Modulation of immune checkpoints and graft-versus-leukemia in allogeneic transplants by antagonizing vasoactive intestinal peptide signaling

Cancer Research

Volumn 76, Issue 23, 2016, Pages 6802-6815

  Li, Jian Ming ^a   Petersen, Christopher T ^a   Li, Jing Xia ^a,b   Panjwani, Reema ^a   Chandra, Daniel J ^a   Giver, Cynthia R ^a   Blazar, Bruce R ^c   Waller, Edmund K ^a  

^a EMORY UNIVERSITY   (United States)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; PROGRAMMED DEATH 1 RECEPTOR; VASOACTIVE INTESTINAL POLYPEPTIDE;

ALLOGENIC BONE MARROW TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL HOMING; CONTROLLED STUDY; DOWN REGULATION; GRAFT VERSUS LEUKEMIA EFFECT; IMMUNOMODULATION; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T CELL DEPLETION; UPREGULATION; ALLOTRANSPLANTATION; ANIMAL; BONE MARROW TRANSPLANTATION; HUMAN; IMMUNOLOGY; MALE; METABOLISM; PROCEDURES; TRANSPLANTATION CONDITIONING;

ANIMALS; BONE MARROW TRANSPLANTATION; GRAFT VS LEUKEMIA EFFECT; HUMANS; MALE; MICE; SIGNAL TRANSDUCTION; TRANSPLANTATION CONDITIONING; TRANSPLANTATION, HOMOLOGOUS; VASOACTIVE INTESTINAL PEPTIDE;

EID: 85002909444     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-0427     Document Type: Article

References (50)

