Cancer immunotherapy: A comprehensive appraisal of its modes of application (Review)
- Authors:
- Mira Hoteit
- Zeina Oneissi
- Ranim Reda
- Fadi Wakim
- Amar Zaidan
- Mohammad Farran
- Elie Abi‑Khalil
- Mirvat El‑Sibai
-
Affiliations: Department of Natural Sciences, School of Arts and Sciences, Lebanese American University, Beirut 1102 2801, Lebanon - Published online on: July 9, 2021 https://doi.org/10.3892/ol.2021.12916
- Article Number: 655
This article is mentioned in:
Abstract
![]() |
Koo SL, Wang WW and Toh HC: Cancer Immunotherapy-The target is precisely on the cancer and also not. Ann Acad Med Singap. 47:381–387. 2018.PubMed/NCBI | |
Meng J, Zhou Y, Lu X, Bian Z, Chen Y, Zhou J, Zhang L, Hao Z, Zhang M and Liang C: Immune response drives outcomes in prostate cancer: Implications for immunotherapy. Mol Oncol. 15:1358–1375. 2021. View Article : Google Scholar : PubMed/NCBI | |
Balachandran VP, Beatty GL and Dougan SK: Broadening the impact of immunotherapy to pancreatic cancer: Challenges and opportunities. Gastroenterology. 156:2056–2072. 2019. View Article : Google Scholar : PubMed/NCBI | |
Parkin J and Cohen B: An overview of the immune system. Lancet. 357:1777–1789. 2001. View Article : Google Scholar : PubMed/NCBI | |
Perales-Puchalt A, Wojtak K, Duperret EK, Yang X, Slager AM, Yan J, Muthumani K, Montaner LJ and Weiner DB: Engineered DNA vaccination against follicle-stimulating hormone receptor delays ovarian cancer progression in animal models. Mol Ther. 27:314–325. 2019. View Article : Google Scholar : PubMed/NCBI | |
Pedersen M, Westergaard MCW, Milne K, Nielsen M, Borch TH, Poulsen LG, Hendel HW, Kennedy M, Briggs G, Ledoux S, et al: Adoptive cell therapy with tumor-infiltrating lymphocytes in patients with metastatic ovarian cancer: A pilot study. OncoImmunology. 7:e15029052018. View Article : Google Scholar : PubMed/NCBI | |
Mitchell DM, Ravkov EV and Williams MA: Distinct roles for IL-2 and IL-15 in the differentiation and survival of CD8+ effector and memory T cells. J Immunol. 184:6719–6730. 2010. View Article : Google Scholar : PubMed/NCBI | |
Jaeckel E, Kretschmer K, Apostolou I and von Boehmer H: Instruction of Treg commitment in peripheral T cells is suited to reverse autoimmunity. Semin Immunol. 18:89–92. 2006. View Article : Google Scholar : PubMed/NCBI | |
Brisslert M, Bokarewa M, Larsson P, Wing K, Collins LV and Tarkowski A: Phenotypic and functional characterization of human CD25+ B cells. Immunology. 117:548–557. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kim HP, Imbert J and Leonard WJ: Both integrated and differential regulation of components of the IL-2/IL-2 receptor system. Cytokine Growth Factor Rev. 17:349–366. 2006. View Article : Google Scholar : PubMed/NCBI | |
Smith FO, Downey SG, Klapper JA, Yang JC, Sherry RM, Royal RE, Kammula US, Hughes MS, Restifo NP, Levy CL, et al: Treatment of metastatic melanoma using interleukin-2 alone or in conjunction with vaccines. Clin Cancer Res. 14:5610–5618. 2008. View Article : Google Scholar : PubMed/NCBI | |
Lopes JE, Fisher JL, Flick HL, Wang C, Sun L, Ernstoff MS, Alvarez JC and Losey HC: ALKS 4230: A novel engineered IL-2 fusion protein with an improved cellular selectivity profile for cancer immunotherapy. J Immunother Cancer. 8:e0006732020. View Article : Google Scholar : PubMed/NCBI | |
Attridge K, Wang CJ, Wardzinski L, Kenefeck R, Chamberlain JL, Manzotti C, Kopf M and Walker LS: IL-21 inhibits T cell IL-2 production and impairs Treg homeostasis. Blood. 119:4656–4664. 2012. View Article : Google Scholar : PubMed/NCBI | |
Zimmerman RJ, Aukerman SL, Katre NV, Winkelhake JL and Young JD: Schedule dependency of the antitumor activity and toxicity of polyethylene glycol-modified interleukin 2 in murine tumor models. Cancer Res. 49:6521–6528. 1989.PubMed/NCBI | |
Rosenberg SA: IL-2: The first effective immunotherapy for human cancer. J Immunol. 192:5451–5458. 2014. View Article : Google Scholar : PubMed/NCBI | |
Grimm EA, Mazumder A, Zhang HZ and Rosenberg SA: Lymphokine-activated killer cell phenomenon. Lysis of natural killer-resistant fresh solid tumor cells by interleukin 2-activated autologous human peripheral blood lymphocytes. J Exp Med. 155:1823–1841. 1982. View Article : Google Scholar : PubMed/NCBI | |
