AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Article Link
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article

Efficient delivery of clay-based nanovaccines to the mouse spleen promotes potent anti-tumor immunity for both prevention and treatment of lymphoma

Ling-Xiao Zhang1,3,4,5,,§Ying-Bo Jia4,5,§Ya-Ru Huang4,5Hui-Na Liu1,2Xia-Mei Sun4Ting Cai1,2( )Rui-Tian Liu4( )Zhi Ping Xu3( )
Hwa Mei Hospital, University of Chinese Academy of Sciences (Ningbo No.2 Hospital), Ningbo 315010, China
Ningbo Institute of Life and Health Industry, University of Chinese Academy of Sciences, Ningbo 315010, China
Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, St Lucia, QLD 4072, Australia
State Key Laboratory of Biochemical Engineering, Institute of Process Engineering, Chinese Academy of Sciences, Beijing 100190, China
School of Chemical Engineering, University of Chinese Academy of Sciences, Beijing 100049, China
Show Author Information

Graphical Abstract

Abstract

Cancer therapeutic nanovaccines are ideal tools to inhibit tumor growth and provide the body with continuous protecting immune surveillance. However, the conventional subcutaneous (SC) vaccination normally induces limited anti-tumor immune responses with low therapeutic efficacy. Herein, we devised clay-based nanovaccines and directly delivered them to the spleen via intravenous (IV) injection to induce the stronger anti-tumor immunity with higher efficacy for tumor prevention and treatment. The clay, i.e., layered double hydroxide (LDH) was prepared as nanoadjuvant with the average size from 77 to 285 nm and co-loaded with the model antigen ovalbumin (OVA) and bioadjuvant CpG to form CpG/OVA-LDH (CO-LDH) nanovaccines. We found that CO-LDH-215 (the size of LDH was 215 nm) promoted dendritic cells to present the most antigen, and moreover showed the highest spleen enrichment (~ 1.67% of CO-LDH-215 enriched in the spleen at 24 h post IV injection). The in vivo immunologic data showed that CO-LDH-215 induced the most potent anti-tumor immune responses and completely prevented the growth of E.G7-OVA tumor in the mouse model. Furthermore, IV injected CO-LDH-215 nanovaccine more effectively delayed tumor growth than that SC injected, largely due to the direct and quick delivery of more nanovaccines to the spleen. This study demonstrates that the therapeutic efficacy of nanovaccines can be greatly enhanced by targeted delivery of nanovaccines to the spleen via the proper vaccination route.

Electronic Supplementary Material

Download File(s)
12274_2020_3175_MOESM1_ESM.pdf (1.9 MB)

