Intratumoral immunotherapy of murine pheochromocytoma shows no age-dependent differences in its efficacy

. 2023 ; 14 () : 1030412. [epub] 20230508

Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, Research Support, N.I.H., Intramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37342258

Cancer immunotherapy has shown remarkable clinical progress in recent years. Although age is one of the biggest leading risk factors for cancer development and older adults represent a majority of cancer patients, only a few new cancer immunotherapeutic interventions have been preclinically tested in aged animals. Thus, the lack of preclinical studies focused on age-dependent effect during cancer immunotherapy could lead to different therapeutic outcomes in young and aged animals and future modifications of human clinical trials. Here, we compare the efficacy of previously developed and tested intratumoral immunotherapy, based on the combination of polysaccharide mannan, toll-like receptor ligands, and anti-CD40 antibody (MBTA immunotherapy), in young (6 weeks) and aged (71 weeks) mice bearing experimental pheochromocytoma (PHEO). The presented results point out that despite faster growth of PHEO in aged mice MBTA intratumoral immunotherapy is effective approach without age dependence and could be one of the possible therapeutic interventions to enhance immune response to pheochromocytoma and perhaps other tumor types in aged and young hosts.

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DePinho RA. The age of cancer. Nature (2000) 408(6809):248–54. doi: 10.1038/35041694 PubMed DOI

Walford RL. The immunologic theory of aging. Gerontologist (1964) 4:195–7. doi: 10.1093/geront/4.4.195 PubMed DOI

Herrera AP, Snipes SA, King DW, Torres-Vigil I, Goldberg DS, Weinberg AD. Disparate inclusion of older adults in clinical trials: priorities and opportunities for policy and practice change. Am J Public Health (2010) 100 Suppl 1:S105–12. doi: 10.2105/AJPH.2009.162982 PubMed DOI PMC

Aapro MS, Kohne CH, Cohen HJ, Extermann M. Never too old? age should not be a barrier to enrollment in cancer clinical trials. Oncologist (2005) 10(3):198–204. doi: 10.1634/theoncologist.10-3-198 PubMed DOI

Ruiter R, Burggraaf J, Rissmann R. Under-representation of elderly in clinical trials: an analysis of the initial approval documents in the food and drug administration database. Br J Clin Pharmacol (2019) 85(4):838–44. doi: 10.1111/bcp.13876 PubMed DOI PMC

Garred P, Genster N, Pilely K, Bayarri-Olmos R, Rosbjerg A, Ma YJ, et al. . A journey through the lectin pathway of complement-MBL and beyond. Immunol Rev (2016) 274(1):74–97. doi: 10.1111/imr.12468 PubMed DOI

Janotova T, Jalovecka M, Auerova M, Svecova I, Bruzlova P, Maierova V, et al. . The use of anchored agonists of phagocytic receptors for cancer immunotherapy: B16-F10 murine melanoma model. PloS One (2014) 9(1):e85222. doi: 10.1371/journal.pone.0085222 PubMed DOI PMC

Figueiredo RT, Carneiro LA, Bozza MT. Fungal surface and innate immune recognition of filamentous fungi. Front Microbiol (2011) 2:248. doi: 10.3389/fmicb.2011.00248 PubMed DOI PMC

Matsumoto M, Seya T. TLR3: interferon induction by double-stranded RNA including poly(I:C). Adv Drug Delivery Rev (2008) 60(7):805–12. doi: 10.1016/j.addr.2007.11.005 PubMed DOI

Seo HS, Michalek SM, Nahm MH. Lipoteichoic acid is important in innate immune responses to gram-positive bacteria. Infect Immun (2008) 76(1):206–13. doi: 10.1128/IAI.01140-07 PubMed DOI PMC

Wu JJ, Huang DB, Tyring SK. Resiquimod: a new immune response modifier with potential as a vaccine adjuvant for Th1 immune responses. Antiviral Res (2004) 64(2):79–83. doi: 10.1016/j.antiviral.2004.07.002 PubMed DOI

Khong A, Nelson DJ, Nowak AK, Lake RA, Robinson BWS. The use of agonistic anti-CD40 therapy in treatments for cancer. Int Rev Immunol (2012) 31(4):246–66. doi: 10.3109/08830185.2012.698338 PubMed DOI

Rakhmilevich AL, Alderson KL, Sondel PM. T-Cell-independent antitumor effects of CD40 ligation. Int Rev Immunol (2012) 31(4):267–78. doi: 10.3109/08830185.2012.698337 PubMed DOI PMC

Caisova V, Li L, Gupta G, Jochmanova I, Jha A, Uher O, et al. . The significant reduction or complete eradication of subcutaneous and metastatic lesions in a pheochromocytoma mouse model after immunotherapy using mannan-BAM, TLR ligands, and anti-CD40. Cancers (Basel) (2019) 11(5):654. doi: 10.3390/cancers11050654 PubMed DOI PMC

Caisova V, Uher O, Nedbalova P, Jochmanova I, Kvardova K, Masakova K, et al. . Effective cancer immunotherapy based on combination of TLR agonists with stimulation of phagocytosis. Int Immunopharmacol. (2018) 59:86–96. doi: 10.1016/j.intimp.2018.03.038 PubMed DOI

Medina R, Wang H, Caisova V, Cui J, Indig IH, Uher O, et al. . Induction of immune response against metastatic tumors via vaccination of mannan-BAM, TLR ligands and anti-CD40 antibody (MBTA). Adv Ther (Weinh) (2020) 3(9). doi: 10.1002/adtp.202000044 PubMed DOI PMC

Uher O, Caisova V, Padoukova L, Kvardova K, Masakova K, Lencova R, et al. . And anti-CD40 immunotherapy in established murine pancreatic adenocarcinoma: understanding therapeutic potentials and limitations. Cancer Immunol Immunother. (2021) 70(11):3303–12. doi: 10.1007/s00262-021-02920-9 PubMed DOI PMC

Uher O, Huynh TT, Zhu B, Horn LA, Caisova V, Hadrava Vanova K, et al. . Identification of immune cell infiltration in murine pheochromocytoma during combined mannan-BAM, TLR ligand, and anti-CD40 antibody-based immunotherapy. Cancers (Basel) (2021) 13(16):3942. doi: 10.3390/cancers13163942 PubMed DOI PMC

Lenders JW, Eisenhofer G, Mannelli M, Pacak K. Phaeochromocytoma. In: Lancet Elsevier: London, England: (2005) 366:665–75. PubMed

Eisenhofer G, Timmers HJ, Lenders JW, Bornstein SR, Tiebel O, Mannelli M, et al. . Age at diagnosis of pheochromocytoma differs according to catecholamine phenotype and tumor location. J Clin Endocrinol Metab (2011) 96(2):375–84. doi: 10.1210/jc.2010-1588 PubMed DOI PMC

Choat H, Derrevere K, Knight L, Brown W, Mack EH. SDHB-associated paraganglioma in a pediatric patient and literature review on hereditary pheochromocytoma-paraganglioma syndromes. Case Rep Endocrinol (2014) 2014:502734. doi: 10.1155/2014/502734 PubMed DOI PMC

Dutta S, Sengupta P. Men and mice: relating their ages. Life Sci (2016) 152:244–8. doi: 10.1016/j.lfs.2015.10.025 PubMed DOI

Korpershoek E, Pacak K, Martiniova L. Murine models and cell lines for the investigation of pheochromocytoma: applications for future therapies? Endocr Pathol (2012) 23(1):43–54. doi: 10.1007/s12022-012-9194-y PubMed DOI PMC

Martiniova L, Lai EW, Elkahloun AG, Abu-Asab M, Wickremasinghe A, Solis DC, et al. . Characterization of an animal model of aggressive metastatic pheochromocytoma linked to a specific gene signature. Clin Exp Metastasis. (2009) 26(3):239–50. doi: 10.1007/s10585-009-9236-0 PubMed DOI PMC

Waldmannova E, Caisova V, Faberova J, Svackova P, Kovarova M, Svackova D, et al. . The use of zymosan a and bacteria anchored to tumor cells for effective cancer immunotherapy: B16-F10 murine melanoma model. Int Immunopharmacol. (2016) 39:295–306. doi: 10.1016/j.intimp.2016.08.004 PubMed DOI

Holness CL, Simmons DL. Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood (1993) 81(6):1607–13. doi: 10.1182/blood.V81.6.1607.1607 PubMed DOI

Robert C. A decade of immune-checkpoint inhibitors in cancer therapy. Nat Commun (2020) 11(1):3801. doi: 10.1038/s41467-020-17670-y PubMed DOI PMC

Ascierto PA, Del Vecchio M, Robert C, Mackiewicz A, Chiarion-Sileni V, Arance A, et al. . Ipilimumab 10 mg/kg versus ipilimumab 3 mg/kg in patients with unresectable or metastatic melanoma: a randomised, double-blind, multicentre, phase 3 trial. Lancet Oncol (2017) 18(5):611–22. doi: 10.1016/S1470-2045(17)30231-0 PubMed DOI

