Journal Article
. 2009 Sep; 69(19):7747-55.
doi: 10.1158/0008-5472.CAN-08-3289.

Tumor vaccines expressing flt3 ligand synergize with ctla-4 blockade to reject preimplanted tumors

Michael A Curran 1 James P Allison  
  • PMID: 19738077
  •     43 References
  •     71 citations


The transformation of a healthy cell into a malignant neoplasm involves numerous genetic mutations and aberrations in gene expression. As few of these changes are shared between individuals or types of cancer, the best source for eliciting broad-spectrum tumor immunity remains each patient's own tumor. Previously, we have shown that combining blockade of the T-cell-negative costimulatory molecule CTL-associated antigen 4 (CTLA-4) and vaccination with irradiated B16 tumor expressing granulocyte macrophage colony-stimulating factor (GM-CSF; Gvax) promotes rejection of established murine melanomas. Here we show that, like GM-CSF, the cytokine Flt3 ligand (Flt3L) expressed in B16 and coupled with CTLA-4 blockade promotes both prophylactic and therapeutic rejection of B16. When administered at the site of growing tumor, Gvax fails to prevent tumor outgrowth in any mice, whereas the B16-Flt3L vaccine (Fl3vax) induces the rejection of 75% of melanomas implanted 3 days before vaccination. Relative to Gvax, Fl3vax promotes greater infiltration of both the vaccine site and the tumor site by CD8+ T cells and "sentinel" and plasmacytoid dendritic cells. Gvax and Fl3vax did not synergize when used in combination in treating B16 melanoma even in the context of CD25+ regulatory T-cell depletion. Further, we show that a combination of Flt3L expression and CTLA-4 blockade can also promote the rejection of established TRAMP prostate adenocarcinomas, proving that the utility of this treatment extends beyond melanoma. Engineering Flt3L to be constitutively secreted and attaching an IgG2a tail yielded a B16 vaccine that, when combined with CTLA-4 blockade, prevented the outgrowth of significantly more 5-day implanted B16-BL6 tumors than did Gvax.

Manipulation of T cell costimulatory and inhibitory signals for immunotherapy of prostate cancer.
E D Kwon, A A Hurwitz, +5 authors, J P Allison.
Proc Natl Acad Sci U S A, 1997 Jul 22; 94(15). PMID: 9223321    Free PMC article.
Highly Cited.
FLT3: receptor and ligand. Biology and potential clinical application.
M R Shurin, C Esche, M T Lotze.
Cytokine Growth Factor Rev, 1998 Aug 28; 9(1). PMID: 9720755
Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified.
E Maraskovsky, K Brasel, +4 authors, H J McKenna.
J Exp Med, 1996 Nov 01; 184(5). PMID: 8920882    Free PMC article.
Highly Cited.
The CXCR3 targeting chemokine CXCL11 has potent antitumor activity in vivo involving attraction of CD8+ T lymphocytes but not inhibition of angiogenesis.
Paul J Hensbergen, Pepijn G J T B Wijnands, +3 authors, Cornelis P Tensen.
J Immunother, 2005 Jul 08; 28(4). PMID: 16000952
The IP-10 chemokine binds to a specific cell surface heparan sulfate site shared with platelet factor 4 and inhibits endothelial cell proliferation.
A D Luster, S M Greenberg, P Leder.
J Exp Med, 1995 Jul 01; 182(1). PMID: 7790818    Free PMC article.
Highly Cited.
Principles and use of anti-CTLA4 antibody in human cancer immunotherapy.
Karl S Peggs, Sergio A Quezada, Alan J Korman, James P Allison.
Curr Opin Immunol, 2006 Feb 09; 18(2). PMID: 16464564
Highly Cited. Review.
Intrinsic ability of GM+IL-4 but not Flt3L-induced rat dendritic cells to promote allogeneic T cell hyporesponsiveness.
Aurele Taieb, Jeremy J Breitinger, +5 authors, Maryam Feili-Hariri.
Clin Immunol, 2007 Feb 06; 123(2). PMID: 17276735
Migration of dendritic cells in response to formyl peptides, C5a, and a distinct set of chemokines.
S Sozzani, F Sallusto, +7 authors, A Mantovani.
J Immunol, 1995 Oct 01; 155(7). PMID: 7561021
GM-CSF-based cellular vaccines: a review of the clinical experience.
