Journal Article
. 2020 Oct; 5(52):.
doi: 10.1126/sciimmunol.aba0759.

Regulatory T cell control of systemic immunity and immunotherapy response in liver metastasis

James C Lee 1 Sadaf Mehdizadeh 2 Jennifer Smith 2 Arabella Young 2 Ilgiz A Mufazalov 2 Cody T Mowery 3 Adil Daud 4 Jeffrey A Bluestone 5 
  • PMID: 33008914
  •     71 References
  •     26 citations


Patients with cancer with liver metastasis demonstrate significantly worse outcomes than those without liver metastasis when treated with anti-PD-1 immunotherapy. The mechanism of liver metastases-induced reduction in systemic antitumor immunity is unclear. Using a dual-tumor immunocompetent mouse model, we found that the immune response to tumor antigen presence within the liver led to the systemic suppression of antitumor immunity. The immune suppression was antigen specific and associated with the coordinated activation of regulatory T cells (Tregs) and modulation of intratumoral CD11b+ monocytes. The dysfunctional immune state could not be reversed by anti-PD-1 monotherapy unless Treg cells were depleted (anti-CTLA-4) or destabilized (EZH2 inhibitor). Thus, this study provides a mechanistic understanding and rationale for adding Treg and CD11b+ monocyte targeting agents in combination with anti-PD-1 to treat patients with cancer with liver metastasis.

Gut microbiome-mediated bile acid metabolism regulates liver cancer via NKT cells.
Chi Ma, Miaojun Han, +20 authors, Tim F Greten.
Science, 2018 May 26; 360(6391). PMID: 29798856    Free PMC article.
Highly Cited.
Defining the emergence of myeloid-derived suppressor cells in breast cancer using single-cell transcriptomics.
Hamad Alshetaiwi, Nicholas Pervolarakis, +10 authors, Kai Kessenbrock.
Sci Immunol, 2020 Feb 23; 5(44). PMID: 32086381    Free PMC article.
Organ-specific response to nivolumab in patients with non-small cell lung cancer (NSCLC).
Sabine Schmid, Stefan Diem, +7 authors, Martin Früh.
Cancer Immunol Immunother, 2018 Sep 02; 67(12). PMID: 30171269
Baseline Tumor Size Is an Independent Prognostic Factor for Overall Survival in Patients with Melanoma Treated with Pembrolizumab.
Richard W Joseph, Jeroen Elassaiss-Schaap, +19 authors, Tara C Gangadhar.
Clin Cancer Res, 2018 Apr 25; 24(20). PMID: 29685882    Free PMC article.
Highly Cited.
Antigen-presenting cell function in the tolerogenic liver environment.
Angus W Thomson, Percy A Knolle.
Nat Rev Immunol, 2010 Oct 26; 10(11). PMID: 20972472
Highly Cited. Review.
Predictive factors for hyperprogressive disease during nivolumab as anti-PD1 treatment in patients with advanced gastric cancer.
Akinori Sasaki, Yoshiaki Nakamura, +10 authors, Kohei Shitara.
Gastric Cancer, 2019 Jan 11; 22(4). PMID: 30627987
Highly Cited.
Integrating single-cell transcriptomic data across different conditions, technologies, and species.
Andrew Butler, Paul Hoffman, +2 authors, Rahul Satija.
Nat Biotechnol, 2018 Apr 03; 36(5). PMID: 29608179    Free PMC article.
Highly Cited.
Presentation of hepatocellular antigens.
Arash Grakoui, Ian Nicholas Crispe.
Cell Mol Immunol, 2016 Mar 01; 13(3). PMID: 26924525    Free PMC article.
DNA of neutrophil extracellular traps promotes cancer metastasis via CCDC25.
Linbin Yang, Qiang Liu, +12 authors, Erwei Song.
Nature, 2020 Jun 13; 583(7814). PMID: 32528174
Tumor-Expressed IDO Recruits and Activates MDSCs in a Treg-Dependent Manner.
Rikke B Holmgaard, Dmitriy Zamarin, +5 authors, Jedd D Wolchok.
Cell Rep, 2015 Sep 29; 13(2). PMID: 26411680    Free PMC article.
Highly Cited.
