Human mesothelioma induces defects in dendritic cell numbers and antigen-processing function which predict survival outcomes

References

• Robinson BW, Lake RA. Advances in malignant mesothelioma. N Engl J Med 2005; 353:1591-603; PMID:16221782; http://dx.doi.org/10.1056/NEJMra050152
   PubMed Web of Science ®Google Scholar
• Kao SC, Pavlakis N, Harvie R, Vardy JL, Boyer MJ, van Zandwijk N, Clarke SJ. High blood neutrophil-to-lymphocyte ratio is an indicator of poor prognosis in malignant mesothelioma patients undergoing systemic therapy. Clin Cancer Res 2010; 16:5805-13; PMID:20956618; http://dx.doi.org/10.1158/1078-0432.CCR-10-2245
   PubMed Web of Science ®Google Scholar
• Linton A, Pavlakis N, O'Connell R, Soeberg M, Kao S, Clarke S, Vardy J, van Zandwijk N. Factors associated with survival in a large series of patients with malignant pleural mesothelioma in New South Wales. Br J Cancer 2014; 111:1860-9; PMID:25188323; http://dx.doi.org/10.1038/bjc.2014.478
   PubMed Web of Science ®Google Scholar
• Bianchi C, Giarelli L, Grandi G, Brollo A, Ramani L, Zuch C. Latency periods in asbestos-related mesothelioma of the pleura. Eur J Cancer Prev 1997; 6:162-6; PMID:9237066; http://dx.doi.org/10.1159/000343599
   PubMed Web of Science ®Google Scholar
• Fulop T, Larbi A, Kotb R, Pawelec G. Immunology of aging and cancer development. Interdiscip Top Gerontol 2013; 38:38-48; PMID:23503514; http://dx.doi.org/10.1159/000343599
   PubMedGoogle Scholar
• Gravekamp C, Jahangir A. Is cancer vaccination feasible at older age? Exp Gerontol 2014; 54:138-44; PMID:24509231; http://dx.doi.org/10.1016/j.exger.2014.01.025
   PubMed Web of Science ®Google Scholar
• Izzi V, Masuelli L, Tresoldi I, Foti C, Modesti A, Bei R. Immunity and malignant mesothelioma: from mesothelial cell damage to tumor development and immune response-based therapies. Cancer Lett 2012; 322:18-34; PMID:22394996; http://dx.doi.org/10.1016/j.canlet.2012.02.034
   PubMed Web of Science ®Google Scholar
• Jackaman C, Cornwall S, Lew AM, Zhan Y, Robinson BW, Nelson DJ. Local effector failure in mesothelioma is not mediated by CD4+ CD25+ T-regulator cells. Eur Respir J 2009; 34:162-75; PMID:19251786; http://dx.doi.org/10.1183/09031936.00101008
   PubMed Web of Science ®Google Scholar
• Hassan R, Miller AC, Sharon E, Thomas A, Reynolds JC, Ling A, Kreitman RJ, Miettinen MM, Steinberg SM, Fowler DH et al. Major cancer regressions in mesothelioma after treatment with an anti-mesothelin immunotoxin and immune suppression. Sci Transl Med 2013; 5:208ra147; PMID:24154601; http://dx.doi.org/10.1126/scitranslmed.3006941
   PubMed Web of Science ®Google Scholar
• Calabro L, Morra A, Fonsatti E, Cutaia O, Fazio C, Annesi D, Lenoci M, Amato G, Danielli R, Altomonte M et al. Efficacy and safety of an intensified schedule of tremelimumab for chemotherapy-resistant malignant mesothelioma: an open-label, single-arm, phase 2 study. Lancet Respir Med 2015; 3(4):301-9; PMID:25819643; http://dx.doi.org/10.1016/S2213-2600(15)00092-2
   PubMed Web of Science ®Google Scholar
• Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Pulendran B, Palucka K. Immunobiology of dendritic cells. Annu Rev Immunol 2000; 18:767-811; PMID:10837075; http://dx.doi.org/10.1146/annurev.immunol.18.1.767
   PubMed Web of Science ®Google Scholar
