. 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 
  • PMID: 28694739
  •     216 References
  •     41 citations


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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Berna C Özdemir, Tsvetelina Pentcheva-Hoang, +18 authors, Raghu Kalluri.
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Trends Immunol, 2012 Sep 25; 34(2). PMID: 23000011
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Oncotarget, 2014 Sep 23; 5(18). PMID: 25238263    Free PMC article.
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Claudia Sorrentino, Lucio Miele, +2 authors, Silvana Morello.
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J Cancer Sci Ther, 2013 Aug 19; 5. PMID: 25798214    Free PMC article.
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Am J Cancer Res, 2015 Jun 06; 5(3). PMID: 26046003    Free PMC article.
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JAMA, 2010 Sep 09; 304(10). PMID: 20823433
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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.
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Proc Natl Acad Sci U S A, 2009 Apr 07; 106(16). PMID: 19346489    Free PMC article.
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Farbod Shojaei, Xiumin Wu, +13 authors, Napoleone Ferrara.
Nature, 2007 Dec 08; 450(7171). PMID: 18064003
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Tomoya Kawase, Yumiko Yasui, +8 authors, Keisuke Hino.
BMC Gastroenterol, 2015 Sep 04; 15. PMID: 26330349    Free PMC article.
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J Immunol, 2008 Oct 04; 181(8). PMID: 18832739    Free PMC article.
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Immunity, 2010 Jul 08; 32(6). PMID: 20605485
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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.
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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.
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Pancreatology, 2010 May 21; 10(2-3). PMID: 20484957
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Annu Rev Immunol, 2012 Nov 20; 31. PMID: 23157435
Highly Cited. Review.
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Immunity, 2014 Jul 19; 41(1). PMID: 25035950    Free PMC article.
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Tumor-induced STAT3 activation in monocytic myeloid-derived suppressor cells enhances stemness and mesenchymal properties in human pancreatic cancer.
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Cancer Immunol Immunother, 2014 Mar 22; 63(5). PMID: 24652403    Free PMC article.
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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.
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Nat Cell Biol, 2016 Apr 19; 18(5). PMID: 27088855    Free PMC article.
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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.
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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.
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Biochim Biophys Acta Gen Subj, 2016 Oct 18; 1861(2). PMID: 27750041
Critical role of Trib1 in differentiation of tissue-resident M2-like macrophages.
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Nature, 2013 Mar 22; 495(7442). PMID: 23515163
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The cellular and molecular origin of tumor-associated macrophages.
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Science, 2014 May 09; 344(6186). PMID: 24812208    Free PMC article.
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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.
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J Immunol, 2002 Dec 24; 170(1). PMID: 12496409
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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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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.
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Clin Cancer Res, 2010 Sep 11; 16(21). PMID: 20829331
Macrophages mediate gemcitabine resistance of pancreatic adenocarcinoma by upregulating cytidine deaminase.
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Oncogene, 2013 Sep 03; 33(29). PMID: 23995783
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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.
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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.
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Gastroenterology, 2013 Jul 31; 145(5). PMID: 23891972    Free PMC article.
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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.
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Cancer Res, 2013 Feb 26; 73(8). PMID: 23436796
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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.
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Lancet, 2015 Nov 30; 387(10018). PMID: 26615328
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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
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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
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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.
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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.
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Blood, 2007 Sep 22; 111(1). PMID: 17885078    Free PMC article.
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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.
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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.
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Med Hypotheses, 2016 Jan 31; 87. PMID: 26826638
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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.
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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).
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Lancet, 2016 Jun 07; 388(10041). PMID: 27265347
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Int J Cancer, 2016 Jan 13; 138(11). PMID: 26756887
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Immunity, 2013 Sep 10; 39(3). PMID: 24012420    Free PMC article.
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Int J Cancer, 2014 Jan 25; 135(4). PMID: 24458546
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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.
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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.
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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.
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Cancer Cell, 2008 Jan 03; 13(1). PMID: 18167337    Free PMC article.
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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.
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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.
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Clin Cancer Res, 2011 Jul 27; 17(17). PMID: 21788356
Murine pancreatic adenocarcinoma dampens SHIP-1 expression and alters MDSC homeostasis and function.
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PLoS One, 2011 Dec 02; 6(11). PMID: 22132131    Free PMC article.
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Cancer Res, 2013 May 02; 73(13). PMID: 23633481    Free PMC article.
Macrophage polarization in pancreatic carcinoma: role of heparanase enzyme.
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J Natl Cancer Inst, 2014 Oct 19; 106(12). PMID: 25326645    Free PMC article.
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Cancer Cell, 2011 Apr 13; 19(4). PMID: 21481792
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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.
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Curr Opin Immunol, 2010 Feb 23; 22(2). PMID: 20171075
Highly Cited. Review.
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Pancreatic stellate cell secreted IL-6 stimulates STAT3 dependent invasiveness of pancreatic intraepithelial neoplasia and cancer cells.
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5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity.
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Cancer Res, 2010 Apr 15; 70(8). PMID: 20388795
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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
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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.
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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.
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Interleukin-27 inhibits malignant behaviors of pancreatic cancer cells by targeting M2 polarized tumor associated macrophages.
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