1. Li JM, Giver CR, Lu Y, Hossain MS, Akhtari M, Waller EK. Separating graft-versus-leukemia from graft-versus-host disease in allogeneic hematopoietic stem cell transplantation. Immunotherapy 2009;1:599-621.
2. Varela N, Chorny A, Gonzalez-Rey E, Delgado M. Tuning inflammation with anti-inflammatory neuropeptides. Expert Opin Biol Ther 2007;7:461-78.
3. Delgado M, Pozo D, Ganea D. The significance of vasoactive intestinal peptide in immunomodulation. Pharmacol Rev 2004;56:249-90.
4. 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;166:2522-30.
5. Harmar AJ, Arimura A, Gozes I, Journot L, Laburthe M, Pisegna JR, et al. International Union of Pharmacology. XVIII. Nomenclature of receptors for vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide. Pharmacol Rev 1998;50:265-70.
6. Chorny A, Gonzalez-Rey E, Varela N, Robledo G, Delgado M. Signaling mechanisms of vasoactive intestinal peptide in inflammatory conditions. Regul Pept 2006;137:67-74.
7. 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;30:2537-51.
8. Delgado M, Chorny A, Gonzalez-Rey E, Ganea D. Vasoactive intestinal peptide generates CD4+CD25+ regulatory T cells in vivo. J Leukoc Biol 2005;78:1327-38.
9. 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;75:1122-30.
10. Delgado M, Gonzalez-Rey E, Ganea D. The neuropeptide vasoactive intestinal peptide generates tolerogenic dendritic cells. J Immunol 2005;175:7311-24.
11. Li JM, Southerland L, Hossain MS, Giver CR, Wang Y, Darlak K, et al. Absence of vasoactive intestinal Peptide expression in hematopoietic cells enhances Th1 polarization and antiviral immunity in mice. J Immunol 2011;187:1057-65.
12. 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;121:2347-51.
13. Li JM, Darlak KA, Southerland L, Hossain MS, Jaye DL, Josephson CD, et al. VIPhyb, an antagonist of vasoactive intestinal peptide receptor, enhances cellular antiviral immunity in murine cytomegalovirus infected mice. PLoS One 2013;8:e63381.
14. Colwell CS, Michel S, Itri J, Rodriguez W, Tam J, Lelievre V, et al. Disrupted circadian rhythms in VIP- and PHI-deficient mice. Am J Physiol Regul Integr Comp Physiol 2003;285:R939-49.
15. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012;366:2455-65.
16. Armand P, Nagler A, Weller EA, Devine SM, Avigan DE, Chen YB, et al. Disabling immune tolerance by programmed death-1 blockade with pidilizumab after autologous hematopoietic stem-cell transplantation for diffuse large B-cell lymphoma: results of an international phase II trial. J Clin Oncol 2013;31:4199-206.
17. Naidoo J, Page DB, Li BT, Connell LC, Schindler K, Lacouture ME, et al. Toxicities of the anti-PD-1 and anti-PD-L1 immune checkpoint antibodies. Ann Oncol 2015;26:2375-91.
18. Chorny A, Gonzalez-Rey E, Fernandez-Martin A, Ganea D, Delgado M. Vasoactive intestinal peptide induces regulatory dendritic cells that prevent acute graft-versus-host disease while maintaining the graft-versus-tumor response. Blood 2006;107:3787-94.
19. Moody TW, Zia F, Draoui M, Brenneman DE, Fridkin M, Davidson A, et al. A vasoactive intestinal peptide antagonist inhibits non-small cell lung cancer growth. Proc Natl Acad Sci U S A 1993;90:4345-9.
20. Lu Y, Giver CR, Sharma A, Li JM, Darlak KA, Owens LM, et al. IFN-gamma and indoleamine 2,3-dioxygenase signaling between donor dendritic cells and T cells regulates graft versus host and graft versus leukemia activity. Blood 2012;119:1075-85.
21. Taylor PA, Ehrhardt MJ, Lees CJ, Tolar J, Weigel BJ, Panoskaltsis-Mortari A, et al. Insights into the mechanism of FTY720 and compatibility with regulatory T cells for the inhibition of graft-versus-host disease (GVHD). Blood 2007;110:3480-8.
22. Grubin CE, Kovats S, deRoos P, Rudensky AY. Deficient positive selection of CD4 T cells in mice displaying altered repertoires of MHC class II-bound self-peptides. Immunity 1997;7:197-208.
23. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. 'Green mice' as a source of ubiquitous green cells. FEBS Lett 1997;407:313-9.
24. Waller EK, Ship AM, Mittelstaedt S, Murray TW, Carter R, Kakhniashvili I, et al. Irradiated donor leukocytes promote engraftment of allogeneic bone marrow in major histocompatibility complex mismatched recipients without causing graft-versus-host disease. Blood 1999;94:3222-33.
25. Cooke KR, Kobzik L, Martin TR, Brewer J, Delmonte J Jr, Crawford JM, et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood 1996;88:3230-9.
26. Moody TW, Dudek J, Zakowicz H, Walters J, Jensen RT, Petricoin E, et al. VIP receptor antagonists inhibit mammary carcinogenesis in C3(1)SV40T antigen mice. Life Sci 2004;74:1345-57.
27. Li JM, Southerland LT, Lu Y, Darlak KA, Giver CR, McMillin DW, et al. Activation, immune polarization, and graft-versus-leukemia activity of donor T cells are regulated by specific subsets of donor bone marrow antigen-presenting cells in allogeneic hemopoietic stem cell transplantation. J Immunol 2009;183:7799-809.
