Enhancement of Pancreatic Cancer Therapy Efficacy by Type-1 Matrix Metalloproteinase-Functionalized Nanoparticles for the Selective Delivery of Gemcitabine and Erlotinib

References

• SiegelRL, MillerKD, JemalA. Cancer statistics, 2018. CA Cancer J Clin. 2018;68(1):7–30. doi:10.3322/caac.2144229313949
   PubMed Web of Science ®Google Scholar
• RawlaP, SunkaraT, GaduputiV. Epidemiology of pancreatic cancer: global trends, etiology and risk factors. World J Oncol. 2019;10(1):10–27. doi:10.14740/wjon116630834048
   PubMedGoogle Scholar
• RahibL, SmithBD, AizenbergR, RosenzweigAB, FleshmanJM, MatrisianLM. Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. Cancer Res. 2014;74(11):2913–2921. doi:10.1158/0008-5472.CAN-14-015524840647
   PubMed Web of Science ®Google Scholar
• PeixotoRD, HoM, RenoufDJ, et al. Eligibility of metastatic pancreatic cancer patients for first-line palliative intent nab-paclitaxel plus gemcitabine versus FOLFIRINOX. Am J Clin Oncol. 2017;40(5):507–511. doi:10.1097/COC.000000000000019325844823
   PubMed Web of Science ®Google Scholar
• OettleH, PostS, NeuhausP, et al. Adjuvant chemotherapy with gemcitabine vs observation in patients undergoing curative-intent resection of pancreatic cancer: a randomized controlled trial. JAMA. 2007;297(3):267–277. doi:10.1001/jama.297.3.26717227978
   PubMed Web of Science ®Google Scholar
• OettleH, NeuhausP, HochhausA, et al. Adjuvant chemotherapy with gemcitabine and long-term outcomes among patients with resected pancreatic cancer: the CONKO-001 randomized trial. JAMA. 2013;310(14):1473–1481. doi:10.1001/jama.2013.27920124104372
   PubMed Web of Science ®Google Scholar
• ShipleyLA, BrownTJ, CornpropstJD, HamiltonM, DanielsWD, CulpHW. Metabolism and disposition of gemcitabine, and oncolytic deoxycytidine analog, in mice, rats, and dogs. Drug Metab Dispos. 1992;20(6):849–855.1362937
   PubMed Web of Science ®Google Scholar
• SunJ, WanZ, ChenY, et al. Triple drugs co-delivered by a small gemcitabine-based carrier for pancreatic cancer immunochemotherapy. Acta Biomater. 2020;106:289–300. doi:10.1016/j.actbio.2020.01.03932004652
   PubMed Web of Science ®Google Scholar
• SarvepalliD, RashidMU, RahmanAU, et al. Gemcitabine: a review of chemoresistance in pancreatic cancer. Critical Reviews™ in Oncogenesis. 2019;24(2):199–212. doi:10.1615/CritRevOncog.2019031641
   PubMedGoogle Scholar
• Von HoffDD, ErvinT, ArenaFP, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med. 2013;369(18):1691–1703. doi:10.1056/NEJMoa130436924131140
   PubMed Web of Science ®Google Scholar
• SamantaK, SetuaS, KumariS, JaggiM, YallapuMM, ChauhanSC. Gemcitabine combination nano therapies for pancreatic cancer. Pharmaceutics. 2019;11(11):pii: E574. doi:10.3390/pharmaceutics11110574
   PubMed Web of Science ®Google Scholar
• MooreMJ, GoldsteinD, HammJ, et al. Erlotinib plus gemcitabine compared with gemcitabine alone in patients with advanced pancreatic cancer: a phase iii trial of the National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol. 2007;25(15):1960–1966.17452677
   PubMed Web of Science ®Google Scholar
• MillerAL, GarciaPL, YoonKJ. Developing effective combination therapy for pancreatic cancer: an overview. Pharmacol Res. 2020;155:104740. doi:10.1016/j.phrs.2020.10474032135247
   PubMed Web of Science ®Google Scholar
• JamshedMB, MunirF, ShahidN, et al. Antitumor activity and combined inhibitory effect of ceritinib with gemcitabine in pancreatic cancer. Am J Physiol Gastrointest Liver Physiol. 2020;318(1):G109–G119. doi:10.1152/ajpgi.00130.201931736340
   PubMed Web of Science ®Google Scholar
• WangY, HuGF, ZhangQQ, et al. Efficacy and safety of gemcitabine plus erlotinib for locally advanced or metastatic pancreatic cancer: a systematic review and meta-analysis. Drug Des Devel Ther. 2016;10:1961–1972. doi:10.2147/DDDT.S105442
   PubMed Web of Science ®Google Scholar