Ivan Borrello, Drew Pardoll.
Cytokine Growth Factor Rev, 2002 Mar 20; 13(2). PMID: 11900993
Induction of natural killer cell migration by monocyte chemotactic protein-1, -2 and -3.
P Allavena, G Bianchi, +4 authors, A Mantovani.
Eur J Immunol, 1994 Dec 01; 24(12). PMID: 7805752
Flt-3 ligand: a potent dendritic cell stimulator and novel antitumor agent.
Jian Dong, Christopher M McPherson, Peter J Stambrook.
Cancer Biol Ther, 2002 Dec 24; 1(5). PMID: 12496473
Enhancement of antitumor immunity by CTLA-4 blockade.
D R Leach, M F Krummel, J P Allison.
Science, 1996 Mar 22; 271(5256). PMID: 8596936
Highly Cited.
Combination immunotherapy of primary prostate cancer in a transgenic mouse model using CTLA-4 blockade.
A A Hurwitz, B A Foster, +5 authors, J P Allison.
Cancer Res, 2000 May 16; 60(9). PMID: 10811122
Highly Cited.
Elucidating the autoimmune and antitumor effector mechanisms of a treatment based on cytotoxic T lymphocyte antigen-4 blockade in combination with a B16 melanoma vaccine: comparison of prophylaxis and therapy.
A van Elsas, R P Sutmuller, +8 authors, J P Allison.
J Exp Med, 2001 Aug 22; 194(4). PMID: 11514604    Free PMC article.
MFG-E8-mediated uptake of apoptotic cells by APCs links the pro- and antiinflammatory activities of GM-CSF.
Masahisa Jinushi, Yukoh Nakazaki, +3 authors, Glenn Dranoff.
J Clin Invest, 2007 Jun 09; 117(7). PMID: 17557120    Free PMC article.
MCP-3 (CCL7) delivered by parvovirus MVMp reduces tumorigenicity of mouse melanoma cells through activation of T lymphocytes and NK cells.
Kristiane Wetzel, Sofie Struyf, +6 authors, Christiane Dinsart.
Int J Cancer, 2006 Dec 13; 120(6). PMID: 17154174
GM-CSF-secreting melanoma vaccines.
Glenn Dranoff.
Oncogene, 2003 Jun 06; 22(20). PMID: 12789295
IP-10, a -C-X-C- chemokine, elicits a potent thymus-dependent antitumor response in vivo.
A D Luster, P Leder.
J Exp Med, 1993 Sep 01; 178(3). PMID: 8350046    Free PMC article.
Highly Cited.
Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model.
B A Foster, J R Gingrich, +2 authors, N M Greenberg.
Cancer Res, 1997 Aug 15; 57(16). PMID: 9269988
Highly Cited.
Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation.
A van Elsas, A A Hurwitz, J P Allison.
J Exp Med, 1999 Aug 03; 190(3). PMID: 10430624    Free PMC article.
Highly Cited.
Flt3 in regulation of type I interferon-producing cell and dendritic cell development.
Nobuyuki Onai, Aya Obata-Onai, Michael A Schmid, Markus G Manz.
Ann N Y Acad Sci, 2007 Mar 16; 1106. PMID: 17360795
In vivo cross-priming of MHC class I-restricted antigens requires the TAP transporter.
A Y Huang, A T Bruce, D M Pardoll, H I Levitsky.
Immunity, 1996 Apr 01; 4(4). PMID: 8612129
Antitumor effects of the MIG and IP-10 genes transferred with poly [D,L-2,4-diaminobutyric acid] on murine neuroblastoma.
M Tominaga, Y Iwashita, +6 authors, S Kitano.
Cancer Gene Ther, 2007 May 22; 14(8). PMID: 17514193
Comparison of the functional properties of murine dendritic cells generated in vivo with Flt3 ligand, GM-CSF and Flt3 ligand plus GM-SCF.
Elizabeth Daro, Eric Butz, +3 authors, Hilary J McKenna.
Cytokine, 2002 Mar 16; 17(3). PMID: 11895330
Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma.
Giao Q Phan, James C Yang, +14 authors, Steven A Rosenberg.
Proc Natl Acad Sci U S A, 2003 Jun 27; 100(14). PMID: 12826605    Free PMC article.
Highly Cited.