Cross-talk between tumors at anatomically distinct sites.
Amanda J Oliver, Phillip K Darcy, +2 authors, Clare Y Slaney.
FEBS J, 2020 Apr 06; 288(1). PMID: 32248616
CD83 expression in CD4+ T cells modulates inflammation and autoimmunity.
Simone Reinwald, Carsten Wiethe, +6 authors, Wiebke Hansen.
J Immunol, 2008 Apr 22; 180(9). PMID: 18424708
A natural killer-dendritic cell axis defines checkpoint therapy-responsive tumor microenvironments.
Kevin C Barry, Joy Hsu, +19 authors, Matthew F Krummel.
Nat Med, 2018 Jun 27; 24(8). PMID: 29942093    Free PMC article.
Highly Cited.
The landscape of metastatic progression patterns across major human cancers.
Jan Budczies, Moritz von Winterfeld, +10 authors, Albrecht Stenzinger.
Oncotarget, 2014 Nov 18; 6(1). PMID: 25402435    Free PMC article.
CD83 expression is essential for Treg cell differentiation and stability.
Marina Doebbeler, Christina Koenig, +20 authors, Matthias Lechmann.
JCI Insight, 2018 Jun 08; 3(11). PMID: 29875316    Free PMC article.
Immunity, tolerance and autoimmunity in the liver: A comprehensive review.
Derek G Doherty.
J Autoimmun, 2015 Sep 12; 66. PMID: 26358406
Highly Cited. Review.
Higher frequencies of GARP(+)CTLA-4(+)Foxp3(+) T regulatory cells and myeloid-derived suppressor cells in hepatocellular carcinoma patients are associated with impaired T-cell functionality.
Suresh Kalathil, Amit A Lugade, +2 authors, Yasmin Thanavala.
Cancer Res, 2013 Feb 21; 73(8). PMID: 23423978    Free PMC article.
Highly Cited.
Treg cell-based therapies: challenges and perspectives.
Caroline Raffin, Linda T Vo, Jeffrey A Bluestone.
Nat Rev Immunol, 2019 Dec 08; 20(3). PMID: 31811270    Free PMC article.
Interleukin-5 facilitates lung metastasis by modulating the immune microenvironment.
Rinat Zaynagetdinov, Taylor P Sherrill, +10 authors, Timothy S Blackwell.
Cancer Res, 2015 Feb 19; 75(8). PMID: 25691457    Free PMC article.
Anti-CTLA-4 antibodies of IgG2a isotype enhance antitumor activity through reduction of intratumoral regulatory T cells.
Mark J Selby, John J Engelhardt, +4 authors, Alan J Korman.
Cancer Immunol Res, 2014 Apr 30; 1(1). PMID: 24777248
Highly Cited.
Suppression of a broad spectrum of liver autoimmune pathologies by single peptide-MHC-based nanomedicines.
Channakeshava Sokke Umeshappa, Santiswarup Singha, +7 authors, Pere Santamaria.
Nat Commun, 2019 May 16; 10(1). PMID: 31089130    Free PMC article.
High-Dimensional Analysis Delineates Myeloid and Lymphoid Compartment Remodeling during Successful Immune-Checkpoint Cancer Therapy.
Matthew M Gubin, Ekaterina Esaulova, +16 authors, Maxim N Artyomov.
Cell, 2018 Oct 23; 175(4). PMID: 30343900    Free PMC article.
Highly Cited.
CD4+CD25+ regulatory T cells control CD8+ T-cell effector differentiation by modulating IL-2 homeostasis.
Alice McNally, Geoffrey R Hill, +2 authors, Raymond J Steptoe.
Proc Natl Acad Sci U S A, 2011 Apr 20; 108(18). PMID: 21502514    Free PMC article.
Regulatory T cells in cancer immunotherapy.
Atsushi Tanaka, Shimon Sakaguchi.
Cell Res, 2016 Dec 21; 27(1). PMID: 27995907    Free PMC article.
Highly Cited. Review.
Inducible costimulator (ICOS) is a marker for highly suppressive antigen-specific T cells sharing features of TH17/TH1 and regulatory T cells.
Marc Vocanson, Aurore Rozieres, +8 authors, Jean-François Nicolas.
