Immune Cell Production of Interleukin 17 Induces Stem Cell Features of Pancreatic Intraepithelial Neoplasia Cells

Gastroenterology - Tập 155 - Trang 210-223.e3 - 2018
Yu Zhang1, Michelle Zoltan1, Erick Riquelme1, Hanwen Xu1, Ismet Sahin2, Susana Castro-Pando1, Maria Fernanda Montiel1, Kyle Chang1, Zhengyu Jiang3, Jianhua Ling4, Sonal Gupta5, William Horne6, Melissa Pruski7, Huamin Wang5, Shao-Cong Sun8, Guillermina Lozano9, Paul Chiao4, Anirban Maitra5, Steven D. Leach10, Jay K. Kolls6
1Department of Clinical Cancer Prevention, The University of Texas MD Anderson Cancer Center, Houston, Texas
2Department of Engineering, Texas Southern University, Houston, Texas
3Herbert Irving Comprehensive Cancer Center, Columbia University Medical Center, New York, New York
4Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas
5Department of Pathology, University of Texas MD Anderson Cancer Center, Houston, Texas
6Richard King Mellon Foundation Institute for Pediatric Research, Children’s Hospital of Pittsburgh, Pittsburgh, Pennsylvania
7Division of Gastroenterology, Hepatology and Nutrition, Department of Internal Medicine, University of Texas Health Science Center, Houston, Texas
8Department of Immunology, University of Texas Health Sciences Center, Houston, Texas
9Department of Genetics, The University of Texas MD Anderson Cancer Center, Houston, Texas
10Center for Pancreatic Cancer Research, Memorial Sloan Kettering Cancer Center, New York, New York

Tài liệu tham khảo

Kamisawa, 2016, Pancreatic cancer, Lancet, 388, 73, 10.1016/S0140-6736(16)00141-0 Bailey, 2016, Genomic analyses identify molecular subtypes of pancreatic cancer, Nature, 531, 47, 10.1038/nature16965 Numasaki, 2005, IL-17 enhances the net angiogenic activity and in vivo growth of human non-small cell lung cancer in SCID mice through promoting CXCR-2-dependent angiogenesis, J Immunol, 175, 6177, 10.4049/jimmunol.175.9.6177 Benevides, 2015, IL17 promotes mammary tumor progression by changing the behavior of tumor cells and eliciting tumorigenic neutrophils recruitment, Cancer Res, 75, 3788, 10.1158/0008-5472.CAN-15-0054 Kryczek, 2009, Endogenous IL-17 contributes to reduced tumor growth and metastasis, Blood, 114, 357, 10.1182/blood-2008-09-177360 Habbe, 2008, Spontaneous induction of murine pancreatic intraepithelial neoplasia (mPanIN) by acinar cell targeting of oncogenic Kras in adult mice, Proc Natl Acad Sci U S A, 105, 18913, 10.1073/pnas.0810097105 McAllister, 2014, Oncogenic Kras activates a hematopoietic-to-epithelial IL-17 signaling axis in preinvasive pancreatic neoplasia, Cancer Cell, 25, 621, 10.1016/j.ccr.2014.03.014 McAllister, 2005, Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis, J Immunol, 175, 404, 10.4049/jimmunol.175.1.404 Conti, 2009, Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis, J Exp Med, 206, 299, 10.1084/jem.20081463 Kryczek, 2014, IL-22(+)CD4(+) T cells promote colorectal cancer stemness via STAT3 transcription factor activation and induction of the methyltransferase DOT1L, Immunity, 40, 772, 10.1016/j.immuni.2014.03.010 Fang, 2017, IL-33 promotes colon cancer cell stemness via JNK activation and macrophage recruitment, Cancer Res, 77, 10.1158/0008-5472.CAN-16-1602 Bie, 2016, Non-tumor tissue derived interleukin-17B activates IL-17RB/AKT/beta-catenin pathway to enhance the stemness of gastric cancer, Sci Rep, 6, 25447, 10.1038/srep25447 Li, 2009, Identification of human pancreatic cancer stem cells, Methods Mol Biol, 568, 161, 10.1007/978-1-59745-280-9_10 Rasheed, 2010, Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma, J Natl Cancer Inst, 102, 340, 10.1093/jnci/djp535 Li, 2015, Suppression of cancer relapse and metastasis by inhibiting cancer stemness, Proc Natl Acad Sci U S A, 112, 1839, 