References

[1]
C. J. M. Melief,; T. van Hall,; R. Arens,; F. Ossendorp,; S. H. van Der Burg, Therapeutic cancer vaccines. J. Clin. Invest. 2015, 125, 3401-3412.
[2]
I. Melero,; G. Gaudernack,; W. Gerritsen,; C. Huber,; G. Parmiani,; S. Scholl,; N. Thatcher,; J. Wagstaff,; C. Zielinski,; I. Faulkner, et al. Therapeutic vaccines for cancer: An overview of clinical trials. Nat. Rev. Clin. Oncol. 2014, 11, 509-524.
[3]
H. Wang,; D. J. Mooney, Biomaterial-assisted targeted modulation of immune cells in cancer treatment. Nat. Mater. 2018, 17, 761-772.
[4]
W. Y. Chen,; H. L. Zuo,; B. Li,; C. C. Duan,; B. Rolfe,; B. Zhang,; T. J. Mahony,; Z. P. Xu, Clay nanoparticles elicit long-term immune responses by forming biodegradable depots for sustained antigen stimulation. Small 2018, 14, 1704465.
[5]
A. W. Li,; M. C. Sobral,; S. Badrinath,; Y. Choi,; A. Graveline,; A. G. Stafford,; J. C. Weaver,; M. O. Dellacherie,; T. Y. Shih,; O. A. Ali, et al. A facile approach to enhance antigen response for personalized cancer vaccination. Nat. Mater. 2018, 17, 528-534.
[6]
Y. F. Xia,; J. Wu,; W. Wei,; Y. Q. Du,; T. Wan,; X. W. Ma,; W. Q. An,; A. Y. Guo,; C. Y. Miao,; H. Yue, et al. Exploiting the pliability and lateral mobility of Pickering emulsion for enhanced vaccination. Nat. Mater. 2018, 17, 187-194.
[7]
A. A. Itano,; M. K. Jenkins, Antigen presentation to naive CD4 T cells in the lymph node. Nat. Immunol. 2003, 4, 733-739.
[8]
U. H. Von Andrian,; T. R. Mempel, Homing and cellular traffic in lymph nodes. Nat. Rev. Immunol 2003, 3, 867-878.
[9]
J. G. Cyster, Chemokines and the homing of dendritic cells to the T cell areas of lymphoid organs. J. Exp. Med. 1999, 189, 447-450.
[10]
M. F. Bachmann,; G. T. Jennings, Vaccine delivery: A matter of size, geometry, kinetics and molecular patterns. Nat. Rev. Immunol. 2010, 10, 787-796.
[11]
J. Liu,; H. J. Li,; Y. L. Luo,; C. F. Xu,; X. J. Du,; J. Z. Du,; J. Wang, Enhanced primary tumor penetration facilitates nanoparticle draining into lymph nodes after systemic injection for tumor metastasis inhibition. ACS Nano 2019, 13, 8648-8658.
[12]
L. X. Zhang,; X. X. Xie,; D. Q. Liu,; Z. P. Xu,; R. T. Liu, Efficient co-delivery of neo-epitopes using dispersion-stable layered double hydroxide nanoparticles for enhanced melanoma immunotherapy. Biomaterials 2018, 174, 54-66.
[13]
H. Sultan,; T. Kumai,; T. Nagato,; J. Wu,; A. M. Salazar,; E. Celis, The route of administration dictates the immunogenicity of peptide-based cancer vaccines in mice. Cancer Immunol. Immunother. 2019, 68, 455-466.
[14]
X. Han,; S. F. Shen,; Q. Fan,; G. J. Chen,; E. Archibong,; G. Dotti,; Z. Liu,; Z. Gu,; C. Wang, Red blood cell-derived nanoerythrosome for antigen delivery with enhanced cancer immunotherapy. Sci. Adv. 2019, 5, eaaw6870.
[15]
V. Bronte,; M. J. Pittet, The spleen in local and systemic regulation of immunity. Immunity 2013, 39, 806-818.
[16]
L. M. Kranz,; M. Diken,; H. Haas,; S. Kreiter,; C. Loquai,; K. C. Reuter,; M. Meng,; D. Fritz,; F. Vascotto,; H. Hefesha, et al. Systemic RNA delivery to dendritic cells exploits antiviral defence for cancer immunotherapy. Nature 2016, 534, 396-401.
[17]
J. P. Liu,; R. Zhang,; Z. P. Xu, Nanoparticle-based nanomedicines to promote cancer immunotherapy: Recent advances and future directions. Small 2019, 15, 1900262.
[18]
