Review
. 2017 Jul; 17:68.
doi: 10.1186/s12935-017-0437-3.

Chemotherapy and tumor microenvironment of pancreatic cancer

Qiaofei Liu 1 Quan Liao 1 Yupei Zhao 1 
Affiliations
  • PMID: 28694739
  •     216 References
  •     41 citations

Abstract

Pancreatic cancer is an extremely dismal malignance. Chemotherapy has been widely applied to treat this intractable tumor. It has exclusive tumor microenvironment (TME), characterized by dense desmoplasia and profound infiltrations of immunosuppressive cells. Interactions between stromal cells and cancer cells play vital roles to affect the biological behaviors of pancreatic cancer. Targeting the stromal components of pancreatic cancer has shown promising results. In addition to the direct toxic effects of chemotherapeutic drugs on cancer cells, they can also remodel the TME, eventually affecting their efficacy. Herein, we reviewed the following four aspects; (1) clinical landmark advances of chemotherapy in pancreatic cancer, since 2000; (2) interactions and mechanisms between stromal cells and pancreatic cancer cells; (3) remodeling effects and mechanisms of chemotherapy on TME; (4) targeting stromal components in pancreatic cancer.

Keywords: Cancer associated fibroblasts; Chemotherapy; Myeloid derived suppressor cells; Pancreatic cancer; Pancreatic stellate cells; Tumor associated macrophages; Tumor microenvironment.

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J Exp Med, 2006 Nov 15; 203(12). PMID: 17101732    Free PMC article.
Highly Cited.
Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival.
Berna C Özdemir, Tsvetelina Pentcheva-Hoang, +18 authors, Raghu Kalluri.
Cancer Cell, 2014 May 27; 25(6). PMID: 24856586    Free PMC article.
Highly Cited.
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John A Hamilton, Adrian Achuthan.
Trends Immunol, 2012 Sep 25; 34(2). PMID: 23000011
Highly Cited. Review.
IL-6-stimulated CD11b+ CD14+ HLA-DR- myeloid-derived suppressor cells, are associated with progression and poor prognosis in squamous cell carcinoma of the esophagus.
Miao-Fen Chen, Feng-Che Kuan, +5 authors, Kuan-Der Lee.
Oncotarget, 2014 Sep 23; 5(18). PMID: 25238263    Free PMC article.
Targeted depletion of an MDSC subset unmasks pancreatic ductal adenocarcinoma to adaptive immunity.
Ingunn M Stromnes, J Scott Brockenbrough, +5 authors, Sunil R Hingorani.
Gut, 2014 Feb 22; 63(11). PMID: 24555999    Free PMC article.
Highly Cited.
Myeloid-derived suppressor cells contribute to A2B adenosine receptor-induced VEGF production and angiogenesis in a mouse melanoma model.
Claudia Sorrentino, Lucio Miele, +2 authors, Silvana Morello.
Oncotarget, 2015 Sep 01; 6(29). PMID: 26317647    Free PMC article.
Myxomaviral Anti-Inflammatory Serpin Reduces Myeloid-Derived Suppressor Cells and Human Pancreatic Cancer Cell Growth in Mice.
Donghang Zheng, Hao Chen, +5 authors, Alexandra R Lucas.
J Cancer Sci Ther, 2013 Aug 19; 5. PMID: 25798214    Free PMC article.
Contribution of microRNAs in understanding the pancreatic tumor microenvironment involving cancer associated stellate and fibroblast cells.
Shadan Ali, Raagini Suresh, +6 authors, Fazlul H Sarkar.
Am J Cancer Res, 2015 Jun 06; 5(3). PMID: 26046003    Free PMC article.
Adjuvant chemotherapy with fluorouracil plus folinic acid vs gemcitabine following pancreatic cancer resection: a randomized controlled trial.
John P Neoptolemos, Deborah D Stocken, +25 authors, European Study Group for Pancreatic Cancer.
JAMA, 2010 Sep 09; 304(10). PMID: 20823433
Highly Cited.
Hypoxia promotes glioma-associated macrophage infiltration via periostin and subsequent M2 polarization by upregulating TGF-beta and M-CSFR.
Xiaofan Guo, Hao Xue, +11 authors, Gang Li.