10.1073/pnas.1424171112 Duong, 2012, Aldehyde dehydrogenase 1A1 confers intrinsic and acquired resistance to gemcitabine in human pancreatic adenocarcinoma MIA PaCa-2 cells, Int J Oncol, 41, 855, 10.3892/ijo.2012.1516 Delgiorno, 2014, Identification and manipulation of biliary metaplasia in pancreatic tumors, Gastroenterology, 146, 233, 10.1053/j.gastro.2013.08.053 Westphalen, 2014, Long-lived intestinal tuft cells serve as colon cancer-initiating cells, J Clin Invest, 124, 1283, 10.1172/JCI73434 Bailey, 2014, DCLK1 marks a morphologically distinct subpopulation of cells with stem cell properties in preinvasive pancreatic cancer, Gastroenterology, 146, 245, 10.1053/j.gastro.2013.09.050 May, 2010, Identification of a novel putative pancreatic stem/progenitor cell marker DCAMKL-1 in normal mouse pancreas, Am J Physiol Gastrointest Liver Physiol, 299, G303, 10.1152/ajpgi.00146.2010 Saqui-Salces, 2011, Gastric tuft cells express DCLK1 and are expanded in hyperplasia, Histochem Cell Biol, 136, 191, 10.1007/s00418-011-0831-1 Westphalen, 2016, Dclk1 defines quiescent pancreatic progenitors that promote injury-induced regeneration and tumorigenesis, Cell Stem Cell, 18, 441, 10.1016/j.stem.2016.03.016 Zubarik, 2011, Screening for pancreatic cancer in a high-risk population with serum CA 19-9 and targeted EUS: a feasibility study, Gastrointest Endosc, 74, 87, 10.1016/j.gie.2011.03.1235 Cerami, 2012, The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data, Cancer Discov, 2, 401, 10.1158/2159-8290.CD-12-0095 Colaprico, 2016, TCGAbiolinks: an R/Bioconductor package for integrative analysis of TCGA data, Nucleic Acids Res, 44, e71, 10.1093/nar/gkv1507 Shen, 2005, Cytokines link osteoblasts and inflammation: microarray analysis of interleukin-17- and TNF-alpha-induced genes in bone cells, J Leukoc Biol, 77, 388, 10.1189/jlb.0904490 Chen, 2013, IL-17A induces pro-inflammatory cytokines production in macrophages via MAPKinases, NF-kappaB and AP-1, Cell Physiol Biochem, 32, 1265, 10.1159/000354525 Fortunel, 2003, Comment on “’Stemness’: transcriptional profiling of embryonic and adult stem cells” and “a stem cell molecular signature”, Science, 302, 393, 10.1126/science.1086384 Ramalho-Santos, 2002, “Stemness”: transcriptional profiling of embryonic and adult stem cells, Science, 298, 597, 10.1126/science.1072530 Ivanova, 2002, A stem cell molecular signature, Science, 298, 601, 10.1126/science.1073823 Munoz, 2012, The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent ‘+4’ cell markers, EMBO J, 31, 3079, 10.1038/emboj.2012.166 Gerbe, 2016, Intestinal epithelial tuft cells initiate type 2 mucosal immunity to helminth parasites, Nature, 529, 226, 10.1038/nature16527 Westphalen, 2016, Functional implication of Dclk1 and Dclk1-expressing cells in cancer, Small GTPases, 1 Rovira, 2010, Isolation and characterization of centroacinar/terminal ductal progenitor cells in adult mouse pancreas, Proc Natl Acad Sci U S A, 107, 75, 10.1073/pnas.0912589107 Tomita, 2016, Aldehyde dehydrogenase 1A1 in stem cells and cancer, Oncotarget, 7, 11018, 10.18632/oncotarget.6920 Weygant, 2014, Small molecule kinase inhibitor LRRK2-IN-1 demonstrates potent activity against colorectal and pancreatic cancer through inhibition of doublecortin-like kinase 1, Mol Cancer, 13, 103, 10.1186/1476-4598-13-103 Deng, 2011, Characterization of a selective inhibitor of the Parkinson's disease kinase LRRK2, Nat Chem Biol, 7, 203, 10.1038/nchembio.538 Xie, 2010, IL-17 activates the canonical NF-kappaB signaling pathway in autoimmune B cells of BXD2 mice to upregulate the expression of regulators of G-protein signaling 16, J Immunol, 184, 2289, 10.4049/jimmunol.0903133 Gu, 2011, IL-17 induces AKT-dependent IL-6/JAK2/STAT3 activation and tumor progression in