J Allergy Clin Immunol, 2010 Jul 14; 126(2). PMID: 20624644
Distinct Cellular Mechanisms Underlie Anti-CTLA-4 and Anti-PD-1 Checkpoint Blockade.
Spencer C Wei, Jacob H Levine, +8 authors, James P Allison.
Cell, 2017 Aug 15; 170(6). PMID: 28803728    Free PMC article.
Highly Cited.
Unifying concepts in CD28, ICOS and CTLA4 co-receptor signalling.
Christopher E Rudd, Helga Schneider.
Nat Rev Immunol, 2003 Jul 24; 3(7). PMID: 12876557
Regulatory T cells mediate specific suppression by depleting peptide-MHC class II from dendritic cells.
Billur Akkaya, Yoshihiro Oya, +8 authors, Ethan M Shevach.
Nat Immunol, 2019 Jan 16; 20(2). PMID: 30643268    Free PMC article.
Highly Cited.
Site-specific response patterns, pseudoprogression, and acquired resistance in patients with melanoma treated with ipilimumab combined with anti-PD-1 therapy.
Ines Pires da Silva, Serigne Lo, +4 authors, Alexander M Menzies.
Cancer, 2019 Oct 05; 126(1). PMID: 31584722
Immune tolerance in liver disease.
Ian N Crispe.
Hepatology, 2014 Jun 11; 60(6). PMID: 24913836    Free PMC article.
Highly Cited.
Engagement of the ICOS pathway markedly enhances efficacy of CTLA-4 blockade in cancer immunotherapy.
Xiaozhou Fan, Sergio A Quezada, +2 authors, James P Allison.
J Exp Med, 2014 Apr 02; 211(4). PMID: 24687957    Free PMC article.
Highly Cited.
Magnitude of Therapeutic STING Activation Determines CD8+ T Cell-Mediated Anti-tumor Immunity.
Kelsey E Sivick, Anthony L Desbien, +22 authors, Sarah M McWhirter.
Cell Rep, 2018 Dec 13; 25(11). PMID: 30540940
Highly Cited.
Macrophage-dependent nitric oxide expression regulates tumor cell detachment and metastasis after IL-2/anti-CD40 immunotherapy.
Jonathan M Weiss, Lisa A Ridnour, +8 authors, Robert H Wiltrout.
J Exp Med, 2010 Oct 06; 207(11). PMID: 20921282    Free PMC article.
Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression.
Christoph Hafemeister, Rahul Satija.
Genome Biol, 2019 Dec 25; 20(1). PMID: 31870423    Free PMC article.
Highly Cited.
Liver Metastasis and Treatment Outcome with Anti-PD-1 Monoclonal Antibody in Patients with Melanoma and NSCLC.
Paul C Tumeh, Matthew D Hellmann, +31 authors, Adil Daud.
Cancer Immunol Res, 2017 Apr 16; 5(5). PMID: 28411193    Free PMC article.
Highly Cited.
Hepatic T cells and liver tolerance.
Ian Nicholas Crispe.
Nat Rev Immunol, 2003 Jan 04; 3(1). PMID: 12511875
Highly Cited. Review.
Targets for immunotherapy of liver cancer.
Tim F Greten, Bruno Sangro.
J Hepatol, 2017 Sep 20;. PMID: 28923358    Free PMC article.
GILZ promotes production of peripherally induced Treg cells and mediates the crosstalk between glucocorticoids and TGF-β signaling.
Oxana Bereshchenko, Maddalena Coppo, +7 authors, Carlo Riccardi.
Cell Rep, 2014 Apr 08; 7(2). PMID: 24703841
Liver-Mediated Adaptive Immune Tolerance.
Meijuan Zheng, Zhigang Tian.
Front Immunol, 2019 Dec 04; 10. PMID: 31787967    Free PMC article.
Hepatocytes as Immunological Agents.
Ian N Crispe.
J Immunol, 2015 Dec 20; 196(1). PMID: 26685314    Free PMC article.
Non-conventional Inhibitory CD4+Foxp3-PD-1hi T Cells as a Biomarker of Immune Checkpoint Blockade Activity.
Roberta Zappasodi, Sadna Budhu, +13 authors, Jedd D Wolchok.
