Administration of a vasoactive intestinal peptide antagonist enhances the autologous anti-leukemia T cell response in murine models of acute leukemia

References

• Kohrt HE, Tumeh PC, Benson D, Bhardwaj N, Brody J, Formenti S, Fox BA, Galon J, June CH, Kalos M et al. Immunodynamics: a cancer immunotherapy trials network review of immune monitoring in immuno-oncology clinical trials. J Immunother Cancer 2016; 4:15; PMID: 26981245; https://doi.org/10.1186/s40425-016-0118-0
   PubMed Web of Science ®Google Scholar
• Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363(8):711-23; PMID: 20525992; https://doi.org/10.1056/NEJMoa1003466
   PubMed Web of Science ®Google Scholar
• Lichtman MA Battling the hematological malignancies: the 200 years' war. Oncologist 2008; 13(2):126-38; PMID: 18305057; https://doi.org/10.1634/theoncologist.2007-0228
   PubMed Web of Science ®Google Scholar
• Li JM, Hossain MS, Southerland L, Waller EK. Pharmacological inhibition of VIP signaling enhances antiviral immunity and improves survival in murine cytomegalovirus-infected allogeneic bone marrow transplant recipients. Blood 2013; 121(12):2347-51; PMID: 23325838; https://doi.org/10.1182/blood-2012-06-437640
   PubMed Web of Science ®Google Scholar
• Li JM, Darlak KA, Southerland L, Hossain MS, Jaye DL, Josephson CD, Rosenthal H, Waller EK. VIPhyb, an antagonist of vasoactive intestinal peptide receptor, enhances cellular antiviral immunity in murine cytomegalovirus infected mice. PLoS One 2013; 8(5):e63381; PMID: 23723978; https://doi.org/10.1371/journal.pone.0063381
   PubMed Web of Science ®Google Scholar
• Delgado M, Pozo D, Ganea D. The significance of vasoactive intestinal peptide in immunomodulation. Pharmacol Rev 2004; 56(2):249-90; PMID: 15169929; https://doi.org/10.1124/pr.56.2.7
   PubMed Web of Science ®Google Scholar
• Said SI, Mutt V. Polypeptide with broad biological activity: isolation from small intestine. Science 1970; 169(3951):1217-8; PMID: 5450698; https://doi.org/10.1126/science.169.3951.1217
   PubMed Web of Science ®Google Scholar
• Delgado M, Ganea D. Vasoactive intestinal peptide: a neuropeptide with pleiotropic immune functions. Amino Acids 2013; 45(1):rr25-39; PMID:22139413; https://doi.org/10.1007/s00726-011-1184-8
   PubMed Web of Science ®Google Scholar
• Hermann RJ, Van der Steen T, Vomhof-Dekrey EE, Al-Badrani S, Wanjara SB, Failing JJ, Haring JS, Dorsam GP. Characterization and use of a rabbit-anti-mouse VPAC1 antibody by flow cytometry. J Immunol Methods 2012; 376(1-2):20-31; PMID: 22079255; https://doi.org/10.1016/j.jim.2011.10.009
   PubMed Web of Science ®Google Scholar
• Metwali A, Blum AM, Li J, Elliott DE, Weinstock JV IL-4 regulates VIP receptor subtype 2 mRNA (VPAC2) expression in T cells in murine schistosomiasis. FASEB J 2000; 14(7):948-54. PMID: 10783149; https://doi.org/10.1096/fj.1530-6860
   PubMed Web of Science ®Google Scholar
• Lara-Marquez M, O'Dorisio M, O'Dorisio T, Shah M, Karacay B. Selective gene expression and activation-dependent regulation of vasoactive intestinal peptide receptor type 1 and type 2 in human T cells. J Immunol 2001; 166(4):2522-30; PMID: 11160313; https://doi.org/10.4049/jimmunol.166.4.2522
   PubMed Web of Science ®Google Scholar
• Chorny A, Gonzalez-Rey E, Varela N, Robledo G, Delgado M. Signaling mechanisms of vasoactive intestinal peptide in inflammatory conditions. Regul Pept 2006; 137(1-2):67-74; PMID: 16949684; https://doi.org/10.1016/j.regpep.2006.04.021
   PubMedGoogle Scholar
• Varela N, Chorny A, Gonzalez-Rey E, Delgado M. Tuning inflammation with anti-inflammatory neuropeptides. Expert Opin Biol Ther 2007; 7(4):461-78; PMID: 17373898; https://doi.org/10.1517/14712598.7.4.461
   PubMed Web of Science ®Google Scholar
• Delgado M, Leceta J, Gomariz RP, Ganea D. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide stimulate the induction of Th2 responses by up-regulating B7.2 expression. J Immunol 1999; 163(7):3629-35. PMID: 10490956.