• Oliveira-CunhaM, NewmanWG, SiriwardenaAK. Epidermal growth factor receptor in pancreatic cancer. Cancers. 2011;3(2):1513–1526. doi:10.3390/cancers302151324212772
   PubMedGoogle Scholar
• AdamskaA, DomenichiniA, FalascaM. Pancreatic ductal adenocarcinoma: current and evolving therapies. Int J Mol Sci. 2017;18(7):pii: E1338. doi:10.3390/ijms18071338
   PubMed Web of Science ®Google Scholar
• MarslinG, SheebaCJ, KalaichelvanVK, ManavalanR, ReddyPN, FranklinG. Poly(D,L-lactic-co-glycolic acid) nanoencapsulation reduces Erlotinib-induced subacute toxicity in rat. J Biomed Nanotechnol. 2009;5(5):464–471. doi:10.1166/jbn.2009.107520201419
   PubMed Web of Science ®Google Scholar
• FleigeE, QuadirMA, HaagR. Stimuli-responsive polymeric nanocarriers for the controlled transport of active compounds: concepts and applications. Adv Drug Deliv Rev. 2012;64(9):866–884. doi:10.1016/j.addr.2012.01.02022349241
   PubMed Web of Science ®Google Scholar
• KulkarniPS, HaldarMK, NahireRR, et al. Mmp-9 responsive PEG cleavable nanovesicles for efficient delivery of chemotherapeutics to pancreatic cancer. Mol Pharm. 2014;11(7):2390–2399. doi:10.1021/mp500108p24827725
   PubMed Web of Science ®Google Scholar
• HimelsteinBP, Canete-SolerR, BernhardEJ, DilksDW, MuschelRJ. Metalloproteinases in tumor progression: the contribution of MMP-9. Invasion Metastasis. 1994;14(1–6):246–258.7657517
   PubMedGoogle Scholar
• BloomstonM, ZervosEE, RosemurgyAS. Matrix metalloproteinases and their role in pancreatic cancer: a review of preclinical studies and clinical trials. Ann Surg Oncol. 2002;9(7):668–674. doi:10.1007/BF0257448312167581
   PubMed Web of Science ®Google Scholar
• GrünwaldB, VandoorenJ, LocatelliE, et al. Matrix metalloproteinase-9 (MMP-9) as an activator of nanosystems for targeted drug delivery in pancreatic cancer. J Control Release. 2016;239:39–48. doi:10.1016/j.jconrel.2016.08.01627545397
   PubMed Web of Science ®Google Scholar
• KrantzSB, ShieldsMA, Dangi-GarimellaS, et al. MT1-MMP cooperates with Kras(G12D) to promote pancreatic fibrosis through increased TGF-β signaling. Mol Cancer Res. 2011;9:1294–1304. doi:10.1158/1541-7786.MCR-11-002321856775
   PubMed Web of Science ®Google Scholar
• KnapinskaAM, EstradaCA, FieldsGB. The roles of matrix metalloproteinases in pancreatic cancer. Prog Mol Biol Transl Sci. 2017;148:339–354.28662827
   PubMed Web of Science ®Google Scholar
• GuG, GaoX, HuQ, et al. The influence of the penetrating peptide iRGD on the effect of paclitaxel-loaded MT1-AF7p-conjugated nanoparticles on glioma cells. Biomaterials. 2013;34(21):5138–5148. doi:10.1016/j.biomaterials.2013.03.03623582684
   PubMed Web of Science ®Google Scholar
• Dangi-GarimellaS, KrantzSB, BarronMR, et al. Three-dimensional collagen I promotes gemcitabine resistance in pancreatic cancer through MT1-MMP-mediated expression of HMGA2. Cancer Res. 2011;71(3):1019–1028. doi:10.1158/0008-5472.CAN-10-185521148071
   PubMed Web of Science ®Google Scholar
• ElechalawarCK, HossenMN, ShankarappaP, et al. Targeting pancreatic cancer cells and stellate cells using designer nanotherapeutics in vitro. Int J Nanomedicine. 2020;15:991–1003. doi:10.2147/IJN.S23411232103952
   PubMed Web of Science ®Google Scholar
• ZhangS, WangJ, PanJ. Baicalin-loaded PEGylated lipid nanoparticles: characterization, pharmacokinetics, and protective effects on acute myocardial ischemia in rats. Drug Deliv. 2016;23(9):3696–3703. doi:10.1080/10717544.2016.122321827749105
   PubMed Web of Science ®Google Scholar
• YuW, LiuC, YeJ, ZouW, ZhangN, XuW. Novel cationic SLN containing a synthesized single-tailed lipid as a modifier for gene delivery. Nanotechnology. 2009;20(21):215102. doi:10.1088/0957-4484/20/21/21510219423923
   PubMed Web of Science ®Google Scholar
• ZhuangB, DuL, XuH, et al. Self-assembled micelle loading cabazitaxel for therapy of lung cancer. Int J Pharm. 2016;499(1–2):146–155. doi:10.1016/j.ijpharm.2015.12.07326762884