Oncotarget, 2016 Sep 08; 7(49). PMID: 27602954    Free PMC article.
G-CSF-initiated myeloid cell mobilization and angiogenesis mediate tumor refractoriness to anti-VEGF therapy in mouse models.
Farbod Shojaei, Xiumin Wu, +5 authors, Napoleone Ferrara.
Proc Natl Acad Sci U S A, 2009 Apr 07; 106(16). PMID: 19346489    Free PMC article.
Highly Cited.
Bv8 regulates myeloid-cell-dependent tumour angiogenesis.
Farbod Shojaei, Xiumin Wu, +13 authors, Napoleone Ferrara.
Nature, 2007 Dec 08; 450(7171). PMID: 18064003
Highly Cited.
Fibroblast activation protein-α-expressing fibroblasts promote the progression of pancreatic ductal adenocarcinoma.
Tomoya Kawase, Yumiko Yasui, +8 authors, Keisuke Hino.
BMC Gastroenterol, 2015 Sep 04; 15. PMID: 26330349    Free PMC article.
Subsets of myeloid-derived suppressor cells in tumor-bearing mice.
Je-In Youn, Srinivas Nagaraj, Michelle Collazo, Dmitry I Gabrilovich.
J Immunol, 2008 Oct 04; 181(8). PMID: 18832739    Free PMC article.
Highly Cited.
Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription factor.
Ilaria Marigo, Erika Bosio, +13 authors, Vincenzo Bronte.
Immunity, 2010 Jul 08; 32(6). PMID: 20605485
Highly Cited.
Kindlin-2 in pancreatic stellate cells promotes the progression of pancreatic cancer.
Naoki Yoshida, Atsushi Masamune, +5 authors, Tooru Shimosegawa.
Cancer Lett, 2017 Jan 18; 390. PMID: 28093281
Fate mapping analysis reveals that adult microglia derive from primitive macrophages.
Florent Ginhoux, Melanie Greter, +9 authors, Miriam Merad.
Science, 2010 Oct 23; 330(6005). PMID: 20966214    Free PMC article.
Highly Cited.
Granulocytic myeloid-derived suppressor cells maintain feto-maternal tolerance by inducing Foxp3 expression in CD4+CD25-T cells by activation of the TGF-β/β-catenin pathway.
Xiaomin Kang, Xiaoxin Zhang, +4 authors, Aimin Zhao.
Mol Hum Reprod, 2016 Mar 27; 22(7). PMID: 27016139
Pancreatic stellate cells promote hapto-migration of cancer cells through collagen I-mediated signalling pathway.
J Lu, S Zhou, +3 authors, M G Bachem.
Br J Cancer, 2013 Nov 10; 110(2). PMID: 24201748    Free PMC article.
Pancreatic stellate cells increase the invasion of human pancreatic cancer cells through the stromal cell-derived factor-1/CXCR4 axis.
Zhenjun Gao, Xingpeng Wang, +2 authors, Guoyong Hu.
Pancreatology, 2010 May 21; 10(2-3). PMID: 20484957
Immunogenic cell death in cancer therapy.
Guido Kroemer, Lorenzo Galluzzi, Oliver Kepp, Laurence Zitvogel.
Annu Rev Immunol, 2012 Nov 20; 31. PMID: 23157435
Highly Cited. Review.
Macrophage activation and polarization: nomenclature and experimental guidelines.
Peter J Murray, Judith E Allen, +22 authors, Thomas A Wynn.
Immunity, 2014 Jul 19; 41(1). PMID: 25035950    Free PMC article.
Highly Cited.
Tumor-induced STAT3 activation in monocytic myeloid-derived suppressor cells enhances stemness and mesenchymal properties in human pancreatic cancer.
Roheena Z Panni, Dominic E Sanford, +9 authors, David C Linehan.
Cancer Immunol Immunother, 2014 Mar 22; 63(5). PMID: 24652403    Free PMC article.
Highly Cited.
Macrophage delivery of an oncolytic virus abolishes tumor regrowth and metastasis after chemotherapy or irradiation.
Munitta Muthana, Samuel Rodrigues, +6 authors, Claire E Lewis.