hepatocellular carcinoma, Mol Cancer, 10, 150, 10.1186/1476-4598-10-150 Li, 2016, IL-17 mediates inflammatory reactions via p38/c-Fos and JNK/c-Jun activation in an AP-1-dependent manner in human nucleus pulposus cells, J Transl Med, 14, 77, 10.1186/s12967-016-0833-9 Ajibade, 2012, TAK1 negatively regulates NF-kappaB and p38 MAP kinase activation in Gr-1+CD11b+ neutrophils, Immunity, 36, 43, 10.1016/j.immuni.2011.12.010 Israel, 2010, The IKK complex, a central regulator of NF-kappaB activation, Cold Spring Harb Perspect Biol, 2, a000158, 10.1101/cshperspect.a000158 Ho, 2010, IL-17RC is required for immune signaling via an extended SEF/IL-17R signaling domain in the cytoplasmic tail, J Immunol, 185, 1063, 10.4049/jimmunol.0903739 Hu, 2010, IL-17RC is required for IL-17A- and IL-17F-dependent signaling and the pathogenesis of experimental autoimmune encephalomyelitis, J Immunol, 184, 4307, 10.4049/jimmunol.0903614 Beringer, 2016, IL-17 in chronic inflammation: from discovery to targeting, Trends Mol Med, 22, 230, 10.1016/j.molmed.2016.01.001 He, 2010, IL-17 promotes tumor development through the induction of tumor promoting microenvironments at tumor sites and myeloid-derived suppressor cells, J Immunol, 184, 2281, 10.4049/jimmunol.0902574 Numasaki, 2003, Interleukin-17 promotes angiogenesis and tumor growth, Blood, 101, 2620, 10.1182/blood-2002-05-1461 Wang, 2014, Interleukin-17 receptor a signaling in transformed enterocytes promotes early colorectal tumorigenesis, Immunity, 41, 1052, 10.1016/j.immuni.2014.11.009 Wang, 2013, IL-17 and TNF synergistically modulate cytokine expression while suppressing melanogenesis: potential relevance to psoriasis, J Invest Dermatol, 133, 2741, 10.1038/jid.2013.237 Gaeta, 2013, Sequential addition of reprogramming factors improves efficiency, Nat Cell Biol, 15, 725, 10.1038/ncb2800 Zepp, 2017, IL-17A-induced PLET1 expression contributes to tissue repair and colon tumorigenesis, J Immunol, 199, 3849, 10.4049/jimmunol.1601540 Haider, 2014, A multi-gene signature predicts outcome in patients with pancreatic ductal adenocarcinoma, Genome Med, 6, 105, 10.1186/s13073-014-0105-3 Pinto, 2015, StemChecker: a web-based tool to discover and explore stemness signatures in gene sets, Nucleic Acids Res, 43, W72, 10.1093/nar/gkv529 Nathaniel Weygant, 2016, Systemic delivery of CBT-15G DCLK1-targeted monoclonal antibody dramatically decreases tumorigenesis in a xenograft model of pancreatic cancer Zhang, 2006, Aberrant promoter methylation and silencing of the POU2F3 gene in cervical cancer, Oncogene, 25, 5436, 10.1038/sj.onc.1209530 Kosanam, 2013, Laminin, gamma 2 (LAMC2): a promising new putative pancreatic cancer biomarker identified by proteomic analysis of pancreatic adenocarcinoma tissues, Mol Cell Proteomics, 12, 2820, 10.1074/mcp.M112.023507 Huang, 2017, Overexpression of LAMC2 predicts poor prognosis in colorectal cancer patients and promotes cancer cell proliferation, migration, and invasion, Tumour Biol, 39, 10.1177/1010428317705849 Garg, 2014, Laminin-5gamma-2 (LAMC2) is highly expressed in anaplastic thyroid carcinoma and is associated with tumor progression, migration, and invasion by modulating signaling of EGFR, J Clin Endocrinol Metab, 99, E62, 10.1210/jc.2013-2994 Fedchenko, 2014, Different approaches for interpretation and reporting of immunohistochemistry analysis results in the bone tissue—a review, Diagn Pathol, 9, 221, 10.1186/s13000-014-0221-9 McAllister, 2014, Oncogenic Kras activates a hematopoietic-to-epithelial IL-17 signaling axis in preinvasive pancreatic neoplasia, Cancer Cell, 25, 621, 10.1016/j.ccr.2014.03.014 Pinto, 2015, StemChecker: a web-based tool to discover and explore stemness signatures in gene sets, Nucleic Acids Res, 43, W72, 10.1093/nar/gkv529