Immune checkpoint inhibition mediated with liposomal nanomedicine for cancer therapy

Guang-Long Ma; Wei-Feng Lin

doi:10.1186/s40779-023-00455-x

Your Location：

Home >

Browse articles >

Immune checkpoint inhibition mediated with liposomal nanomedicine for cancer therapy

REVIEW | Updated：2025-12-13

- Immune checkpoint inhibition mediated with liposomal nanomedicine for cancer therapy
- Military Medical Research Vol. 11, Issue 1, Pages: 98-114(2024)
- Affiliations：
  
  1.Faculty of Medicine, Centre for Cancer Immunology, University of Southampton, Southampton SO16 6YD, UK
  2.Department of Molecular Chemistry and Materials Science, Weizmann Institute of Science, 76100 Rehovot, Israel
  3.Key Laboratory of Bio-Inspired Smart Interfacial Science and Technology of Ministry of Education, School of Chemistry, Beihang University, Beijing 100191, China
- Author bio：
  
  * linwf@buaa.edu.cn
- Funds：
- DOI：10.1186/s40779-023-00455-x
  CLC：
- Published：2024-02
- Accepted：
Scan QR Code
Cite this article as: Ma GL, Lin WF. Immune checkpoint inhibition mediated with liposomal nanomedicine for cancer therapy. Mil Med Res. 2023;10(1):20.
DOI：

Cite this article as: Ma GL, Lin WF. Immune checkpoint inhibition mediated with liposomal nanomedicine for cancer therapy. Mil Med Res. 2023;10(1):20. DOI： 10.1186/s40779-023-00455-x.

摘要

Abstract

Immune checkpoint blockade (ICB) therapy for cancer has achieved great success both in clinical results and on the market. At the same time

success drives more attention from scientists to improve it. However

only a small portion of patients are responsive to this therapy

and it comes with a unique spectrum of side effects termed immune-related adverse events (irAEs). The use of nanotechnology could improve ICBs’ delivery to the tumor

assist them in penetrating deeper into tumor tissues and alleviate their irAEs. Liposomal nanomedicine has been investigated and used for decades

and is well-recognized as the most successful nano-drug delivery system. The successful combination of ICB with liposomal nanomedicine could help improve the efficacy of ICB therapy. In this review

we highlighted recent studies using liposomal nanomedicine (including new emerging exosomes and their inspired nano-vesicles) in associating ICB therapy.

关键词

Keywords

references

Sung H , Ferlay J , Siegel RL , Laversanne M , Soerjomataram I , Jemal A , et al . Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries . CA Cancer J Clin . 2021 ; 71 ( 3 ): 209 – 49 .

Jiang X , Liu G , Li Y , Pan Y . Immune checkpoint: the novel target for antitumor therapy . Genes Dis . 2021 ; 8 ( 1 ): 25 – 37 .

Aguilar EJ , Ricciuti B , Gainor JF , Kehl KL , Kravets S , Dahlberg S , et al . Outcomes to first-line pembrolizumab in patients with non-small-cell lung cancer and very high PD-L1 expression . Ann Oncol . 2019 ; 30 ( 10 ): 1653 – 9 .

Peters S , Kerr KM , Stahel R . PD-1 blockade in advanced NSCLC: a focus on pembrolizumab . Cancer Treat Rev . 2018 ; 62 : 39 – 49 .

Khoja L , Butler MO , Kang SP , Ebbinghaus S , Joshua AM . Pembrolizumab . J Immunother Cancer . 2015 ; 3 : 36 .

Chen Y , Wang L , Zheng M , Zhu C , Wang G , Xia Y , et al . Engineered extracellular vesicles for concurrent anti-PDL1 immunotherapy and chemotherapy . Bioact Mater . 2022 ; 9 : 251 – 65 .

Deng R , Bumbaca D , Pastuskovas CV , Boswell CA , West D , Cowan KJ , et al . Preclinical pharmacokinetics, pharmacodynamics, tissue distribution, and tumor penetration of anti-PD-L1 monoclonal antibody, an immune checkpoint inhibitor . MAbs . 2016 ; 8 ( 3 ): 593 – 603 .

Cruz E , Kayser V . Monoclonal antibody therapy of solid tumors: clinical limitations and novel strategies to enhance treatment efficacy . Biologics . 2019 ; 13 : 33 – 51 .

Ai L , Chen J , Yan H , He Q , Luo P , Xu Z , et al . Research status and outlook of PD-1/PD-L1 inhibitors for cancer therapy . Drug Des Devel Ther . 2020 ; 14 : 3625 – 49 .

Xiao WY , Wang Y , An HW , Hou D , Mamuti M , Wang MD , et al . Click reaction-assisted peptide immune checkpoint blockade for solid tumor treatment . ACS Appl Mater Interfaces . 2020 ; 12 ( 36 ): 40042 – 51 .