• Caux C, Vanbervliet B, Massacrier C, Dezutter-Dambuyant C, de Saint-Vis B, Jacquet C, Yoneda K, Imamura S, Schmitt D, Banchereau J. CD34+ hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to GM-CSF+TNF α. J Exp Med 1996; 184:695-706; PMID:8760823; http://dx.doi.org/10.1084/jem.184.2.695
   PubMed Web of Science ®Google Scholar
• Rissoan MC, Soumelis V, Kadowaki N, Grouard G, Briere F, de Waal Malefyt R, Liu YJ. Reciprocal control of T helper cell and dendritic cell differentiation. Science 1999; 283:1183-6; PMID:10024247; http://dx.doi.org/10.1126/science.283.5405.1183
   PubMed Web of Science ®Google Scholar
• Robbins SH, Walzer T, Dembele D, Thibault C, Defays A, Bessou G, Xu H, Vivier E, Sellars M, Pierre P et al. Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol 2008; 9:R17; PMID:18218067; http://dx.doi.org/10.1186/gb-2008-9-1-r17
   PubMed Web of Science ®Google Scholar
• Blom B, Ho S, Antonenko S, Liu YJ. Generation of interferon α-producing predendritic cell (Pre-DC)2 from human CD34(+) hematopoietic stem cells. J Exp Med 2000; 192:1785-96; PMID:11120775; http://dx.doi.org/10.1084/jem.192.12.1785
   PubMed Web of Science ®Google Scholar
• Grouard G, Rissoan MC, Filgueira L, Durand I, Banchereau J, Liu YJ. The enigmatic plasmacytoid T cells develop into dendritic cells with interleukin (IL)-3 and CD40-ligand. J Exp Med 1997; 185:1101-11; PMID:9091583; http://dx.doi.org/10.1084/jem.185.6.1101
   PubMed Web of Science ®Google Scholar
• Soumelis V, Liu YJ. From plasmacytoid to dendritic cell: morphological and functional switches during plasmacytoid pre-dendritic cell differentiation. Eur J Immunol 2006; 36:2286-92; PMID:16892183; http://dx.doi.org/10.1002/eji.200636026
   PubMed Web of Science ®Google Scholar
• Hart DN. Dendritic cells: unique leukocyte populations which control the primary immune response. Blood 1997; 90:3245-87; PMID:9345009
   PubMed Web of Science ®Google Scholar
• Hoffmann TK, Muller-Berghaus J, Ferris RL, Johnson JT, Storkus WJ, Whiteside TL. Alterations in the frequency of dendritic cell subsets in the peripheral circulation of patients with squamous cell carcinomas of the head and neck. Clin Cancer Res 2002; 8:1787-93; PMID:12060618
   PubMed Web of Science ®Google Scholar
• Ma XJ, Pan XL, Lv ZH, Xu FL, Liu da Y, Lei da P, Xia M, Luan XY. Therapeutic influence on circulating and monocyte-derived dendritic cells in laryngeal squamous cell carcinoma patients. Acta Otolaryngol 2009; 129:84-91; PMID:18607895; http://dx.doi.org/10.1080/00016480802020459
   PubMed Web of Science ®Google Scholar
• Sakakura K, Chikamatsu K, Takahashi K, Whiteside TL, Furuya N. Maturation of circulating dendritic cells and imbalance of T-cell subsets in patients with squamous cell carcinoma of the head and neck. Cancer Immunol Immunother 2006; 55:151-9; PMID:15889251; http://dx.doi.org/10.1007/s00262-005-0697-y
   PubMed Web of Science ®Google Scholar
• Sciarra A, Lichtner M, Autran GA, Mastroianni C, Rossi R, Mengoni F, Cristini C, Gentilucci A, Vullo V, Di Silverio F. Characterization of circulating blood dendritic cell subsets DC123+ (lymphoid) and DC11C+ (myeloid) in prostate adenocarcinoma patients. Prostate 2007; 67:1-7; PMID:17075798; http://dx.doi.org/10.1002/pros.20431
   PubMed Web of Science ®Google Scholar
• Della Bella S, Nicola S, Brambilla L, Riva A, Ferrucci S, Presicce P, Boneschi V, Berti E, Villa ML. Quantitative and functional defects of dendritic cells in classic Kaposi's sarcoma. Clin Immunol 2006; 119:317-29; PMID:16527545; http://dx.doi.org/10.1016/j.clim.2006.01.011
