2,450
Views
2
CrossRef citations to date
0
Altmetric
Report

Development of a nonhuman primate challenge model to evaluate CD8+ T cell responses to an adenovirus-based vaccine expressing SIV proteins upon repeat-dose treatment with checkpoint inhibitors

, , , , , , , , & show all
Article: 1979447 | Received 26 Mar 2021, Accepted 25 Aug 2021, Published online: 20 Dec 2021

References

  • Chen DS, Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39(1):1–15. doi:10.1016/j.immuni.2013.07.012.
  • van Meer PJK, Graham ML, Schuurman HJ. The safety, efficacy and regulatory triangle in drug development: impact for animal models and the use of animals. Eur J Pharmacol. 2015;759:3–13. doi:10.1016/j.ejphar.2015.02.055.
  • Chen DS, and Mellman I. Oncology meets immunology: the cancer-immunity cycle. Immunity. 2013;39(1):1-10.
  • Lesterhuis WJ, Haanen JBAG, and Punt CJA. Cancer immunotherapy – revisited. Nat Rev Drug Discov. 2011;10(8):591-600.
  • Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252-64.
  • Herzyk DJ, and Haggerty HG. Cancer immunotherapy: factors important for the evaluation of safety in nonclinical studies. AAPS J. 2018;20(2):28.
  • Lebrec H, Molinier B, Boverhof D, Collinge M, Freebern W, Henson K, Mytych DT, Ochs HD, Wange R, Yang Y, et al. The T-cell-dependent antibody response assay in nonclinical studies of pharmaceuticals and chemicals: study design, data analysis, interpretation. Regul Toxicol Pharmacol. 2014;69(1):7–21. doi:10.1016/j.yrtph.2014.02.008.
  • Olson B, Li Y, Lin Y, Liu ET, Patnaik A. Mouse models for cancer immunotherapy research. Cancer Discov. 2018;8(11):1358–65. doi:10.1158/2159-8290.CD-18-0044.
  • Overgaard NH, Fan TM, Schachtschneider KM, Principe DR, Schook LB, Jungersen G. Of mice, dogs, pigs, and men: choosing the appropriate model for immuno-oncology research. ILAR J. 2018;59:247–62.
  • Schachtschneider KM, Schwind RM, Newson J, Kinachtchouk N, Rizko M, Mendoza-Elias N, Grippo P, Principe DR, Park A, and Overgaard NH, et al. The oncopig cancer model: an innovative large animal translational oncology platform. Front Oncol. 2017;7:190.
  • Zitvogel L, Pitt JM, Daillère R, Smyth MJ, Kroemer G. Mouse models in oncoimmunology. Nat Rev Cancer. 2016;16(12):759–73. doi:10.1038/nrc.2016.91.
  • Galluzzi L, Buqué A, Kepp O, Zitvogel L, Kroemer G. Immunological effects of conventional chemotherapy and targeted anticancer agents. Cancer Cell. 2015;28(6):690–714. doi:10.1016/j.ccell.2015.10.012.
  • Curran M, Mairesse M, Matas-Céspedes A, Bareham B, Pellegrini G, Liaunardy A, Powell E, Sargeant R, Cuomo E, and Stebbings R, et al. Recent advancements and applications of human immune system mice in preclinical immuno-oncology. Toxicol Pathol. 2019Feb;48(2):302-316.
  • De La Rochere P, Guil-Luna S, Decaudin D, Azar G, Sidhu SS, Piaggio E. Humanized mice for the study of immuno-oncology. Trends Immunol. 2018;39(9):748–63. doi:10.1016/j.it.2018.07.001.
  • Gillet J-P, Calcagno AM, Varma S, Marino M, Green LJ, Vora MI, Patel C, Orina JN, Eliseeva TA, Singal V, et al. Redefining the relevance of established cancer cell lines to the study of mechanisms of clinical anti-cancer drug resistance. Proc Natl Acad Sci U S A. 2011;108(46):18708–13. doi:10.1073/pnas.1111840108.