Alimohammadi R , Alibeigi R , Nikpoor AR , Chalbatani GM , Webster TJ , Jaafari MR , et al . Encapsulated checkpoint blocker before chemotherapy: the optimal sequence of anti-CTLA-4 and doxil combination therapy . Int J Nanomedicine . 2020 ; 15 : 5279 – 88 .

Deveuve Q , Lajoie L , Barrault B , Thibault G . The proteolytic cleavage of therapeutic monoclonal antibody hinge region: more than a matter of subclass . Front Immunol . 2020 ; 11 : 168 .

Collins LK , Chapman MS , Carter JB , Samie FH . Cutaneous adverse effects of the immune checkpoint inhibitors . Curr Probl Cancer . 2017 ; 41 ( 2 ): 125 – 8 .

Morgado M , Placido A , Morgado S , Roque F . Management of the adverse effects of immune checkpoint inhibitors . Vaccines (Basel) . 2020 ; 8 ( 4 ): 575 .

Kahler KC , Hassel JC , Heinzerling L , Loquai C , Thoms KM , Ugurel S , et al . Side effect management during immune checkpoint blockade using CTLA-4 and PD-1 antibodies for metastatic melanoma—an update . J Dtsch Dermatol Ges . 2020 ; 18 ( 6 ): 582 – 609 .

Calvo R . Hematological side effects of immune checkpoint inhibitors: the example of immune-related thrombocytopenia . Front Pharmacol . 2019 ; 10 : 454 .

Lombardi A , Mondelli MU . Review article: immune checkpoint inhibitors and the liver, from therapeutic efficacy to side effects . Aliment Pharmacol Ther . 2019 ; 50 ( 8 ): 872 – 84 .

Barrueto L , Caminero F , Cash L , Makris C , Lamichhane P , Deshmukh RR . Resistance to checkpoint inhibition in cancer immunotherapy . Transl Oncol . 2020 ; 13 ( 3 ): 100738 .

Russell BL , Sooklal SA , Malindisa ST , Daka LJ , Ntwasa M . The tumor microenvironment factors that promote resistance to immune checkpoint blockade therapy . Front Oncol . 2021 ; 11 : 641428 .

Spranger S . Mechanisms of tumor escape in the context of the T-cell-inflamed and the non-T-cell-inflamed tumor microenvironment . Int Immunol . 2016 ; 28 ( 8 ): 383 – 91 .

Bulbake U , Doppalapudi S , Kommineni N , Khan W . Liposomal formulations in clinical use: an updated review . Pharmaceutics . 2017 ; 9 ( 4 ): 12 .

Lamichhane N , Udayakumar TS , D’souza WD , Simone CB 2nd , Raghavan SR , Polf J , et al . Liposomes: clinical applications and potential for imageguided drug delivery . Molecules . 2018 ; 23 ( 2 ): 288 .

Lu Y , Gao Y , Yang H , Hu Y , Li X . Nanomedicine-boosting icaritin-based immunotherapy of advanced hepatocellular carcinoma . Mil Med Res . 2022 ; 9 ( 1 ): 69 .

Guimaraes D , Cavaco-Paulo A , Nogueira E . Design of liposomes as drug delivery system for therapeutic applications . Int J Pharm . 2021 ; 601 : 120571 .

López-Camacho A , Higuera-Ciapara I , Velázquez-Fernández JB , Beltrán-Gracia E , Vallejo-Cardona AA . Nanomedicine review: clinical developments in liposomal applications . Cancer Nanotechnol . 2019 ; 10 ( 1 ): 1 – 40 .

Allen TM , Cullis PR . Liposomal drug delivery systems: from concept to clinical applications . Adv Drug Deliv Rev . 2013 ; 65 ( 1 ): 36 – 48 .

Barenholz Y . Doxil®–the first FDA-approved nano-drug: lessons learned . J Control Release . 2012 ; 160 ( 2 ): 117 – 34 .

Anselmo AC , Mitragotri S . Nanoparticles in the clinic: an update . Bioeng Transl Med . 2019 ; 4 ( 3 ): e10143 .

Maeda H , Wu J , Sawa T , Matsumura Y , Hori K . Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review . J Control Release . 2000 ; 65 ( 1 ): 271 – 84 .

Allen TM , Hansen CB , de Menezes DEL . Pharmacokinetics of longcirculating liposomes . Adv Drug Deliver Rev . 1995 ; 16 ( 2 ): 267 – 84 .

Kobayashi H , Watanabe R , Choyke PL . Improving conventional enhanced permeability and retention (EPR) effects; what is the appropriate target? . Theranostics . 2013 ; 4 ( 1 ): 81 – 9 .

Wu J . The enhanced permeability and retention (EPR) effect: the significance of the concept and methods to enhance its application . J Pers Med . 2021 ; 11 ( 8 ): 771 .

Thakkar S , Sharma D , Kalia K , Tekade RK . Tumor microenvironment targeted nanotherapeutics for cancer therapy and diagnosis: a review . Acta Biomater . 2020 ; 101 : 43 – 68 .

Wei X , Chen X , Ying M , Lu W . Brain tumor-targeted drug delivery strategies . Acta Pharm Sin B . 2014 ; 4 ( 3 ): 193 – 201 .

Maeda H , Bharate GY , Daruwalla J . Polymeric drugs for efficient tumortargeted drug delivery based on EPR-effect . Eur J Pharm Biopharm . 2009 ; 71 ( 3 ): 409 – 19 .

Large DE , Soucy JR , Hebert J , Auguste DT . Advances in receptor-mediated, tumor-targeted drug delivery . Adv Therap . 2019 ; 2 : 1800091 .

Gullotti E , Yeo Y . Extracellularly activated nanocarriers: a new paradigm of tumor targeted drug delivery . Mol Pharm . 2009 ; 6 ( 4 ): 1041 – 51 .

Qin SY , Zhang AQ , Zhang XZ . Recent advances in targeted tumor chemotherapy based on smart nanomedicines . Small . 2018 ; 14 ( 45 ): e1802417 .

He Q , Chen J , Yan J , Cai S , Xiong H , Liu Y , et al . Tumor microenvironment responsive drug delivery systems . Asian J Pharm Sci . 2020 ; 15 ( 4 ): 416 – 48 .

Guo X , Cheng Y , Zhao X , Luo Y , Chen J , Yuan WE . Advances in redox-responsive drug delivery systems of tumor microenvironment . J Nanobiotechnology . 2018 ; 16 ( 1 ): 74 .

Jia R , Teng L , Gao L , Su T , Fu L , Qiu Z , et al . Advances in multiple stimuli-responsive drug-delivery systems for cancer therapy . Int J Nanomedicine . 2021 ; 16 : 1525 – 51 .

Shein SA , Kuznetsov II , Abakumova TO , Chelushkin PS , Melnikov PA , Korchagina AA , et al . VEGF- and VEGFR2-targeted liposomes for cisplatin delivery to glioma cells . Mol Pharm . 2016 ; 13 ( 11 ): 3712 – 23 .

Zhou Q , Shao S , Wang J , Xu C , Xiang J , Piao Y , et al . Enzyme-activatable polymer-drug conjugate augments tumour penetration and treatment efficacy . Nat Nanotechnol . 2019 ; 14 ( 8 ): 799 – 809 .

Hou X , Zaks T , Langer R , Dong Y . Lipid nanoparticles for mRNA delivery . Nat Rev Mater . 2021 ; 6 ( 12 ): 1078 – 94 .

Man F , Gawne PJ , de Rosales RTM . Nuclear imaging of liposomal drug delivery systems: a critical review of radiolabelling methods and applications in nanomedicine . Adv Drug Deliv Rev . 2019 ; 143 : 134 – 60 .

Kim EM , Jeong HJ . Liposomes: biomedical applications . Chonnam Med J . 2021 ; 57 ( 1 ): 27 – 35 .

Cheng X , Gao J , Ding Y , Lu Y , Wei Q , Cui D , et al . Multi-functional liposome: a powerful theranostic nano-platform enhancing photodynamic therapy . Adv Sci (Weinh) . 2021 ; 8 ( 16 ): e2100876 .

Xia Y , Xu C , Zhang X , Ning P , Wang Z , Tian J , et al . Liposome-based probes for molecular imaging: from basic research to the bedside . Nanoscale . 2019 ; 11 ( 13 ): 5822 – 38 .

Gu ZL , Da Silva CG , Van Der Maaden K , Ossendorp F , Cruz LJ . Liposome-based drug delivery systems in cancer immunotherapy . Pharmaceutics . 2020 ; 12 ( 11 ): 1054 .

Xing C , Li H , Li RJ , Yin L , Zhang HF , Huang ZN , et al . The roles of exosomal immune checkpoint proteins in tumors . Mil Med Res . 2021 ; 8 ( 1 ): 56 .

Ou W , Jiang L , Gu Y , Soe ZC , Kim BK , Gautam M , et al . Regulatory T cells tailored with pH-responsive liposomes shape an immunoantitumor milieu against tumors . ACS Appl Mater Interfaces . 2019 ; 11 ( 40 ): 36333 – 46 .

Merino M , Contreras A , Casares N , Troconiz IF , Ten Hagen TL , Berraondo P , et al . A new immune-nanoplatform for promoting adaptive antitumor immune response . Nanomedicine . 2019 ; 17 : 13 – 25 .

Li YJ , Wu JY , Hu XB , Ding T , Tang T , Xiang DX . Biomimetic liposome with surface-bound elastase for enhanced tumor penetration and chemoimmumotherapy . Adv Healthc Mater . 2021 ; 10 ( 19 ): e2100794 .

Zhao H , Zhao B , Wu L , Xiao H , Ding K , Zheng C , et al . Amplified cancer immunotherapy of a surface-engineered antigenic microparticle vaccine by synergistically modulating tumor microenvironment . ACS Nano . 2019 ; 13 ( 11 ): 12553 – 66 .

Li C , Qiu Q , Gao X , Yan X , Fan C , Luo X , et al . Sialic acid conjugate-modified liposomal platform modulates immunosuppressive tumor microenvironment in multiple ways for improved immune checkpoint blockade therapy . J Control Release . 2021 ; 337 : 393 – 406 .

Huang TY , Huang GL , Zhang CY , Zhuang BW , Liu BX , Su LY , et al . Supramolecular photothermal nanomedicine mediated distant tumor inhibition via PD-1 and TIM-3 blockage . Front Chem . 2020 ; 8 : 1 .

Cremolini C , Vitale E , Rastaldo R , Giachino C . Advanced nanotechnology for enhancing immune checkpoint blockade therapy . Nanomaterials (Basel) . 2021 ; 11 ( 3 ): 661 .

Lahori DG , Varamini P . Nanotechnology-based platforms to improve immune checkpoint blockade efficacy in cancer therapy . Future Oncol . 2021 ; 17 ( 6 ): 711 – 22 .

Phung CD , Pham TT , Nguyen HT , Nguyen TT , Ou W , Jeong JH , et al . Anti-CTLA-4 antibody-functionalized dendritic cell-derived exosomes targeting tumor-draining lymph nodes for effective induction of antitumor T-cell responses . Acta Biomater . 2020 ; 115 : 371 – 82 .

Sobhani N , Tardiel-Cyril DR , Davtyan A , Generali D , Roudi R , Li Y . CTLA-4 in regulatory T cells for cancer immunotherapy . Cancers . 2021 ; 13 ( 6 ): 1440 .

Vaddepally RK , Kharel P , Pandey R , Garje R , Chandra AB . Review of indications of FDA-approved immune checkpoint inhibitors per NCCN guidelines with the level of evidence . Cancers . 2020 ; 12 ( 3 ): 738 .

Zhang Y , Du X , Liu M , Tang F , Zhang P , Ai C , et al . Hijacking antibody-induced CTLA-4 lysosomal degradation for safer and more effective cancer immunotherapy . Cell Res . 2019 ; 29 ( 8 ): 609 – 27 .

Nikpoor AR , Tavakkol-Afshari J , Sadri K , Jalali SA , Jaafari MR . Improved tumor accumulation and therapeutic efficacy of CTLA-4-blocking antibody using liposome-encapsulated antibody: in vitro and in vivo studies . Nanomedicine . 2017 ; 13 ( 8 ): 2671 – 82 .

Sharpe AH , Pauken KE . The diverse functions of the PD1 inhibitory pathway . Nat Rev Immunol . 2018 ; 18 ( 3 ): 153 – 67 .

Topalian SL , Taube JM , Anders RA , Pardoll DM . Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy . Nat Rev Cancer . 2016 ; 16 ( 5 ): 275 – 87 .

Wu Y , Chen W , Xu ZP , Gu W . PD-L1 distribution and perspective for cancer immunotherapy-blockade, knockdown, or inhibition . Front Immunol . 2019 ; 10 : 2022 .

Merino M , Lozano T , Casares N , Lana H , Troconiz IF , Ten Hagen TLM , et al . Dual activity of PD-L1 targeted Doxorubicin immunoliposomes promoted an enhanced efficacy of the antitumor immune response in melanoma murine model . J Nanobiotechnology . 2021 ; 19 ( 1 ): 102 .

He ZD , Zhang M , Wang YH , He Y , Wang HR , Chen BF , et al . Anti-PD-L1 mediating tumor-targeted codelivery of liposomal irinotecan/JQ1 for chemo-immunotherapy . Acta Pharmacol Sin . 2021 ; 42 ( 9 ): 1516 – 23 .

Serrano-Del Valle A , Anel A , Naval J , Marzo I . Immunogenic cell death and immunotherapy of multiple myeloma . Front Cell Dev Biol . 2019 ; 7 : 50 .

Zhou J , Wang G , Chen Y , Wang H , Hua Y , Cai Z . Immunogenic cell death in cancer therapy: present and emerging inducers . J Cell Mol Med . 2019 ; 23 ( 8 ): 4854 – 65 .

Jiang G , Deng W , Liu Y , Wang C . General mechanism of JQ1 in inhibiting various types of cancer . Mol Med Rep . 2020 ; 21 ( 3 ): 1021 – 34 .

Burr ML , Sparbier CE , Chan YC , Williamson JC , Woods K , Beavis PA , et al . CMTM6 maintains the expression of PD-L1 and regulates anti-tumour immunity . Nature . 2017 ; 549 ( 7670 ): 101 – 5 .

Yang S , Shim MK , Song S , Cho H , Choi J , Jeon SI , et al . Liposome-mediated PD-L1 multivalent binding promotes the lysosomal degradation of PD-L1 for T cell-mediated antitumor immunity . Biomaterials . 2022 ; 290 : 121841 .

Huang L , Li Y , Du Y , Zhang Y , Wang X , Ding Y , et al . Mild photothermal therapy potentiates anti-PD-L1 treatment for immunologically cold tumors via an all-in-one and all-in-control strategy . Nat Commun . 2019 ; 10 ( 1 ): 4871 .

Ma G , Kostevsek N , Monaco I , Ruiz A , Markelc B , Cheung CCL , et al . PD1 blockade potentiates the therapeutic efficacy of photothermally-activated and MRI-guided low temperature-sensitive magnetoliposomes . J Control Release . 2021 ; 332 : 419 – 33 .

Yu J , He X , Wang Z , Wang Y , Liu S , Li X , et al . Combining PD-L1 inhibitors with immunogenic cell death triggered by chemo-photothermal therapy via a thermosensitive liposome system to stimulate tumorspecific immunological response . Nanoscale . 2021 ; 13 ( 30 ): 12966 – 78 .

Li Y , Teng X , Wang Y , Yang C , Yan X , Li J . Neutrophil delivered hollow titania covered persistent luminescent nanosensitizer for ultrosound augmented chemo/immuno glioblastoma therapy . Adv Sci . 2021 ; 8 ( 17 ): 2004381 .

Lin B , Chen H , Liang D , Lin W , Qi X , Liu H , et al . Acidic pH and high-H 2 O 2 dual tumor microenvironment-responsive nanocatalytic graphene oxide for cancer selective therapy and recognition . ACS Appl Mater Interfaces . 2019 ; 11 ( 12 ): 11157 – 66 .

Boedtkjer E , Pedersen SF . The acidic tumor microenvironment as a driver of cancer . Annu Rev Physiol . 2020 ; 82 : 103 – 26 .

Feng L , Dong Z , Tao D , Zhang Y , Liu Z . The acidic tumor microenvironment: a target for smart cancer nano-theranostics . Natl Sci Rev . 2018 ; 5 ( 2 ): 269 – 86 .

Gu Z , Wang Q , Shi Y , Huang Y , Zhang J , Zhang X , et al . Nanotechnology-mediated immunochemotherapy combined with docetaxel and PD-L1 antibody increase therapeutic effects and decrease systemic toxicity . J Control Release . 2018 ; 286 : 369 – 80 .

Banstola A , Poudel K , Pathak S , Shrestha P , Kim JO , Jeong JH , et al . Hypoxia-mediated ROS amplification triggers mitochondria-mediated apoptotic cell death via PD-L1/ROS-responsive, dual-targeted, drug-laden thioketal nanoparticles . ACS Appl Mater Interfaces . 2021 ; 13 ( 19 ): 22955 – 69 .

Daund V , Chalke S , Sherje AP , Kale PP . ROS responsive mesoporous silica nanoparticles for smart drug delivery: a review . J Drug Deliver Sci Technol . 2021 ; 64 : 102599 .

Li Y , Chen M , Yao B , Lu X , Song B , Vasilatos SN , et al . Dual pH/ROS-responsive nanoplatform with deep tumor penetration and self-amplified drug release for enhancing tumor chemotherapeutic efficacy . Small . 2020 ; 16 ( 32 ): e2002188 .

Wang Y , Yu J , Li D , Zhao L , Sun B , Wang J , et al . Paclitaxel derivative-based liposomal nanoplatform for potentiated chemo-immunotherapy . J Control Release . 2022 ; 341 : 812 – 27 .

Brown GT , Murray GI . Current mechanistic insights into the roles of matrix metalloproteinases in tumour invasion and metastasis . J Pathol . 2015 ; 237 ( 3 ): 273 – 81 .

Curran S , Murray GI . Matrix metalloproteinases in tumour invasion and metastasis . J Pathol . 1999 ; 189 ( 3 ): 300 – 8 .

Isaacson KJ , Martin Jensen M , Subrahmanyam NB , Ghandehari H . Matrix-metalloproteinases as targets for controlled delivery in cancer: an analysis of upregulation and expression . J Control Release . 2017 ; 259 : 62 – 75 .

Zhang M , Fang Z , Zhang H , Cui M , Wang M , Liu K . Reversing tumor immunosuppressive microenvironment via targeting codelivery of CpG ODNs/PD-L1 peptide antagonists to enhance the immune checkpoint blockade-based anti-tumor effect . Eur J Pharm Sci . 2022 ; 168 : 106044 .

Lang T , Liu Y , Zheng Z , Ran W , Zhai Y , Yin Q , et al . Cocktail strategy based on spatio-temporally controlled nano device improves therapy of breast cancer . Adv Mater . 2019 ; 31 ( 5 ): 1806202 .

Batlle E , Clevers H . Cancer stem cells revisited . Nat Med . 2017 ; 23 ( 10 ): 1124 – 34 .

Yu Z , Pestell TG , Lisanti MP , Pestell RG . Cancer stem cells . Int J Biochem Cell Biol . 2012 ; 44 ( 12 ): 2144 – 51 .

Lu S , Yang N , He J , Gong W , Lai Z , Xie L , et al . Generation of cancer-specific cytotoxic PD-1-T cells using liposome-encapsulated CRISPR/Cas system with dendritic/tumor fusion cells . J Biomed Nanotechnol . 2019 ; 15 ( 3 ): 593 – 601 .

Lian S , Xie R , Ye Y , Xie X , Li S , Lu Y , et al . Simultaneous blocking of CD47 and PD-L1 increases innate and adaptive cancer immune responses and cytokine release . EBioMedicine . 2019 ; 42 : 281 – 95 .

Barati M , Mirzavi F , Nikpoor AR , Sankian M , Namdar Ahmadabad H , Soleimani A , et al . Enhanced antitumor immune response in melanoma tumor model by anti-PD-1 small interference RNA encapsulated in nanoliposomes . Cancer Gene Ther . 2021 ; 29 ( 6 ): 814 – 24 .

Pardoll DM . The blockade of immune checkpoints in cancer immunotherapy . Nat Rev Cancer . 2012 ; 12 ( 4 ): 252 – 64 .

Liao Q , Zhou Y , Xia L , Cao D . Lipid metabolism and immune checkpoints . Adv Exp Med Biol . 2021 ; 1316 : 191 – 211 .

Mellman I , Coukos G , Dranoff G . Cancer immunotherapy comes of age . Nature . 2011 ; 480 ( 7378 ): 480 – 9 .

Boone CE , Wang L , Gautam A , Newton IG , Steinmetz NF . Combining nanomedicine and immune checkpoint therapy for cancer immunotherapy . Wiley Interdiscip Rev Nanomed Nanobiotechnol . 2022 ; 14 ( 1 ): e1739 .

Guo M , Han S , Liu Y , Guo W , Zhao Y , Liu F , et al . Inhibition of allogeneic islet graft rejection by VISTA-conjugated liposome . Biochem Biophys Res Commun . 2019 ; 516 ( 3 ): 914 – 20 .

Torphy R , Schulick R , Zhu Y . Newly emerging immune checkpoints: promises for future cancer therapy . Int J Mol Sci . 2017 ; 18 ( 12 ): 2642 .

Chen YL , Lin HW , Chien CL , Lai YL , Sun WZ , Chen CA , et al . BTLA blockade enhances cancer therapy by inhibiting IL-6/IL-10-induced CD19-high B lymphocytes . J Immunother Cancer . 2019 ; 7 ( 1 ): 313 .

Chen S , Wainwright DA , Wu JD , Wan Y , Matei DE , Zhang Y , et al . CD73: an emerging checkpoint for cancer immunotherapy . Immunotherapy . 2019 ; 11 ( 11 ): 983 – 97 .

Zhou W , Guo S , Liu M , Burow ME , Wang G . Targeting CXCL12/CXCR4 axis in tumor immunotherapy . Cur Med Chem . 2019 ; 26 ( 17 ): 3026 – 41 .

Guo F , Wang Y , Liu J , Mok SC , Xue F , Zhang W . CXCL12/CXCR4: a symbiotic bridge linking cancer cells and their stromal neighbors in oncogenic communication networks . Oncogene . 2016 ; 35 ( 7 ): 816 – 26 .

Shi Y , Riese DJ 2nd , Shen J . The role of the CXCL12/CXCR4/CXCR7 chemokine axis in cancer . Front Pharmacol . 2020 ; 11 : 574667 .

Lu G , Qiu Y , Su X . Targeting CXCL12-CXCR4 signaling enhances immune checkpoint blockade therapy against triple negative breast cancer . Eur J Pharm Sci . 2021 ; 157 : 105606 .

Hornyak L , Dobos N , Koncz G , Karanyi Z , Pall D , Szabo Z , et al . The role of indoleamine-2,3-dioxygenase in cancer development, diagnostics, and therapy . Front Immunol . 2018 ; 9 : 151 .