L. X. Zhang,; D. Q. Liu,; S. W. Wang,; X. L. Yu,; M. Ji,; X. X. Xie,; S. Y. Liu,; R. T. Liu, MgAl-layered double hydroxide nanoparticles co-delivering siIDO and Trp2 peptide effectively reduce IDO expression and induce cytotoxic T-lymphocyte responses against melanoma tumor in mice. J. Mater. Chem. B 2017, 5, 6266-6276.
[19]
W. Y. Chen,; B. Zhang,; T. Mahony,; W. Y. Gu,; B. Rolfe,; Z. P. Xu, Efficient and durable vaccine against intimin β of diarrheagenic E. Coli induced by clay nanoparticles. Small 2016, 12, 1627-1639.
[20]
S. Y. Yan,; B. E. Rolfe,; B. Zhang,; Y. H. Mohammed,; W. Y. Gu,; Z. P. Xu, Polarized immune responses modulated by layered double hydroxides nanoparticle conjugated with CpG. Biomaterials 2014, 35, 9508-9516.
[21]
S. Y. Yan,; W. Y. Gu,; B. Zhang,; B. E. Rolfe,; Z. P. Xu, High adjuvant activity of layered double hydroxide nanoparticles and nanosheets in anti-tumour vaccine formulations. Dalton Trans. 2018, 47, 2956-2964.
[22]
Z. P. Xu,; G. S. Stevenson,; C. Q. Lu,; G. Q. Lu,; P. F. Bartlett,; P. P. Gray, Stable suspension of layered double hydroxide nanoparticles in aqueous solution. J. Am. Chem. Soc. 2006, 128, 36-37.
[23]
Z. Gu,; H. L. Zuo,; L. Li,; A. H. Wu,; Z. P. P. Xu, Pre-coating layered double hydroxide nanoparticles with albumin to improve colloidal stability and cellular uptake. J. Mater. Chem. B 2015, 3, 3331-3339.
[24]
P. R. Wei,; S. H. Cheng,; W. N. Liao,; K. C. Kao,; C. F. Weng,; C. H. Lee, Synthesis of chitosan-coated near-infrared layered double hydroxide nanoparticles for in vivo optical imaging. J. Mater. Chem. 2012, 22, 5503-5513.
[25]
L. X. Zhang,; X. M. Sun,; Z. P. Xu,; R. T. Liu, Development of multifunctional clay-based nanomedicine for elimination of primary invasive breast cancer and prevention of its lung metastasis and distant inoculation. ACS Appl. Mater. Interfaces 2019, 11, 35566-35576.
[26]
V. Raeesi,; L. Y. T. Chou,; W. C. W. Chan, Tuning the drug loading and release of DNA-assembled gold-nanorod superstructures. Adv. Mater. 2016, 28, 8511-8518.
[27]
Z. P. Zhang,; S. Tongchusak,; Y. Mizukami,; Y. J. Kang,; T. Ioji,; M. Touma,; B. Reinhold,; D. B. Keskin,; E. L. Reinherz,; T. Sasada, Induction of anti-tumor cytotoxic T cell responses through PLGA-nanoparticle mediated antigen delivery. Biomaterials 2011, 32, 3666-3678.
[28]
Q. Zeng,; H. Jiang,; T. Wang,; Z. R. Zhang,; T. Gong,; X. Sun, Cationic micelle delivery of Trp2 peptide for efficient lymphatic draining and enhanced cytotoxic T-lymphocyte responses. J. Controlled Release 2015, 200, 1-12.
[29]
D. Q. Liu,; S. Lu,; L. X. Zhang,; M. Ji,; S. Y. Liu,; S. W. Wang,; R. T. Liu, An indoleamine 2, 3-dioxygenase siRNA nanoparticle-coated and Trp2-displayed recombinant yeast vaccine inhibits melanoma tumor growth in mice. J. Controlled Release 2018, 273, 1-12.
[30]
Z. P. Xu,; M. Niebert,; K. Porazik,; T. L. Walker,; H. M. Cooper,; A. P. J. Middelberg,; P. P. Gray,; P. F. Bartlett,; G. Q. Lu, Subcellular compartment targeting of layered double hydroxide nanoparticles. J. Controlled Release 2008, 130, 86-94.
[31]
D. Q. Liu,; S. Lu,; L. Zhang,; L. X. Zhang,; M. Ji,; X. G. Liu,; Z. Yu,; R. T. Liu, A biomimetic yeast shell vaccine coated with layered double hydroxides induces a robust humoral and cellular immune response against tumors. Nanoscale Adv. 2020, 2, 3494-3506.
[32]