   PubMed Web of Science ®Google Scholar
• Harrison SJ, Franklin IM, Campbell JD. Enumeration of blood dendritic cells in patients with multiple myeloma at presentation and through therapy. Leuk Lymphoma 2008; 49:2272-83; PMID:19052974; http://dx.doi.org/10.1080/10428190802464729
   PubMed Web of Science ®Google Scholar
• Pinzon-Charry A, Ho CS, Maxwell T, McGuckin MA, Schmidt C, Furnival C, Pyke CM, López JA. Numerical and functional defects of blood dendritic cells in early- and late-stage breast cancer. Br J Cancer 2007; 97:1251-9; PMID:17923873; http://dx.doi.org/10.1038/sj.bjc.6604018
   PubMed Web of Science ®Google Scholar
• Tjomsland V, Sandstrom P, Spangeus A, Messmer D, Emilsson J, Falkmer U, Falkmer S, Magnusson KE, Borch K, Larsson M. Pancreatic adenocarcinoma exerts systemic effects on the peripheral blood myeloid and plasmacytoid dendritic cells: an indicator of disease severity? BMC Cancer 2010; 10:87; PMID:20214814; http://dx.doi.org/10.1186/1471-2407-10-87
   PubMed Web of Science ®Google Scholar
• Troy A, Davidson P, Atkinson C, Hart D. Phenotypic characterisation of the dendritic cell infiltrate in prostate cancer. J Urol 1998; 160:214-9; PMID:9628653; http://dx.doi.org/10.1016/S0022-5347(01)63093-3
   PubMed Web of Science ®Google Scholar
• Ninomiya T, Akbar SM, Masumoto T, Horiike N, Onji M. Dendritic cells with immature phenotype and defective function in the peripheral blood from patients with hepatocellular carcinoma. J Hepatol 1999; 31:323-31; PMID:10453947; http://dx.doi.org/10.1016/S0168-8278(99)80231-1
   PubMed Web of Science ®Google Scholar
• Jackaman C, Bundell CS, Kinnear BF, Smith AM, Filion P, van Hagen D, Robinson BW, Nelson DJ. IL-2 intratumoral immunotherapy enhances CD8+ T cells that mediate destruction of tumor cells and tumor-associated vasculature: a novel mechanism for IL-2. J Immunol 2003; 171:5051-63; PMID:14607902; http://dx.doi.org/10.4049/jimmunol.171.10.5051
   PubMed Web of Science ®Google Scholar
• Cernadas M, Lu J, Watts G, Brenner MB. CD1a expression defines an interleukin-12 producing population of human dendritic cells. Clin Exp Immunol 2009; 155:523-33; PMID:19220838; http://dx.doi.org/10.1111/j.1365-2249.2008.03853.x
   PubMed Web of Science ®Google Scholar
• Zeng Z, Xu X, Zhang Y, Xing J, Long J, Gu L, Wang X, Sun D, Ka W, Yao W et al. Tumor-derived factors impaired motility and immune functions of dendritic cells through derangement of biophysical characteristics and reorganization of cytoskeleton. Cell Motil Cytoskeleton 2007; 64:186-98; PMID:17183544; http://dx.doi.org/10.1002/cm.20175
   PubMed Web of Science ®Google Scholar
• Imai K, Minamiya Y, Koyota S, Ito M, Saito H, Sato Y, Motoyama S, Sugiyama T, Ogawa J. Inhibition of dendritic cell migration by transforming growth factor-beta1 increases tumor-draining lymph node metastasis. J Exp Clin Cancer Res 2012; 31:3; http://dx.doi.org/10.1186/1756-9966-31-3
   PubMed Web of Science ®Google Scholar
• Esche C, Gambotto A, Satoh Y, Gerein V, Robbins PD, Watkins SC, Lotze MT, Shurin MR. CD154 inhibits tumor-induced apoptosis in dendritic cells and tumor growth. Eur J Immunol 1999; 29:2148-55; PMID:10427977; http://dx.doi.org/10.1002/(SICI)1521-4141(199907)29:07%3c2148::AID-IMMU2148%3e3.0.CO;2-F
   PubMed Web of Science ®Google Scholar
• DeLong P, Carroll RG, Henry AC, Tanaka T, Ahmad S, Leibowitz MS, Sterman DH, June CH, Albelda SM, Vonderheide RH. Regulatory T cells and cytokines in malignant pleural effusions secondary to mesothelioma and carcinoma. Cancer Biol Ther 2005; 4:342-6; PMID:15846066; http://dx.doi.org/10.4161/cbt.4.3.1644
   PubMed Web of Science ®Google Scholar
• Murillo O, Dubrot J, Palazon A, Arina A, Azpilikueta A, Alfaro C, Solano S, Ochoa MC, Berasain C, Gabari I et al. In vivo depletion of DC impairs the anti-tumor effect of agonistic anti-CD137 mAb. Eur J Immunol 2009; 39:2424-36; PMID:19662633; http://dx.doi.org/10.1002/eji.200838958
   PubMed Web of Science ®Google Scholar
• van Cruijsen H, van der Veldt AA, Vroling L, Oosterhoff D, Broxterman HJ, Scheper RJ, Giaccone G, Haanen JB, van den Eertwegh AJ, Boven E et al. Sunitinib-induced myeloid lineage redistribution in renal cell cancer patients: CD1c+ dendritic cell frequency predicts progression-free survival. Clin Cancer Res 2008; 14:5884-92; PMID:18794101; http://dx.doi.org/10.1158/1078-0432.CCR-08-0656
   PubMed Web of Science ®Google Scholar
• Jackaman C, Cornwall S, Graham PT, Nelson DJ. CD40-activated B cells contribute to mesothelioma tumor regression. Immunol Cell Biol 2011; 89:255-67; PMID:20628372; http://dx.doi.org/10.1038/icb.2010.88
   PubMed Web of Science ®Google Scholar
• Jackaman C, Lew AM, Zhan Y, Allan JE, Koloska B, Graham PT, Robinson BW, Nelson DJ. Deliberately provoking local inflammation drives tumors to become their own protective vaccine site. Int Immunol 2008; 20:1467-79; PMID:18824504; http://dx.doi.org/10.1093/intimm/dxn104
   PubMed Web of Science ®Google Scholar
• Jackaman C, Lansley S, Allan JE, Robinson BW, Nelson DJ. IL-2/CD40-driven NK cells install and maintain potency in the anti-mesothelioma effector/memory phase. Int Immunol 2012; 24:357-68; PMID:22354912; http://dx.doi.org/10.1093/intimm/dxs005
   PubMed Web of Science ®Google Scholar
• Broomfield SA, van der Most RG, Prosser AC, Mahendran S, Tovey MG, Smyth MJ, Robinson BW, Currie AJ. Locally administered TLR7 agonists drive systemic antitumor immune responses that are enhanced by anti-CD40 immunotherapy. J Immunol 2009; 182:5217-24; PMID:19380767; http://dx.doi.org/10.4049/jimmunol.0803826
   PubMed Web of Science ®Google Scholar
• McDonnell AM, Lesterhuis WJ, Khong A, Nowak AK, Lake RA, Currie AJ, Robinson BW. Tumor-infiltrating dendritic cells exhibit defective cross-presentation of tumor antigens, but is reversed by chemotherapy. Eur J Immunol 2015; 45:49-59; PMID:25316312; http://dx.doi.org/10.1002/eji.201444722
   PubMed Web of Science ®Google Scholar
• Lesterhuis WJ, Salmons J, Nowak AK, Rozali EN, Khong A, Dick IM, Harken JA, Robinson BW, Lake RA. Synergistic effect of CTLA-4 blockade and cancer chemotherapy in the induction of anti-tumor immunity. PloS one 2013; 8:e61895; PMID:23626745; http://dx.doi.org/10.1371/journal.pone.0061895
   PubMed Web of Science ®Google Scholar
• Nowak AK, Robinson BW, Lake RA. Synergy between chemotherapy and immunotherapy in the treatment of established murine solid tumors. Cancer Res 2003; 63:4490-6; PMID:12907622
   PubMed Web of Science ®Google Scholar
• Broomfield S, Currie A, van der Most RG, Brown M, van Bruggen I, Robinson BW, Lake RA. Partial, but not complete, tumor-debulking surgery promotes protective antitumor memory when combined with chemotherapy and adjuvant immunotherapy. Cancer Res 2005; 65:7580-4; PMID:16140921; http://dx.doi.org/10.1158/0008-5472.CAN-05-0328
   PubMed Web of Science ®Google Scholar
• Khong A, Cleaver AL, Fahmi Alatas M, Wylie BC, Connor T, Fisher SA, Broomfield S, Lesterhuis WJ, Currie AJ, Lake RA et al. The efficacy of tumor debulking surgery is improved by adjuvant immunotherapy using imiquimod and anti-CD40. BMC Cancer 2014; 14:969; PMID:25518732; http://dx.doi.org/10.1186/1471-2407-14-969
   PubMed Web of Science ®Google Scholar
• Alley EW, Molife LR, Santoro A, Beckey K, Yuan S, Cheng JD, Piperdi B, Schellens JHM. Clinical safety and efficacy of pembrolizumab (MK-3475) in patients with malignant pleural mesothelioma: Preliminary results from KEYNOTE-028 American Association for Cancer Research conference abstract number CT103 2015
   Google Scholar
• Stumbles PA, Himbeck R, Frelinger JA, Collins EJ, Lake RA, Robinson BW. Cutting edge: tumor-specific CTL are constitutively cross-armed in draining lymph nodes and transiently disseminate to mediate tumor regression following systemic CD40 activation. J Immunol 2004; 173:5923-8; PMID:15528325; http://dx.doi.org/10.4049/jimmunol.173.10.5923
   PubMed Web of Science ®Google Scholar
• Homet Moreno B, Parisi G, Robert L, Ribas A. Anti-PD-1 Therapy in Melanoma. Semin Oncol 2015; 42:466-73; PMID:25965365; http://dx.doi.org/10.1053/j.seminoncol.2015.02.008
   PubMed Web of Science ®Google Scholar
• Di Giacomo AM, Danielli R, Guidoboni M, Calabro L, Carlucci D, Miracco C, Volterrani L, Mazzei MA, Biagioli M, Altomonte M et al. Therapeutic efficacy of ipilimumab, an anti-CTLA-4 monoclonal antibody, in patients with metastatic melanoma unresponsive to prior systemic treatments: clinical and immunological evidence from three patient cases. Cancer Immunol Immunother 2009; 58:1297-306; PMID:19139884; http://dx.doi.org/10.1007/s00262-008-0642-y
   PubMed Web of Science ®Google Scholar
• Ott PA, Hodi FS, Robert C. CTLA-4 and PD-1/PD-L1 blockade: new immunotherapeutic modalities with durable clinical benefit in melanoma patients. Clin Cancer Res 2013; 19:5300-9; PMID:24089443; http://dx.doi.org/10.1158/1078-0432.CCR-13-0143
   PubMed Web of Science ®Google Scholar
• Cannizzo ES, Clement CC, Morozova K, Valdor R, Kaushik S, Almeida LN, Follo C, Sahu R, Cuervo AM, Macian F et al. Age-related oxidative stress compromises endosomal proteostasis. Cell Rep 2012; 2:136-49; PMID:22840404; http://dx.doi.org/10.1016/j.celrep.2012.06.005
   PubMed Web of Science ®Google Scholar
• Whiteside TL, Stanson J, Shurin MR, Ferrone S. Antigen-processing machinery in human dendritic cells: up-regulation by maturation and down-regulation by tumor cells. J Immunol 2004; 173:1526-34; PMID:15265880; http://dx.doi.org/10.4049/jimmunol.173.3.1526
   PubMed Web of Science ®Google Scholar
• Onishi H, Morisaki T, Baba E, Kuga H, Kuroki H, Matsumoto K, Tanaka M, Katano M. Dysfunctional and short-lived subsets in monocyte-derived dendritic cells from patients with advanced cancer. Clin Immunol 2002; 105:286-95; PMID:12498810; http://dx.doi.org/10.1006/clim.2002.5293
   PubMed Web of Science ®Google Scholar
• Gabrilovich DI, Corak J, Ciernik IF, Kavanaugh D, Carbone DP. Decreased antigen presentation by dendritic cells in patients with breast cancer. Clin Cancer Res 1997; 3:483-90; PMID:9815709.
