-1 (PD-1) polymorphism is associated with gastric cardia adenocarcinoma.
Weifeng Tang, Yu Chen, +3 authors, Mingqiang Kang.
Int J Clin Exp Med, 2015 Jul 30; 8(5). PMID: 26221374    Free PMC article.
Long-term survival of adoptively transferred tumor-infiltrating lymphocytes in mice.
R B Alexander, S A Rosenberg.
J Immunol, 1990 Sep 01; 145(5). PMID: 1974569
CDC20, a potential cancer therapeutic target, is negatively regulated by p53.
T Kidokoro, C Tanikawa, +3 authors, K Matsuda.
Oncogene, 2007 Sep 18; 27(11). PMID: 17873905
Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes.
Mark E Dudley, John R Wunderlich, +16 authors, Steven A Rosenberg.
Science, 2002 Sep 21; 298(5594). PMID: 12242449    Free PMC article.
Highly Cited.
Role of regulatory T-cells in H. pylori-induced gastritis and gastric cancer.
Arne Kandulski, Peter Malfertheiner, Thomas Wex.
Anticancer Res, 2010 Jun 10; 30(4). PMID: 20530414
Review.
Prognostic implications of immunosuppressive protein expression in tumors as well as immune cell infiltration within the tumor microenvironment in gastric cancer.
Jin Won Kim, Kyung Han Nam, +11 authors, Keun-Wook Lee.
Gastric Cancer, 2014 Nov 27; 19(1). PMID: 25424150
Highly Cited.
VISTA, a novel mouse Ig superfamily ligand that negatively regulates T cell responses.
Li Wang, Rotem Rubinstein, +10 authors, Randolph J Noelle.
J Exp Med, 2011 Mar 09; 208(3). PMID: 21383057    Free PMC article.
Highly Cited.
PD-L1 expression analysis in gastric carcinoma tissue and blocking of tumor-associated PD-L1 signaling by two functional monoclonal antibodies.
J Sun, K Xu, +7 authors, X Zhang.
Tissue Antigens, 2007 Jan 11; 69(1). PMID: 17212704
VISTA Regulates the Development of Protective Antitumor Immunity.
Isabelle Le Mercier, Wenna Chen, +5 authors, Li Wang.
Cancer Res, 2014 Apr 03; 74(7). PMID: 24691994    Free PMC article.
Highly Cited.
Preparation and antitumor effects of nanovaccines with MAGE-3 peptides in transplanted gastric cancer in mice.
Jun Yang, Zhi-Hua Li, +4 authors, Li-Qun Yang.
Chin J Cancer, 2010 Mar 30; 29(4). PMID: 20346208
Immunotherapy for Esophageal and Gastric Cancer.
Ronan J Kelly.
Am Soc Clin Oncol Educ Book, 2017 Jun 01; 37. PMID: 28561677
Review.
PD-L1 is an independent prognostic predictor in gastric cancer of Western patients.
Christine Böger, Hans-Michael Behrens, +3 authors, Christoph Röcken.
Oncotarget, 2016 Mar 25; 7(17). PMID: 27009855    Free PMC article.
Highly Cited.
Messenger RNA-based vaccines with dual activity induce balanced TLR-7 dependent adaptive immune responses and provide antitumor activity.
Mariola Fotin-Mleczek, Katharina M Duchardt, +4 authors, Karl-Josef Kallen.
J Immunother, 2010 Dec 15; 34(1). PMID: 21150709
Association between CTLA-4 60G/A and -1661A/G polymorphisms and the risk of cancers: a meta-analysis.
Qing Yan, Pin Chen, +2 authors, Aihua Gu.
PLoS One, 2014 Jan 01; 8(12). PMID: 24376736    Free PMC article.
Immune-checkpoint proteins VISTA and PD-1 nonredundantly regulate murine T-cell responses.
Jun Liu, Ying Yuan, +8 authors, Li Wang.
Proc Natl Acad Sci U S A, 2015 May 13; 112(21). PMID: 25964334    Free PMC article.
Highly Cited.
Combined cellular immunotherapy and chemotherapy improves clinical outcome in patients with gastric carcinoma.
Jiuwei Cui, Lingyu Li, +11 authors, Wei Li.
Cytotherapy, 2015 Apr 22; 17(7). PMID: 25890480
PD-L1 and Survival in Solid Tumors: A Meta-Analysis.
Pin Wu, Dang Wu, +2 authors, Jian Huang.
PLoS One, 2015 Jun 27; 10(6). PMID: 26114883    Free PMC article.