  • Mak IW, Evaniew N, Ghert M Review article lost in translation: animal models and clinical trials in cancer treatment [Internet]. 2014. Available from: www.ajtr.org
  • Sanmamed MF, Chester C, Melero I, and Kohrt H. Defining the optimal murine models to investigate immune checkpoint blockers and their combination with other immunotherapies downloaded from [internet]. Ann Oncol. 2016 Jul;27(7):1190-8. . Available from: http://annonc.oxfordjournals.org/
  • Fisher TS, Kamperschroer C, Oliphant T, Love VA, Lira PD, Doyonnas R, Bergqvist S, Baxi SM, Rohner A, Shen AC, et al. Targeting of 4-1BB by monoclonal antibody PF-05082566 enhances T-cell function and promotes anti-tumor activity. Cancer Immunol Immunother. 2012;61(10):1721–33. doi:10.1007/s00262-012-1237-1.
  • Herzyk DJ, Haggerty HG. Cancer immunotherapy: factors important for the evaluation of safety in nonclinical studies. AAPS J. 2018;20(2). doi:10.1208/s12248-017-0184-3.
  • Iwasaki K, Uno Y, Utoh M, Yamazaki H. Importance of cynomolgus monkeys in development of monoclonal antibody drugs. Drug Metab Pharmacokinet. 2019;34(1):55–63. doi:10.1016/j.dmpk.2018.02.003.
  • Messaoudi I, Estep R, Robinson B, Wong SW Nonhuman primate models of human immunology.
  • van Meer PJK, Kooijman M, Brinks V, Gispen-De Wied CC, Silva-Lima B, Moors EHM, Schellekens H. Immunogenicity of mAbs in non-human primates during nonclinical safety assessment. mAbs. 2013;5(5):810–16. doi:10.4161/mabs.25234.
  • Weinberg AD, Thalhofer C, Morris N, Walker JM, Seiss D, Wong S, Axthelm MK, Picker LJ, Urba WJ Anti-OX40 (CD134) administration to nonhuman primates: immunostimulatory effects and toxicokinetic study. 2006.
  • Satterwhite CM, Comba RW, Oldendorp A, and Prell R Investigation of KLH (Keyhole Limpet Hemocyanin) antigen dose response in male and female cynomolgus monkeys to establish an optimal response to study immune enhancement. SOT 55th Annual Meeting and ToxExpo. New Orleans, LA. 2016.
  • Wang C, Thudium KB, Han M, Wang XT, Huang H, Feingersh D, Garcia C, Wu Y, Kuhne M, Srinivasan M, et al. In vitro characterization of the anti-PD-1 antibody nivolumab, BMS-936558, and in vivo toxicology in non-human primates. Cancer Immunol Res. 2014;2(9):846–56. doi:10.1158/2326-6066.CIR-14-0040.
  • Loffredo J, Vuyyuru R, Spires V, Beyer S, Fox M, Ehrmann J, Taylor K, Engelhardt J, Korman A, and Graziano R Non-fucosylated anti-CTLA-4 antibody enhances vaccine-induced T cell responses in a non-human primate pharmacodynamic vaccine model-32nd Annual Meeting and Pre-Conference Programs of the Society for Immunotherapy of Cancer (SITC 2017). In: Journal for ImmunoTherapy of Cancer. National Harbor, Maryland. 2017.
  • Keler T, Halk E, Vitale L, O’Neill T, Blanset D, Lee S, Srinivasan M, Graziano RF, Davis T, and Lonberg N, et al. Activity and safety of CTLA-4 blockade combined with vaccines in cynomolgus macaques. J Immunol. 2003;171(11):6251-9.
  • Gonzalez AM, Manrique ML, Swiech L, Horn T, Breous E, Waight J, Savitsky D, Liu Y, Lin S, Clarke C, et al. Abstract 4703: INCAGN1949, an anti-OX40 antibody with an optimal agonistic profile and the ability to selectively deplete intratumoral regulatory T cells. In: Clinical Research (Excluding Clinical Trials). American Association for Cancer Research; 2017.
  • Macoin J, Blein S, Monney T, Sancheti P, Reddy V, Back J GBR830, a true OX40 antagonist antibody with potent suppressive effects on T cell-mediated pathological responses [abstract]. In: Arthritis & Rheumatology. American College of Rheumatology; 2018.
  • U. S. Food and Drug Administration. https://www.accessdata.fda.gov/drugsatfda_docs/nda/2017/761069Orig1s000PharmR.pdf, December 2020.
  • European Medicines Agency: EMA assessment report EMA/CHMP/392114/2015, https://www.ema.europa.eu/en/documents/assessment-report/nivolumab-bms-epar-public-assessment-report_en.pdf, Access date 01 Dec 2020 .