Dudley ME, Wunderlich JR, Yang JC, Sherry RM, Topalian SL, Restifo NP, Royal RE, Kammula U, White DE, Mavroukakis SA, et al: Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J Clin Oncol. 23:2346–2357. 2005. View Article : Google Scholar : PubMed/NCBI | |
Krieg C, Létourneau S, Pantaleo G and Boyman O: Improved IL-2 immunotherapy by selective stimulation of IL-2 receptors on lymphocytes and endothelial cells. Proc Natl Acad Sci USA. 107:11906–11911. 2010. View Article : Google Scholar : PubMed/NCBI | |
Nasreddine G, El-Sibai M and Abi-Habib RJ: Cytotoxicity of [HuArgI (co)-PEG5000]-induced arginine deprivation to ovarian cancer cells is autophagy dependent. Invest New Drugs. 38:10–19. 2020. View Article : Google Scholar : PubMed/NCBI | |
Ingersoll SB, Ahmad S, McGann HC, Banks RK, Stavitzski NM, Srivastava M, Ali G, Finkler NJ, Edwards JR and Holloway RW: Cellular therapy in combination with cytokines improves survival in a xenograft mouse model of ovarian cancer. Mol Cell Biochem. 407:281–287. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ingersoll SB, Patel S, Caballero L, Ahmad S, Edwards D, Holloway RW and Edwards JR: Synergistic cytotoxicity of interferonalpha-2b and interleukin-2 in combination with PBMC against ovarian cancer: Development of an experimental model for cellular therapy. Gynecol Oncol. 112:192–198. 2009. View Article : Google Scholar : PubMed/NCBI | |
Di Scala M, Gil-Fariña I, Olagüe C, Vales A, Sobrevals L, Fortes P, Corbacho D and González-Aseguinolaza G: Identification of IFN-γ-producing T cells as the main mediators of the side effects associated to mouse interleukin-15 sustained exposure. Oncotarget. 7:49008–49026. 2016. View Article : Google Scholar : PubMed/NCBI | |
Miller JS, Morishima C, McNeel DG, Patel MR, Kohrt HEK, Thompson JA, Sondel PM, Wakelee HA, Disis ML, Kaiser JC, et al: A First-in-Human Phase I Study of subcutaneous outpatient recombinant human IL15 (rhIL15) in adults with advanced solid tumors. Clin Cancer Res. 24:1525–1535. 2018. View Article : Google Scholar : PubMed/NCBI | |
Conlon KC, Lugli E, Welles HC, Rosenberg SA, Fojo AT, Morris JC, Fleisher TA, Dubois SP, Perera LP, Stewart DM, et al: Redistribution, hyperproliferation, activation of natural killer cells and CD8 T cells, and cytokine production during First-in-Human clinical trial of recombinant human Interleukin-15 in patients with cancer. J Clin Oncol. 33:74–82. 2015. View Article : Google Scholar : PubMed/NCBI | |
Rubinstein MP, Kovar M, Purton JF, Cho JH, Boyman O, Surh CD and Sprent J: Converting IL-15 to a superagonist by binding to soluble IL-15R{alpha}. Proc Natl Acad Sci USA. 103:9166–9171. 2006. View Article : Google Scholar : PubMed/NCBI | |
Ochoa MC, Fioravanti J, Rodriguez I, Hervas-Stubbs S, Azpilikueta A, Mazzolini G, Gúrpide A, Prieto J, Pardo J, Berraondo P and Melero I: Antitumor immunotherapeutic and toxic properties of an HDL-Conjugated Chimeric IL-15 fusion protein. Cancer Res. 73:139–149. 2013. View Article : Google Scholar : PubMed/NCBI | |
Mortier E, Quéméner A, Vusio P, Lorenzen I, Boublik Y, Grötzinger J, Plet A and Jacques Y: Soluble interleukin-15 receptor alpha (IL-15R alpha)-sushi as a selective and potent agonist of IL-15 action through IL-15R beta/gamma. Hyperagonist IL-15 × IL-15R alpha fusion proteins. J Biol Chem. 281:1612–1619. 2006. View Article : Google Scholar : PubMed/NCBI | |
Ochoa MC, Minute L, López A, Pérez-Ruiz E, Gomar C, Vasquez M, Inoges S, Etxeberria I, Rodriguez I, Garasa S, et al: Enhancement of antibody-dependenT cellular cytotoxicity of cetuximab by a chimeric protein encompassing interleukin-15. Oncoimmunology. 7:e13935972017. View Article : Google Scholar : PubMed/NCBI | |
Rhode PR, Egan JO, Xu W, Hong H, Webb GM, Chen X, Liu B, Zhu X, Wen J, You L, et al: Comparison of the superagonist complex, ALT-803, to IL15 as cancer immunotherapeutics in animal models. Cancer Immunol Res. 4:49–60. 2016. View Article : Google Scholar : PubMed/NCBI | |
Romee R, Cooley S, Berrien-Elliott MM, Westervelt P, Verneris MR, Wagner JE, Weisdorf DJ, Blazar BR, Ustun C, DeFor TE, et al: First-in-human phase 1 clinical study of the IL-15 superagonist complex ALT-803 to treat relapse after transplantation. Blood. 131:2515–2527. 2018. View Article : Google Scholar : PubMed/NCBI | |
Rosser CJ, Nix L, Ferguson L, Hernandez L and Wong HC: Phase Ib trial of ALT-803, an IL-15 superagonist, plus BCG for the treatment of BCG-naïve patients with non-muscle-invasive bladder cancer. J Clin Oncol. 36 (Suppl 6):5102021. View Article : Google Scholar | |
Timmerman JM, Byrd JC, Andorsky DJ, Yamada RE, Kramer J, Muthusamy N, Hunder N and Pagel JM: A phase I dose-finding trial of recombinant interleukin-21 and rituximab in relapsed and refractory low grade B-cell lymphoproliferative disorders. Clin Cancer Res. 18:5752–5760. 2012. View Article : Google Scholar : PubMed/NCBI | |
Fioravanti J, Di Lucia P, Magini D, Moalli F, Boni C, Benechet AP, Fumagalli V, Inverso D, Vecchi A, Fiocchi A, et al: Effector CD8+ T cell-derived interleukin-10 enhances acute liver immunopathology. J Hepatol. 67:543–548. 2017. View Article : Google Scholar : PubMed/NCBI | |
Koski A, Kangasniemi L, Escutenaire S, Pesonen S, Cerullo V, Diaconu I, Nokisalmi P, Raki M, Rajecki M, Guse K, et al: Treatment of cancer patients with a serotype 5/3 chimeric oncolytic adenovirus expressing GMCSF. Mol Ther. 18:1874–1884. 2010. View Article : Google Scholar : PubMed/NCBI | |
Spaapen RM, Leung MY, Fuertes MB, Kline JP, Zhang L, Zheng Y, Fu YX, Luo X, Cohen KS and Gajewski TF: Therapeutic activity of High-Dose Intratumoral IFN-β requires direct effect on the tumor vasculature. J Immunol. 193:4254–4260. 2014. View Article : Google Scholar : PubMed/NCBI | |
Herndon TM, Demko SG, Jiang X, He K, Gootenberg JE, Cohen MH, Keegan P and Pazdur R: U.S. Food and Drug Administration Approval: Peginterferon-alfa-2b for the adjuvant treatment of patients with melanoma. Oncologist. 17:1323–1328. 2012. View Article : Google Scholar : PubMed/NCBI | |
Bellobuono A, Mondazzi L, Tempini S, Silini E, Vicari F and Idéo; G. Ribavirin and interferon-alpha combination therapy vs interferon-alpha alone in the retreatment of chronic hepatitis C, : A randomized clinical trial. J Viral Hepat. 4:185–191. 1997. View Article : Google Scholar : PubMed/NCBI | |
Gogas H, Ioannovich J, Dafni U, Stavropoulou-Giokas C, Frangia K, Tsoutsos D, Panagiotou P, Polyzos A, Papadopoulos O, Stratigos A, et al: Prognostic significance of autoimmunity during treatment of melanoma with interferon. N Engl J Med. 354:709–718. 2006. View Article : Google Scholar : PubMed/NCBI | |
Fioravanti J, González I, Medina-Echeverz J, Larrea E, Ardaiz N, González-Aseguinolaza G, Prieto J and Berraondo P: Anchoring interferon alpha to apolipoprotein A-I reduces hematological toxicity while enhancing immunostimulatory properties. Hepatology. 53:1864–1873. 2011. View Article : Google Scholar : PubMed/NCBI | |
Cauwels A, Van Lint S, Paul F, Garcin G, De Koker S, Van Parys A, Wueest T, Gerlo S, Van der Heyden J, Bordat Y, et al: Delivering Type I interferon to dendritic cells empowers tumor eradication and immune combination treatments. Cancer Res. 78:463–474. 2018. View Article : Google Scholar : PubMed/NCBI | |
Palladino MA, Bahjat FR, Theodorakis EA and Moldawer LL: Anti-TNF-alpha therapies: The next generation. Nat Rev Drug Discov. 2:736–746. 2003. View Article : Google Scholar : PubMed/NCBI | |
Creaven PJ, Plager JE, Dupere S, Huben RP, Takita H, Mittelman A and Proefrock A: Phase I clinical trial of recombinant human tumor necrosis factor. Cancer Chemother Pharmacol. 20:137–144. 1987. View Article : Google Scholar : PubMed/NCBI | |
Zheng L, Fisher G, Miller RE, Peschon J, Lynch DH and Lenardo MJ: Induction of apoptosis in mature T cells by tumour necrosis factor. Nature. 377:348–351. 1995. View Article : Google Scholar : PubMed/NCBI | |
Kahn JO, Kaplan LD, Volberding PA, Ziegler JL, Crowe S, Saks SR and Abrams DI: Intralesional recombinant tumor necrosis factor-alpha for AIDS-associated Kaposi's sarcoma: A randomized, double-blind trial. J Acquir Immune Defic Syndr. 2:217–223. 1989.PubMed/NCBI | |
