Evaluation of innate and adaptive immunity contributing to the antitumor effects of PD1 blockade in an orthotopic murine model of pancreatic cancer

References

• Lowenfels AB, Maisonneuve P. Epidemiology and prevention of pancreatic cancer. Jpn J Clin Oncol 2004; 34:238-44; PMID:15231857; http://dx.doi.org/10.1093/jjco/hyh045
   PubMed Web of Science ®Google Scholar
• Morton JP, Timpson P, Karim SA, Ridgway RA, Athineos D, Doyle B, Jamieson NB, Oien KA, Lowy AM, Brunton VG et al. Mutant p53 drives metastasis and overcomes growth arrest/senescence in pancreatic cancer. Proc Natl Acad Sci USA 2010; 107:246-51; PMID:20018721; http://dx.doi.org/10.1073/pnas.0908428107
   PubMed Web of Science ®Google Scholar
• Whatcott C, Han H, Posner RG, Von Hoff DD. Tumor-stromal interactions in pancreatic cancer. Crit Rev Oncog 2013; 18:135-51; PMID:23237556; http://dx.doi.org/10.1615/CritRevOncog.v18.i1-2.80
   PubMedGoogle Scholar
• Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54; PMID:22658127; http://dx.doi.org/10.1056/NEJMoa1200690
   PubMed Web of Science ®Google Scholar
• Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N, Okazaki T, Byrne MC et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 2000; 192:1027-34; PMID:11015443; http://dx.doi.org/10.1084/jem.192.7.1027
   PubMed Web of Science ®Google Scholar
• Latchman Y, Wood CR, Chernova T, Chaudhary D, Borde M, Chernova I, Iwai Y, Long AJ, Brown JA, Nunes R et al. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol 2001; 2:261-8; PMID:11224527; http://dx.doi.org/10.1038/85330
   PubMed Web of Science ®Google Scholar
• Zitvogel L, Kroemer G. Targeting PD-1/PD-L1 interactions for cancer immunotherapy. Oncoimmunology 2012; 1:1223-5; PMID:23243584; http://dx.doi.org/10.4161/onci.21335
   PubMed Web of Science ®Google Scholar
• Nomi T, Sho M, Akahori T, Hamada K, Kubo A, Kanehiro H, Nakamura S, Enomoto K, Yagita H, Azuma M et al. Clinical significance and therapeutic potential of the programmed death-1 ligand/programmed death-1 pathway in human pancreatic cancer. Clin Cancer Res 2007; 13:2151-7; PMID:17404099; http://dx.doi.org/10.1158/1078-0432.CCR-06-2746
   PubMed Web of Science ®Google Scholar
• Flies DB, Sandler BJ, Sznol M, Chen L. Blockade of the B7-H1/PD-1 pathway for cancer immunotherapy. Yale J Biol Med 2011; 84:409-21; PMID:22180678;
   PubMedGoogle Scholar
• McDermott DF, Drake CG, Sznol M, Choueiri TK, Powderly JD, Smith DC, Brahmer JR, Carvajal RD, Hammers HJ, Puzanov I et al. Survival, durable response, and long-term safety in patients with previously treated advanced renal cell carcinoma receiving nivolumab. J Clin Oncol 2015; 33:2013-20; PMID:25800770; http://dx.doi.org/10.1200/JCO.2014.58.1041
   PubMed Web of Science ®Google Scholar
• Sundar R, Cho BC, Brahmer JR, Soo RA. Nivolumab in NSCLC: latest evidence and clinical potential. Ther Adv Med Oncol 2015; 7:85-96; PMID:25755681; http://dx.doi.org/10.1177/1758834014567470
   PubMed Web of Science ®Google Scholar
• Ryan DP, Hong TS, Bardeesy N. Pancreatic adenocarcinoma. N Engl J Med 2014; 371:1039-49; PMID:25207767; http://dx.doi.org/10.1056/NEJMra1404198
   PubMed Web of Science ®Google Scholar
• Manuel ER, Chen J, D'Apuzzo M, Lampa MG, Kaltcheva TI, Thompson CB, Ludwig T, Chung V, Diamond DJ. Salmonella-Based Therapy Targeting Indoleamine 2,3-Dioxygenase Coupled with Enzymatic Depletion of Tumor Hyaluronan Induces Complete Regression of Aggressive Pancreatic Tumors. Cancer Immunol Res 2015; 3:1096-107; PMID:26134178; http://dx.doi.org/10.1158/2326-6066.CIR-14-0214
   PubMed Web of Science ®Google Scholar
• Gallina G, Dolcetti L, Serafini P, De Santo C, Marigo I, Colombo MP, Basso G, Brombacher F, Borrello I, Zanovello P et al. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J Clin Invest 2006; 116:2777-90; PMID:17016559; http://dx.doi.org/10.1172/JCI28828