Highly Cited. Systematic Review.
Intraperitoneal injection of in vitro expanded Vγ9Vδ2 T cells together with zoledronate for the treatment of malignant ascites due to gastric cancer.
Ikuo Wada, Hirokazu Matsushita, +6 authors, Kazuhiro Kakimi.
Cancer Med, 2014 Feb 12; 3(2). PMID: 24515916    Free PMC article.
Acute heart failure due to autoimmune myocarditis under pembrolizumab treatment for metastatic melanoma.
Heinz Läubli, Cathrin Balmelli, +3 authors, Alfred Zippelius.
J Immunother Cancer, 2015 Apr 23; 3. PMID: 25901283    Free PMC article.
Highly Cited.
A progress report on the treatment of 157 patients with advanced cancer using lymphokine-activated killer cells and interleukin-2 or high-dose interleukin-2 alone.
S A Rosenberg, M T Lotze, +7 authors, J T Rubin.
N Engl J Med, 1987 Apr 09; 316(15). PMID: 3493432
Highly Cited.
Generation of specific antitumor reactivity by the stimulation of spleen cells from gastric cancer patients with MAGE-3 synthetic peptide.
T Fujie, F Tanaka, +6 authors, T Akiyoshi.
Cancer Immunol Immunother, 1999 Aug 04; 48(4). PMID: 10431688
Helicobacter pylori secreted peptidyl prolyl cis, trans-isomerase drives Th17 inflammation in gastric adenocarcinoma.
Amedeo Amedei, Fabio Munari, +10 authors, Mario Milco D'Elios.
Intern Emerg Med, 2012 Oct 12; 9(3). PMID: 23054412
Circulating myeloid-derived suppressor cells are increased and correlate to immune suppression, inflammation and hypoproteinemia in patients with cancer.
Shinji Ohki, Masahiko Shibata, +8 authors, Seiichi Takenoshita.
Oncol Rep, 2012 May 23; 28(2). PMID: 22614133
Molecular analysis of gastric cancer identifies subtypes associated with distinct clinical outcomes.
Razvan Cristescu, Jeeyun Lee, +31 authors, Amit Aggarwal.
Nat Med, 2015 Apr 22; 21(5). PMID: 25894828
Highly Cited.
Emerging molecular classifications and therapeutic implications for gastric cancer.
Tao Chen, Xiao-Yue Xu, Ping-Hong Zhou.
Chin J Cancer, 2016 May 29; 35. PMID: 27233623    Free PMC article.
Review.
Identification of HLA-A*0201/-A*2402-restricted CTL epitope-peptides derived from a novel cancer/testis antigen, MCAK, and induction of a specific antitumor immune response.
Megumi Kawamoto, Fumiaki Tanaka, +3 authors, Masaki Mori.
Oncol Rep, 2010 Dec 18; 25(2). PMID: 21165574
Immunotherapy in Gastrointestinal Cancers.
Letizia Procaccio, Marta Schirripa, +9 authors, Sara Lonardi.
Biomed Res Int, 2017 Aug 02; 2017. PMID: 28758114    Free PMC article.
Review.
Natural killer cells: role in local tumor growth and metastasis.
Inge Langers, Virginie M Renoux, +2 authors, Nathalie Jacobs.
Biologics, 2012 Apr 26; 6. PMID: 22532775    Free PMC article.
Bone marrow-derived mesenchymal stem cells favor the immunosuppressive T cells skewing in a Helicobacter pylori model of gastric cancer.
Rong Lin, Huan Ma, +4 authors, Xiaohua Hou.
Stem Cells Dev, 2013 Jun 20; 22(21). PMID: 23777268
Efficiency of adjuvant immunochemotherapy following curative resection in patients with locally advanced gastric cancer.
Tadeusz Popiela, Jan Kulig, +2 authors, Marek Zembala.
Gastric Cancer, 2004 Dec 24; 7(4). PMID: 15616772
[Clinical application of adoptive immunotherapy by cytotoxic T lymphocytes induced from tumor-infiltrating lymphocytes].
H Yamaue, H Tanimura, +4 authors, M Tamai.
Nihon Gan Chiryo Gakkai Shi, 1990 May 20; 25(5). PMID: 2391445
Induction of T lymphocytes specific to human gastric cancer using HLA-A matched allogeneic gastric tumor cells.
Yongzhan Nie, Kaichun Wu, +4 authors, Daiming Fan.
J Immunother, 2003 Sep 16; 26(5). PMID: 12973029
Classifying Cancers Based on T-cell Infiltration and PD-L1.