Cancer Res, 2012 Nov 23; 73(2). PMID: 23172310
Macrophage-secreted granulin supports pancreatic cancer metastasis by inducing liver fibrosis.
Sebastian R Nielsen, Valeria Quaranta, +15 authors, Michael C Schmid.
Nat Cell Biol, 2016 Apr 19; 18(5). PMID: 27088855    Free PMC article.
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Pancreatic stellate cells radioprotect pancreatic cancer cells through β1-integrin signaling.
Tine S Mantoni, Serena Lunardi, +2 authors, Thomas B Brunner.
Cancer Res, 2011 May 12; 71(10). PMID: 21558392    Free PMC article.
Sorafenib perpetuates cellular anticancer effector functions by modulating the crosstalk between macrophages and natural killer cells.
Martin Franz Sprinzl, Florian Reisinger, +11 authors, Ulrike Protzer.
Hepatology, 2013 Feb 21; 57(6). PMID: 23424039
Paracrine IL-6 signaling mediates the effects of pancreatic stellate cells on epithelial-mesenchymal transition via Stat3/Nrf2 pathway in pancreatic cancer cells.
Yuan Seng Wu, Ivy Chung, +3 authors, Chung Yeng Looi.
Biochim Biophys Acta Gen Subj, 2016 Oct 18; 1861(2). PMID: 27750041
Critical role of Trib1 in differentiation of tissue-resident M2-like macrophages.
Takashi Satoh, Hiroyasu Kidoya, +8 authors, Shizuo Akira.
Nature, 2013 Mar 22; 495(7442). PMID: 23515163
Highly Cited.
The cellular and molecular origin of tumor-associated macrophages.
Ruth A Franklin, Will Liao, +5 authors, Ming O Li.
Science, 2014 May 09; 344(6186). PMID: 24812208    Free PMC article.
Highly Cited.
Adjuvant chemotherapy with gemcitabine and long-term outcomes among patients with resected pancreatic cancer: the CONKO-001 randomized trial.
Helmut Oettle, Peter Neuhaus, +10 authors, Hanno Riess.
JAMA, 2013 Oct 10; 310(14). PMID: 24104372
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IL-4-induced arginase 1 suppresses alloreactive T cells in tumor-bearing mice.
Vincenzo Bronte, Paolo Serafini, +9 authors, Paola Zanovello.
J Immunol, 2002 Dec 24; 170(1). PMID: 12496409
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Epidemiology, risk factors, and the promotion of pancreatic cancer: role of the stellate cell.
Stephen Pandol, Anna Gukovskaya, +4 authors, Aurelia Lugea.
J Gastroenterol Hepatol, 2012 Feb 15; 27 Suppl 2. PMID: 22320930    Free PMC article.
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Lactic acid polarizes macrophages to a tumor-promoting state.
Oscar R Colegio.
Oncoimmunology, 2016 May 04; 5(3). PMID: 27141329    Free PMC article.
PF-03732010: a fully human monoclonal antibody against P-cadherin with antitumor and antimetastatic activity.
Cathy C Zhang, Zhengming Yan, +15 authors, Todd VanArsdale.
Clin Cancer Res, 2010 Sep 11; 16(21). PMID: 20829331
Macrophages mediate gemcitabine resistance of pancreatic adenocarcinoma by upregulating cytidine deaminase.
N Weizman, Y Krelin, +4 authors, Z Gil.
Oncogene, 2013 Sep 03; 33(29). PMID: 23995783
Highly Cited.
The anti-fibrotic agent pirfenidone synergizes with cisplatin in killing tumor cells and cancer-associated fibroblasts.
Melanie Mediavilla-Varela, Kingsley Boateng, David Noyes, Scott J Antonia.
BMC Cancer, 2016 Mar 05; 16. PMID: 26935219    Free PMC article.
Macrophage scavenger receptor a promotes tumor progression in murine models of ovarian and pancreatic cancer.
Claudine Neyen, Annette Plüddemann, +4 authors, Thorsten Hagemann.
J Immunol, 2013 Mar 01; 190(7). PMID: 23447685    Free PMC article.
Podoplanin-expressing cancer-associated fibroblasts inhibit small cell lung cancer growth.
Akiko Takahashi, Genichiro Ishii, +13 authors, Atsushi Ochiai.