   PubMed Web of Science ®Google Scholar
• Delgado M, Reduta A, Sharma V, Ganea D. VIP/PACAP oppositely affects immature and mature dendritic cell expression of CD80/CD86 and the stimulatory activity for CD4(+) T cells. J Leukoc Biol 2004; 75(6):1122-30; PMID: 15020654; https://doi.org/10.1189/jlb.1203626
   PubMed Web of Science ®Google Scholar
• Delgado M, Chorny A, Gonzalez-Rey E, Ganea D. Vasoactive intestinal peptide generates CD4+CD25+ regulatory T cells in vivo. J Leukoc Biol 2005; 78(6):1327-38; PMID: 16204628; https://doi.org/10.1189/jlb.0605299
   PubMed Web of Science ®Google Scholar
• Anderson P, Gonzalez-Rey E. Vasoactive intestinal peptide induces cell cycle arrest and regulatory functions in human T cells at multiple levels. Mol Cell Biol 2010; 30(10):2537-51; PMID: 20231362; https://doi.org/10.1128/MCB.01282-09
   PubMed Web of Science ®Google Scholar
• Gonzalez-Rey E, Chorny A, Fernandez-Martin A, Ganea D, Delgado M. Vasoactive intestinal peptide generates human tolerogenic dendritic cells that induce CD4 and CD8 regulatory T cells. Blood 2006; 107(9):3632-8; PMID: 16397128; https://doi.org/10.1182/blood-2005-11-4497
   PubMed Web of Science ®Google Scholar
• Boudard F, Bastide M, Inhibition of mouse T-cell proliferation by CGRP and VIP: effects of these neuropeptides on IL-2 production and cAMP synthesis. J Neurosci Res 1991; 29(1):29-41; PMID: 1653367; https://doi.org/10.1002/jnr.490290104
   PubMed Web of Science ®Google Scholar
• Colwell CS, Michel S, Itri J, Rodriguez W, Tam J, Lelievre V, Hu Z, Liu X, Waschek JA. Disrupted circadian rhythms in VIP- and PHI-deficient mice. Am J Physiol Regul Integr Comp Physiol 2003; 285(5):R939-49; PMID: 12855416; https://doi.org/10.1152/ajpregu.00200.2003
   PubMed Web of Science ®Google Scholar
• Taylor PA, Ehrhardt MJ, Lees CJ, Tolar J, Weigel BJ, Panoskaltsis-Mortari A, Serody JS, Brinkmann V, Blazar BR. Insights into the mechanism of FTY720 and compatibility with regulatory T cells for the inhibition of graft-versus-host disease (GVHD). Blood 2007; 110(9):3480-8; PMID: 17606761; https://doi.org/10.1182/blood-2007-05-087940
   PubMed Web of Science ®Google Scholar
• Lu Y, Giver CR, Sharma A, Li JM, Darlak KA, Owens LM, Roback JD, Galipeau J, Waller EK. IFN-γ and indoleamine 2,3-dioxygenase signaling between donor dendritic cells and T cells regulates graft versus host and graft versus leukemia activity. Blood 2012; 119(4):1075-85; PMID: 22130799; https://doi.org/10.1182/blood-2010-12-322891
   PubMed Web of Science ®Google Scholar
• Zhang L, Gajewski TF, Kline J, PD-1/PD-L1 interactions inhibit antitumor immune responses in a murine acute myeloid leukemia model. Blood 2009; 114(8):1545-52; PMID: 19417208; https://doi.org/10.1182/blood-2009-03-206672
   PubMed Web of Science ®Google Scholar
• Gonzalez-Rey E, Fernandez-Martin A, Chorny A, Martin J, Pozo D, Ganea D, Delgado M. Therapeutic effect of vasoactive intestinal peptide on experimental autoimmune encephalomyelitis: down-regulation of inflammatory and autoimmune responses. Am J Pathol 2006; 168(4):1179-88; PMID: 16565493; https://doi.org/10.2353/ajpath.2006.051081
   PubMed Web of Science ®Google Scholar
• Li JM et al. Modulation of immune checkpoints and graft-versus-leukemia in allogeneic transplants by vasoactive intestinal peptide. Cancer Res, 2016.