   PubMed Web of Science ®Google Scholar
• Drake CG, Jaffee E, Pardoll DM. Mechanisms of immune evasion by tumors. Adv Immunol 2006; 90:51-81; PMID:16730261; http://dx.doi.org/10.1016/S0065-2776(06)90002-9
   PubMed Web of Science ®Google Scholar
• Bronte V, Apolloni E, Cabrelle A, Ronca R, Serafini P, Zamboni P, Restifo NP, Zanovello P. Identification of a CD11b(+)/Gr-1(+)/CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells. Blood 2000; 96:3838-46; PMID:11090068
   PubMed Web of Science ®Google Scholar
• Yamaguchi T, Sakaguchi S. Regulatory T cells in immune surveillance and treatment of cancer. Semin Cancer Biol 2006; 16:115-23; PMID:16376102; http://dx.doi.org/10.1016/j.semcancer.2005.11.005
   PubMed Web of Science ®Google Scholar
• Okazaki T, Chikuma S, Iwai Y, Fagarasan S, Honjo T. A rheostat for immune responses: the unique properties of PD-1 and their advantages for clinical application. Nat Immunol 2013; 14:1212-8; PMID:24240160; http://dx.doi.org/10.1038/ni.2762
   PubMed Web of Science ®Google Scholar
• Calzascia T, Pellegrini M, Hall H, Sabbagh L, Ono N, Elford AR, Mak TW, Ohashi PS. TNF-α is critical for antitumor but not antiviral T cell immunity in mice. J Clin Invest 2007; 117:3833-45; PMID:17992258; http://dx.doi.org/10.1172/JCI32567
   PubMed Web of Science ®Google Scholar
• Schoenborn JR, Wilson CB. Regulation of interferon-gamma during innate and adaptive immune responses. Adv Immunol 2007; 96:41-101; PMID:17981204; http://dx.doi.org/10.1016/S0065-2776(07)96002-2
   PubMed Web of Science ®Google Scholar
• Dienz O, Rincon M. The effects of IL-6 on CD4 T cell responses. Clin Immunol 2009; 130:27-33; PMID:18845487; http://dx.doi.org/10.1016/j.clim.2008.08.018
   PubMed Web of Science ®Google Scholar
• Akahoshi T, Endo H, Kondo H, Kashiwazaki S, Kasahara T, Mukaida N, Harada A, Matsushima K. Essential involvement of interleukin-8 in neutrophil recruitment in rabbits with acute experimental arthritis induced by lipopolysaccharide and interleukin-1. Lymphokine Cytokine Res 1994; 13:113-6; PMID:8061112
   PubMedGoogle Scholar
• Oft M. IL-10: master switch from tumor-promoting inflammation to antitumor immunity. Cancer Immunol Res 2014; 2:194-9; PMID:24778315; http://dx.doi.org/10.1158/2326-6066.CIR-13-0214
   PubMed Web of Science ®Google Scholar
• Voron T, Colussi O, Marcheteau E, Pernot S, Nizard M, Pointet AL, Latreche S, Bergaya S, Benhamouda N, Tanchot C et al. VEGF-A modulates expression of inhibitory checkpoints on CD8+ T cells in tumors. J Exp Med 2015; 212:139-48; PMID:25601652; http://dx.doi.org/10.1084/jem.20140559
   PubMed Web of Science ®Google Scholar
• Voron T, Marcheteau E, Pernot S, Colussi O, Tartour E, Taieb J, Terme M. Control of the immune response by pro-angiogenic factors. Front Oncol 2014; 4:70; PMID:24765614; http://dx.doi.org/10.3389/fonc.2014.00070
   PubMedGoogle Scholar
• Braumuller H, Wieder T, Brenner E, Assmann S, Hahn M, Alkhaled M, Schilbach K, Essmann F, Kneilling M, Griessinger C et al. T-helper-1-cell cytokines drive cancer into senescence. Nature 2013; 494:361-5; PMID:23376950; http://dx.doi.org/10.1038/nature11824
   PubMed Web of Science ®Google Scholar
• Alvarez IB, Pasquinelli V, Jurado JO, Abbate E, Musella RM, de la Barrera SS, Garcia VE. Role Played by the Programmed Death-1-Programmed Death Ligand Pathway during Innate Immunity against Mycobacterium tuberculosis. J Infect Dis 2010; 202:524-32; PMID:20617899; http://dx.doi.org/10.1086/654932
   PubMed Web of Science ®Google Scholar
• Lazar-Molnar E, Chen B, Sweeney KA, Wang EJ, Liu W, Lin J, Porcelli SA, Almo SC, Nathenson SG, Jacobs WR, Jr. Programmed death-1 (PD-1)-deficient mice are extraordinarily sensitive to tuberculosis. Proc Natl Acad Sci U S A 2010; 107:13402-7; PMID:20624978; http://dx.doi.org/10.1073/pnas.1007394107