Oncotarget, 2015 Apr 25; 6(11). PMID: 25909164    Free PMC article.
Hypoxia induces macrophage polarization and re-education toward an M2 phenotype in U87 and U251 glioblastoma models.
Marine M Leblond, Aurélie N Gérault, +4 authors, Samuel Valable.
Oncoimmunology, 2016 Mar 05; 5(1). PMID: 26942063    Free PMC article.
Targeting CXCL12 from FAP-expressing carcinoma-associated fibroblasts synergizes with anti-PD-L1 immunotherapy in pancreatic cancer.
Christine Feig, James O Jones, +12 authors, Douglas T Fearon.
Proc Natl Acad Sci U S A, 2013 Nov 28; 110(50). PMID: 24277834    Free PMC article.
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Gemcitabine plus bevacizumab compared with gemcitabine plus placebo in patients with advanced pancreatic cancer: phase III trial of the Cancer and Leukemia Group B (CALGB 80303).
Hedy Lee Kindler, Donna Niedzwiecki, +12 authors, Richard M Goldberg.
J Clin Oncol, 2010 Jul 08; 28(22). PMID: 20606091    Free PMC article.
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Tumor-associated macrophages regulate murine breast cancer stem cells through a novel paracrine EGFR/Stat3/Sox-2 signaling pathway.
Jian Yang, Debbie Liao, +6 authors, Yunping Luo.
Stem Cells, 2012 Nov 22; 31(2). PMID: 23169551
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Radiation promotes epithelial-to-mesenchymal transition and invasion of pancreatic cancer cell by activating carcinoma-associated fibroblasts.
Doudou Li, Chao Qu, +6 authors, Zhiqiang Meng.
Am J Cancer Res, 2016 Nov 09; 6(10). PMID: 27822411    Free PMC article.
Activated pancreatic stellate cells sequester CD8+ T cells to reduce their infiltration of the juxtatumoral compartment of pancreatic ductal adenocarcinoma.
Abasi Ene-Obong, Andrew J Clear, +9 authors, Hemant M Kocher.
Gastroenterology, 2013 Jul 31; 145(5). PMID: 23891972    Free PMC article.
Highly Cited.
Acinar cell-specific knockout of the PTHrP gene decreases the proinflammatory and profibrotic responses in pancreatitis.
Vandanajay Bhatia, Cristiana Rastellini, +3 authors, Miriam Falzon.
Am J Physiol Gastrointest Liver Physiol, 2014 Jul 19; 307(5). PMID: 25035110    Free PMC article.
Chemotherapy alters monocyte differentiation to favor generation of cancer-supporting M2 macrophages in the tumor microenvironment.
Eveline M Dijkgraaf, Moniek Heusinkveld, +7 authors, Sjoerd H van der Burg.
Cancer Res, 2013 Feb 26; 73(8). PMID: 23436796
Highly Cited.
Retinoic acid inhibits pancreatic cancer cell migration and EMT through the downregulation of IL-6 in cancer associated fibroblast cells.
Jian Guan, Hui Zhang, +7 authors, Jie Chen.
Cancer Lett, 2013 Dec 18; 345(1). PMID: 24334138
Polarization of Monocytic Myeloid-Derived Suppressor Cells by Hepatitis B Surface Antigen Is Mediated via ERK/IL-6/STAT3 Signaling Feedback and Restrains the Activation of T Cells in Chronic Hepatitis B Virus Infection.
Zhong Fang, Jin Li, +10 authors, Zhenghong Yuan.
J Immunol, 2015 Sep 30; 195(10). PMID: 26416274
Nanoliposomal irinotecan with fluorouracil and folinic acid in metastatic pancreatic cancer after previous gemcitabine-based therapy (NAPOLI-1): a global, randomised, open-label, phase 3 trial.
Andrea Wang-Gillam, Chung-Pin Li, +19 authors, NAPOLI-1 Study Group.
Lancet, 2015 Nov 30; 387(10018). PMID: 26615328
Highly Cited.
Comparison of gemcitabine versus the matrix metalloproteinase inhibitor BAY 12-9566 in patients with advanced or metastatic adenocarcinoma of the pancreas: a phase III trial of the National Cancer Institute of Canada Clinical Trials Group.
