1,045
Views
6
CrossRef citations to date
0
Altmetric
Research Paper

Enhanced therapeutic efficacy of Listeria-based cancer vaccine with codon-optimized HPV16 E7

, , ORCID Icon, , , , , , ORCID Icon & ORCID Icon show all
Pages 1568-1577 | Received 15 Jul 2020, Accepted 13 Oct 2020, Published online: 15 Jan 2021

References

  • Wakeham K, Kavanagh K. The burden of HPV-associated anogenital cancers. Curr Oncol Rep. 2014;16(9):402. doi:10.1007/s11912-014-0402-4.
  • Small W, Bacon MA Jr, Bajaj A, Chuang LT, Fisher BJ, Harkenrider MM, Jhingran A, Kitchener HC, Mileshkin LR, Viswanathan AN, et al. Cervical cancer: A global health crisis. Cancer. 2017;123(13):2404–12. doi:10.1002/cncr.30667.
  • Luo X, Donnelly CR, Gong W, Heath BR, Hao Y, Donnelly LA, Moghbeli T, Tan YS, Lin X, Bellile E, et al. HPV16 drives cancer immune escape via NLRX1-mediated degradation of STING. J Clin Invest. 2020;130(4):1635–52. doi:10.1172/JCI129497.
  • Zhu B, Xiao Y, Yeager M, Clifford G, Wentzensen N, Cullen M, Boland JF, Bass S, Steinberg MK, Raine-Bennett T, et al. Mutations in the HPV16 genome induced by APOBEC3 are associated with viral clearance. Nat Commun. 2020;11(1):886. doi:10.1038/s41467-020-14730-1.
  • Kim HJ, Kim HJ. Current status and future prospects for human papillomavirus vaccines. Arch Pharm Res. 2017;40(9):1050–63. doi:10.1007/s12272-017-0952-8.
  • Kash N, MA L, Kollipara R, Downing C, Guidry J, Tyring SK. Safety and efficacy data on vaccines and immunization to human papillomavirus. J Clin Med. 2015;4(4):614–33. doi:10.3390/jcm4040614.
  • Yang A, Jeang J, Cheng K, Cheng T, Yang B, Wu TC, Hung CF. Current state in the development of candidate therapeutic HPV vaccines. Expert Rev Vaccines. 2016;15(8):989–1007. doi:10.1586/14760584.2016.1157477.
  • Nomura T, Kawamura I, Tsuchiya K, Kohda C, Baba H, Ito Y, Kimoto T, Watanabe I, Mitsuyama M. Essential role of interleukin-12 (IL-12) and IL-18 for gamma interferon production induced by listeriolysin O in mouse spleen cells. Infect Immun. 2002;70(3):1049–55. doi:10.1128/IAI.70.3.1049-1055.2002.
  • Stockinger S, Kastner R, Kernbauer E, Pilz A, Westermaye S, Reutterer B, Soulat D, Stengl G, Vogl C, Frenz T, et al. Characterization of the interferon-producing cell in mice infected with Listeria monocytogenes. PLoS Pathog. 2009;5(3):e1000355. doi:10.1371/journal.ppat.1000355.
  • Pamer EG. Immune responses to Listeria monocytogenes. Nat Rev Immunol. 2004;4(10):812–23. doi:10.1038/nri1461.
  • Pillich H, Chakraborty T, Mraheil MA. Cell-autonomous responses in Listeria monocytogenes infection. Future Microbiol. 2015;10(4):583–97. doi:10.2217/fmb.15.4.
  • Maciag PC, Radulovic S, Rothman J. The first clinical use of a live-attenuated Listeria monocytogenes vaccine: a Phase I safety study of Lm-LLO-E7 in patients with advanced carcinoma of the cervix. Vaccine. 2009;27(30):3975–83. doi:10.1016/j.vaccine.2009.04.041.
  • Jia YY, Tan WJ, Duan FF, Pan ZM, Chen X, Yin YL, Jiao XA. A genetically modified attenuated Listeria vaccine expressing HPV16 E7 kill tumor cells in direct and antigen-specific manner. Front Cell Infect Microbiol. 2017;7:279. doi:10.3389/fcimb.2017.00279.
  • Yin Y, Lian K, Zhao D, Tao C, Chen X, Tan W, Wang X, Xu Z, Hu M, Rao Y, et al. A promising Listeria-vectored vaccine induces Th1-type immune responses and confers protection against tuberculosis. Front Cell Infect Microbiol. 2017;7:407. doi:10.3389/fcimb.2017.00407.
  • Basu P, Mehta A, Jain M, Gupta S, Nagarkar RV, John S, Petit R. A randomized phase 2 study of ADXS11-001 Listeria monocytogenes-listeriolysin O immunotherapy with or without cisplatin in treatment of advanced cervical cancer. Int J Gynecol Cancer. 2018;28(4):764–72. doi:10.1097/IGC.0000000000001235.
  • Ginaldi L, Loreto MF, Corsi MP, Modesti M, De Martinis M. Immunosenescence and infectious diseases. Microbes Infect. 2001;3(10):851–57. doi:10.1016/S1286-4579(01)01443-5.
  • Lithwick G, Margalit H. Hierarchy of sequence-dependent features associated with prokaryotic translation. Genome Res. 2003;13(12):2665–73. doi:10.1101/gr.1485203.
  • Gustafsson C, Govindarajan S, Minshull J. Codon bias and heterologous protein expression. Trends Biotechnol. 2004;22(7):346–53. doi:10.1016/j.tibtech.2004.04.006.
  • Maertens B, Spriestersbach A, von Groll U, Roth U, Kubicek J, Gerrits M, Graf M, Liss M, Daubert D, Wagner R, et al. Gene optimization mechanisms: a multi-gene study reveals a high success rate of full-length human proteins expressed in Escherichia coli. Protein Sci. 2010;19(7):1312–26. doi:10.1002/pro.408.
  • Xiang L, Wang Q, Zhou Y, Yin L, Zhang G, Ma Y. High-level expression of a ZEN-detoxifying gene by codon optimization and biobrick in Pichia pastoris. Microbiol Res. 2016;193:48–56. doi:10.1016/j.micres.2016.09.004.
  • Zhao KN, Chen J. Codon usage roles in human papillomavirus. Rev Med Virol. 2011;21(6):397–411. doi:10.1002/rmv.707.
  • Takakura Y, Katayama S, Nagata Y. High-level expression of tamavidin 2 in human cells by codon-usage optimization. Biosci Biotechnol Biochem. 2015;79(4):610–16. doi:10.1080/09168451.2014.991690.
  • Lafay B, Lloyd AT, McLean MJ, Devine KM, Sharp PM, Wolfe KH. Proteome composition and codon usage in spirochaetes: species-specific and DNA strand-specific mutational biases. Nucleic Acids Res. 1999;27(7):1642–49. doi:10.1093/nar/27.7.1642.
  • Sharp PM, Bailes E, Grocock RJ, Peden JF, Sockett RE. Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res. 2005;33(4):1141–53. doi:10.1093/nar/gki242.
  • Yin Y, Zhang C, Dong H, Niu Z, Pan Z, Huang J, Jiao X. Protective immunity induced by a LLO-deficient Listeria monocytogenes. Microbiol Immunol. 2010;54(4):175–83. doi:10.1111/j.1348-0421.2010.00211.x.
  • Park SF, Stewart GS. High-efficiency transformation of Listeria monocytogenes by electroporation of penicillin-treated cells. Gene. 1990;94(1):129–32. doi:10.1016/0378-1119(90)90479-B.
  • Zhou J, Liu WJ, Peng SW, Sun XY, Frazer I. Papillomavirus capsid protein expression level depends on the match between codon usage and tRNA availability. J Virol. 1999;73(6):4972–82. doi:10.1128/JVI.73.6.4972-4982.1999.
  • Jia Y, Yin Y, Tan W, Duan F, Pan Z, Chen X, Jiao XA. Construction and characterization of an attenuated recombinant Listeria monocytogenes vector vaccine delivering HPV16 E7. Chinese J Biotechnol. 2016;32:683–92.
  • Forman D, de Martel C, Lacey CJ, Soerjomataram I, Lortet-Tieulent J, Bruni L, Vignat J, Ferlay J, Bray F, Plummer M, et al. Global burden of human papillomavirus and related diseases. Vaccine. 2012;30:F12–F23. doi:10.1016/j.vaccine.2012.07.055.
  • Gupta SM, Mania-Pramanik J. Molecular mechanisms in progression of HPV-associated cervical carcinogenesis. J Biomed Sci. 2019;26:28.
  • Miles BA, Monk BJ, Safran HP. Mechanistic insights into ADXS11-001 human papillomavirus-associated cancer immunotherapy. Gynecol Oncol Res Pract. 2017;4:9. doi:10.1186/s40661-017-0046-9.
  • Petit RG, Mehta A, Jain M, Gupta S, Nagarkar R, Kumar V, Premkumar S, Neve R, John S, Basu P. ADXS11-001 immunotherapy targeting HPV-E7: final results from a Phase II study in Indian women with recurrent cervical cancer. J ImmunoTher Cancer. 2014;2(S3):1–2. doi:10.1186/2051-1426-2-S3-P92.
  • Kawana K, Adachi K, Kojima S, Taguchi A, Tomio K, Yamashita A, Nishida H, Nagasaka K, Arimoto T, Yokoyama T, et al. Oral vaccination against HPV E7 for treatment of cervical intraepithelial neoplasia grade 3 (CIN3) elicits E7-specific mucosal immunity in the cervix of CIN3 patients. Vaccine. 2014;32(47):6233–39. doi:10.1016/j.vaccine.2014.09.020.
  • Komatsu A, Igimi S, Kawana K. Optimization of human papillomavirus (HPV) type 16 E7-expressing lactobacillus-based vaccine for induction of mucosal E7-specific IFNγ-producing cells. Vaccine. 2018;36(24):3423–26. doi:10.1016/j.vaccine.2018.05.009.
  • Bosch FX, de Sanjosé S. Chapter 1: human papillomavirus and cervical cancer–burden and assessment of causality. J Natl Cancer Inst Monogr. 2003;2003(31):3–13. doi:10.1093/oxfordjournals.jncimonographs.a003479.
  • Adachi K, Kawana K, Yokoyama T, Fujii T, Tomio A, Miura S, Tomio K, Kojima S, Oda K, Sewaki T, et al. Oral immunization with a Lactobacillus casei vaccine expressing human papillomavirus (HPV) type 16 E7 is an effective strategy to induce mucosal cytotoxic lymphocytes against HPV16 E7. Vaccine. 2010;28(16):2810–17. doi:10.1016/j.vaccine.2010.02.005.
  • Huddleston JR. Horizontal gene transfer in the human gastrointestinal tract: potential spread of antibiotic resistance genes. Infect Drug Resist. 2014;7:167–76. doi:10.2147/IDR.S48820.
  • Sacco JJ, Evans M, Harrington KJ, Man S, Powell N, Shaw RJ, Jones TM. Systemic listeriosis following vaccination with the attenuated Listeria monocytogenes therapeutic vaccine, ADXS11-001. Hum Vaccin Immunother. 2016;12(4):1085–86. doi:10.1080/21645515.2015.1121338.
  • Yang A, Farmer E, Wu TC, Hung CF. Perspectives for therapeutic HPV vaccine development. J Biomed Sci. 2016;23(1):75. doi:10.1186/s12929-016-0293-9.
  • Fares E, McCloskey CB, Gutierrez A, Princiotta M, Salinas LJ, Drevets DA. Vaccine strain Listeria monocytogenes bacteremia occurring 31 months after immunization. Infection. 2019;47(3):489–92. doi:10.1007/s15010-018-1249-7.
  • Wang S, Huang W, Li K, Yao Y, Yang X, Bai H, Sun W, Liu C, Ma Y. Engineered outer membrane vesicle is potent to elicit HPV16E7-specific cellular immunity in a mouse model of TC-1 graft tumor. Int J Nanomedicine. 2017;12:6813–25. doi:10.2147/IJN.S143264.
  • Ang KS, Kyriakopoulos S, Li W, Lee DY. Multi-omics data driven analysis establishes reference codon biases for synthetic gene design in microbial and mammalian cells. Methods. 2016;102:26–35. doi:10.1016/j.ymeth.2016.01.016.
  • Wu J, Ma H, Qu Q, Zhou WJ, Luo YP, Thangaraj H, Lowrie DB, XY F. Incorporation of immunostimulatory motifs in the transcribed region of a plasmid DNA vaccine enhances Th1 immune responses and therapeutic effect against Mycobacterium tuberculosis in mice. Vaccine. 2011;29(44):7624–30. doi:10.1016/j.vaccine.2011.08.020.
  • Fan RL, Valkenburg SA, Wong CK, Li OT, Nicholls JM, Rabadan R, Peiris JS, Poon LL. Generation of live attenuated influenza virus by using codon usage bias. J Virol. 2015;89(21):10762–73. doi:10.1128/JVI.01443-15.
  • Soleimanjahi H, Razavinikoo H, Fotouhi F, Ardebili A. Antitumor response to a codon-optimized HPV-16 E7/HSP70 fusion antigen DNA vaccine. Iran J Immunol. 2017;14:180–91.
  • Latanova AA, Petkov S, Kilpelainen A, Jansons J, Latyshev OE, Kuzmenko YV, Hinkula J, Abakumov MA, Valuev-Elliston VT, Gomelsky M, et al. Codon optimization and improved delivery/immunization regimen enhance the immune response against wild-type and drug-resistant HIV-1 reverse transcriptase, preserving its Th2-polarity. Sci Rep. 2018;8(1):8078. doi:10.1038/s41598-018-26281-z.
  • Suschak JJ, Dupuy LC, Shoemaker CJ, Six C, Kwilas SA, Spik KW, Williams JA, Schmaljohn CS. Nanoplasmid vectors co-expressing innate immune agonists enhance DNA vaccines for Venezuelan Equine Encephalitis virus and Ebola virus. Molecular therapy. Mol Ther Methods Clin Dev. 2020;17:810–21. doi:10.1016/j.omtm.2020.04.009.
  • Shahabi V, Reyes-Reyes M, Wallecha A, Rivera S, Paterson Y, Maciag P. Development of a Listeria monocytogenes based vaccine against prostate cancer. Cancer Immunol Immunother. 2008;57(9):1301–13. doi:10.1007/s00262-008-0463-z.
  • Wood LM, Attenuated PY. Listeria monocytogenes: a powerful and versatile vector for the future of tumor immunotherapy. Front Cell Infect Microbiol. 2014;4:51. doi:10.3389/fcimb.2014.00051.
  • Ikemura T. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. J Mol Biol. 1981;151(3):389–409. doi:10.1016/0022-2836(81)90003-6.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.