Cancer Cell, 2018 Oct 10; 34(4). PMID: 30300585    Free PMC article.
Partially exhausted tumor-infiltrating lymphocytes predict response to combination immunotherapy.
Kimberly Loo, Katy K Tsai, +14 authors, Adil I Daud.
JCI Insight, 2017 Jul 21; 2(14). PMID: 28724802    Free PMC article.
Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice.
Jeong M Kim, Jeffrey P Rasmussen, Alexander Y Rudensky.
Nat Immunol, 2006 Dec 01; 8(2). PMID: 17136045
Highly Cited.
Glucocorticoid receptor in T cells mediates protection from autoimmunity in pregnancy.
Jan Broder Engler, Nina Kursawe, +8 authors, Manuel A Friese.
Proc Natl Acad Sci U S A, 2017 Jan 05; 114(2). PMID: 28049829    Free PMC article.
Regulatory T cell development in the absence of functional Foxp3.
Wen Lin, Dipica Haribhai, +4 authors, Talal A Chatila.
Nat Immunol, 2007 Feb 03; 8(4). PMID: 17273171
Highly Cited.
Establishment of Orthotopic Liver Tumors by Surgical Intrahepatic Tumor Injection in Mice with Underlying Non-Alcoholic Fatty Liver Disease.
Zachary J Brown, Bernd Heinrich, Tim F Greten.
Methods Protoc, 2019 Jun 06; 1(2). PMID: 31164564    Free PMC article.
Is autoimmunity the Achilles' heel of cancer immunotherapy?
Carl H June, Jeremy T Warshauer, Jeffrey A Bluestone.
Nat Med, 2017 May 06; 23(5). PMID: 28475571
Highly Cited.
Sites of metastasis and association with clinical outcome in advanced stage cancer patients treated with immunotherapy.
Mehmet Asim Bilen, Julie M Shabto, +17 authors, R Donald Harvey.
BMC Cancer, 2019 Aug 30; 19(1). PMID: 31464611    Free PMC article.
Five-Year Survival and Correlates Among Patients With Advanced Melanoma, Renal Cell Carcinoma, or Non-Small Cell Lung Cancer Treated With Nivolumab.
Suzanne L Topalian, F Stephen Hodi, +17 authors, Mario Sznol.
JAMA Oncol, 2019 Jul 26; 5(10). PMID: 31343665    Free PMC article.
Highly Cited.
Meta-Analysis Evaluating the Impact of Site of Metastasis on Overall Survival in Men With Castration-Resistant Prostate Cancer.
Susan Halabi, William Kevin Kelly, +22 authors, Eric J Small.
J Clin Oncol, 2016 Mar 10; 34(14). PMID: 26951312    Free PMC article.
Highly Cited.
Nanoparticle-based autoantigen delivery to Treg-inducing liver sinusoidal endothelial cells enables control of autoimmunity in mice.
Antonella Carambia, Barbara Freund, +17 authors, Johannes Herkel.
J Hepatol, 2015 Jan 27; 62(6). PMID: 25617499
T-cell invigoration to tumour burden ratio associated with anti-PD-1 response.
Alexander C Huang, Michael A Postow, +31 authors, E John Wherry.
Nature, 2017 Apr 12; 545(7652). PMID: 28397821    Free PMC article.
Highly Cited.
Comprehensive Integration of Single-Cell Data.
Tim Stuart, Andrew Butler, +7 authors, Rahul Satija.
Cell, 2019 Jun 11; 177(7). PMID: 31178118    Free PMC article.
Highly Cited.
Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
Tyler R Simpson, Fubin Li, +11 authors, Sergio A Quezada.
J Exp Med, 2013 Jul 31; 210(9). PMID: 23897981    Free PMC article.
Highly Cited.
Depletion of myeloid-derived suppressor cells during interleukin-12 immunogene therapy does not confer a survival advantage in experimental malignant glioma.
B Thaci, A U Ahmed, +8 authors, M S Lesniak.
Cancer Gene Ther, 2014 Jan 18; 21(1). PMID: 24434573    Free PMC article.
PD-1+ regulatory T cells amplified by PD-1 blockade promote hyperprogression of cancer.