Michele W L Teng, Shin Foong Ngiow, Antoni Ribas, Mark J Smyth.
Cancer Res, 2015 May 16; 75(11). PMID: 25977340    Free PMC article.
Highly Cited. Review.
Lymphocyte-rich gastric cancer: associations with Epstein-Barr virus, microsatellite instability, histology, and survival.
Karen L Grogg, Christine M Lohse, +2 authors, Thomas C Smyrk.
Mod Pathol, 2003 Jul 16; 16(7). PMID: 12861059
Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy.
Janis M Taube, Alison Klein, +7 authors, Robert A Anders.
Clin Cancer Res, 2014 Apr 10; 20(19). PMID: 24714771    Free PMC article.
Highly Cited.
Association between PD-L1 Expression on Tumour-Infiltrating Lymphocytes and Overall Survival in Patients with Gastric Cancer.
Wenfeng Fang, Ying Chen, +7 authors, Li Zhang.
J Cancer, 2017 Aug 05; 8(9). PMID: 28775777    Free PMC article.
Oncology meets immunology: the cancer-immunity cycle.
Daniel S Chen, Ira Mellman.
Immunity, 2013 Jul 31; 39(1). PMID: 23890059
Highly Cited. Review.
Mice that express human interleukin-8 have increased mobilization of immature myeloid cells, which exacerbates inflammation and accelerates colon carcinogenesis.
Samuel Asfaha, Alexander N Dubeykovskiy, +11 authors, Timothy C Wang.
Gastroenterology, 2012 Oct 09; 144(1). PMID: 23041326    Free PMC article.
Helicobacter pylori and gastric cancer: a new paradigm for inflammation-associated epithelial cancers.
JeanMarie Houghton, Timothy C Wang.
Gastroenterology, 2005 May 12; 128(6). PMID: 15887152
Review.
Patterns of PD-L1 expression and CD8 T cell infiltration in gastric adenocarcinomas and associated immune stroma.
Elizabeth D Thompson, Marianna Zahurak, +9 authors, Ronan J Kelly.
Gut, 2016 Jan 24; 66(5). PMID: 26801886    Free PMC article.
Highly Cited.
DC-based cancer vaccines.
Eli Gilboa.
J Clin Invest, 2007 May 04; 117(5). PMID: 17476349    Free PMC article.
Highly Cited. Review.
Efficient induction of specific cytotoxic T lymphocytes against gastric adenocarcinoma by a survivin peptide.
Yi Gang, Xiaoyin Zhang, +4 authors, Daiming Fan.
Biochem Cell Biol, 2012 Sep 21; 90(6). PMID: 22992138
Prognostic value of intratumoral natural killer cells in gastric carcinoma.
S Ishigami, S Natsugoe, +6 authors, T Aikou.
Cancer, 2000 Jan 29; 88(3). PMID: 10649250
Highly Cited.
Programmed Death-Ligand 1 Expression Is Common in Gastric Cancer Associated With Epstein-Barr Virus or Microsatellite Instability.
Changqing Ma, Krishna Patel, +4 authors, Weijing Sun.
Am J Surg Pathol, 2016 Oct 19; 40(11). PMID: 27465786
Highly Cited.
Prognostic role of tumor-infiltrating lymphocytes in gastric cancer: a meta-analysis.
Xiao Zheng, Xing Song, +9 authors, Jingting Jiang.
Oncotarget, 2017 Sep 17; 8(34). PMID: 28915679    Free PMC article.
Treatment of patients with metastatic melanoma with autologous tumor-infiltrating lymphocytes and interleukin 2.
S A Rosenberg, J R Yannelli, +7 authors, D E White.
J Natl Cancer Inst, 1994 Aug 03; 86(15). PMID: 8028037
Highly Cited.
Concepts and mechanisms underlying chemotherapy induced immunogenic cell death: impact on clinical studies and considerations for combined therapies.
Simon Gebremeskel, Brent Johnston.
Oncotarget, 2015 Oct 22; 6(39). PMID: 26486085    Free PMC article.
Review.
Tumor-intrinsic oncogene pathways mediating immune avoidance.
Stefani Spranger, Thomas F Gajewski.
Oncoimmunology, 2016 May 04; 5(3). PMID: 27141343    Free PMC article.
Highly Cited. Review.
ImmunoScore Signature: A Prognostic and Predictive Tool in Gastric Cancer.
Yuming Jiang, Qi Zhang, +12 authors, Xiaolong Qi.
Ann Surg, 2016 Dec 22; 267(3). PMID: 28002059
Highly Cited.