   PubMed Web of Science ®Google Scholar
• Nausch N, Galani IE, Schlecker E, Cerwenka A. Mononuclear myeloid-derived “suppressor” cells express RAE-1 and activate natural killer cells. Blood 2008; 112:4080-9; PMID:18753637; http://dx.doi.org/10.1182/blood-2008-03-143776
   PubMed Web of Science ®Google Scholar
• Eruslanov EB, Bhojnagarwala PS, Quatromoni JG, Stephen TL, Ranganathan A, Deshpande C, Akimova T, Vachani A, Litzky L, Hancock WW et al. Tumor-associated neutrophils stimulate T cell responses in early-stage human lung cancer. J Clin Invest 2014; 124:5466-80; PMID:25384214; http://dx.doi.org/10.1172/JCI77053
   PubMed Web of Science ®Google Scholar
• Fridlender ZG, Albelda SM. Tumor-associated neutrophils: friend or foe? Carcinogenesis 2012; 33:949-55; PMID:22425643; http://dx.doi.org/10.1093/carcin/bgs123
   PubMed Web of Science ®Google Scholar
• Andoniou CE, Coudert JD, Degli-Esposti MA. Killers and beyond: NK-cell-mediated control of immune responses. Eur J Immunol 2008; 38:2938-42; PMID:18979519; http://dx.doi.org/10.1002/eji.200838882
   PubMed Web of Science ®Google Scholar
• Roopenian DC, Akilesh S. FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol 2007; 7:715-25; PMID:17703228; http://dx.doi.org/10.1038/nri2155
   PubMed Web of Science ®Google Scholar
• Dai H, Wan N, Zhang S, Moore Y, Wan F, Dai Z. Cutting edge: programmed death-1 defines CD8+CD122+ T cells as regulatory versus memory T cells. J Immunol 2010; 185:803-7; PMID:20548035; http://dx.doi.org/10.4049/jimmunol.1000661
   PubMed Web of Science ®Google Scholar
• Schietinger A, Greenberg PD. Tolerance and exhaustion: defining mechanisms of T cell dysfunction. Trends Immunol 2014; 35:51-60; PMID:24210163; http://dx.doi.org/10.1016/j.it.2013.10.001
   PubMed Web of Science ®Google Scholar
• Sun H, Sun C, Tian Z, Xiao W. NK cells in immunotolerant organs. Cell Mol Immunol 2013; 10:202-12; PMID:23563087; http://dx.doi.org/10.1038/cmi.2013.9
   PubMed Web of Science ®Google Scholar
• Muller WA. New mechanisms and pathways for monocyte recruitment. J Exp Med 2001; 194:F47-51; PMID:11696603; http://dx.doi.org/10.1084/jem.194.9.f47
   PubMedGoogle Scholar
• Jablonska J, Wu CF, Andzinski L, Leschner S, Weiss S. CXCR2-mediated tumor-associated neutrophil recruitment is regulated by IFN-β. Int J Cancer 2014; 134:1346-58; PMID:24154944; http://dx.doi.org/10.1002/ijc.28551
   PubMed Web of Science ®Google Scholar
• Cheng M, Chen Y, Xiao W, Sun R, Tian Z. NK cell-based immunotherapy for malignant diseases. Cell Mol Immunol 2013; 10:230-52; PMID:23604045; http://dx.doi.org/10.1038/cmi.2013.10
   PubMed Web of Science ®Google Scholar
• Motz GT, Coukos G. The parallel lives of angiogenesis and immunosuppression: cancer and other tales. Nat Rev Immunol 2011; 11:702-11; PMID:21941296; http://dx.doi.org/10.1038/nri3064
   PubMed Web of Science ®Google Scholar
• Mack B, Eggert C, Eder K, Imrich S, Baumeister P, Harreus U, Gires O. Rapid and non-enzymatic in vitro retrieval of tumour cells from surgical specimens. PLoS One 2013; 8:e55540; PMID:23383219; http://dx.doi.org/10.1371/journal.pone.0055540
   PubMedGoogle Scholar
• Kim MP, Evans DB, Wang H, Abbruzzese JL, Fleming JB, Gallick GE. Generation of orthotopic and heterotopic human pancreatic cancer xenografts in immunodeficient mice. Nat Protoc 2009; 4:1670-80; PMID:19876027; http://dx.doi.org/10.1038/nprot.2009.171
   PubMed Web of Science ®Google Scholar
• Agata Y, Kawasaki A, Nishimura H, Ishida Y, Tsubata T, Yagita H, Honjo T. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int Immunol 1996; 8:765-72; PMID:8671665; http://dx.doi.org/10.1093/intimm/8.5.765
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi.org/10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar