Nanotechnology

Targeted delivery of MerTK protein via cell membrane engineered nanoparticle enhances efferocytosis and attenuates atherosclerosis in diabetic ApoE−/− Mice | Journal of Nanobiotechnology


  • Visseren FLJ, Mach F, Smulders YM, Carballo D, Koskinas KC, Black M, Benetos A, Biffi A, Boavida JM, Capodanno D, et al. 2021 ESC Guidelines on cardiovascular disease prevention in clinical practice. Eur Heart J. 2021;42:3227–337.

    Article 
    PubMed 

    Google Scholar
     

  • Townsend N, Kazakiewicz D, Lucy Wright F, Timmis A, Huculeci R, Torbica A, Gale CP, Achenbach S, Weidinger F, Vardas P. Epidemiology of cardiovascular disease in Europe. Nat Rev Cardiol. 2022;19:133–43.

    Article 
    PubMed 

    Google Scholar
     

  • Libby P, Buring JE, Badimon L, Hansson GK, Deanfield J, Bittencourt MS, Tokgözoğlu L, Lewis EF. Atherosclerosis. Nat Rev Dis Primers. 2019;5:56.

    Article 
    PubMed 

    Google Scholar
     

  • Echouffo-Tcheugui JB, Ndumele CE, Zhang S, Florido R, Matsushita K, Coresh J, Skali H, Shah AM, Selvin E. Diabetes and progression of heart failure: the atherosclerosis risk in communities (ARIC) study. J Am Coll Cardiol. 2022;79:2285–93.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ohkuma T, Komorita Y, Peters SAE, Woodward M. Diabetes as a risk factor for heart failure in women and men: a systematic review and meta-analysis of 47 cohorts including 12 million individuals. Diabetologia. 2019;62:1550–60.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Aune D, Schlesinger S, Neuenschwander M, Feng T, Janszky I, Norat T, Riboli E. Diabetes mellitus, blood glucose and the risk of heart failure: a systematic review and meta-analysis of prospective studies. Nutr Metab Cardiovasc Dis. 2018;28:1081–91.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Dunlay SM, Givertz MM, Aguilar D, Allen LA, Chan M, Desai AS, Deswal A, Dickson VV, Kosiborod MN, Lekavich CL, et al. Type 2 diabetes mellitus and heart failure: a scientific statement from the american heart association and the heart failure society of america: this statement does not represent an update of the 2017 ACC/AHA/HFSA heart failure guideline update. Circulation. 2019;140:e294–324.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Doran AC, Yurdagul A, Tabas I. Efferocytosis in health and disease. Nat Rev Immunol. 2020;20:254–67.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gerlach BD, Ampomah PB, Yurdagul A, Liu C, Lauring MC, Wang X, Kasikara C, Kong N, Shi J, Tao W, Tabas I. Efferocytosis induces macrophage proliferation to help resolve tissue injury. Cell Metab. 2021;33:2445-2463.e2448.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tao H, Yancey PG, Babaev VR, Blakemore JL, Zhang Y, Ding L, Fazio S, Linton MF. Macrophage SR-BI mediates efferocytosis via Src/PI3K/Rac1 signaling and reduces atherosclerotic lesion necrosis. J Lipid Res. 2015;56:1449–60.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Thorp E, Cui D, Schrijvers DM, Kuriakose G, Tabas I. Mertk receptor mutation reduces efferocytosis efficiency and promotes apoptotic cell accumulation and plaque necrosis in atherosclerotic lesions of apoe-/- mice. Arterioscler Thromb Vasc Biol. 2008;28:1421–8.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang S, Weinberg S, DeBerge M, Gainullina A, Schipma M, Kinchen JM, Ben-Sahra I, Gius DR, Yvan-Charvet L, Chandel NS, et al. Efferocytosis fuels requirements of fatty acid oxidation and the electron transport chain to polarize macrophages for tissue repair. Cell Metab. 2019;29:443-456.e445.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Suzuki J, Denning DP, Imanishi E, Horvitz HR, Nagata S. Xk-related protein 8 and CED-8 promote phosphatidylserine exposure in apoptotic cells. Science. 2013;341:403–6.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Trzeciak A, Wang YT, Perry JSA. First we eat, then we do everything else: the dynamic metabolic regulation of efferocytosis. Cell Metab. 2021;33:2126–41.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Boada-Romero E, Martinez J, Heckmann BL, Green DR. The clearance of dead cells by efferocytosis. Nat Rev Mol Cell Biol. 2020;21:398–414.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Cai B, Thorp EB, Doran AC, Sansbury BE, Daemen MJ, Dorweiler B, Spite M, Fredman G, Tabas I. MerTK receptor cleavage promotes plaque necrosis and defective resolution in atherosclerosis. J Clin Invest. 2017;127:564–8.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Fourgeaud L, Través PG, Tufail Y, Leal-Bailey H, Lew ED, Burrola PG, Callaway P, Zagórska A, Rothlin CV, Nimmerjahn A, Lemke G. TAM receptors regulate multiple features of microglial physiology. Nature. 2016;532:240–4.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bosurgi L, Cao YG, Cabeza-Cabrerizo M, Tucci A, Hughes LD, Kong Y, Weinstein JS, Licona-Limon P, Schmid ET, Pelorosso F, et al. Macrophage function in tissue repair and remodeling requires IL-4 or IL-13 with apoptotic cells. Science. 2017;356:1072–6.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Huang R, Zhang L, Li X, Liu F, Cheng X, Ran H, Wang Z, Li Y, Feng Y, Liang L, et al. Anti-CXCR2 antibody-coated nanoparticles with an erythrocyte-platelet hybrid membrane layer for atherosclerosis therapy. J Control Release. 2023;356:610–22.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Li X, Yuan P, Yang H, Zong X, Yang C, Chen X, Li Y, Yan X, Wen Y, Zhu T, et al. Virus-like nanotherapeutic for spatiotemporally enhancing antigen presentation and cross-presentation toward potential personalized immunotherapy. Adv Healthc Mater. 2023;1:e2300921.