Manusama ER, Nooijen PT, Stavast J, Durante NM, Marquet RL and Eggermont AM: Synergistic antitumour effect of recombinant human tumour necrosis factor alpha with melphalan in isolated limb perfusion in the rat. Br J Surg. 83:551–555. 1996. View Article : Google Scholar : PubMed/NCBI | |
Lejeune FJ, Liénard D, Matter M and Rüegg C: Efficiency of recombinant human TNF in human cancer therapy. Cancer Immun. 6:62006.PubMed/NCBI | |
van Horssen R, Ten Hagen TL and Eggermont AM: TNF-alpha in cancer treatment: Molecular insights, antitumor effects, and clinical utility. Oncologist. 11:397–408. 2006. View Article : Google Scholar : PubMed/NCBI | |
Herzberg B, Campo MJ and Gainor JF: Immune checkpoint inhibitors in non-small cell lung cancer. Oncologist. 22:81–88. 2017. View Article : Google Scholar : PubMed/NCBI | |
Delgobo M and Frantz S: Heart failure in cancer: Role of checkpoint inhibitors. J Thorac Dis. 10 (Suppl 35):S4323–S4334. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wolchok JD, Chiarion-Sileni V, Gonzalez R, Rutkowski P, Grob JJ, Cowey CL, Lao CD, Wagstaff J, Schadendorf D, Ferrucci PF, et al: Overall survival with combined nivolumab and ipilimumab in advanced melanoma. N Engl J Med. 377:1345–1356. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kamath SD and Kumthekar PU: Immune checkpoint inhibitors for the treatment of central nervous system (CNS) metastatic disease. Front Oncol. 8:4142018. View Article : Google Scholar : PubMed/NCBI | |
Heinzerling L, Ott PA, Hodi FS, Husain AN, Tajmir-Riahi A, Tawbi H, Pauschinger M, Gajewski TF, Lipson EJ and Luke JJ: Cardiotoxicity associated with CTLA4 and PD1 blocking immunotherapy. J Immunother Cancer. 4:502016. View Article : Google Scholar : PubMed/NCBI | |
Sznol M, Postow MA, Davies MJ, Pavlick AC, Plimack ER, Shaheen M, Veloski C and Robert C: Endocrine-related adverse events associated with immune checkpoint blockade and expert insights on their management. Cancer Treat Rev. 58:70–76. 2017. View Article : Google Scholar : PubMed/NCBI | |
Hassel JC, Heinzerling L, Aberle J, Bähr O, Eigentler TK, Grimm MO, Grünwald V, Leipe J, Reinmuth N, Tietze JK, et al: Combined immune checkpoint blockade (anti-PD-1/anti-CTLA-4): Evaluation and management of adverse drug reactions. Cancer Treat Rev. 57:36–49. 2017. View Article : Google Scholar : PubMed/NCBI | |
Simonaggio A, Michot JM, Voisin AL, Le Pavec J, Collins M, Lallart A, Cengizalp G, Vozy A, Laparra A, Varga A, et al: Evaluation of readministration of immune checkpoint inhibitors after immune-related adverse events in patients with cancer. JAMA Oncol. 5:1310–1317. 2019. View Article : Google Scholar : PubMed/NCBI | |
Santini FC, Rizvi H, Plodkowski AJ, Ni A, Lacouture ME, Gambarin-Gelwan M, Wilkins O, Panora E, Halpenny DF, Long NM, et al: Safety and efficacy of re-treating with immunotherapy after immune-related adverse events in patients with NSCLC. Cancer Immunol Res. 6:1093–1099. 2018. View Article : Google Scholar : PubMed/NCBI | |
Kluger HM, Zito CR, Turcu G, Baine MK, Zhang H, Adeniran A, Sznol M, Rimm DL, Kluger Y, Chen L, et al: PD-L1 studies across tumor types, its differential expression and predictive value in patients treated with immune checkpoint inhibitors. Clin Cancer Res. 23:4270–4279. 2017. View Article : Google Scholar : PubMed/NCBI | |
Fan J, Shang D, Han B, Song J, Chen H and Yang JM: Adoptive cell transfer: Is it a promising immunotherapy for colorectal cancer? Theranostics. 8:5784–5800. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wrangle J, Paulos CM, Smith TW, Nishimura MI and Rubinstein MP: Inducible enhancement of T cell function and anti-tumor activity after adoptive transfer. Mol Ther. 25:1995–1996. 2017. View Article : Google Scholar : PubMed/NCBI | |
Rohaan MW, Wilgenhof S and Haanen JBAG: Adoptive cellular therapies: The current landscape. Virchows Arch. 474:449–461. 2019. View Article : Google Scholar : PubMed/NCBI | |
Mitchison NA: Studies on the immunological response to foreign tumor transplants in the mouse. I. The role of lymph node cells in conferring immunity by adoptive transfer. J Exp Med. 102:157–177. 1955. View Article : Google Scholar : PubMed/NCBI | |
Fefer A: Immunotherapy and chemotherapy of Moloney sarcoma virus-induced tumors in mice. Cancer Res. 29:2177–2183. 1969.PubMed/NCBI | |
Rosenberg SA and Terry WD: Passive immunotherapy of cancer in animals and man. Adv Cancer Res. 25:323–388. 1977. View Article : Google Scholar : PubMed/NCBI | |
Kono K, Ichihara F, Iizuka H, Sekikawa T and Matsumoto Y: Expression of signal transducing T-cell receptor zeta molecules after adoptive immunotherapy in patients with gastric and colon cancer. Int J Cancer. 78:301–305. 1998. View Article : Google Scholar : PubMed/NCBI | |
Lu TL, Pugach O, Somerville R, Rosenberg SA, Kochenderfer JN, Better M and Feldman SA: A Rapid cell expansion process for production of engineered autologous CAR-T cell therapies. Hum Gene Ther Methods. 27:209–218. 2016. View Article : Google Scholar : PubMed/NCBI | |
Xiao L, Cen D, Gan H, Sun Y, Huang N, Xiong H, Jin Q, Su L, Liu X, Wang K, et al: Adoptive transfer of NKG2D CAR mRNA-Engineered natural killer cells in colorectal cancer patients. Mol Ther. 27:1114–1125. 2019. View Article : Google Scholar : PubMed/NCBI | |
Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, Yokoyama WM and Ugolini S: Innate or adaptive immunity? The example of natural killer cells. Science. 331:44–49. 2011. View Article : Google Scholar : PubMed/NCBI | |
Morvan MG and Lanier LL: NK cells and cancer: You can teach innate cells new tricks. Nat Rev Cancer. 16:7–19. 2016. View Article : Google Scholar : PubMed/NCBI | |
Basar R, Daher M and Rezvani K: Next-generation cell therapies: The emerging role of CAR-NK cells. Blood Adv. 4:5868–5876. 2020. View Article : Google Scholar : PubMed/NCBI | |
Zhou J, Bethune MT, Malkova N, Sutherland AM, Comin-Anduix B, Su Y, Baltimore D, Ribas A and Heath JR: A kinetic investigation of interacting, stimulated T cells identifies conditions for rapid functional enhancement, minimal phenotype differentiation, and improved adoptive cell transfer tumor eradication. PLoS One. 13:e01916342018. View Article : Google Scholar : PubMed/NCBI | |
Hinrichs CS, Borman ZA, Cassard L, Gattinoni L, Spolski R, Yu Z, Sanchez-Perez L, Muranski P, Kern SJ, Logun C, et al: Adoptively transferred effector cells derived from naive rather than central memory CD8+ T cells mediate superior antitumor immunity. Proc Natl Acad Sci USA. 106:17469–17474. 2009. View Article : Google Scholar : PubMed/NCBI | |
De Sanctis F, Trovato R and Ugel S: Anti-telomerase T cells adoptive transfer. Aging (Albany NY). 9:2239–2240. 2017. View Article : Google Scholar | |
Kondo T, Imura Y, Chikuma S, Hibino S, Omata-Mise S, Ando M, Akanuma T, Iizuka M, Sakai R, Morita R and Yoshimura A: Generation and application of human induced-stem cell memory T cells for adoptive immunotherapy. Cancer Sci. 109:2130–2140. 2018. View Article : Google Scholar : PubMed/NCBI | |
Foley KC, Nishimura MI and Moore TV: Combination immunotherapies implementing adoptive T-cell transfer for advanced-stage melanoma. Melanoma Res. 28:171–184. 2018. View Article : Google Scholar : PubMed/NCBI | |
Abi-Habib RJ, Singh R, Leppla SH, Greene JJ, Ding Y, Berghuis B, Duesbery NS and Frankel AE: Systemic anthrax lethal toxin therapy produces regressions of subcutaneous human melanoma tumors in athymic nude mice. Clin Cancer Res. 12:7437–7443. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kong LY, Abou-Ghazal MK, Wei J, Chakraborty A, Sun W, Qiao W, Fuller GN, Fokt I, Grimm EA, Schmittling RJ, et al: A novel inhibitor of signal transducers and activators of transcription 3 activation is efficacious against established central nervous system melanoma and inhibits regulatory T cells. Clin Cancer Res. 14:5759–5768. 2008. View Article : Google Scholar : PubMed/NCBI | |
Weiss T, Weller M, Guckenberger M, Sentman CL and Roth P: NKG2D-Based CAR T cells and radiotherapy exert synergistic efficacy in glioblastoma. Cancer Res. 78:1031–1043. 2018. View Article : Google Scholar : PubMed/NCBI | |