Monocyte chemotactic proteins MCP-1, MCP-2, and MCP-3 are major attractants for human CD4+ and CD8+ T lymphocytes.
P Loetscher, M Seitz, +2 authors, B Moser.
FASEB J, 1994 Oct 01; 8(13). PMID: 7926371
Granulocyte-macrophage colony-stimulating factor (GM-CSF) and T-cell responses: what we do and don't know.
Yufang Shi, Catherine H Liu, +9 authors, Satish Devadas.
Cell Res, 2006 Feb 14; 16(2). PMID: 16474424
Highly Cited. Review.
Cytotoxic T lymphocyte antigen-4-dependent down-modulation of costimulatory molecules on dendritic cells in CD4+ CD25+ regulatory T-cell-mediated suppression.
Cecilia Oderup, Lukas Cederbom, +2 authors, Fredrik Ivars.
Immunology, 2006 Jun 15; 118(2). PMID: 16771859    Free PMC article.
Differential development of murine dendritic cells by GM-CSF versus Flt3 ligand has implications for inflammation and trafficking.
Yuekang Xu, Yifan Zhan, +2 authors, Michael H Kershaw.
J Immunol, 2007 Nov 21; 179(11). PMID: 18025203
Highly Cited.
Structural and functional identification of two human, tumor-derived monocyte chemotactic proteins (MCP-2 and MCP-3) belonging to the chemokine family.
J Van Damme, P Proost, J P Lenaerts, G Opdenakker.
J Exp Med, 1992 Jul 01; 176(1). PMID: 1613466    Free PMC article.
New strategies for active immunotherapy with genetically engineered tumor cells.
D Pardoll.
Curr Opin Immunol, 1992 Oct 01; 4(5). PMID: 1418729
Targeting rare populations of murine antigen-specific T lymphocytes by retroviral transduction for potential application in gene therapy for autoimmune disease.
G L Costa, J M Benson, +3 authors, G P Nolan.
J Immunol, 2000 Mar 22; 164(7). PMID: 10725713
Differences in dendritic cells stimulated in vivo by tumors engineered to secrete granulocyte-macrophage colony-stimulating factor or Flt3-ligand.
N Mach, S Gillessen, +3 authors, G Dranoff.
Cancer Res, 2000 Jun 24; 60(12). PMID: 10866317
Highly Cited.
Episomal vectors rapidly and stably produce high-titer recombinant retrovirus.
T M Kinsella, G P Nolan.
Hum Gene Ther, 1996 Aug 01; 7(12). PMID: 8844199
Highly Cited.
Combinational FLt3 ligand and granulocyte macrophage colony-stimulating factor treatment promotes enhanced tumor infiltration by dendritic cells and antitumor CD8(+) T-cell cross-priming but is ineffective as a therapy.
Aklile Berhanu, Jian Huang, +2 authors, Walter J Storkus.
Cancer Res, 2006 May 03; 66(9). PMID: 16651446
Enhanced induction of antitumor T-cell responses by cytotoxic T lymphocyte-associated molecule-4 blockade: the effect is manifested only at the restricted tumor-bearing stages.
Y F Yang, J P Zou, +6 authors, T Hamaoka.
Cancer Res, 1997 Oct 27; 57(18). PMID: 9307290
CXCL10-CXCR3 interactions play an important role in the pathogenesis of acute graft-versus-host disease in the skin following allogeneic stem-cell transplantation.
Karen P Piper, Claire Horlock, +5 authors, Paul A H Moss.
Blood, 2007 Sep 04; 110(12). PMID: 17766680
The development of murine plasmacytoid dendritic cell precursors is differentially regulated by FLT3-ligand and granulocyte/macrophage colony-stimulating factor.
Michel Gilliet, Andre Boonstra, +5 authors, Yong-Jun Liu.
J Exp Med, 2002 Apr 03; 195(7). PMID: 11927638    Free PMC article.
Highly Cited.
T cell infiltration and chemokine expression: relevance to the disease localization in murine graft-versus-host disease.
J Y New, B Li, +5 authors, H Z Hu.
Bone Marrow Transplant, 2002 Jul 05; 29(12). PMID: 12098066
Reduced tumorigenicity and augmented leukocyte infiltration after monocyte chemotactic protein-3 (MCP-3) gene transfer: perivascular accumulation of dendritic cells in peritumoral tissue and neutrophil recruitment within the tumor.