   Web of Science ®Google Scholar
• Mussai F, De Santo C, Abu-Dayyeh I, Booth S, Quek L, McEwen-Smith RM, Qureshi A, Dazzi F, Vyas P, Cerundolo V. Acute myeloid leukemia creates an arginase-dependent immunosuppressive microenvironment. Blood 2013; 122(5):749-58; PMID: 23733335; https://doi.org/10.1182/blood-2013-01-480129
   PubMed Web of Science ®Google Scholar
• Hadrup S, Donia M, Thor Straten P. Effector CD4 and CD8 T cells and their role in the tumor microenvironment. Cancer Microenviron 2013; 6(2):123-33; PMID: 23242673; https://doi.org/10.1007/s12307-012-0127-6
   PubMedGoogle Scholar
• Schulz S, Mann A, Novakhov B, Piggins HD, Lupp A. VPAC2 receptor expression in human normal and neoplastic tissues: evaluation of the novel MAB SP235. Endocr Connect 2015; 4(1):18-26; PMID: 25504760; https://doi.org/10.1530/EC-14-0051
   PubMed Web of Science ®Google Scholar
• Dorsam GP, Benton K, Failing J, Batra S. Vasoactive intestinal peptide signaling axis in human leukemia. World J Biol Chem, 2011; 2(6):146-60; PMID: 21765981; https://doi.org/10.4331/wjbc.v2.i6.146
   PubMedGoogle Scholar
• Moody TW, Zia F, Draoui M, Brenneman DE, Fridkin M, Davidson A, Gozes I. A vasoactive intestinal peptide antagonist inhibits non-small cell lung cancer growth. Proc Natl Acad Sci U S A 1993; 90(10):4345-9; PMID: 8389448; https://doi.org/10.1073/pnas.90.10.4345
   PubMed Web of Science ®Google Scholar
• Sharma A, Walters J, Gozes Y, Fridkin M, Brenneman D, Gozes I, Moody TW. A vasoactive intestinal peptide antagonist inhibits the growth of glioblastoma cells. J Mol Neurosci 2001; 17(3):331-9; PMID: 11859929; https://doi.org/10.1385/JMN:17:3:331
   PubMed Web of Science ®Google Scholar
• Wen AY, Sakamoto KM, Miller LS. The role of the transcription factor CREB in immune function. J Immunol 2010; 185(11):6413-9; PMID: 21084670; https://doi.org/10.4049/jimmunol.1001829
   PubMed Web of Science ®Google Scholar
• Parry GC, Mackman N. Role of cyclic AMP response element-binding protein in cyclic AMP inhibition of NF-kappaB-mediated transcription. J Immunol 1997; 159(11):5450-6. PMID: 9548485; https://doi.org/10.1074/jbc.271.34.20828
   PubMed Web of Science ®Google Scholar
• Ollivier V, Parry GC, Cobb RR, de Prost D, Mackman N. Elevated cyclic AMP inhibits NF-kappaB-mediated transcription in human monocytic cells and endothelial cells. J Biol Chem 1996; 271(34):20828-35; PMID: 8702838; https://doi.org/10.1074/jbc.271.34.20828
   PubMed Web of Science ®Google Scholar
• Martinez C, Delgado M, Abad C, Gomariz RP, Ganea D, Leceta J. Regulation of VIP production and secretion by murine lymphocytes. J Neuroimmunol 1999; 93(1-2):126-38; PMID: 10378876; https://doi.org/10.1016/S0165-5728(98)00216-1
   PubMed Web of Science ®Google Scholar
• Kong Y, Zhang J, Claxton DF, Ehmann WC, Rybka WB, Zhu L, Zeng H, Schell TD, Zheng H. PD-1(hi)TIM-3(+) T cells associate with and predict leukemia relapse in AML patients post allogeneic stem cell transplantation. Blood Cancer J 2015; 5:e330; PMID: 26230954; https://doi.org/10.1038/bcj.2015.58
   PubMed Web of Science ®Google Scholar
• Sehgal A, Whiteside TL, Boyiadzis M, Programmed death-1 checkpoint blockade in acute myeloid leukemia. Expert Opin Biol Ther 2015; 15(8):1191-203; PMID: 26036819; https://doi.org/10.1517/14712598.2015.1051028
   PubMed Web of Science ®Google Scholar
• Krupka C, Kufer P, Kischel R, Zugmaier G, Lichtenegger FS, Köhnke T, Vick B, Jeremias I, Metzeler KH, Altmann T et al. Blockade of the PD-1/PD-L1 axis augments lysis of AML cells by the CD33/CD3 BiTE antibody construct AMG 330: reversing a T-cell-induced immune escape mechanism. Leukemia 2016; 30(2):484-91; PMID: 26239198; https://doi.org/10.1038/leu.2015.214
   PubMed Web of Science ®Google Scholar
• Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, Sharpe AH, Freeman GJ, Ahmed R. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006; 439(7077):682-7; PMID: 16382236; https://doi.org/10.1038/nature04444
   PubMed Web of Science ®Google Scholar
• Mittal D, Young A, Stannard K, Yong M, Teng MW, Allard B, Stagg J, Smyth MJ. Antimetastatic effects of blocking PD-1 and the adenosine A2A receptor. Cancer Res 2014; 74(14):3652-8; PMID: 24986517; https://doi.org/10.1158/0008-5472.CAN-14-0957
   PubMed Web of Science ®Google Scholar