    Article 

    Google Scholar
     

  • Wang Y, Zhang K, Li T, Maruf A, Qin X, Luo L, Zhong Y, Qiu J, McGinty S, Pontrelli G, et al. Macrophage membrane functionalized biomimetic nanoparticles for targeted anti-atherosclerosis applications. Theranostics. 2021;11:164–80.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liam-Or R, Faruqu FN, Walters A, Han S, Xu L, Wang JT, Oberlaender J, Sanchez-Fueyo A, Lombardi G, Dazzi F, et al: Cellular uptake and in vivo distribution of mesenchymal-stem-cell-derived extracellular vesicles are protein corona dependent. Nat Nanotechnol 2024.

  • Sun L, Zhang M, Shi Y, Fang L, Cao F. Rational design of mixed nanomicelle eye drops with structural integrity investigation. Acta Biomater. 2022;141:164–77.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Yang L, Patel KD, Rathnam C, Thangam R, Hou Y, Kang H, Lee KB. Harnessing the therapeutic potential of extracellular vesicles for biomedical applications using multifunctional magnetic nanomaterials. Small. 2022;18: e2104783.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhao Y, Nie Z, Hong H, Qiu X, Han S, Yu Y, Liu M, Qiu X, Liu K, Meng S, et al. Spectroscopic visualization and phase manipulation of chiral charge density waves in 1T-TaS2. Nat Commun. 2023;14:2223.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang H, Yu D, Liu S, Liu C, Liu Z, Ren J, Qu X. NIR-II Hydrogen-Bonded Organic Frameworks (HOFs) used for target-specific amyloid-β photooxygenation in an alzheimer’s disease model. Angew Chem Int Ed Engl. 2022;61:e202109068.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Brinck J, Hagström E, Nåtman J, Franzén S, Eeg-Olofsson K, Nathanson D, Eliasson B. Cardiovascular outcomes in patients with both diabetes and phenotypic familial hypercholesterolemia: a nationwide register-based cohort study. Diabetes Care. 2022;45:3040–9.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • García-Carro C, Vergara A, Agraz I, Jacobs-Cachá C, Espinel E, Seron D, Soler MJ. The new era for reno-cardiovascular treatment in type 2 diabetes. J Clin Med. 2019;8:1.

