Generic placeholder image

Current Pharmaceutical Biotechnology

Author(s): Momeneh Ghanaat, Hami Kaboosi*, Babak Negahdari*, Esmail Fattahi and Ziba Veisi Malekshahi

DOI: 10.2174/1389201023666220922122531

DownloadDownload PDF Flyer Cite As
Heterologous Prime-boost Vaccination Using Adenovirus and Albumin Nanoparticles as Carriers for Human Papillomavirus 16 E7 Epitope

Page: [1195 - 1203] Pages: 9

  • * (Excluding Mailing and Handling)

Abstract

Background: Nanocarriers are these days considered an attractive approach in cancer immunotherapy owing to their ability to deliver antigens to antigen-presenting cells (APCs) for stimulating robust immune cells against the tumor.

Objectives: The objective of this study was to construct nanocomplexes using two nanocarriers with negative surface charge, adenovirus (Ad) and human serum albumin nanoparticle (HSA-NP), and coat their surface with a modified and positively-charged HPV16 E7 MHC-I specific epitope to assess their anti-tumor effects in a TC-1 mouse model.

Methods: After the construction of Ad and HSA-NP, their complexes with HPV16 E7 MHC-I specific epitope were characterized by zeta potential and dynamic light scattering. Then, the cellular immunity and CTL responses in immunized mice were assessed by measuring the levels of IL-10 and IFN-γ and the expression of CD107a, a marker of CTL response, as well as tumor inhibition.

Results: The zeta potential and dynamic light scattering results showed that incubation of the oppositely- charged nanocarriers and MHC-I specific epitope led to the formation of nanocomplexes in which the surface charge of nanocarriers was changed from negative to positive with minimal changes in the particle size. We demonstrated that the nanocomplex platforms in heterologous primeboost regimens generate significantly higher E7-specific IL-10, IFN-γ, and CTL responses. Moreover, the heterologous nanocomplex regimens, Alb/Pep-Ad/Pep and Ad/Pep-Alb/Pep, significantly suppressed the growth of TC-1 tumors in vivo compared with mice receiving homologous regimens and naked nanocarriers.

Conclusion: The heterologous nanocomplexes might serve as an effective vaccine strategy against HPV-induced cervical cancer.

Keywords: Nanocarriers, Immunotherapy, Adenovirus, Albumin, nanoparticle, Epitope.