Pallotta MT , Rossini S , Suvieri C , Coletti A , Orabona C , Macchiarulo A , et al . Indoleamine 2,3-dioxygenase 1 (IDO1): an up-to-date overview of an eclectic immunoregulatory enzyme . FEBS J . 2022 ; 289 ( 20 ): 6099 – 118 .

Tang K , Wu YH , Song Y , Yu B . Indoleamine 2,3-dioxygenase 1 (IDO1) inhibitors in clinical trials for cancer immunotherapy . J Hematol Oncol . 2021 ; 14 ( 1 ): 68 .

Huang Z , Wei G , Zeng Z , Huang Y , Huang L , Shen Y , et al . Enhanced cancer therapy through synergetic photodynamic/immune checkpoint blockade mediated by a liposomal conjugate comprised of porphyrin and IDO inhibitor . Theranostics . 2019 ; 9 ( 19 ): 5542 – 57 .

Liu D , Chen B , Mo Y , Wang Z , Qi T , Zhang Q , et al . Redox-activated porphyrin-based liposome remote-loaded with indoleamine 2,3-dioxygenase (IDO) inhibitor for synergistic photoimmunotherapy through induction of immunogenic cell death and blockage of IDO pathway . Nano Lett . 2019 ; 19 ( 10 ): 6964 – 76 .

Cheng L , Hill AF . Therapeutically harnessing extracellular vesicles . Nat Rev Drug Discov . 2022 ; 21 ( 5 ): 379 – 99 .

Antimisiaris SG , Mourtas S , Marazioti A . Exosomes and exosome-inspired vesicles for targeted drug delivery . Pharmaceutics . 2018 ; 10 ( 4 ): 218 .

Ozverel CS . Exosome mimetic nanovesicles; are they next best alternative therapeutic approach combating cancer? . Cyprus J Med Sci . 2020 ; 5 ( 4 ): 361 – 4 .

Lu M , Huang YY . Bioinspired exosome-like therapeutics and delivery nanoplatforms . Biomaterials . 2020 ; 242 : 23 .

Kenific CM , Zhang H , Lyden D . An exosome pathway without an ESCRT . Cell Res . 2021 ; 31 ( 2 ): 105 – 6 .

Chen L , Wang L , Zhu L , Xu Z , Liu Y , Li Z , et al . Exosomes as drug carriers in anti-cancer therapy . Front Cell Dev Biol . 2022 ; 10 : 728616 .

Chinnappan M , Srivastava A , Amreddy N , Razaq M , Pareek V , Ahmed R , et al . Exosomes as drug delivery vehicle and contributor of resistance to anticancer drugs . Cancer Lett . 2020 ; 486 : 18 – 28 .

Zhao Y , Liu L , Sun R , Cui G , Guo S , Han S , et al . Exosomes in cancer immunoediting and immunotherapy . Asian J Pharm Sci . 2022 ; 17 ( 2 ): 193 – 205 .

Zhou K , Guo S , Li F , Sun Q , Liang G . Exosomal PD-L1: new insights into tumor immune escape mechanisms and therapeutic strategies . Front Cell Dev Biol . 2020 ; 8 : 569219 .

Chen H , Wang L , Zeng X , Schwarz H , Nanda HS , Peng X , et al . Exosomes, a new star for targeted delivery . Front Cell Dev Biol . 2021 ; 9 : 751079 .

Herrmann IK , Wood MJA , Fuhrmann G . Extracellular vesicles as a next-generation drug delivery platform . Nat Nanotechnol . 2021 ; 16 ( 7 ): 748 – 59 .

Liang Y , Duan L , Lu J , Xia J . Engineering exosomes for targeted drug delivery . Theranostics . 2021 ; 11 ( 7 ): 3183 – 95 .

Fan Y , Zhou Y , Lu M , Si H , Li L , Tang B . Responsive dual-targeting exosome as a drug carrier for combination cancer immunotherapy . Research (Wash D C) . 2021 ; 2021 : 9862876 .

Pei X , Zhang X , Zhang L , Yuan M , Sun L , Yu F , et al . Targeted exosomes for co-delivery of siFGL1 and siTGF-β1 trigger combined cancer immunotherapy by remodeling immunosuppressive tumor microenvironment . Chem Eng J . 2021 ; 421 : 129774 .

Severic M , Ma G , Pereira SGT , Ruiz A , Cheung CCL , Al-Jamal WT . Genetically-engineered anti-PSMA exosome mimetics targeting advanced prostate cancer in vitro and in vivo . J Control Release . 2020 ; 330 : 101 – 10 .