M J Moore, J Hamm, +12 authors, National Cancer Institute of Canada Clinical Trials Group.
J Clin Oncol, 2003 Aug 30; 21(17). PMID: 12947065
Tumor-targeted interferon-alpha delivery by Tie2-expressing monocytes inhibits tumor growth and metastasis.
Michele De Palma, Roberta Mazzieri, +11 authors, Luigi Naldini.
Cancer Cell, 2008 Oct 07; 14(4). PMID: 18835032
Role of macrophage targeting in the antitumor activity of trabectedin.
Giovanni Germano, Roberta Frapolli, +21 authors, Paola Allavena.
Cancer Cell, 2013 Feb 16; 23(2). PMID: 23410977
Highly Cited.
Axitinib plus gemcitabine versus placebo plus gemcitabine in patients with advanced pancreatic adenocarcinoma: a double-blind randomised phase 3 study.
Hedy L Kindler, Tatsuya Ioka, +14 authors, Eric Van Cutsem.
Lancet Oncol, 2011 Feb 11; 12(3). PMID: 21306953
Highly Cited.
Direct and differential suppression of myeloid-derived suppressor cell subsets by sunitinib is compartmentally constrained.
Jennifer S Ko, Patricia Rayman, +6 authors, Peter A Cohen.
Cancer Res, 2010 Apr 22; 70(9). PMID: 20406969    Free PMC article.
Highly Cited.
Regulation of tumor metastasis by myeloid-derived suppressor cells.
Thomas Condamine, Indu Ramachandran, Je-In Youn, Dmitry I Gabrilovich.
Annu Rev Med, 2014 Oct 24; 66. PMID: 25341012    Free PMC article.
Highly Cited. Review.
Anti-metastatic potential of somatostatin analog SOM230: Indirect pharmacological targeting of pancreatic cancer-associated fibroblasts.
Siham Moatassim-Billah, Camille Duluc, +11 authors, Corinne Bousquet.
Oncotarget, 2016 May 14; 7(27). PMID: 27177087    Free PMC article.
Reversion of immune tolerance in advanced malignancy: modulation of myeloid-derived suppressor cell development by blockade of stem-cell factor function.
Ping-Ying Pan, George X Wang, +4 authors, Shu-Hsia Chen.
Blood, 2007 Sep 22; 111(1). PMID: 17885078    Free PMC article.
Highly Cited.
Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer.
Kenneth P Olive, Michael A Jacobetz, +34 authors, David A Tuveson.
Science, 2009 May 23; 324(5933). PMID: 19460966    Free PMC article.
Highly Cited.
Hypoxia stimulates pancreatic stellate cells to induce fibrosis and angiogenesis in pancreatic cancer.
Atsushi Masamune, Kazuhiro Kikuta, +3 authors, Tooru Shimosegawa.
Am J Physiol Gastrointest Liver Physiol, 2008 Aug 02; 295(4). PMID: 18669622
Myeloid-derived suppressor cells (MDSC) facilitate distant metastasis of malignancies by shielding circulating tumor cells (CTC) from immune surveillance.
Qiaofei Liu, Quan Liao, Yupei Zhao.
Med Hypotheses, 2016 Jan 31; 87. PMID: 26826638
Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function.
Thomas Condamine, Dmitry I Gabrilovich.
Trends Immunol, 2010 Nov 12; 32(1). PMID: 21067974    Free PMC article.
Highly Cited. Review.
Comprehensive analysis of matrix metalloproteinase and tissue inhibitor expression in pancreatic cancer: increased expression of matrix metalloproteinase-7 predicts poor survival.
Lucie E Jones, Michelle J Humphreys, +2 authors, Mark T Boyd.
Clin Cancer Res, 2004 Apr 23; 10(8). PMID: 15102692
Human pancreatic stellate cells modulate 3D collagen alignment to promote the migration of pancreatic ductal adenocarcinoma cells.
Cole R Drifka, Agnes G Loeffler, +3 authors, W John Kao.
Biomed Microdevices, 2016 Nov 08; 18(6). PMID: 27819128
Podoplanin-positive fibroblasts enhance lung adenocarcinoma tumor formation: podoplanin in fibroblast functions for tumor progression.
Ayuko Hoshino, Genichiro Ishii, +5 authors, Atsushi Ochiai.