Graphical Abstract

[1]
Brüggmann, D.; Kayser, L.; Jaque, J.; Bundschuh, M.; Klingelhöfer, D.; Groneberg, D.A. Human papilloma virus: Global research architecture assessed by density-equalizing mapping. Oncotarget, 2018, 9(31)2196521977
[http://dx.doi.org/10.18632/oncotarget.25136] [PMID: 29774116]
[2]
Ghanaat, M.; Goradel, N.H.; Arashkia, A.; Ebrahimi, N.; Ghorghanlu, S.; Malekshahi, Z.V.; Fattahi, E.; Negahdari, B.; Kaboosi, H. Virus against virus: Strategies for using adenovirus vectors in the treatment of HPV-induced cervical cancer. Acta Pharmacol. Sin., 2021, 42(12), 1981-1990.
[http://dx.doi.org/10.1038/s41401-021-00616-5] [PMID: 33633364]
[3]
Clark, K.T.; Trimble, C.L. Current status of therapeutic HPV vaccines. Gynecol. Oncol., 2020, 156(2), 503-510.
[http://dx.doi.org/10.1016/j.ygyno.2019.12.017] [PMID: 31870557]
[4]
Hoppe-Seyler, K.; Bossler, F.; Braun, J.A.; Herrmann, A.L.; Hoppe-Seyler, F. The HPV E6/E7 oncogenes: Key factors for viral carcinogenesis and therapeutic targets. Trends Microbiol., 2018, 26(2), 158-168.
[http://dx.doi.org/10.1016/j.tim.2017.07.007] [PMID: 28823569]
[5]
Ganguly, N. Human papillomavirus-16 E5 protein: Oncogenic role and therapeutic value. Cell. Oncol., 2012, 35(2), 67-76.
[http://dx.doi.org/10.1007/s13402-011-0069-x] [PMID: 22262402]
[6]
Kim, H.J.; Kim, H.J. Current status and future prospects for human papillomavirus vaccines. Arch. Pharm. Res., 2017, 40(9), 1050-1063.
[http://dx.doi.org/10.1007/s12272-017-0952-8] [PMID: 28875439]
[7]
Li, W.; Joshi, M.; Singhania, S.; Ramsey, K.; Murthy, A. Peptide vaccine: Progress and challenges. Vaccines , 2014, 2(3), 515-536.
[http://dx.doi.org/10.3390/vaccines2030515] [PMID: 26344743]
[8]
Fifis, T.; Mottram, P.; Bogdanoska, V.; Hanley, J.; Plebanski, M. Short peptide sequences containing MHC class I and/or class II epitopes linked to nano-beads induce strong immunity and inhibition of growth of antigen-specific tumour challenge in mice. Vaccine, 2004, 23(2), 258-266.
[http://dx.doi.org/10.1016/j.vaccine.2004.05.022] [PMID: 15531045]
[9]
Lee, S.J.; Kim, J.J.; Kang, K.Y.; Paik, M.J.; Lee, G.; Yee, S.T. Enhanced anti-tumor immunotherapy by silica-coated magnetic nanoparticles conjugated with ovalbumin. Int. J. Nanomedicine, 2019, 14, 8235-8249.
[http://dx.doi.org/10.2147/IJN.S194352] [PMID: 31802864]
[10]
Selvaraja, V.K.; Gudipudi, D.K. Fundamentals to clinical application of nanoparticles in cancer immunotherapy and radiotherapy. Ecancer med. Sci., 2020, 14, 1095.
[PMID: 33082845]
[11]
Thakur, N.; Thakur, S.; Chatterjee, S.; Das, J.; Sil, P.C. Nanoparticles as smart carriers for enhanced cancer immunotherapy. Front Chem., 2020, 8597806
[http://dx.doi.org/10.3389/fchem.2020.597806] [PMID: 33409265]
[12]
Hirosue, S.; Kourtis, I.C.; van der Vlies, A.J.; Hubbell, J.A.; Swartz, M.A. Antigen delivery to dendritic cells by poly(propylene sulfide) nanoparticles with disulfide conjugated peptides: Cross-presentation and T cell activation. Vaccine, 2010, 28(50), 7897-7906.
[http://dx.doi.org/10.1016/j.vaccine.2010.09.077] [PMID: 20934457]
[13]