F Fioretti, D Fradelizi, +7 authors, A Mantovani.
J Immunol, 1998 Jul 01; 161(1). PMID: 9647242
CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells.
Sergio A Quezada, Karl S Peggs, Michael A Curran, James P Allison.
J Clin Invest, 2006 Jun 17; 116(7). PMID: 16778987    Free PMC article.
Highly Cited.
High-dose granulocyte-macrophage colony-stimulating factor-producing vaccines impair the immune response through the recruitment of myeloid suppressor cells.
Paolo Serafini, Rebecca Carbley, +3 authors, Ivan Borrello.
Cancer Res, 2004 Sep 03; 64(17). PMID: 15342423
Highly Cited.
Mechanisms of suppression by suppressor T cells.
Harald von Boehmer.
Nat Immunol, 2005 Mar 24; 6(4). PMID: 15785759
Highly Cited. Review.
PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors.
Michael A Curran, Welby Montalvo, Hideo Yagita, James P Allison.
Proc Natl Acad Sci U S A, 2010 Feb 18; 107(9). PMID: 20160101    Free PMC article.
Highly Cited.
Features of responding T cells in cancer and chronic infection.
Peter S Kim, Rafi Ahmed.
Curr Opin Immunol, 2010 Mar 09; 22(2). PMID: 20207527    Free PMC article.
Highly Cited. Review.
Development of a syngeneic mouse model of epithelial ovarian cancer.
Bridget A Quinn, Fang Xiao, +4 authors, Denise C Connolly.
J Ovarian Res, 2010 Oct 21; 3. PMID: 20958993    Free PMC article.
Enhancement of dendritic cells as vaccines for cancer.
Meghan E Turnis, Cliona M Rooney.
Immunotherapy, 2010 Nov 26; 2(6). PMID: 21091116    Free PMC article.
Selective expansion of merocytic dendritic cells and CD8DCs confers anti-tumour effect of Fms-like tyrosine kinase 3-ligand treatment in vivo.
C M Hennies, R A Reboulet, +3 authors, E M Janssen.
Clin Exp Immunol, 2011 Jan 18; 163(3). PMID: 21235535    Free PMC article.
Shifting the equilibrium in cancer immunoediting: from tumor tolerance to eradication.
Sergio A Quezada, Karl S Peggs, Tyler R Simpson, James P Allison.
Immunol Rev, 2011 Apr 15; 241(1). PMID: 21488893    Free PMC article.
Highly Cited. Review.
Immunological and clinical effects of vaccines targeting p53-overexpressing malignancies.
R Vermeij, N Leffers, +3 authors, H W Nijman.
J Biomed Biotechnol, 2011 May 05; 2011. PMID: 21541192    Free PMC article.
Combination CTLA-4 blockade and 4-1BB activation enhances tumor rejection by increasing T-cell infiltration, proliferation, and cytokine production.
Michael A Curran, Myoungjoo Kim, +2 authors, James P Allison.
PLoS One, 2011 May 12; 6(4). PMID: 21559358    Free PMC article.
Highly Cited.
Blockade of cytotoxic T-lymphocyte antigen-4 as a new therapeutic approach for advanced melanoma.
Xiang-Yang Wang, Daming Zuo, Devanand Sarkar, Paul B Fisher.
Expert Opin Pharmacother, 2011 Nov 15; 12(17). PMID: 22077831    Free PMC article.
Potent induction of tumor immunity by combining tumor cryoablation with anti-CTLA-4 therapy.
Rebecca Waitz, Stephen B Solomon, +4 authors, James P Allison.
Cancer Res, 2011 Nov 24; 72(2). PMID: 22108823    Free PMC article.
Repertoire enhancement with adoptively transferred female lymphocytes controls the growth of pre-implanted murine prostate cancer.
Robert R Jenq, Michael A Curran, +3 authors, Marcel R M van den Brink.
PLoS One, 2012 Apr 12; 7(4). PMID: 22493742    Free PMC article.
Workshop on immunotherapy combinations. Society for Immunotherapy of Cancer annual meeting Bethesda, November 3, 2011.
Ivan Martinez Forero, Hideho Okada, +3 authors, Ignacio Melero.
J Transl Med, 2012 May 30; 10. PMID: 22640522    Free PMC article.