    Article 

    Google Scholar
     

  • Li Y, Cui R, Liu K, Eshak ES, Cui M, Dong J, Imano H, Muraki I, Kiyama M, Kitamura A, et al. Relationship between endothelial dysfunction and prevalence of chronic kidney disease: the circulatory risk in communities study (CIRCS). J Atheroscler Thromb. 2021;28:622–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Poznyak A, Grechko AV, Poggio P, Myasoedova VA, Alfieri V, Orekhov AN. The diabetes mellitus-atherosclerosis connection: the role of lipid and glucose metabolism and chronic inflammation. Int J Mol Sci. 2020;21:1.

    Article 

    Google Scholar
     

  • Capodanno D, Angiolillo DJ. Antithrombotic therapy for atherosclerotic cardiovascular disease risk mitigation in patients with coronary artery disease and diabetes mellitus. Circulation. 2020;142:2172–88.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wu Y, Zou H. Research progress on mitochondrial dysfunction in diabetic retinopathy. Antioxidants (Basel). 2022;11:1.


    Google Scholar
     

  • Libby P. The changing landscape of atherosclerosis. Nature. 2021;592:524–33.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • McMurray JJV, Solomon SD, Inzucchi SE, Køber L, Kosiborod MN, Martinez FA, Ponikowski P, Sabatine MS, Anand IS, Bělohlávek J, et al. Dapagliflozin in patients with heart failure and reduced ejection fraction. N Engl J Med. 2019;381:1995–2008.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Marso SP, Bain SC, Consoli A, Eliaschewitz FG, Jódar E, Leiter LA, Lingvay I, Rosenstock J, Seufert J, Warren ML, et al. Semaglutide and cardiovascular outcomes in patients with type 2 diabetes. N Engl J Med. 2016;375:1834–44.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gerstein HC, Colhoun HM, Dagenais GR, Diaz R, Lakshmanan M, Pais P, Probstfield J, Riesmeyer JS, Riddle MC, Rydén L, et al. Dulaglutide and cardiovascular outcomes in type 2 diabetes (REWIND): a double-blind, randomised placebo-controlled trial. Lancet. 2019;394:121–30.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bäck M, Yurdagul A, Tabas I, Öörni K, Kovanen PT. Inflammation and its resolution in atherosclerosis: mediators and therapeutic opportunities. Nat Rev Cardiol. 2019;16:389–406.

    PubMed 
    PubMed Central 

    Google Scholar
     

  • Doran AC, Ozcan L, Cai B, Zheng Z, Fredman G, Rymond CC, Dorweiler B, Sluimer JC, Hsieh J, Kuriakose G, et al. CAMKIIγ suppresses an efferocytosis pathway in macrophages and promotes atherosclerotic plaque necrosis. J Clin Invest. 2017;127:4075–89.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tao W, Yurdagul A, Kong N, Li W, Wang X, Doran AC, Feng C, Wang J, Islam MA, Farokhzad OC, et al. siRNA nanoparticles targeting CAMKIIγ in lesional macrophages improve atherosclerotic plaque stability in mice. Sci Transl Med. 2020;12:1.

    Article 
    CAS 

    Google Scholar
     

  • Esfahani NS, Wu Q, Kumar N, Ganesan LP, Lafuse WP, Rajaram MVS. Aging influences the cardiac macrophage phenotype and function during steady state and during inflammation. Aging Cell. 2021;20: e13438.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Seki E, de Minicis S, Inokuchi S, Taura K, Miyai K, van Rooijen N, Schwabe RF, Brenner DA. CCR2 promotes hepatic fibrosis in mice. Hepatology. 2009;50:185–97.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Thorp E, Vaisar T, Subramanian M, Mautner L, Blobel C, Tabas I. Shedding of the Mer tyrosine kinase receptor is mediated by ADAM17 protein through a pathway involving reactive oxygen species, protein kinase Cδ, and p38 mitogen-activated protein kinase (MAPK). J Biol Chem. 2011;286:33335–44.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • DeBerge M, Lantz C, Dehn S, Sullivan DP, van der Laan AM, Niessen HWM, Flanagan ME, Brat DJ, Feinstein MJ, Kaushal S, et al. Hypoxia-inducible factors individually facilitate inflammatory myeloid metabolism and inefficient cardiac repair. J Exp Med. 2021;218:1.