28. Caughey GH, Leidig F, Viro NF, Nadel JA. Substance P and vasoactive intestinal peptide degradation by mast cell tryptase and chymase. J Pharmacol Exp Ther 1988;244:133-7.
29. Goetzl EJ, Kodama KT, Turck CW, Schiogolev SA, Sreedharan SP. Unique pattern of cleavage of vasoactive intestinal peptide by human lymphocytes. Immunology 1989;66:554-8.
30. Chamberland S, Salesse C, Topolnik D, Topolnik L. Synapse-specific inhibitory control of hippocampal feedback inhibitory circuit. Front Cell Neurosci 2010;4:130.
31. Wysocki CA, Panoskaltsis-Mortari A, Blazar BR, Serody JS. Leukocyte migration and graft-versus-host disease. Blood 2005;105:4191-9.
32. Sallusto F, Mackay CR, Lanzavecchia A. The role of chemokine receptors in primary, effector, and memory immune responses. Annu Rev Immunol 2000;18:593-620.
33. Lou Y, Liu C, Kim GJ, Liu YJ, Hwu P, Wang G. Plasmacytoid dendritic cells synergize with myeloid dendritic cells in the induction of antigen-specific antitumor immune responses. J Immunol 2007;178:1534-41.
34. Sirianni MC, Annibale B, Tagliaferri F, Fais S, De Luca S, Pallone F, et al. Modulation of human natural killer activity by vasoactive intestinal peptide (VIP) family. VIP, glucagon and GHRF specifically inhibit NK activity. Regl Pept 1992;38:79-87.
35. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, et al. Innate or adaptive immunity? The example of natural killer cells. Science 2011;331:44-9.
36. Fuertes MB, Kacha AK, Kline J, Woo SR, Kranz DM, Murphy KM, et al. Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8{alpha}+ dendritic cells. J Exp Med 2011;208:2005-16.
37. Diamond MS, Kinder M, Matsushita H, Mashayekhi M, Dunn GP, Archambault JM, et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med 2011;208:1989-2003
38. Langenkamp A, Nagata K, Murphy K, Wu L, Lanzavecchia A, Sallusto F. Kinetics and expression patterns of chemokine receptors in human CD4+ T lymphocytes primed by myeloid or plasmacytoid dendritic cells. Eur J Immunol 2003;33:474-82.
39. Grimm MC, Newman R, Hassim Z, Cuan N, Connor SJ, Le Y, et al. Cutting edge: vasoactive intestinal peptide acts as a potent suppressor of inflammation in vivo by trans-deactivating chemokine receptors. J Immunol 2003;171:4990-4.
40. Leister I, Mbachu EM, Post S, Samel ST, Stojanovic T, Gutt CN, et al. Vasoactive intestinal polypeptide and gastrin-releasing peptide attenuate hepatic microvasculatory disturbances following intestinal ischemia and reperfusion. Digestion 2002;66:186-92.
41. Finke U, Seifert J. Differential effects of gastrointestinal hormones on the blood flow of the alimentary tract of the dog. Res Exp Med 1986;186:151-65.
42. Michonneau D, Sagoo P, Breart B, Garcia Z, Celli S, Bousso P. The PD-1 axis enforces an anatomical segregation of CTL activity that creates tumor niches after allogeneic hematopoietic stem cell transplantation. Immunity 2016;44:143-54.
43. Nierkens S, Tel J, Janssen E, Adema GJ. Antigen cross-presentation by dendritic cell subsets: one general or all sergeants? Trends Immunol 2013;34:361-70.
44. Dutt S, Baker J, Kohrt HE, Kambham N, Sanyal M, Negrin RS, et al. CD8+CD44(hi) but not CD4+CD44(hi) memory T cells mediate potent graft antilymphoma activity without GVHD. Blood 2011;117:3230-9.
45. Fontaine P, Roy-Proulx G, Knafo L, Baron C, Roy DC, Perreault C. Adoptive transfer of minor histocompatibility antigen-specific T lymphocytes eradicates leukemia cells without causing graft-versus-host disease. Nat Med 2001;7:789-94.
46. Michalek J, Collins RH, Durrani HP, Vaclavkova P, Ruff LE, Douek DC, et al. Definitive separation of graft-versus-leukemia- and graft-versus-host-specific CD4+ T cells by virtue of their receptor beta loci sequences. Proc Natl Acad Sci U S A 2003;100:1180-4.
47. Abad C, Tan YV, Lopez R, Nobuta H, Dong H, Phan P, et al. Vasoactive intestinal peptide loss leads to impaired CNS parenchymal T-cell infiltration and resistance to experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 2010;107:19555-60.
48. Delgado M, Abad C, Martinez C, Leceta J, Gomariz RP. Vasoactive intestinal peptide prevents experimental arthritis by downregulating both autoimmune and inflammatory components of the disease. Nat Med 2001;7:563-8.
49. Tan YV, Abad C, Lopez R, Dong H, Liu S, Lee A, et al. Pituitary adenylyl cyclase-activating polypeptide is an intrinsic regulator of Treg abundance and protects against experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A 2009;106:2012-7.
50. Souza-Moreira L, Morell M, Delgado-Maroto V, Pedreno M, Martinez-Escudero L, Caro M, et al. Paradoxical effect of cortistatin treatment and its deficiency on experimental autoimmune encephalomyelitis. J Immunol 2013;191:2144-54.