   PubMed Web of Science ®Google Scholar
• Shortman K, Liu YJ. Mouse and human dendritic cell subtypes. Nat Rev Immunol 2002; 2:151-61; PMID:11913066; http://dx.doi.org/10.1038/nri746
   PubMed Web of Science ®Google Scholar
• Fricke I, Mirza N, Dupont J, Lockhart C, Jackson A, Lee JH, Sosman JA, Gabrilovich DI. Vascular endothelial growth factor-trap overcomes defects in dendritic cell differentiation but does not improve antigen-specific immune responses. Clin Cancer Res 2007; 13:4840-8; PMID:17699863; http://dx.doi.org/10.1158/1078-0432.CCR-07-0409
   PubMed Web of Science ®Google Scholar
• Helft J, Bottcher J, Chakravarty P, Zelenay S, Huotari J, Schraml BU, Goubau D, Reis E Sousa C. GM-CSF Mouse Bone Marrow Cultures Comprise a Heterogeneous Population of CD11c(+)MHCII(+) Macrophages and Dendritic Cells. Immunity 2015; 42:1197-211; PMID:26084029; http://dx.doi.org/10.1016/j.immuni.2015.05.018
   PubMed Web of Science ®Google Scholar
• Sterman DH, Recio A, Carroll RG, Gillespie CT, Haas A, Vachani A, Kapoor V, Sun J, Hodinka R, Brown JL et al. A phase I clinical trial of single-dose intrapleural IFN-beta gene transfer for malignant pleural mesothelioma and metastatic pleural effusions: high rate of antitumor immune responses. Clin Cancer Res 2007; 13:4456-66; PMID:17671130; http://dx.doi.org/10.1158/1078-0432.CCR-07-0403
   PubMed Web of Science ®Google Scholar
• Khong A, Nelson DJ, Nowak AK, Lake RA, Robinson BW. The use of agonistic anti-CD40 therapy in treatments for cancer. Int Rev Immunol 2012; 31:246-66; PMID:22804570; http://dx.doi.org/10.3109/08830185.2012.698338
   PubMed Web of Science ®Google Scholar
• Lages CS, Lewkowich I, Sproles A, Wills-Karp M, Chougnet C. Partial restoration of T-cell function in aged mice by in vitro blockade of the PD-1/ PD-L1 pathway. Aging cell 2010; 9:785-98; PMID:20653631; http://dx.doi.org/10.1111/j.1474-9726.2010.00611.x
   PubMed Web of Science ®Google Scholar
• Calabro L, Morra A, Fonsatti E, Cutaia O, Amato G, Giannarelli D, Di Giacomo AM, Danielli R, Altomonte M, Mutti L et al. Tremelimumab for patients with chemotherapy-resistant advanced malignant mesothelioma: an open-label, single-arm, phase 2 trial. Lancet Oncol 2013; 14:1104-11; PMID:24035405; http://dx.doi.org/10.1016/S1470-2045(13)70381-4
   PubMed Web of Science ®Google Scholar
• Romani N, Gruner S, Brang D, Kampgen E, Lenz A, Trockenbacher B, Konwalinka G, Fritsch PO, Steinman RM, Schuler G. Proliferating dendritic cell progenitors in human blood. J Exp Med 1994; 180:83-93; PMID:8006603; http://dx.doi.org/10.1084/jem.180.1.83
   PubMed Web of Science ®Google Scholar
• Nelson D, Bundell C, Robinson B. In vivo cross-presentation of a soluble protein antigen: kinetics, distribution, and generation of effector CTL recognizing dominant and subdominant epitopes. J Immunol 2000; 165:6123-32; PMID:11086045; http://dx.doi.org/10.4049/jimmunol.165.11.6123
   PubMed Web of Science ®Google Scholar