    Article 

    Google Scholar
     

  • Karunakaran D, Geoffrion M, Wei L, Gan W, Richards L, Shangari P, DeKemp EM, Beanlands RA, Perisic L, Maegdefessel L, et al. Targeting macrophage necroptosis for therapeutic and diagnostic interventions in atherosclerosis. Sci Adv. 2016;2:e1600224.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bi X, Stankov S, Lee PC, Wang Z, Wu X, Li L, Ko YA, Cheng L, Zhang H, Hand NJ, Rader DJ. ILRUN Promotes Atherosclerosis Through Lipid-Dependent and Lipid-Independent Factors. Arterioscler Thromb Vasc Biol. 2022;42:1139–51.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Chen R, Yang J, Wu M, Zhao D, Yuan Z, Zeng L, Hu J, Zhang X, Wang T, Xu J, Zhang J. M2 macrophage hybrid membrane-camouflaged targeted biomimetic nanosomes to reprogram inflammatory microenvironment for enhanced enzyme-thermo-immunotherapy. Adv Mater. 2023;1:e2304123.

    Article 

    Google Scholar
     

  • Zou Y, Sun Y, Wang Y, Zhang D, Yang H, Wang X, Zheng M, Shi B. Cancer cell-mitochondria hybrid membrane coated Gboxin loaded nanomedicines for glioblastoma treatment. Nat Commun. 2023;14:4557.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • He W, Li X, Morsch M, Ismail M, Liu Y, Rehman FU, Zhang D, Wang Y, Zheng M, Chung R, et al. Brain-targeted codelivery of Bcl-2/Bcl-xl and Mcl-1 inhibitors by biomimetic nanoparticles for orthotopic glioblastoma therapy. ACS Nano. 2022;16:6293–308.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen L, Hong W, Ren W, Xu T, Qian Z, He Z. Recent progress in targeted delivery vectors based on biomimetic nanoparticles. Signal Transduct Target Ther. 2021;6:225.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Azarmi M, Maleki H, Nikkam N, Malekinejad H. Novel neurolisteriosis therapy using SPION as a drivable nanocarrier in gallic acid delivery to CNS. J Control Release. 2023;353:507–17.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gonçalves T, Marques AT, Manageiro V, Tanoeiro L, Vital JS, Duarte A. J MBV, Caniça M, Manuela Gaspar M, Vale FF: Antimicrobial activity of prophage endolysins against critical Enterobacteriaceae antibiotic-resistant bacteria. Int J Pharm. 2023;1:123758.


    Google Scholar
     

  • Xiao Q, Zoulikha M, Qiu M, Teng C, Lin C, Li X, Sallam MA, Xu Q, He W. The effects of protein corona on in vivo fate of nanocarriers. Adv Drug Deliv Rev. 2022;186: 114356.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Wang D, Xing C, Liang Y, Wang C, Zhao P, Liang X, Li Q, Yuan L. Ultrasound Imaging of Tumor Vascular CD93 with MMRN2 Modified Microbubbles for Immune Microenvironment Prediction. Adv Mater. 2024;1:e2310421.

    Article 

    Google Scholar
     

  • Li X, Yuan P, Yang H, Zong X, Yang C, Chen X, Li Y, Yan X, Wen Y, Zhu T, et al. Virus-like nanotherapeutic for spatiotemporally enhancing antigen presentation and cross-presentation toward potential personalized immunotherapy. Adv Healthc Mater. 2023;12:e2300921.

    Article 
    PubMed 

    Google Scholar
     

  • Gogate PR, Kabadi AM. A review of applications of cavitation in biochemical engineering/biotechnology. Biochem Eng J. 2009;44:60–72.

    Article 
    CAS 

    Google Scholar
     

  • Lai X, Liu XL, Pan H, Zhu MH, Long M, Yuan Y, Zhang Z, Dong X, Lu Q, Sun P, et al. Light-triggered efficient sequential drug delivery of biomimetic nanosystem for multimodal chemo-, antiangiogenic, and anti-mdsc therapy in melanoma. Adv Mater. 2022;34:e2106682.

    Article 
    PubMed 

    Google Scholar
     

  • Qi H, Liu C, Long L, Ren Y, Zhang S, Chang X, Qian X, Jia H, Zhao J, Sun J, et al. Blood exosomes endowed with magnetic and targeting properties for cancer therapy. ACS Nano. 2016;10:3323–33.

    Article 
    CAS 
    PubMed 

    Google Scholar