Galliverti, G.; Tichet, M.; Domingos-Pereira, S.; Hauert, S.; Nardelli-Haefliger, D.; Swartz, M.A.; Hanahan, D.; Wullschleger, S. Nanoparticle conjugation of human papillomavirus 16 E7-long peptides enhances therapeutic vaccine efficacy against solid tumors in mice. Cancer Immunol. Res., 2018, 6(11), 1301-1313.
[http://dx.doi.org/10.1158/2326-6066.CIR-18-0166] [PMID: 30131378]
[14]
Capasso, C.; Hirvinen, M.; Garofalo, M.; Romaniuk, D.; Kuryk, L.; Sarvela, T.; Vitale, A.; Antopolsky, M.; Magarkar, A.; Viitala, T.; Suutari, T.; Bunker, A.; Yliperttula, M.; Urtti, A.; Cerullo, V. Oncolytic adenoviruses coated with MHC-I tumor epitopes increase the antitumor immunity and efficacy against melanoma. OncoImmunology, 2016, 5(4)e1105429
[http://dx.doi.org/10.1080/2162402X.2015.1105429] [PMID: 27141389]
[15]
Garofalo, M.; Iovine, B.; Kuryk, L.; Capasso, C.; Hirvinen, M.; Vitale, A.; Yliperttula, M.; Bevilacqua, M.A.; Cerullo, V. Oncolytic adenovirus loaded with L-carnosine as novel strategy to enhance the antitumor activity. Mol. Cancer Ther., 2016, 15(4), 651-660.
[http://dx.doi.org/10.1158/1535-7163.MCT-15-0559] [PMID: 26861248]
[16]
Xiang, S.D.; Wilson, K.L.; Goubier, A.; Heyerick, A.; Plebanski, M. Design of peptide-based nanovaccines targeting leading antigens from gynecological cancers to induce HLA-A2. 1 restricted CD8+ T cell responses. Front. Immunol., 2018, 9, 2968.
[http://dx.doi.org/10.3389/fimmu.2018.02968] [PMID: 30631324]
[17]
Luis de Redín, I.; Boiero, C.; Martínez-Ohárriz, M.C.; Agüeros, M.; Ramos, R.; Peñuelas, I.; Allemandi, D.; Llabot, J.M.; Irache, J.M. Human serum albumin nanoparticles for ocular delivery of bevacizumab. Int. J. Pharm., 2018, 541(1-2), 214-223.
[http://dx.doi.org/10.1016/j.ijpharm.2018.02.003] [PMID: 29481946]
[18]
Faustino-Rocha, A.; Oliveira, P.A.; Pinho-Oliveira, J.; Teixeira-Guedes, C.; Soares-Maia, R.; da Costa, R.G.; Colaço, B.; Pires, M.J.; Colaço, J.; Ferreira, R.; Ginja, M. Estimation of rat mammary tumor volume using caliper and ultrasonography measurements. Lab. Anim., 2013, 42(6), 217-224.
[http://dx.doi.org/10.1038/laban.254] [PMID: 23689461]
[19]
de Alencar, B.C.G.; Persechini, P.M.; Haolla, F.A.; de Oliveira, G.; Silverio, J.C.; Lannes-Vieira, J.; Machado, A.V.; Gazzinelli, R.T.; Bruna-Romero, O.; Rodrigues, M.M. Perforin and gamma interferon expression are required for CD4+ and CD8+ T-cell-dependent protective immunity against a human parasite, Trypanosoma cruzi, elicited by heterologous plasmid DNA prime-recombinant adenovirus 5 boost vaccination. Infect. Immun., 2009, 77(10), 4383-4395.
[http://dx.doi.org/10.1128/IAI.01459-08] [PMID: 19651871]
[20]
Fasbender, A.; Zabner, J.; Chillón, M.; Moninger, T.O.; Puga, A.P.; Davidson, B.L.; Welsh, M.J. Complexes of adenovirus with polycationic polymers and cationic lipids increase the efficiency of gene transfer in vitro and in vivo. J. Biol. Chem., 1997, 272(10), 6479-6489.
[http://dx.doi.org/10.1074/jbc.272.10.6479] [PMID: 9045673]
[21]
Kamali, M.; Dinarvand, R.; Maleki, H.; Arzani, H.; Mahdaviani, P.; Nekounam, H.; Adabi, M.; Khosravani, M. Preparation of imatinib base loaded human serum albumin for application in the treatment of glioblastoma. RSC Advances, 2015, 5(76), 62214-62219.