Expression of FMS-like tyrosine kinase 3 ligand by oncolytic herpes simplex virus type I prolongs survival in mice bearing established syngeneic intracranial malignant glioma.
Zachary Barnard, Hiroaki Wakimoto, +5 authors, William T Curry.
Neurosurgery, 2012 Jun 02; 71(3). PMID: 22653387    Free PMC article.
CTLA-4 blockade synergizes with cryoablation to mediate tumor rejection.
Rebecca Waitz, Marcella Fassò, James P Allison.
Oncoimmunology, 2012 Jul 04; 1(4). PMID: 22754781    Free PMC article.
Gene therapy-mediated reprogramming tumor infiltrating T cells using IL-2 and inhibiting NF-κB signaling improves the efficacy of immunotherapy in a brain cancer model.
Yohei Mineharu, A K M Ghulam Muhammad, +12 authors, Maria G Castro.
Neurotherapeutics, 2012 Sep 22; 9(4). PMID: 22996231    Free PMC article.
Human prostate tumor antigen-specific CD8+ regulatory T cells are inhibited by CTLA-4 or IL-35 blockade.
Brian M Olson, Ewa Jankowska-Gan, +3 authors, Douglas G McNeel.
J Immunol, 2012 Nov 16; 189(12). PMID: 23152566    Free PMC article.
Suppression, subversion and escape: the role of regulatory T cells in cancer progression.
K Oleinika, R J Nibbs, G J Graham, A R Fraser.
Clin Exp Immunol, 2012 Dec 04; 171(1). PMID: 23199321    Free PMC article.
Immunomodulatory therapy for melanoma: ipilimumab and beyond.
Margaret K Callahan, Michael A Postow, Jedd D Wolchok.
Clin Dermatol, 2013 Feb 27; 31(2). PMID: 23438382    Free PMC article.
CD8+ T cell exhaustion during persistent viral infection is regulated independently of the virus-specific T cell receptor.
Stephanie R Jackson, Melissa M Berrien-Elliott, +2 authors, Ryan M Teague.
Immunol Invest, 2013 Mar 07; 42(3). PMID: 23461613    Free PMC article.
Systemic 4-1BB activation induces a novel T cell phenotype driven by high expression of Eomesodermin.
Michael A Curran, Theresa L Geiger, +5 authors, James P Allison.
J Exp Med, 2013 Apr 03; 210(4). PMID: 23547098    Free PMC article.
Highly Cited.
Indoleamine 2,3-dioxygenase is a critical resistance mechanism in antitumor T cell immunotherapy targeting CTLA-4.
Rikke B Holmgaard, Dmitriy Zamarin, +2 authors, James P Allison.
J Exp Med, 2013 Jun 12; 210(7). PMID: 23752227    Free PMC article.
Highly Cited.
Therapeutic cancer vaccines: past, present, and future.
Chunqing Guo, Masoud H Manjili, +3 authors, Xiang-Yang Wang.
Adv Cancer Res, 2013 Jul 23; 119. PMID: 23870514    Free PMC article.
Highly Cited. Review.
A characterization of four B16 murine melanoma cell sublines molecular fingerprint and proliferation behavior.
Corina Danciu, Alexandra Falamas, +6 authors, Melania F Munteanu.
Cancer Cell Int, 2013 Jul 31; 13. PMID: 23890195    Free PMC article.
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.
Dendritic cell-specific delivery of Flt3L by coronavirus vectors secures induction of therapeutic antitumor immunity.
Christian Perez-Shibayama, Cristina Gil-Cruz, +4 authors, Burkhard Ludewig.
PLoS One, 2013 Dec 07; 8(11). PMID: 24312302    Free PMC article.
Engagement of the ICOS pathway markedly enhances efficacy of CTLA-4 blockade in cancer immunotherapy.
Xiaozhou Fan, Sergio A Quezada, +2 authors, James P Allison.
J Exp Med, 2014 Apr 02; 211(4). PMID: 24687957    Free PMC article.
Highly Cited.
VISTA Regulates the Development of Protective Antitumor Immunity.
Isabelle Le Mercier, Wenna Chen, +5 authors, Li Wang.
Cancer Res, 2014 Apr 03; 74(7). PMID: 24691994    Free PMC article.
Highly Cited.
Parasite fate and involvement of infected cells in the induction of CD4+ and CD8+ T cell responses to Toxoplasma gondii.
Christopher D Dupont, David A Christian, +9 authors, Christopher A Hunter.
PLoS Pathog, 2014 Apr 12; 10(4). PMID: 24722202    Free PMC article.
Combined targeting of costimulatory (OX40) and coinhibitory (CTLA-4) pathways elicits potent effector T cells capable of driving robust antitumor immunity.
William L Redmond, Stefanie N Linch, Melissa J Kasiewicz.
Cancer Immunol Res, 2014 Apr 30; 2(2). PMID: 24778278    Free PMC article.
Going viral with cancer immunotherapy.
Brian D Lichty, Caroline J Breitbach, David F Stojdl, John C Bell.
Nat Rev Cancer, 2014 Jul 06; 14(8). PMID: 24990523
Highly Cited. Review.
Trial watch: Immunostimulatory cytokines in cancer therapy.
Erika Vacchelli, Fernando Aranda, +6 authors, Lorenzo Galluzzi.
Oncoimmunology, 2014 Aug 02; 3. PMID: 25083328    Free PMC article.
Trial Watch: Toll-like receptor agonists in oncological indications.
Fernando Aranda, Erika Vacchelli, +8 authors, Lorenzo Galluzzi.
Oncoimmunology, 2014 Aug 02; 3. PMID: 25083332    Free PMC article.
Dissecting the tumor myeloid compartment reveals rare activating antigen-presenting cells critical for T cell immunity.
Miranda L Broz, Mikhail Binnewies, +12 authors, Matthew F Krummel.
Cancer Cell, 2014 Dec 03; 26(5). PMID: 25446897    Free PMC article.
Highly Cited.
Behaviour of four different B16 murine melanoma cell sublines: C57BL/6J skin.
Corina Danciu, Camelia Oprean, +5 authors, Cristina Dehelean.
Int J Exp Pathol, 2015 Feb 11; 96(2). PMID: 25664478    Free PMC article.
The emerging understanding of myeloid cells as partners and targets in tumor rejection.
Miranda L Broz, Matthew F Krummel.
Cancer Immunol Res, 2015 Apr 08; 3(4). PMID: 25847968    Free PMC article.
Cancer Immunotherapy with Immunomodulatory Anti-CD137 and Anti-PD-1 Monoclonal Antibodies Requires BATF3-Dependent Dendritic Cells.
Alfonso R Sánchez-Paulete, Francisco J Cueto, +9 authors, Ignacio Melero.
Cancer Discov, 2015 Oct 24; 6(1). PMID: 26493961    Free PMC article.
Highly Cited.
Leveraging immunotherapy for the treatment of gynecologic cancers in the era of precision medicine.
Dmitriy Zamarin, Amir A Jazaeri.
Gynecol Oncol, 2016 Mar 27; 141(1). PMID: 27016233    Free PMC article.
Dendritic Cells Coordinate the Development and Homeostasis of Organ-Specific Regulatory T Cells.
Daniel S Leventhal, Dana C Gilmore, +9 authors, Peter A Savage.
Immunity, 2016 Apr 03; 44(4). PMID: 27037189    Free PMC article.
Immune Checkpoint Therapies in Prostate Cancer.
Sangeeta Goswami, Ana Aparicio, Sumit K Subudhi.
Cancer J, 2016 Apr 26; 22(2). PMID: 27111907    Free PMC article.
Targeting myeloid-derived suppressor cells with colony stimulating factor-1 receptor blockade can reverse immune resistance to immunotherapy in indoleamine 2,3-dioxygenase-expressing tumors.
Rikke B Holmgaard, Dmitriy Zamarin, +2 authors, Jedd D Wolchok.
EBioMedicine, 2016 May 24; 6. PMID: 27211548    Free PMC article.
Highly Cited.
Critical Role for CD103(+)/CD141(+) Dendritic Cells Bearing CCR7 for Tumor Antigen Trafficking and Priming of T Cell Immunity in Melanoma.
Edward W Roberts, Miranda L Broz, +7 authors, Matthew F Krummel.
Cancer Cell, 2016 Jul 19; 30(2). PMID: 27424807    Free PMC article.
Highly Cited.
Is There Still Room for Cancer Vaccines at the Era of Checkpoint Inhibitors.
Soumaya Karaki, Marie Anson, +4 authors, Eric Tartour.