Allard B , Pommey S , Smyth MJ , Stagg J . Targeting CD73 enhances the antitumor activity of anti-PD-1 and anti-CTLA-4 mAbs . Clin Cancer Res . 2013 ; 19 ( 20 ): 5626 – 35 .

Zhou Q , Ding W , Qian Z , Zhu Q , Sun C , Yu Q , et al . Immunotherapy strategy targeting programmed cell death ligand 1 and CD73 with macrophage-derived mimetic nanovesicles to treat bladder cancer . Mol Pharm . 2021 ; 18 ( 11 ): 4015 – 28 .

Zhang X , Wang J , Chen Z , Hu Q , Wang C , Yan J , et al . Engineering PD-1-presenting platelets for cancer immunotherapy . Nano Lett . 2018 ; 18 ( 9 ): 5716 – 25 .

Centanni M , Moes D , Troconiz IF , Ciccolini J , Van Hasselt JGC . Clinical pharmacokinetics and pharmacodynamics of immune checkpoint inhibitors . Clin Pharmacokinet . 2019 ; 58 ( 7 ): 835 – 57 .

Feng Y , Masson E , Dai D , Parker SM , Berman D , Roy A . Model-based clinical pharmacology profiling of ipilimumab in patients with advanced melanoma . Br J Clin Pharmacol . 2014 ; 78 ( 1 ): 106 – 17 .

O’brien T , Dolan L . Immune checkpoint inhibitors and timing of administration . Lancet Oncol . 2022 ; 23 ( 2 ): e55 .

Shinno Y , Goto Y , Ohuchi M , Hamada A , Nokihara H , Fujiwara Y , et al . The long half-life of programmed cell death protein 1 inhibitors may increase the frequency of immune-related adverse events after subsequent EGFR tyrosine kinase inhibitor therapy . JTO Clin Res Rep . 2020 ; 1 ( 1 ): 100008 .

Lin W , Kampf N , Goldberg R , Driver MJ , Klein J . Poly-phosphocholinated liposomes form stable superlubrication vectors . Langmuir . 2019 ; 35 ( 18 ): 6048 – 54 .

He H , Liu L , Morin EE , Liu M , Schwendeman A . Survey of clinical translation of cancer nanomedicines-lessons learned from successes and failures . Acc Chem Res . 2019 ; 52 ( 9 ): 2445 – 61 .

Wilhelm S , Tavares AJ , Dai Q , Ohta S , Audet J , Dvorak HF , et al . Analysis of nanoparticle delivery to tumours . Nat Rev Mater . 2016 ; 1 ( 5 ): 16014 .

De Lázaro I , Mooney DJ . A nanoparticle’s pathway into tumours . Nat Mater . 2020 ; 19 ( 5 ): 486 – 7 .

Challenging paradigms in tumour drug delivery . Nat Mater . 2020 ; 19 ( 5 ): 477 .

Sainaga Jyothi VGS , Bulusu R , Rao BVK , Pranothi M , Banda S , Kumar Bolla P , et al . Stability characterization for pharmaceutical liposome product development with focus on regulatory considerations: an update . Int J Pharm . 2022 ; 624 : 122022 .

Nakhaei P , Margiana R , Bokov DO , Abdelbasset WK , Jadidi Kouhbanani MA , Varma RS , et al . Liposomes: structure, biomedical applications, and stability parameters with emphasis on cholesterol . Front Bioeng Biotechnol . 2021 ; 9 : 705886 .

Views

Downloads

CSCD

Alert me when the article has been cited

Submit

Tools

Publicity Resources

Bioengineered exosomal-membrane-camouflaged abiotic nanocarriers: neurodegenerative diseases, tissue engineering and regenerative medicine

Activated Drp1 regulates p62-mediated autophagic flux and aggravates inflammation in cerebral ischemia-reperfusion via the ROS-RIP1/RIP3-exosome axis

Dynamic Response Analysis of Tunnel Foundation by Vehicle Vibration in Metro

Experimental Research on the Maximum Tensile Force in Reinforced Abutment Reinforcement

Kalman Dynamic Adaptive Filtering to Railway Line Measurement Signals of Tilting Train

Related Author

Guang-Long Ma

Ana Cláudia Paiva-Santos

Miguel Pereira-Silva

Joana Lopes

Daniela Lopes

Diana Peixoto

Navid Rabiee

Omid Moradi

Related Institution

Centre for Cancer Immunology, Faculty of Medicine, University of Southampton

School of Engineering, Institute for Bioengineering, the University of Edinburgh

Department of Pulmonary and Critical Care Medicine, Zhongshan Hospital, Fudan University Shanghai Medical College

Integrated Composites Laboratory (ICL), Department of Mechanical and Construction Engineering, Northumbria University

Department of Chemistry, Shahr-e-Qods Branch, Islamic Azad University

⁰