  • Kamperschroer C, O’Donnell LM, Schneider PA, Li D, Roy M, Coskran TM, Kawabata TT. Measuring T-cell responses against LCV and CMV in cynomolgus macaques using ELISPOT: potential application to non-clinical testing of immunomodulatory therapeutics. J Immunotoxicol. 2014;11(1):35–43. doi:10.3109/1547691X.2013.766287.
  • Finnefrock AC, Tang A, Li F, Freed DC, Feng M, Cox KS, Sykes KJ, Guare JP, Miller MD, Olsen DB, et al. PD-1 blockade in rhesus macaques: impact on chronic infection and prophylactic vaccination. J Immunol. 2009;182(2):980–87. doi:10.4049/jimmunol.182.2.980.
  • Tatsis N, Lasaro MO, Lin S-W, Xiang ZQ, Zhou D, DiMenna L, Li H, Bian A, Abdulla S, Li Y, et al. Adenovirus vector-induced immune responses in nonhuman primates: responses to prime boost regimens. J Immunol. 2009;182(10):6587–99. doi:10.4049/jimmunol.0900317.
  • Zak DE, Andersen-Nissen E, Peterson ER, Sato A, Hamilton MK, Borgerding J, Krishnamurty AT, Chang JT, Adams DJ, Hensley TR, et al. Merck Ad5/HIV induces broad innate immune activation that predicts CD8+ T-cell responses but is attenuated by preexisting Ad5 immunity. Proc Natl Acad Sci U S A. 2012;109(50):E3503–12. doi:10.1073/pnas.1208972109.
  • Sakurai F, Nakamura S, Akitomo K, Shibata H, Terao K, Kawabata K, Hayakawa T, and Mizuguchi H. Transduction properties of adenovirus serotype 35 vectors after intravenous administration into nonhuman primates. Mol Ther. 2008;16(4):726-733.
  • Wu J, Chen G, Zhuang F-C, Gao M, Wu C-D, He Z-L, Jiang Y-S, Li J-B, Bao J-Y, Mao Z-A. Long-term toxicity, pharmacokinetics and immune effects of a recombinant adenovirus vaccine expressing human papillomavirus 16 E6 and E7 proteins (HPV16 E6E7-Ad5 Vac) in primates. Am J Transl Res. 2018;10:1539–51.
  • Ni S, Bernt K, Gaggar A, Li Z-Y, Kiem H-P, Lieber A. Evaluation of biodistribution and safety of adenovirus vectors containing group B fibers after intravenous injection into baboons. Hum Gene Ther. 2005;16.
  • Budde ML, Greene JM, Chin EN, Ericsen AJ, Scarlotta M, Cain BT, Pham NH, Becker EA, Harris M, Weinfurter JT, et al. Specific CD8+ T cell responses correlate with control of simian immunodeficiency virus replication in Mauritian cynomolgus macaques. J Virol. 2012;86(14):7596–604. doi:10.1128/JVI.00716-12.
  • Burwitz BJ, Pendley CJ, Greene JM, Detmer AM, Lhost JJ, Karl JA, Piaskowski SM, Rudersdorf RA, Wallace LT, Bimber BN, et al. Mauritian cynomolgus macaques share two exceptionally common major histocompatibility complex class I alleles that restrict simian immunodeficiency virus-specific CD8 + T cells. J Virol. 2009;83(12):6011–19. doi:10.1128/JVI.00199-09.
  • Greene JM, Chin EN, Budde ML, Lhost JJ, Hines PJ, Burwitz BJ, Broman KW, Nelson JE, Friedrich TC, and O’Connor DH. Ex vivo SIV-specific CD8 T cell responses in heterozygous animals are primarily directed against peptides presented by a single MHC haplotype. Plos One. 2012;7(8):e43690.
  • Calcedo R, Vandenberghe LH, Roy S, Somanathan S, Wang L, Wilson JM. Host immune responses to chronic adenovirus infections in human and nonhuman primates. J Virol. 2009;83(6):2623–31. doi:10.1128/JVI.02160-08.
  • del Giudice G, Rappuoli R, Didierlaurent AM. Correlates of adjuvanticity: a review on adjuvants in licensed vaccines. Semin Immunol. 2018;39:14–21.
  • Jeyanathan M, Shao Z, Yu X, Harkness R, Jiang R, Li J, Xing Z, and Zhu T. AdHu5Ag85A respiratory mucosal boost immunization enhances protection against pulmonary tuberculosis in bcg-primed non-human primates. Plos One. 2015;10(8):e0135009.