Takahiro Kamada, Yosuke Togashi, +13 authors, Hiroyoshi Nishikawa.
Proc Natl Acad Sci U S A, 2019 Apr 28; 116(20). PMID: 31028147    Free PMC article.
Highly Cited.
Identification of a CD11b(+)/Gr-1(+)/CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells.
V Bronte, E Apolloni, +5 authors, P Zanovello.
Blood, 2000 Nov 23; 96(12). PMID: 11090068    Free PMC article.
Highly Cited.
Mouse inducible costimulatory molecule (ICOS) expression is enhanced by CD28 costimulation and regulates differentiation of CD4+ T cells.
A J McAdam, T T Chang, +11 authors, G J Freeman.
J Immunol, 2000 Oct 25; 165(9). PMID: 11046032
Highly Cited.
Landscape of Infiltrating T Cells in Liver Cancer Revealed by Single-Cell Sequencing.
Chunhong Zheng, Liangtao Zheng, +13 authors, Zemin Zhang.
Cell, 2017 Jun 18; 169(7). PMID: 28622514
Highly Cited.
Cancer immunotherapy using checkpoint blockade.
Antoni Ribas, Jedd D Wolchok.
Science, 2018 Mar 24; 359(6382). PMID: 29567705    Free PMC article.
Highly Cited. Review.
Cancer Immunotherapy with Immunomodulatory Anti-CD137 and Anti-PD-1 Monoclonal Antibodies Requires BATF3-Dependent Dendritic Cells.
Alfonso R Sánchez-Paulete, Francisco J Cueto, +9 authors, Ignacio Melero.
Cancer Discov, 2015 Oct 24; 6(1). PMID: 26493961    Free PMC article.
Highly Cited.
Modulation of EZH2 expression in T cells improves efficacy of anti-CTLA-4 therapy.
Sangeeta Goswami, Irina Apostolou, +10 authors, Padmanee Sharma.
J Clin Invest, 2018 Jun 16; 128(9). PMID: 29905573    Free PMC article.
CTLA-4-mediated transendocytosis of costimulatory molecules primarily targets migratory dendritic cells.
Vitalijs Ovcinnikovs, Ellen M Ross, +9 authors, Lucy S K Walker.
Sci Immunol, 2019 Jun 04; 4(35). PMID: 31152091    Free PMC article.
Tumor immune profiling predicts response to anti-PD-1 therapy in human melanoma.
Adil I Daud, Kimberly Loo, +15 authors, Michael D Rosenblum.
J Clin Invest, 2016 Aug 16; 126(9). PMID: 27525433    Free PMC article.
Highly Cited.
Rational Selection of Syngeneic Preclinical Tumor Models for Immunotherapeutic Drug Discovery.
Suzanne I S Mosely, John E Prime, +21 authors, Robert W Wilkinson.
Cancer Immunol Res, 2016 Dec 08; 5(1). PMID: 27923825
Highly Cited.
Tumor-infiltrating human CD4+ regulatory T cells display a distinct TCR repertoire and exhibit tumor and neoantigen reactivity.
Mojgan Ahmadzadeh, Anna Pasetto, +4 authors, Steven A Rosenberg.
Sci Immunol, 2019 Jan 13; 4(31). PMID: 30635355    Free PMC article.
Highly Cited.
Modulation of liver tolerance by conventional and nonconventional antigen-presenting cells and regulatory immune cells.
Andrea Kristina Horst, Katrin Neumann, Linda Diehl, Gisa Tiegs.
Cell Mol Immunol, 2016 Apr 05; 13(3). PMID: 27041638    Free PMC article.
Highly Cited. Review.
Regulatory T cells, especially ICOS+ FOXP3+ regulatory T cells, are increased in the hepatocellular carcinoma microenvironment and predict reduced survival.
Jian-Fei Tu, Ya-Hui Ding, +5 authors, Jian-Song Ji.
Sci Rep, 2016 Oct 12; 6. PMID: 27725696    Free PMC article.
Targeting EZH2 Reprograms Intratumoral Regulatory T Cells to Enhance Cancer Immunity.
David Wang, Jason Quiros, +12 authors, Michel DuPage.
Cell Rep, 2018 Jun 14; 23(11). PMID: 29898397    Free PMC article.
Highly Cited.
Regulatory T cells suppress tumor-specific CD8 T cell cytotoxicity through TGF-beta signals in vivo.
Mei-Ling Chen, Mikaël J Pittet, +4 authors, Khashayarsha Khazaie.
Proc Natl Acad Sci U S A, 2004 Dec 30; 102(2). PMID: 15623559    Free PMC article.
Highly Cited.
Coordinated regulation of myeloid cells by tumours.
Dmitry I Gabrilovich, Suzanne Ostrand-Rosenberg, Vincenzo Bronte.
Nat Rev Immunol, 2012 Mar 23; 12(4). PMID: 22437938    Free PMC article.
Highly Cited. Review.
The Immunostimulative Effect and Mechanisms of a Novel Mouse Anti-Human PD-1 Monoclonal Antibody on Jurkat Lymphocytic Cells Cocultured with Hepatoma Cells.
Ziwei Li, Bin Li, +8 authors, Jianhong Chen.
Onco Targets Ther, 2020 Dec 05; 13. PMID: 33273828    Free PMC article.
Pingyangmycin enhances the antitumor efficacy of anti-PD-1 therapy associated with tumor-infiltrating CD8+ T cell augmentation.
Chuan-Kun Shan, Yi-Bo Du, +6 authors, Yong-Su Zhen.
Cancer Chemother Pharmacol, 2021 Jan 04; 87(3). PMID: 33388950
Liver metastasis restrains immunotherapy efficacy via macrophage-mediated T cell elimination.
Jiali Yu, Michael D Green, +37 authors, Weiping Zou.
Nat Med, 2021 Jan 06; 27(1). PMID: 33398162    Free PMC article.
Changes in the Peripheral Blood Treg Cell Proportion in Hepatocellular Carcinoma Patients After Transarterial Chemoembolization With Microparticles.
Zhizhong Ren, Yuanxun Yue, +8 authors, Tianxiao Wang.
Front Immunol, 2021 Mar 16; 12. PMID: 33717135    Free PMC article.
Immune Milieu Established by Postpartum Liver Involution Promotes Breast Cancer Liver Metastasis.
Alexandra Q Bartlett, Nathan D Pennock, Alex Klug, Pepper Schedin.
Cancers (Basel), 2021 May 01; 13(7). PMID: 33916683    Free PMC article.
XYZeq: Spatially resolved single-cell RNA sequencing reveals expression heterogeneity in the tumor microenvironment.
Youjin Lee, Derek Bogdanoff, +16 authors, Chun Jimmie Ye.
Sci Adv, 2021 Apr 23; 7(17). PMID: 33883145    Free PMC article.
Immune Responses against Disseminated Tumor Cells.
Ling Peng, Yongchang Zhang, Zibing Wang.
Cancers (Basel), 2021 Jun 03; 13(11). PMID: 34063848    Free PMC article.
Serum Amyloid A Proteins and Their Impact on Metastasis and Immune Biology in Cancer.
Jesse Lee, Gregory L Beatty.
Cancers (Basel), 2021 Jul 03; 13(13). PMID: 34202272    Free PMC article.
Pan-Cancer Analysis Identifies Liver Metastases as Negative Predictive Factor for Immune Checkpoint Inhibitors Treatment Outcome.
Xiao-Juan Chen, Aiqun Ren, +2 authors, Tao Jiang.
Front Immunol, 2021 Jul 13; 12. PMID: 34248939    Free PMC article.
Clinical Response to Immunotherapy Targeting Programmed Cell Death Receptor 1/Programmed Cell Death Ligand 1 in Patients With Treatment-Resistant Microsatellite Stable Colorectal Cancer With and Without Liver Metastases.
Chongkai Wang, Jaideep Sandhu, +3 authors, Marwan Fakih.
JAMA Netw Open, 2021 Aug 10; 4(8). PMID: 34369992    Free PMC article.
Toward personalized treatment approaches for non-small-cell lung cancer.
Meina Wang, Roy S Herbst, Chris Boshoff.
Nat Med, 2021 Aug 14; 27(8). PMID: 34385702
Mechanisms of regulatory T cell infiltration in tumors: implications for innovative immune precision therapies.