Treatment of advanced gastric cancer by chemotherapy combined with autologous cytokine-induced killer cells.
Jingting Jiang, Ning Xu, +8 authors, Peter Nilsson-Ehle.
Anticancer Res, 2006 Jul 11; 26(3B). PMID: 16821594
CCR7 expression and intratumoral FOXP3+ regulatory T cells are correlated with overall survival and lymph node metastasis in gastric cancer.
Shuang Zhou, Zhenbing Shen, +13 authors, Chunmin Liang.
PLoS One, 2013 Sep 17; 8(9). PMID: 24040244    Free PMC article.
PD-1 Blockade in Tumors with Mismatch-Repair Deficiency.
Dung T Le, Jennifer N Uram, +32 authors, Luis A Diaz.
N Engl J Med, 2015 Jun 02; 372(26). PMID: 26028255    Free PMC article.
Highly Cited.
Molecular classifications of gastric cancers: Novel insights and possible future applications.
Silvio Ken Garattini, Debora Basile, +14 authors, Giuseppe Aprile.
World J Gastrointest Oncol, 2017 Jun 02; 9(5). PMID: 28567184    Free PMC article.
Review.
Prolonged overall survival in gastric cancer patients after adoptive immunotherapy.
Guo-Qing Zhang, Hong Zhao, +8 authors, Shun-Chang Jiao.
World J Gastroenterol, 2015 Mar 12; 21(9). PMID: 25759549    Free PMC article.
Intratumour T cells, their activation status and survival in gastric carcinomas characterised for microsatellite instability and Epstein-Barr virus infection.
Anna Maria Chiaravalli, Maddalena Feltri, +5 authors, Carlo Capella.
Virchows Arch, 2005 Nov 02; 448(3). PMID: 16261379
Decreased intratumoral Foxp3 Tregs and increased dendritic cell density by neoadjuvant chemotherapy associated with favorable prognosis in advanced gastric cancer.
Min Hu, Kai Li, +5 authors, Guifang Yang.
Int J Clin Exp Pathol, 2014 Sep 10; 7(8). PMID: 25197340    Free PMC article.
[Correlation of natural killer cells with the prognosis of gastric adenocarcinoma].
Déborah Rosso, Moacyr P Rigueiro, +4 authors, Laércio G Lourenço.
Arq Bras Cir Dig, 2013 Feb 06; 25(2). PMID: 23381755
Metastasis is regulated via microRNA-200/ZEB1 axis control of tumour cell PD-L1 expression and intratumoral immunosuppression.
Limo Chen, Don L Gibbons, +27 authors, F Xiao-Feng Qin.
Nat Commun, 2014 Oct 29; 5. PMID: 25348003    Free PMC article.
Highly Cited.
Increased circulating myeloid-derived suppressor cells correlate with cancer stages, interleukin-8 and -6 in prostate cancer.
Ning Chi, Zhaohui Tan, +2 authors, Zhizhong Yun.
Int J Clin Exp Med, 2014 Nov 25; 7(10). PMID: 25419348    Free PMC article.
Blocking the immunosuppressive axis with small interfering RNA targeting interleukin (IL)-10 receptor enhances dendritic cell-based vaccine potency.
J H Kim, T H Kang, +7 authors, T W Kim.
Clin Exp Immunol, 2011 May 20; 165(2). PMID: 21592111    Free PMC article.
Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial.
Yung-Jue Bang, Eric Van Cutsem, +14 authors, ToGA Trial Investigators.
Lancet, 2010 Aug 24; 376(9742). PMID: 20728210
Highly Cited.
PD-L1 expression is mainly regulated by interferon gamma associated with JAK-STAT pathway in gastric cancer.
Kousaku Mimura, Jun Liang Teh, +14 authors, Koji Kono.
Cancer Sci, 2017 Oct 17; 109(1). PMID: 29034543    Free PMC article.
Highly Cited.
Cancer immunology.
Olivera J Finn.
N Engl J Med, 2008 Jun 21; 358(25). PMID: 18565863
Highly Cited. Review.
Immunotherapy for gastric cancers: emerging role and future perspectives.
Marta Bonotto, Silvio Ken Garattini, +11 authors, Giuseppe Aprile.
Expert Rev Clin Pharmacol, 2017 Mar 30; 10(6). PMID: 28349740
Review.
Molecular Pathways: Targeting IDO1 and Other Tryptophan Dioxygenases for Cancer Immunotherapy.
Lijie Zhai, Stefani Spranger, +4 authors, Derek A Wainwright.
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