Cancer Res, 2011 May 26; 71(14). PMID: 21610106
Adjuvant chemotherapy of S-1 versus gemcitabine for resected pancreatic cancer: a phase 3, open-label, randomised, non-inferiority trial (JASPAC 01).
Katsuhiko Uesaka, Narikazu Boku, +18 authors, JASPAC 01 Study Group.
Lancet, 2016 Jun 07; 388(10041). PMID: 27265347
Highly Cited.
The influence of myeloid-derived suppressor cells on angiogenesis and tumor growth after cancer surgery.
Jun Wang, Xiaosan Su, +8 authors, Zhipeng Hong.
Int J Cancer, 2016 Jan 13; 138(11). PMID: 26756887
Myeloid-derived suppressor cells enhance stemness of cancer cells by inducing microRNA101 and suppressing the corepressor CtBP2.
Tracy X Cui, Ilona Kryczek, +14 authors, Weiping Zou.
Immunity, 2013 Sep 10; 39(3). PMID: 24012420    Free PMC article.
Highly Cited.
Tumor-associated macrophages exhibit pro- and anti-inflammatory properties by which they impact on pancreatic tumorigenesis.
Ole Helm, Janka Held-Feindt, +10 authors, Susanne Sebens.
Int J Cancer, 2014 Jan 25; 135(4). PMID: 24458546
Highly Cited.
STAT3 regulates arginase-I in myeloid-derived suppressor cells from cancer patients.
David Vasquez-Dunddel, Fan Pan, +9 authors, Young Kim.
J Clin Invest, 2013 Mar 05; 123(4). PMID: 23454751    Free PMC article.
Highly Cited.
B cells regulate macrophage phenotype and response to chemotherapy in squamous carcinomas.
Nesrine I Affara, Brian Ruffell, +13 authors, Lisa M Coussens.
Cancer Cell, 2014 Jun 10; 25(6). PMID: 24909985    Free PMC article.
Highly Cited.
Pancreatic cancer-associated stellate cells: A viable target for reducing immunosuppression in the tumor microenvironment.
Thomas A Mace, Mark Bloomston, Gregory B Lesinski.
Oncoimmunology, 2013 Sep 28; 2(7). PMID: 24073373    Free PMC article.
Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis.
Li Yang, Jianhua Huang, +8 authors, Harold L Moses.
Cancer Cell, 2008 Jan 03; 13(1). PMID: 18167337    Free PMC article.
Highly Cited.
Pancreatic adenocarcinoma induces bone marrow mobilization of myeloid-derived suppressor cells which promote primary tumor growth.
Matthew R Porembka, Jonathan B Mitchem, +6 authors, Peter Goedegebuure.
Cancer Immunol Immunother, 2012 Jan 05; 61(9). PMID: 22215137    Free PMC article.
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Cancer Stem Cells and Macrophages: Implications in Tumor Biology and Therapeutic Strategies.
Bruno Sainz, Emily Carron, Mireia Vallespinós, Heather L Machado.
Mediators Inflamm, 2016 Mar 17; 2016. PMID: 26980947    Free PMC article.
Review.
The interaction of anticancer therapies with tumor-associated macrophages.
Alberto Mantovani, Paola Allavena.
J Exp Med, 2015 Mar 11; 212(4). PMID: 25753580    Free PMC article.
Highly Cited. Review.
Activation of tumor-promoting type 2 macrophages by EGFR-targeting antibody cetuximab.
Jan Pander, Moniek Heusinkveld, +7 authors, Thorbald van Hall.
Clin Cancer Res, 2011 Jul 27; 17(17). PMID: 21788356
Murine pancreatic adenocarcinoma dampens SHIP-1 expression and alters MDSC homeostasis and function.
Shari Pilon-Thomas, Nadine Nelson, +4 authors, Tomar Ghansah.
PLoS One, 2011 Dec 02; 6(11). PMID: 22132131    Free PMC article.
Cancer treatment and survivorship statistics, 2016.
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CA Cancer J Clin, 2016 Jun 03; 66(4). PMID: 27253694
Highly Cited.
Dynamic mast cell-stromal cell interactions promote growth of pancreatic cancer.