Hiroyoshi Nishikawa, Shohei Koyama.
J Immunother Cancer, 2021 Aug 01; 9(7). PMID: 34330764    Free PMC article.
Liver metastases "siphon" off immunotherapy response.
Nina Cortese, Federica Marchesi.
Hepatobiliary Surg Nutr, 2021 Aug 26; 10(4). PMID: 34430535    Free PMC article.
Society for Immunotherapy of Cancer (SITC) clinical practice guideline on immunotherapy for the treatment of breast cancer.
Leisha A Emens, Sylvia Adams, +14 authors, Jennifer K Litton.
J Immunother Cancer, 2021 Aug 15; 9(8). PMID: 34389617    Free PMC article.
Glucocorticoid and PD-1 Cross-Talk: Does the Immune System Become Confused?
Sabrina Adorisio, Lorenza Cannarile, Domenico V Delfino, Emira Ayroldi.
Cells, 2021 Sep 29; 10(9). PMID: 34571982    Free PMC article.
Combination Immunotherapies to Overcome Intrinsic Resistance to Checkpoint Blockade in Microsatellite Stable Colorectal Cancer.
Chang Woo Kim, Hong Jae Chon, Chan Kim.
Cancers (Basel), 2021 Oct 14; 13(19). PMID: 34638390    Free PMC article.
Regulatory T-Cell Therapy in Liver Transplantation and Chronic Liver Disease.
Angus Hann, Ye H Oo, M Thamara P R Perera.
Front Immunol, 2021 Nov 02; 12. PMID: 34721383    Free PMC article.
Uveal Melanoma Metastasis.
Ernesto Rossi, Michela Croce, +6 authors, Adriana Amaro.
Cancers (Basel), 2021 Nov 28; 13(22). PMID: 34830841    Free PMC article.
Tissue-specific Tregs in cancer metastasis: opportunities for precision immunotherapy.
Laura A Huppert, Michael D Green, +4 authors, James C Lee.
Cell Mol Immunol, 2021 Aug 22; 19(1). PMID: 34417572    Free PMC article.
Factors Determining Long-Term Antitumor Responses to Immune Checkpoint Blockade Therapy in Melanoma.
Kimberly Loo, James W Smithy, Michael A Postow, Allison Betof Warner.
Front Immunol, 2022 Jan 29; 12. PMID: 35087529    Free PMC article.
Immune cell profiles of metastatic HER2-positive breast cancer patients according to the sites of metastasis.
Tiia J Honkanen, Milla E K Luukkainen, +4 authors, Jussi P Koivunen.
Breast Cancer Res Treat, 2021 Nov 25; 191(2). PMID: 34817749    Free PMC article.
Angiogenic and molecular diversity determine hepatic melanoma metastasis and response to anti-angiogenic treatment.
Sebastian A Wohlfeil, Verena Häfele, +11 authors, Cyrill Géraud.
J Transl Med, 2022 Feb 04; 20(1). PMID: 35109875    Free PMC article.
The Liver-Immunity Nexus and Cancer Immunotherapy.
James C Lee, Michael D Green, +3 authors, Adil I Daud.
Clin Cancer Res, 2021 Jul 22; 28(1). PMID: 34285059    Free PMC article.
Fusobacterium nucleatum promotes liver metastasis in colorectal cancer by regulating the hepatic immune niche and altering gut microbiota.
Han Yin, Zhuangzhuang Miao, +6 authors, Xianglin Yuan.
Aging (Albany NY), 2022 Feb 26; 14(4). PMID: 35212644    Free PMC article.
Visual Analysis of Colorectal Cancer Immunotherapy: A Bibliometric Analysis From 2012 to 2021.
Long Ma, Jixiang Ma, Muzhou Teng, Yumin Li.
Front Immunol, 2022 Apr 19; 13. PMID: 35432385    Free PMC article.
Biomarkers of Response and Resistance to Immunotherapy in Microsatellite Stable Colorectal Cancer: Toward a New Personalized Medicine.
Nicolas Huyghe, Elena Benidovskaya, Philippe Stevens, Marc Van den Eynde.
Cancers (Basel), 2022 May 15; 14(9). PMID: 35565369    Free PMC article.