Al Hassan M, Fakhoury I, El Masri Z, Ghazale N, Dennaoui R, El Atat O, Kanaan A and El-Sibai M: Metformin treatment inhibits motility and invasion of glioblastoma cancer cells. Anal Cell Pathol (Amst). 2018:59174702018. | |
Khoury O, Ghazale N, Stone E, El-Sibai M, Frankel AE and Abi-Habib RJ: Human recombinant arginase I (Co)-PEG5000 [HuArgI (Co)-PEG5000]-induced arginine depletion is selectively cytotoxic to human glioblastoma cells. J Neurooncol. 122:75–85. 2015. View Article : Google Scholar : PubMed/NCBI | |
Dudley ME and Rosenberg SA: Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat Rev Cancer. 3:666–675. 2003. View Article : Google Scholar : PubMed/NCBI | |
Miao Y, Yang H, Levorse J, Yuan S, Polak L, Sribour M, Singh B, Rosenblum MD and Fuchs E: Adaptive immune resistance emerges from tumor-initiating stem cells. Cell. 177:1172–1186.e14. 2019. View Article : Google Scholar : PubMed/NCBI | |
Agudo J, Park ES, Rose SA, Alibo E, Sweeney R, Dhainaut M, Kobayashi KS, Sachidanandam R, Baccarini A, Merad M and Brown BD: Quiescent tissue stem cells evade immune surveillance. Immunity. 48:271–285.e5. 2018. View Article : Google Scholar : PubMed/NCBI | |
Brown JA, Yonekubo Y, Hanson N, Sastre-Perona A, Basin A, Rytlewski JA, Dolgalev I, Meehan S, Tsirigos A, Beronja S and Schober M: TGF-β-induced quiescence mediates chemoresistance of tumor-propagating cells in squamous cell carcinoma. Cell Stem Cell. 21:650–664.e8. 2017. View Article : Google Scholar : PubMed/NCBI | |
Tey SK: Adoptive T-cell therapy: Adverse events and safety switches. Clin Transl Immunology. 3:e172014. View Article : Google Scholar : PubMed/NCBI | |
Yang JC: Toxicities associated with adoptive T-cell transfer for cancer. Cancer. 21:506–509. 2015. View Article : Google Scholar : PubMed/NCBI | |
Miliotou AN and Papadopoulou LC: CAR T-cell therapy: A new era in cancer immunotherapy. Curr Pharm Biotechnol. 19:5–18. 2018. View Article : Google Scholar : PubMed/NCBI | |
Maeng HM and Berzofsky JA: Strategies for developing and optimizing cancer vaccines. F1000Res 8: F1000 Faculty Rev-654. 2019. View Article : Google Scholar | |
Gatti-Mays ME, Redman JM, Collins JM and Bilusic M: Cancer vaccines: Enhanced immunogenic modulation through therapeutic combinations. Hum Vaccines Immunother. 13:2561–2574. 2017. View Article : Google Scholar : PubMed/NCBI | |
Manthorpe M, Cornefert-Jensen F, Hartikka J, Felgner J, Rundell A, Margalith M and Dwarki V: Gene therapy by intramuscular injection of plasmid DNA: Studies on firefly luciferase gene expression in mice. Hum Gene Ther. 4:419–431. 1993. View Article : Google Scholar : PubMed/NCBI | |
Walters JN, Ferraro B, Duperret EK, Kraynyak KA, Chu J, Saint-Fleur A, Yan J, Levitsky H, Khan AS, Sardesai NY and Weiner DB: A Novel DNA vaccine platform enhances neo-antigen-like T cell responses against WT1 to break tolerance and induce anti-tumor immunity. Mol Ther. 25:976–988. 2017. View Article : Google Scholar : PubMed/NCBI | |
Lopes A, Vanvarenberg K, Kos Š, Lucas S, Colau D, Van den Eynde B, Préat V and Vandermeulen G: Combination of immune checkpoint blockade with DNA cancer vaccine induces potent antitumor immunity against P815 mastocytoma. Sci Rep. 8:157322018. View Article : Google Scholar : PubMed/NCBI | |
Paston SJ, Brentville VA, Symonds P and Durrant LG: Cancer vaccines, adjuvants, and delivery systems. Front Immunol. 12:6279322021. View Article : Google Scholar : PubMed/NCBI | |
Gamat-Huber M, Jeon D, Johnson LE, Moseman JE, Muralidhar A, Potluri HK, Rastogi I, Wargowski E, Zahm CD and McNeel DG: Treatment combinations with DNA vaccines for the treatment of Metastatic Castration-Resistant Prostate Cancer (mCRPC). Cancers (Basel). 12:28312020. View Article : Google Scholar : PubMed/NCBI | |
Li L and Petrovsky N: Molecular mechanisms for enhanced DNA vaccine immunogenicity. Expert Rev Vaccines. 15:313–329. 2016. View Article : Google Scholar : PubMed/NCBI | |
Jahanafrooz Z, Baradaran B, Mosafer J, Hashemzaei M, Rezaei T, Mokhtarzadeh A and Hamblin MR: Comparison of DNA and mRNA vaccines against cancer. Drug Discov Today. 25:552–560. 2020. View Article : Google Scholar : PubMed/NCBI | |