Marabelle A, Tselikas L, de Baere T, Houot R. Intratumoral immunotherapy: using the tumor as the remedy. Ann Oncol (2017) 28(suppl_12):xii33–43. doi: 10.1093/annonc/mdx683 PubMed DOI

Solana R, Tarazona R, Gayoso I, Lesur O, Dupuis G, Fulop T. Innate immunosenescence: effect of aging on cells and receptors of the innate immune system in humans. Semin Immunol (2012) 24(5):331–41. doi: 10.1016/j.smim.2012.04.008 PubMed DOI

Franceschi C, Salvioli S, Garagnani P, de Eguileor M, Monti D, Capri M. Immunobiography and the heterogeneity of immune responses in the elderly: a focus on inflammaging and trained immunity. Front Immunol (2017) 8:982. doi: 10.3389/fimmu.2017.00982 PubMed DOI PMC

Kovacs EJ, Palmer JL, Fortin CF, Fulop T, Jr., Goldstein DR, Linton PJ. Aging and innate immunity in the mouse: impact of intrinsic and extrinsic factors. Trends Immunol (2009) 30(7):319–24. doi: 10.1016/j.it.2009.03.012 PubMed DOI PMC

Nikolich-Zugich J. Aging of the T cell compartment in mice and humans: from no naive expectations to foggy memories. J Immunol (2014) 193(6):2622–9. doi: 10.4049/jimmunol.1401174 PubMed DOI PMC

Yanes RE, Gustafson CE, Weyand CM, Goronzy JJ. Lymphocyte generation and population homeostasis throughout life. Semin Hematol (2017) 54(1):33–8. doi: 10.1053/j.seminhematol.2016.10.003 PubMed DOI PMC

Oh J, Magnuson A, Benoist C, Pittet MJ, Weissleder R. Age-related tumor growth in mice is related to integrin alpha 4 in CD8+ T cells. JCI Insight (2018) 3(21):e122961. doi: 10.1172/jci.insight.122961 PubMed DOI PMC

Maggiorani D, Beausejour C. Senescence and aging: does it impact cancer immunotherapies? Cells (2021) 10(7):1568. doi: 10.3390/cells10071568 PubMed DOI PMC

Duong L, Radley-Crabb HG, Gardner JK, Tomay F, Dye DE, Grounds MD, et al. . Macrophage depletion in elderly mice improves response to tumor immunotherapy, increases anti-tumor T cell activity and reduces treatment-induced cachexia. Front Genet (2018) 9:526. doi: 10.3389/fgene.2018.00526 PubMed DOI PMC

Reed MJ, Karres N, Eyman D, Cruz A, Brekken RA, Plymate S. The effects of aging on tumor growth and angiogenesis are tumor-cell dependent. Int J Canc. (2007) 120(4):753–60. doi: 10.1002/ijc.22351 PubMed DOI

Ishikawa S, Matsui Y, Wachi S, Yamaguchi H, Harashima N, Harada M. Age-associated impairment of antitumor immunity in carcinoma-bearing mice and restoration by oral administration of lentinula edodes mycelia extract. Cancer Immunol Immunother. (2016) 65(8):961–72. doi: 10.1007/s00262-016-1857-y PubMed DOI PMC

McWilliams RR, Maisonneuve P, Bamlet WR, Petersen GM, Li D, Risch HA, et al. . Risk factors for early-onset and very-Early-Onset pancreatic adenocarcinoma: a pancreatic cancer case-control consortium (PanC4) analysis. Pancreas (2016) 45(2):311–6. doi: 10.1097/MPA.0000000000000392 PubMed DOI PMC

Sharma S, Dominguez AL, Hoelzinger DB, Lustgarten J. CpG-ODN but not other TLR-ligands restore the antitumor responses in old mice: the implications for vaccinations in the aged. Cancer Immunol Immunother. (2008) 57(4):549–61. doi: 10.1007/s00262-007-0393-1 PubMed DOI PMC

van Holstein Y, Kapiteijn E, Bastiaannet E, van den Bos F, Portielje J, de Glas NA. Efficacy and adverse events of immunotherapy with checkpoint inhibitors in older patients with cancer. Drugs Aging. (2019) 36(10):927–38. doi: 10.1007/s40266-019-00697-2 PubMed DOI PMC

Kanesvaran R, Cordoba R, Maggiore R. Immunotherapy in older adults with advanced cancers: implications for clinical decision-making and future research. Am Soc Clin Oncol Educ Book. (2018) 38:400–14. doi: 10.1200/EDBK_201435 PubMed DOI

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