Ying Ma, Rosa F Hwang, Craig D Logsdon, Stephen E Ullrich.
Cancer Res, 2013 May 02; 73(13). PMID: 23633481    Free PMC article.
Macrophage polarization in pancreatic carcinoma: role of heparanase enzyme.
Esther Hermano, Amichay Meirovitz, +4 authors, Michael Elkin.
J Natl Cancer Inst, 2014 Oct 19; 106(12). PMID: 25326645    Free PMC article.
Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells.
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Cancer Cell, 2011 Apr 13; 19(4). PMID: 21481792
Highly Cited.
Increase in frequency of myeloid-derived suppressor cells in mice with spontaneous pancreatic carcinoma.
Fei Zhao, Sonja Obermann, +4 authors, Tim F Greten.
Immunology, 2009 Aug 20; 128(1). PMID: 19689743    Free PMC article.
The role of the hepatocyte growth factor/c-MET pathway in pancreatic stellate cell-endothelial cell interactions: antiangiogenic implications in pancreatic cancer.
Mishaal B Patel, Srinivasa P Pothula, +5 authors, Jeremy S Wilson.
Carcinogenesis, 2014 May 31; 35(8). PMID: 24876152
High expression of Galectin-1 in pancreatic stellate cells plays a role in the development and maintenance of an immunosuppressive microenvironment in pancreatic cancer.
Dong Tang, Zhongxu Yuan, +9 authors, Kuirong Jiang.
Int J Cancer, 2011 Jul 23; 130(10). PMID: 21780106
Endoneurial macrophages induce perineural invasion of pancreatic cancer cells by secretion of GDNF and activation of RET tyrosine kinase receptor.
Oren Cavel, Olga Shomron, +8 authors, Ziv Gil.
Cancer Res, 2012 Sep 14; 72(22). PMID: 22971345
A STUDY OF THE LEUKEMOID RESPONSE TO TRANSPLANTABLE A-280 TUMOR IN MICE.
E J LAPPAT, M CAWEIN.
Cancer Res, 1964 Feb 01; 24. PMID: 14115699
High-throughput live-cell imaging reveals differential inhibition of tumor cell proliferation by human fibroblasts.
Emilie Flaberg, Laszlo Markasz, +11 authors, Laszlo Szekely.
Int J Cancer, 2010 Aug 18; 128(12). PMID: 20715102
Myeloid-derived suppressor cell heterogeneity and subset definition.
Elisa Peranzoni, Serena Zilio, +4 authors, Vincenzo Bronte.
Curr Opin Immunol, 2010 Feb 23; 22(2). PMID: 20171075
Highly Cited. Review.
Identification of fibroblast heterogeneity in the tumor microenvironment.
Hikaru Sugimoto, Thomas M Mundel, Mark W Kieran, Raghu Kalluri.
Cancer Biol Ther, 2006 Nov 16; 5(12). PMID: 17106243
Highly Cited.
Pancreatic stellate cell secreted IL-6 stimulates STAT3 dependent invasiveness of pancreatic intraepithelial neoplasia and cancer cells.
Nagaraj S Nagathihalli, Jason A Castellanos, +5 authors, Nipun B Merchant.
Oncotarget, 2016 Sep 08; 7(40). PMID: 27602757    Free PMC article.
Angiotensin II drives the production of tumor-promoting macrophages.
Virna Cortez-Retamozo, Martin Etzrodt, +21 authors, Mikael J Pittet.
Immunity, 2013 Jan 22; 38(2). PMID: 23333075    Free PMC article.
Highly Cited.
CD271⁺ subpopulation of pancreatic stellate cells correlates with prognosis of pancreatic cancer and is regulated by interaction with cancer cells.
Kenji Fujiwara, Kenoki Ohuchida, +8 authors, Masao Tanaka.
PLoS One, 2013 Jan 10; 7(12). PMID: 23300742    Free PMC article.
A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer.
John P Neoptolemos, Deborah D Stocken, +14 authors, European Study Group for Pancreatic Cancer.
N Engl J Med, 2004 Mar 19; 350(12). PMID: 15028824
Highly Cited.
Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation.
M Stein, S Keshav, N Harris, S Gordon.
J Exp Med, 1992 Jul 01; 176(1). PMID: 1613462    Free PMC article.