Bhuyan PK, Dallas M, Kraynyak K, Herring T, Morrow M, Boyer J, Duff S, Kim J and Weiner DB: Durability of response to VGX-3100 treatment of HPV16/18 positive cervical HSIL. Hum Vaccin Immunother. 17:1288–1293. 2021. View Article : Google Scholar : PubMed/NCBI | |
Lopes A, Vandermeulen G and Préat V: Cancer DNA vaccines: Current preclinical and clinical developments and future perspectives. J Exp Clin Cancer Res. 38:1462019. View Article : Google Scholar : PubMed/NCBI | |
Malonis RJ, Lai JR and Vergnolle O: Peptide-based vaccines: Current progress and future challenges. Chem Rev. 120:3210–3229. 2020. View Article : Google Scholar : PubMed/NCBI | |
Li W, Joshi MD, Singhania S, Ramsey KH and Murthy AK: Peptide vaccine: Progress and challenges. Vaccines (Basel). 2:515–536. 2014. View Article : Google Scholar : PubMed/NCBI | |
Curry JM, Besmer DM, Erick TK, Steuerwald N, Das Roy L, Grover P, Rao S, Nath S, Ferrier JW, Reid RW and Mukherjee P: Indomethacin enhances anti-tumor efficacy of a MUC1 peptide vaccine against breast cancer in MUC1 transgenic mice. PLoS One. 14:e02243092019. View Article : Google Scholar : PubMed/NCBI | |
Pan J, Zhang Q, Palen K, Wang L, Qiao L, Johnson B, Sei S, Shoemaker RH, Lubet RA, Wang Y and You M: Potentiation of Kras peptide cancer vaccine by avasimibe, a cholesterol modulator. EBioMedicine. 49:72–81. 2019. View Article : Google Scholar : PubMed/NCBI | |
Zhang R, Yuan F, Shu Y, Tian Y, Zhou B, Yi L, Zhang X, Ding Z, Xu H and Yang L: Personalized neoantigen-pulsed dendritic cell vaccines show superior immunogenicity to neoantigen-adjuvant vaccines in mouse tumor models. Cancer Immunol Immunother. 69:135–145. 2020. View Article : Google Scholar : PubMed/NCBI | |
Neek M, Kim TI and Wang SW: Protein-based nanoparticles in cancer vaccine development. Nanomedicine. 15:164–174. 2019. View Article : Google Scholar : PubMed/NCBI | |
Rousseau RF, Hirschmann-Jax C, Takahashi S and Brenner MK: Cancer vaccines. Hematol Oncol Clin North Am. 15:741–773. 2001. View Article : Google Scholar : PubMed/NCBI | |
Steinman RM and Cohn ZA: Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morphology, quantitation, tissue distribution. J Exp Med. 137:1142–1162. 1973. View Article : Google Scholar : PubMed/NCBI | |
Santos PM and Butterfield LH: Dendritic cell-based cancer vaccines. J Immunol. 200:443–449. 2018. View Article : Google Scholar : PubMed/NCBI | |
Alvarez-Dominguez C, Calderón-Gonzalez R, Terán-Navarro H, Salcines-Cuevas D, Garcia-Castaño A, Freire J, Gomez-Roman J and Rivera F: Dendritic cell therapy in melanoma. Ann Transl Med. 5:3862017. View Article : Google Scholar : PubMed/NCBI | |
de Gruijl TD, van den Eertwegh AJM, Pinedo HM and Scheper RJ: Whole-cell cancer vaccination: From autologous to allogeneic tumor- and dendritic cell-based vaccines. Cancer Immunol Immunother. 57:1569–1577. 2008. View Article : Google Scholar | |
Fu C, Zhou L, Mi QS and Jiang A: DC-Based vaccines for cancer immunotherapy. Vaccines (Basel). 8:7062020. View Article : Google Scholar : PubMed/NCBI | |
Wculek SK, Amores-Iniesta J, Conde-Garrosa R, Khouili SC, Melero I and Sancho D: Effective cancer immunotherapy by natural mouse conventional type-1 dendritic cells bearing dead tumor antigen. J Immunother Cancer. 7:1002019. View Article : Google Scholar : PubMed/NCBI | |
Lai X and Friedman A: Combination therapy of cancer with cancer vaccine and immune checkpoint inhibitors: A mathematical model. PLoS One. 12:e01784792017. View Article : Google Scholar : PubMed/NCBI | |
Anassi E and Ndefo UA: Sipuleucel-T (provenge) injection: The first immunotherapy agent (vaccine) for hormone-refractory prostate cancer. P T. 36:197–202. 2011.PubMed/NCBI | |
Ayoub NM, Al-Shami KM and Yaghan RJ: Immunotherapy for HER2-positive breast cancer: Recent advances and combination therapeutic approaches. Breast Cancer (Dove Med Press). 11:53–69. 2019.PubMed/NCBI | |
Han Q, Wang Y, Pang M and Zhang J: STAT3-blocked whole-cell hepatoma vaccine induces cellular and humoral immune response against HCC. J Exp Clin Cancer Res. 36:1562017. View Article : Google Scholar : PubMed/NCBI | |