Vaccines (Basel), 2016 Nov 10; 4(4). PMID: 27827885    Free PMC article.
New Combination Strategies Using Programmed Cell Death 1/Programmed Cell Death Ligand 1 Checkpoint Inhibitors as a Backbone.
Siwen Hu-Lieskovan, Antoni Ribas.
Cancer J, 2017 Jan 24; 23(1). PMID: 28114250    Free PMC article.
DNA vaccines for prostate cancer.
Christopher D Zahm, Viswa Teja Colluru, Douglas G McNeel.
Pharmacol Ther, 2017 Feb 12; 174. PMID: 28185916    Free PMC article.
The blood-borne sialyltransferase ST6Gal-1 is a negative systemic regulator of granulopoiesis.
Christopher W L Dougher, Alexander Buffone, +4 authors, Joseph T Y Lau.
J Leukoc Biol, 2017 May 28; 102(2). PMID: 28550122    Free PMC article.
De Novo Epigenetic Programs Inhibit PD-1 Blockade-Mediated T Cell Rejuvenation.
Hazem E Ghoneim, Yiping Fan, +8 authors, Ben Youngblood.
Cell, 2017 Jun 27; 170(1). PMID: 28648661    Free PMC article.
Highly Cited.
Intratumoral STING Activation with T-cell Checkpoint Modulation Generates Systemic Antitumor Immunity.
Casey R Ager, Matthew J Reilley, +3 authors, Michael A Curran.
Cancer Immunol Res, 2017 Jul 05; 5(8). PMID: 28674082    Free PMC article.
Highly Cited.
Synergy of Immune Checkpoint Blockade with a Novel Synthetic Consensus DNA Vaccine Targeting TERT.
Elizabeth K Duperret, Megan C Wise, +8 authors, David B Weiner.
Mol Ther, 2017 Dec 19; 26(2). PMID: 29249395    Free PMC article.
LXR/ApoE Activation Restricts Innate Immune Suppression in Cancer.
Masoud F Tavazoie, Ilana Pollack, +21 authors, Sohail F Tavazoie.
Cell, 2018 Jan 18; 172(4). PMID: 29336888    Free PMC article.
Highly Cited.
Robust Antitumor Responses Result from Local Chemotherapy and CTLA-4 Blockade.
Charlotte E Ariyan, Mary Sue Brady, +19 authors, James P Allison.
Cancer Immunol Res, 2018 Jan 18; 6(2). PMID: 29339377    Free PMC article.
Molecular regulation of dendritic cell development and function in homeostasis, inflammation, and cancer.
Taylor T Chrisikos, Yifan Zhou, +3 authors, Haiyan S Li.
Mol Immunol, 2018 Mar 20; 110. PMID: 29549977    Free PMC article.
The Toll like receptor 4 ligand cold-inducible RNA-binding protein as vaccination platform against cancer.
Lorea Villanueva, Leyre Silva, +9 authors, Pablo Sarobe.
Oncoimmunology, 2018 Apr 11; 7(4). PMID: 29632721    Free PMC article.
Targeted hypoxia reduction restores T cell infiltration and sensitizes prostate cancer to immunotherapy.
Priyamvada Jayaprakash, Midan Ai, +15 authors, Michael A Curran.
J Clin Invest, 2018 Sep 07; 128(11). PMID: 30188869    Free PMC article.
Highly Cited.
TLR9 activation cooperates with T cell checkpoint blockade to regress poorly immunogenic melanoma.
Matthew J Reilley, Brittany Morrow, +3 authors, Michael A Curran.
J Immunother Cancer, 2019 Nov 28; 7(1). PMID: 31771649    Free PMC article.
A Pilot Trial of the Combination of Transgenic NY-ESO-1-reactive Adoptive Cellular Therapy with Dendritic Cell Vaccination with or without Ipilimumab.
Theodore S Nowicki, Beata Berent-Maoz, +18 authors, Antoni Ribas.
Clin Cancer Res, 2018 Dec 24; 25(7). PMID: 30573690    Free PMC article.
Hyperglycemia and T Cell infiltration are associated with stromal and epithelial prostatic hyperplasia in the nonobese diabetic mouse.
LaTayia M Aaron-Brooks, Takeshi Sasaki, +5 authors, Simon W Hayward.
Prostate, 2019 Apr 19; 79(9). PMID: 30999385    Free PMC article.