S. J. Choi,; J. H. Choy, Layered double hydroxide nanoparticles as target-specific delivery carriers: Uptake mechanism and toxicity. Nanomedicine 2011, 6, 803-814.
[33]
J. M. Oh,; S. J. Choi,; G. E. Lee,; J. E. Kim,; J. H. Choy, Inorganic metal hydroxide nanoparticles for targeted cellular uptake through clathrin-mediated endocytosis. Chem. Asian J. 2009, 4, 67-73.
[34]
J. M. Oh,; S. J. Choi,; S. T. Kim,; J. H. Choy, Cellular uptake mechanism of an inorganic nanovehicle and its drug conjugates: Enhanced efficacy due to clathrin-mediated endocytosis. Bioconjugate Chem. 2006, 17, 1411-1417.
[35]
H. Y. Dong,; H. S. Parekh,; Z. P. Xu, Particle size- and number-dependent delivery to cells by layered double hydroxide nanoparticles. J. Colloid Interface Sci. 2015, 437, 10-16.
[36]
B. Li,; J. Tang,; W. Y. Chen,; G. Y. Hao,; N. Kurniawan,; Z. Gu,; Z. P. Xu, Novel theranostic nanoplatform for complete mice tumor elimination via MR imaging-guided acid-enhanced photothermo-/chemo-therapy. Biomaterials 2018, 177, 40-51.
[37]
S. M. Moghimi,; H. Hedeman,; I. S. Muir,; L. Illum,; S. S. Davis, An investigation of the filtration capacity and the fate of large filtered sterically-stabilized microspheres in rat spleen. Biochi. Biophys. Acta (BBA) -Gen. Subj. 1993, 1157, 233-240.
[38]
S. M. Moghimi,; A. C. Hunter,; T. L. Andresen, Factors controlling nanoparticle pharmacokinetics: An integrated analysis and perspective. Annu. Rev. Pharmacol. Toxicol. 2012, 52, 481-503.
[39]
M. Cataldi,; C. Vigliotti,; T. Mosca,; M. Cammarota,; D. Capone, Emerging role of the spleen in the pharmacokinetics of monoclonal antibodies, nanoparticles and exosomes. Int. J. Mol. Sci. 2017, 18, 1249.
[40]
M. Demoy,; J. P. Andreux,; C. Weingarten,; B. Gouritin,; V. Guilloux,; P. Couvreur, In vitro evaluation of nanoparticles spleen capture. Life Sci. 1999, 64, 1329-1337.
[41]
M. J. Ernsting,; M. Murakami,; A. Roy,; S. D. Li, Factors controlling the pharmacokinetics, biodistribution and intratumoral penetration of nanoparticles. J. Controlled Release 2013, 172, 782-794.
[42]
L. X. Zhang,; X. M. Sun,; Y. B. Jia,; X. G. Liu,; M. D. Dong,; Z. P. Xu,; R. T. Liu, Nanovaccine’s rapid induction of anti-tumor immunity significantly improves malignant cancer immunotherapy. Nano Today 2020, 35, 100923.
[43]
A. Schroeder,; D. A. Heller,; M. M. Winslow,; J. E. Dahlman,; G. W. Pratt,; R. Langer,; T. Jacks,; D. G. Anderson, Treating metastatic cancer with nanotechnology. Nat. Rev. Cancer 2012, 12, 39-50.
[44]
F. Li,; Y. Chen,; S. B. Liu,; X. Pan,; Y. L. Liu,; H. T. Zhao,; X. J. Yin,; C. L. Yu,; W. Kong,; Y. Zhang, The effect of size, dose, and administration route on zein nanoparticle immunogenicity in BALB/c mice. Int. J. Nanomedicine 2019, 14, 9917-9928.
Nano Research
Pages 1326-1334
Cite this article:
Zhang L-X, Jia Y-B, Huang Y-R, et al. Efficient delivery of clay-based nanovaccines to the mouse spleen promotes potent anti-tumor immunity for both prevention and treatment of lymphoma. Nano Research, 2021, 14(5): 1326-1334. https://doi.org/10.1007/s12274-020-3175-0
Topics:

671

Views

31

Crossref

N/A

Web of Science

31

Scopus

0

CSCD

Altmetrics

Received: 30 June 2020
Revised: 10 October 2020
Accepted: 11 October 2020
Published: 19 November 2020
© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature
Return