  • Kim JR, Holbrook BC, Hayward SL, Blevins LK, Jorgensen MJ, Kock ND, De Paris K, D’Agostino RB, Aycock ST, Mizel SB, et al. Inclusion of flagellin during vaccination against influenza enhances recall responses in nonhuman primate neonates. J Virol. 2015;89(14):7291–303. doi:10.1128/JVI.00549-15.
  • McDade TW, Borja JB, Kuzawa CW, Perez TLL, Adair LS. C-reactive protein response to influenza vaccination as a model of mild inflammatory stimulation in the Philippines. Vaccine. 2015;33(17):2004–08. doi:10.1016/j.vaccine.2015.03.019.
  • Sabins NC, Harman BC, Barone LR, Shen S, and Santulli-Marotto S. Differential expression of immune checkpoint modulators on in vitro primed CD4+ and CD8+ T cells. Front Immunol. 2016;7:221.
  • Bottermann M, Foss S, van Tienen LM, Vaysburd M, Cruickshank J, O’Connell K, Clark J, Mayes K, Higginson K, Hirst JC, et al. TRIM21 mediates antibody inhibition of adenovirus-based gene delivery and vaccination. Proc Natl Acad Sci U S A. 2018;115(41):10440–45. doi:10.1073/pnas.1806314115.
  • Choi JH, Jonsson-Schmunk K, Qiu X, Shedlock DJ, Strong J, Xu JX, Michie KL, Audet J, Fernando L, Myers MJ, et al. A single dose respiratory recombinant adenovirus-based vaccine provides long-term protection for non-human primates from lethal Ebola infection. Mol Pharm. 2015;12(8):2712–31. doi:10.1021/mp500646d.
  • Lawrence M, Foellmer H, Elsworth J, Kim J, Leranth C, Kozlowski D, Bothwell A, Davidson B, Bohn M, and Redmond JD Inflammatory responses and their impact on-galactosidase transgene expression following adenovirus vector delivery to the primate caudate nucleus [Internet]. Gene Ther.1999;6(8):1368-79. Available from: http://www.stockton-press.co.uk/gt
  • Schirmbeck R, Reimann J, Kochanek S, Kreppel F. The immunogenicity of adenovirus vectors limits the multispecificity of CD8 T-cell responses to vector-encoded transgenic antigens. Mol Ther. 2008;16(9):1609–16. doi:10.1038/mt.2008.141.
  • t’Hart BA, Vervoordeldonk M, Heeney JL, Tak PP. Gene therapy in nonhuman primate models of human autoimmune disease. Gene Ther. 2003;10(10):890–901. doi:10.1038/sj.gt.3302017.
  • Young LS, Mautner V. The promise and potential hazards of adenovirus gene therapy. Gut. 2001;48(48):733–36. doi:10.1136/gut.48.5.733.
  • Fehlings M, Jhunjhunwala S, Kowanetz M, O’Gorman WE, Hegde PS, Sumatoh H, Lee BH, Nardin A, Becht E, Flynn S, et al. Late-differentiated effector neoantigen-specific CD8+ T cells are enriched in peripheral blood of non-small cell lung carcinoma patients responding to atezolizumab treatment. J ImmunoTher Cancer. 2019;7.
  • Lopez JS, Camidge R, Iafolla M, Rottey S, Schuler M, Hellmann M, Balmanoukian A, Dirix L, Gordon M, Sullivan R, et al. Abstract CT301: a phase Ib study to evaluate RO7198457, an individualized Neoantigen Specific immunoTherapy (iNeST), in combination with atezolizumab in patients with locally advanced or metastatic solid tumors. In: Bioinformatics, Convergence Science, and Systems Biology. American Association for Cancer Research; 2020.
  • Budde ML, Lhost JJ, Burwitz BJ, Becker EA, Burns CM, O’Connor SL, Karl JA, Wiseman RW, Bimber BN, Zhang GL, et al. Transcriptionally abundant major histocompatibility complex class I alleles are fundamental to nonhuman primate simian immunodeficiency virus-specific CD8 + T cell responses. J Virol. 2011;85(7):3250–61. doi:10.1128/JVI.02355-10.
  • Mbitikon-Kobo FM, Bonneville M, Sekaly RP, Trautmann L. Ex vivo measurement of the cytotoxic capacity of human primary antigen-specific CD8 T cells. J Immunol Methods. 2012;375(1–2):252–57. doi:10.1016/j.jim.2011.09.008.