Intradermal DNA vaccination combined with dual CTLA-4 and PD-1 blockade provides robust tumor immunity in murine melanoma.
Spela Kos, Alessandra Lopes, +6 authors, Gaelle Vandermeulen.
PLoS One, 2019 Jun 01; 14(5). PMID: 31150505    Free PMC article.
Activation of 4-1BB on Liver Myeloid Cells Triggers Hepatitis via an Interleukin-27-Dependent Pathway.
Todd Bartkowiak, Ashvin R Jaiswal, +8 authors, Michael A Curran.
Clin Cancer Res, 2018 Jan 06; 24(5). PMID: 29301830    Free PMC article.
Adjuvant Screen Identifies Synthetic DNA-Encoding Flt3L and CD80 Immunotherapeutics as Candidates for Enhancing Anti-tumor T Cell Responses.
Amy Haseley Thorne, Kirsten N Malo, +8 authors, Laurent Humeau.
Front Immunol, 2020 Mar 13; 11. PMID: 32161596    Free PMC article.
Cross-Presenting XCR1+ Dendritic Cells as Targets for Cancer Immunotherapy.
Katherine M Audsley, Alison M McDonnell, Jason Waithman.
Cells, 2020 Mar 04; 9(3). PMID: 32121071    Free PMC article.
Using Preclinical Data to Design Combination Clinical Trials of Radiation Therapy and Immunotherapy.
Michael J Gough, Shay Sharon, Marka R Crittenden, Kristina H Young.
Semin Radiat Oncol, 2020 May 10; 30(2). PMID: 32381295    Free PMC article.
A guide to cancer immunotherapy: from T cell basic science to clinical practice.
Alex D Waldman, Jill M Fritz, Michael J Lenardo.
Nat Rev Immunol, 2020 May 21; 20(11). PMID: 32433532    Free PMC article.
Safety, immunogenicity, and clinical efficacy of durvalumab in combination with folate receptor alpha vaccine TPIV200 in patients with advanced ovarian cancer: a phase II trial.
Dmitriy Zamarin, Sven Walderich, +16 authors, Jason A Konner.
J Immunother Cancer, 2020 Jun 07; 8(1). PMID: 32503949    Free PMC article.
Cancer systems immunology.
Nathan E Reticker-Flynn, Edgar G Engleman.
Elife, 2020 Jul 14; 9. PMID: 32657757    Free PMC article.
Immunological Targets for Immunotherapy: Inhibitory T Cell Receptors.
Diwakar Davar, Hassane M Zarour.
Methods Mol Biol, 2019 Sep 11; 2055. PMID: 31502146    Free PMC article.
Dendritic Cells and Cancer: From Biology to Therapeutic Intervention.
Ben Wylie, Christophe Macri, Justine D Mintern, Jason Waithman.
Cancers (Basel), 2019 Apr 14; 11(4). PMID: 30979057    Free PMC article.
Melanoma Evolves Complete Immunotherapy Resistance through the Acquisition of a Hypermetabolic Phenotype.
Ashvin R Jaiswal, Arthur J Liu, +17 authors, Michael A Curran.
Cancer Immunol Res, 2020 Sep 13; 8(11). PMID: 32917656    Free PMC article.
Single-cell analyses reveal the clonal and molecular aetiology of Flt3L-induced emergency dendritic cell development.
Dawn S Lin, Luyi Tian, +13 authors, Shalin H Naik.
Nat Cell Biol, 2021 Mar 03; 23(3). PMID: 33649477
The Flt3L/Flt3 Axis in Dendritic Cell Biology and Cancer Immunotherapy.
Francisco J Cueto, David Sancho.
Cancers (Basel), 2021 Apr 04; 13(7). PMID: 33810248    Free PMC article.
Explant Modeling of the Immune Environment of Head and Neck Cancer.
Shay Sharon, Thomas Duhen, +9 authors, Michael Gough.
Front Oncol, 2021 Jul 06; 11. PMID: 34221953    Free PMC article.
Leveraging the Treg-intrinsic CTLA4-PKCη signaling pathway for cancer immunotherapy.
Hsin-Yu Liu, Christophe Pedros, +3 authors, Amnon Altman.
J Immunother Cancer, 2021 Oct 01; 9(9). PMID: 34588224    Free PMC article.