[http://dx.doi.org/10.1039/C5RA08501B]
[22]
Toubaji, A.; Hill, S.; Terabe, M.; Qian, J.; Floyd, T.; Simpson, R.M.; Berzofsky, J.A.; Khleif, S.N. The combination of GM-CSF and IL-2 as local adjuvant shows synergy in enhancing peptide vaccines and provides long term tumor protection. Vaccine, 2007, 25(31), 5882-5891.
[http://dx.doi.org/10.1016/j.vaccine.2007.05.040] [PMID: 17602804]
[23]
Lin, K.; Doolan, K.; Hung, C.F.; Wu, T.C. Perspectives for preventive and therapeutic HPV vaccines. J. Formos. Med. Assoc., 2010, 109(1), 4-24.
[http://dx.doi.org/10.1016/S0929-6646(10)60017-4] [PMID: 20123582]
[24]
Geutskens, S.B.; van der Eb, M.M.; Plomp, A.C.; Jonges, L.E.; Cramer, S.J.; Ensink, N.G.; Kuppen, P.J.K.; Hoeben, R.C. Recombinant adenoviral vectors have adjuvant activity and stimulate T cell responses against tumor cells. Gene Ther., 2000, 7(16), 1410-1416.
[http://dx.doi.org/10.1038/sj.gt.3301251] [PMID: 10981668]
[25]
Coughlan, L. Factors which contribute to the immunogenicity of non-replicating adenoviral vectored vaccines. Front. Immunol., 2020, 11, 909.
[http://dx.doi.org/10.3389/fimmu.2020.00909] [PMID: 32508823]
[26]
Tamanini, A.; Nicolis, E.; Bonizzato, A.; Bezzerri, V.; Melotti, P.; Assael, B.M.; Cabrini, G. Interaction of adenovirus type 5 fiber with the coxsackievirus and adenovirus receptor activates inflammatory response in human respiratory cells. J. Virol., 2006, 80(22), 11241-11254.
[http://dx.doi.org/10.1128/JVI.00721-06] [PMID: 16956941]
[27]
Schoggins, J.W.; Nociari, M.; Philpott, N.; Falck-Pedersen, E. Influence of fiber detargeting on adenovirus-mediated innate and adaptive immune activation. J. Virol., 2005, 79(18), 11627-11637.
[http://dx.doi.org/10.1128/JVI.79.18.11627-11637.2005] [PMID: 16140740]
[28]
Zhou, Y.C.; Zhang, Y.N.; Yang, X.; Wang, S.B.; Hu, P.Y. Delivery systems for enhancing oncolytic adenoviruses efficacy. Int. J. Pharm., 2020, 591119971
[http://dx.doi.org/10.1016/j.ijpharm.2020.119971] [PMID: 33059014]
[29]
Danaei, M.; Dehghankhold, M.; Ataei, S.; Hasanzadeh Davarani, F.; Javanmard, R.; Dokhani, A.; Khorasani, S.; Mozafari, M. Impact of particle size and polydispersity index on the clinical applications of lipidic nanocarrier systems. Pharmaceutics, 2018, 10(2), 57.
[http://dx.doi.org/10.3390/pharmaceutics10020057] [PMID: 29783687]
[30]
Cho, E.C.; Xie, J.; Wurm, P.A.; Xia, Y. Understanding the role of surface charges in cellular adsorption versus internalization by selectively removing gold nanoparticles on the cell surface with a I2/KI etchant. Nano Lett., 2009, 9(3), 1080-1084.
[http://dx.doi.org/10.1021/nl803487r] [PMID: 19199477]
[31]
Zhao, F.; Zhao, Y.; Liu, Y. Cellular uptake, intracellular trafficking, and cytotoxicity of nanomaterials. Small, 2011, 7(10), 1322-1337.
[32]
Wang, H.X.; Zuo, Z.Q.; Du, J.Z.; Wang, Y.C.; Sun, R.; Cao, Z.T.; Ye, X.D.; Wang, J.L.; Leong, K.W.; Wang, J. Surface charge critically affects tumor penetration and therapeutic efficacy of cancer nanomedicines. Nano Today, 2016, 11(2), 133-144.
[http://dx.doi.org/10.1016/j.nantod.2016.04.008]
[33]