Sheikhi A, Jafarzadeh A, Kokhaei P and Hojjat-Farsangi M: Whole tumor cell vaccine adjuvants: Comparing IL-12 to IL-2 and IL-15. Iran J Immunol. 13:148–166. 2016.PubMed/NCBI | |
Xia L, Schrump DS and Gildersleeve JC: Whole-Cell cancer vaccines induce large antibody responses to carbohydrates and glycoproteins. Cell Chem Biol. 23:1515–1525. 2016. View Article : Google Scholar : PubMed/NCBI | |
Chen G, Gupta R, Petrik S, Laiko M, Leatherman JM, Asquith JM, Daphtary MM, Garrett-Mayer E, Davidson NE, Hirt K, et al: A feasibility study of cyclophosphamide, trastuzumab, and an allogeneic GM-CSF-secreting breast tumor vaccine for HER2+ Metastatic breast cancer. Cancer Immunol Res. 2:949–961. 2014. View Article : Google Scholar : PubMed/NCBI | |
Constantino J, Gomes C, Falcão A, Cruz MT and Neves BM: Antitumor dendritic cell-based vaccines: Lessons from 20 years of clinical trials and future perspectives. Transl Res. 168:74–95. 2016. View Article : Google Scholar : PubMed/NCBI | |
Köhler G and Milstein C: Continuous cultures of fused cells secreting antibody of predefined specificity. Nature. 256:495–497. 1975. View Article : Google Scholar | |
Chung S, Lin YL, Reed C, Ng C, Cheng ZJ, Malavasi F, Yang J, Quarmby V and Song A: Characterization of in vitro antibody-dependenT cell-mediated cytotoxicity activity of therapeutic antibodies-impact of effector cells. J Immunol Methods. 407:63–75. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang W, Erbe AK, Hank JA, Morris ZS and Sondel PM: NK Cell-Mediated Antibody-DependenT cellular cytotoxicity in cancer immunotherapy. Front Immunol. 6:3682015. View Article : Google Scholar : PubMed/NCBI | |
Harris TJ and Drake CG: Primer on tumor immunology and cancer immunotherapy. J Immunother Cancer. 1:122013. View Article : Google Scholar : PubMed/NCBI | |
Mayor M, Yang N, Sterman D, Jones DR and Adusumilli PS: Immunotherapy for non-small cell lung cancer: Current concepts and clinical trials. Eur J Cardiothorac Surg. 49:1324–1333. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kimiz-Gebologlu I, Gulce-Iz S and Biray-Avci C: Monoclonal antibodies in cancer immunotherapy. Mol Biol Rep. 45:2935–2940. 2018. View Article : Google Scholar : PubMed/NCBI | |
Karlitepe A, Ozalp O and Avci CB: New approaches for cancer immunotherapy. Tumour Biol. 36:4075–4078. 2015. View Article : Google Scholar : PubMed/NCBI | |
Sathyanarayanan V and Neelapu SS: Cancer immunotherapy: Strategies for personalization and combinatorial approaches. Mol Oncol. 9:2043–2053. 2015. View Article : Google Scholar : PubMed/NCBI | |
Posner J, Barrington P, Brier T and Datta-Mannan A: Monoclonal antibodies: Past, present and future. Handb Exp Pharmacol. 260:81–141. 2019. View Article : Google Scholar : PubMed/NCBI | |
Zahavi D and Weiner L: Monoclonal Antibodies in Cancer Therapy. Antibodies (Basel). 9:342020. View Article : Google Scholar : PubMed/NCBI | |
Loi S, Giobbie-Hurder A, Gombos A, Bachelot T, Hui R, Curigliano G, Campone M, Biganzoli L, Bonnefoi H, Jerusalem G, et al: Pembrolizumab plus trastuzumab in trastuzumab-resistant, advanced, HER2-positive breast cancer (PANACEA): A single-arm, multicentre, phase 1b-2 trial. Lancet Oncol. 20:371–382. 2019. View Article : Google Scholar : PubMed/NCBI | |
ClinicalTrials.gov, . A Dose Escalation and Cohort Expansion Study of NKTR-214 in Combination With Nivolumab and Other Anti-Cancer Therapies in Patients With Select Advanced Solid Tumors (PIVOT-02). linicalTrials.gov Identifier: NCT02983045. U.S.National Library of Medicine; Bethesda, MD: 2016, https://clinicaltrials.gov/ct2/show/NCT02983045December 6–2016 | |
ClinicalTrials.gov, . Bempegaldesleukin and Pembrolizumab With or Without Chemotherapy in Locally Advanced or Metastatic Solid Tumors (PROPEL). ClinicalTrials.gov Identifier: NCT03138889. U.S.National Library of Medicine; Bethesda, MD: 2017, https://clinicaltrials.gov/ct2/show/NCT03138889May 3–2017 | |
Zimmer L, Goldinger SM, Hofmann L, Loquai C, Ugurel S, Thomas I, Schmidgen MI, Gutzmer R, Utikal JS, Göppner D, et al: Neurological, respiratory, musculoskeletal, cardiac and ocular side-effects of anti-PD-1 therapy. Eur J Cancer. 60:210–225. 2016. View Article : Google Scholar : PubMed/NCBI |