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5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity.
Julie Vincent, Grégoire Mignot, +7 authors, François Ghiringhelli.
Cancer Res, 2010 Apr 15; 70(8). PMID: 20388795
Highly Cited.
Galectin-1 is a novel functional receptor for tissue plasminogen activator in pancreatic cancer.
Oriol Roda, Elena Ortiz-Zapater, +8 authors, Pilar Navarro.
Gastroenterology, 2009 Jan 28; 136(4). PMID: 19171142
Pancreatic stellate cells respond to inflammatory cytokines: potential role in chronic pancreatitis.
P Mews, P Phillips, +4 authors, M Apte.
Gut, 2002 Mar 13; 50(4). PMID: 11889076    Free PMC article.
Hypoxia Inducible Factor 1 (HIF-1) Recruits Macrophage to Activate Pancreatic Stellate Cells in Pancreatic Ductal Adenocarcinoma.
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Amino-biphosphonate-mediated MMP-9 inhibition breaks the tumor-bone marrow axis responsible for myeloid-derived suppressor cell expansion and macrophage infiltration in tumor stroma.
Cecilia Melani, Sabina Sangaletti, +2 authors, Mario P Colombo.
Cancer Res, 2007 Dec 07; 67(23). PMID: 18056472    Free PMC article.
Highly Cited.
Inactivation of chemokine (C-C motif) receptor 1 (CCR1) suppresses colon cancer liver metastasis by blocking accumulation of immature myeloid cells in a mouse model.
Takanori Kitamura, Teruaki Fujishita, +5 authors, Makoto M Taketo.
Proc Natl Acad Sci U S A, 2010 Jul 10; 107(29). PMID: 20616008    Free PMC article.
Apoptosis and anergy of T cell induced by pancreatic stellate cells-derived galectin-1 in pancreatic cancer.
Dong Tang, Jun Gao, +10 authors, Kuirong Jiang.
Tumour Biol, 2015 Mar 03; 36(7). PMID: 25725585
Exclusion of T Cells From Pancreatic Carcinomas in Mice Is Regulated by Ly6C(low) F4/80(+) Extratumoral Macrophages.
Gregory L Beatty, Rafael Winograd, +8 authors, Robert H Vonderheide.
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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.
Update on phase I studies in advanced pancreatic adenocarcinoma. Hunting in darkness?
Alexios S Strimpakos, Muhammad Wasif Saif.
JOP, 2013 Jul 13; 14(4). PMID: 23846926
Periostin deposition in the stroma of invasive and intraductal neoplasms of the pancreas.
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Mod Pathol, 2008 May 20; 21(8). PMID: 18487994
Interleukin-27 inhibits malignant behaviors of pancreatic cancer cells by targeting M2 polarized tumor associated macrophages.
Lutian Yao, Mengyi Wang, +5 authors, Yupei Zhao.
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Stage IA Patients With Pancreatic Ductal Adenocarcinoma Cannot Benefit From Chemotherapy: A Propensity Score Matching Study.
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CAFs and TGF-β Signaling Activation by Mast Cells Contribute to Resistance to Gemcitabine/Nabpaclitaxel in Pancreatic Cancer.
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Ocoxin Oral Solution Exerts an Antitumoral Effect in Pancreatic Cancer and Reduces the Stromal-Mediated Chemoresistance.
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Immune-Based Therapies and the Role of Microsatellite Instability in Pancreatic Cancer.
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High Expression of PD-L1 Is Associated with Better Survival in Pancreatic/Periampullary Cancers and Correlates with Epithelial to Mesenchymal Transition.
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Pancreatic Cancer Signaling Pathways, Genetic Alterations, and Tumor Microenvironment: The Barriers Affecting the Method of Treatment.
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Therapeutic Potential of Targeting Stromal Crosstalk-Mediated Immune Suppression in Pancreatic Cancer.
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AXL Is a Key Factor for Cell Plasticity and Promotes Metastasis in Pancreatic Cancer.
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Immune-Related Circulating miR-125b-5p and miR-99a-5p Reveal a High Recurrence Risk Group of Pancreatic Cancer Patients after Tumor Resection.
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The Function of cGAS-STING Pathway in Treatment of Pancreatic Cancer.
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