Xiao, K.; Li, Y.; Luo, J.; Lee, J.S.; Xiao, W.; Gonik, A.M.; Agarwal, R.G.; Lam, K.S. The effect of surface charge on in vivo biodistribution of PEG-oligocholic acid based micellar nanoparticles. Biomaterials, 2011, 32(13), 3435-3446.
[http://dx.doi.org/10.1016/j.biomaterials.2011.01.021] [PMID: 21295849]
[34]
Roser, M.; Fischer, D.; Kissel, T. Surface-modified biodegradable albumin nano- and microspheres. II: Effect of surface charges on in vitro phagocytosis and biodistribution in rats. Eur. J. Pharm. Biopharm., 1998, 46(3), 255-263.
[http://dx.doi.org/10.1016/S0939-6411(98)00038-1] [PMID: 9885296]
[35]
Dobrovolskaia, M.A.; Aggarwal, P.; Hall, J.B.; McNeil, S.E. Preclinical studies to understand nanoparticle interaction with the immune system and its potential effects on nanoparticle biodistribution. Mol. Pharm., 2008, 5(4), 487-495.
[http://dx.doi.org/10.1021/mp800032f] [PMID: 18510338]
[36]
Khan, M.A.; Malik, A.; Alzohairy, M.A.; Alruwetei, A.M.; Alhatlani, B.Y.; Rugaie, O.A.; Khan, A. Liposome-mediated delivery of MERS antigen induces potent humoral and cell-mediated immune response in mice. Molecules, 2022, 27(2), 403.
[http://dx.doi.org/10.3390/molecules27020403] [PMID: 35056718]
[37]
Khan, M.A.; Malik, A.; Alruwetei, A.M.; Alzohairy, M.A.; Alhatlani, B.Y.; Al Rugaie, O.; Alhumaydhi, F.A.; Khan, A. Delivery of MERS antigen encapsulated in α-GalCer-bearing liposomes elicits stronger antigen-specific immune responses. J. Drug Target., 2022, 1-10.
[http://dx.doi.org/10.1080/1061186X.2022.2066681] [PMID: 35418263]
[38]
Lin, T.; Liang, S.; Meng, F.; Han, Q.; Guo, C.; Sun, L.; Chen, Y.; Liu, Z.; Yu, Z.; Xie, H.; Ding, J.; Fan, D. Enhanced immunogenicity and antitumour effects with heterologous prime-boost regime using vaccines based on MG7-Ag mimotope of gastric cancer. Clin. Exp. Immunol., 2006, 144(2), 319-325.
[http://dx.doi.org/10.1111/j.1365-2249.2006.03065.x] [PMID: 16634806]
[39]
Lemke, C.D.; Geary, S.M.; Joshi, V.B.; Salem, A.K. Antigen-coated poly α-hydroxy acid based microparticles for heterologous prime-boost adenovirus based vaccinations. Biomaterials, 2013, 34(10), 2524-2529.
[http://dx.doi.org/10.1016/j.biomaterials.2012.12.030] [PMID: 23312902]
[40]
Ring, S.S.; Królik, M.; Hartmann, F.; Schmidt, E.; Hasan Ali, O.; Ludewig, B.; Kochanek, S.; Flatz, L. Heterologous prime boost vaccination induces protective melanoma-specific CD8+ T cell responses. Mol. Ther. Oncolytics, 2020, 19, 179-187.
[http://dx.doi.org/10.1016/j.omto.2020.10.001] [PMID: 33209978]
[41]
van der Burg, S.H.; Kwappenberg, K.M.C.; O’Neill, T.; Brandt, R.M.P.; Melief, C.J.M.; Hickling, J.K.; Offringa, R. Pre-clinical safety and efficacy of TA-CIN, a recombinant HPV16 L2E6E7 fusion protein vaccine, in homologous and heterologous prime-boost regimens. Vaccine, 2001, 19(27), 3652-3660.
[http://dx.doi.org/10.1016/S0264-410X(01)00086-X] [PMID: 11395199]
[42]
Mackova, J.; Stasikova, J.; Kutinova, L.; Masin, J.; Hainz, P.; Simsova, M.; Gabriel, P.; Sebo, P.; Nemeckova, S. Prime/boost immunotherapy of HPV16-induced tumors with E7 protein delivered by Bordetella adenylate cyclase and modified vaccinia virus Ankara. Cancer Immunol. Immunother., 2006, 55(1), 39-46.
[http://dx.doi.org/10.1007/s00262-005-0700-7] [PMID: 15926077]