   PubMed Web of Science ®Google Scholar
• NooraniM, AzarpiraN, KarimianK, HeliH. Erlotinib-loaded albumin nanoparticles: a novel injectable form of erlotinib and its in vivo efficacy against pancreatic adenocarcinoma ASPC-1 and PANC-1 cell lines. Int J Pharm. 2017;531(1):299–305. doi:10.1016/j.ijpharm.2017.08.10228847671
   PubMed Web of Science ®Google Scholar
• ZhuS, Lansakara-PDS, LiX, CuiZ. Lysosomal delivery of a lipophilic gemcitabine prodrug using novel acid-sensitive micelles improved its antitumor activity. Bioconjug Chem. 2012;23(5):966–980. doi:10.1021/bc200594522471294
   PubMed Web of Science ®Google Scholar
• ZhangR, RuY, GaoY, LiJ, MaoS. Layer-by-layer nanoparticles co-loading gemcitabine and platinum (IV) prodrugs for synergistic combination therapy of lung cancer. Drug Des Devel Ther. 2017;5(11):2631–2642. doi:10.2147/DDDT.S143047
   Web of Science ®Google Scholar
• ZhengG, ZhengM, YangB, FuH, LiY. Improving breast cancer therapy using doxorubicin loaded solid lipid nanoparticles: synthesis of a novel arginine-glycine-aspartic tripeptide conjugated, pH sensitive lipid and evaluation of the nanomedicine in vitro and in vivo. Biomed Pharmacother. 2019;116:109006. doi:10.1016/j.biopha.2019.10900631152925
   PubMed Web of Science ®Google Scholar
• ZhangJ, XiaoX, ZhuJ, et al. Lactoferrin- and RGD-comodified, temozolomide and vincristine-coloaded nanostructured lipid carriers for gliomatosis cerebri combination therapy. Int J Nanomedicine. 2018;13:3039–3051. doi:10.2147/IJN.S16116329861635
   PubMed Web of Science ®Google Scholar
• VrignaudS, HureauxJ, WackS, BenoitJ-P, SaulnierP. Design, optimization and in vitro evaluation of reverse micelle-loaded lipid nanocarriers containing erlotinib hydrochloride. Int J Pharm. 2012;436(1–2):194–200. doi:10.1016/j.ijpharm.2012.06.02622721853
   PubMed Web of Science ®Google Scholar
• YalcinTE, Ilbasmis-TamerS, TakkaS. Antitumor activity of gemcitabine hydrochloride loaded lipid polymer hybrid nanoparticles (LPHNs): in vitro and in vivo. Int J Pharm. 2020;580:119246. doi:10.1016/j.ijpharm.2020.11924632205141
   PubMed Web of Science ®Google Scholar
• ZhangY, KimWY, HuangL. Systemic delivery of gemcitabine triphosphate via LCP nanoparticles for NSCLC and pancreatic cancer therapy. Biomaterials. 2013;34(13):3447–3458. doi:10.1016/j.biomaterials.2013.01.06323380359
   PubMed Web of Science ®Google Scholar
• CuiN, HuM, KhalilRA. Biochemical and biological attributes of matrix metalloproteinases. Prog Mol Biol Transl Sci. 2017;147:1–73.28413025
   PubMed Web of Science ®Google Scholar
• YaoQ, KouL, TuY, ZhuL. MMP-responsive ‘smart’ drug delivery and tumor targeting. Trends Pharmacol Sci. 2018;39(8):766–781. doi:10.1016/j.tips.2018.06.00330032745
   PubMed Web of Science ®Google Scholar
• RenL, WangY, ZhuL, et al. Optimization of a MT1-MMP-targeting peptide and its application in near-infrared fluorescence tumor imaging. Sci Rep. 2018;8(1):10334. doi:10.1038/s41598-018-28493-929985410
   PubMed Web of Science ®Google Scholar
• MorcilloMÁ, García de LucasÁ, OteoM, et al. MT1-MMP as a PET imaging biomarker for pancreas cancer management. Contrast Media Mol Imaging. 2018;2018:8382148.30224904
   PubMed Web of Science ®Google Scholar
• YuW, ZhangN. Surface modification of nanocarriers for cancer therapy. Curr Nanosci. 2009;5(2):123–134. doi:10.2174/157341309788185370
   Web of Science ®Google Scholar
• PeetersL, SandersNN, JonesA, DemeesterJ, De SmedtSC. Post-pegylated lipoplexes are promising vehicles for gene delivery in RPE cells. J Control Release. 2007;121(3):208–217. doi:10.1016/j.jconrel.2007.05.03317630013
   PubMed Web of Science ®Google Scholar
• DuJ, LiL. Which one performs better for targeted lung cancer combination therapy: pre- or post-bombesin-decorated nanostructured lipid carriers? Drug Deliv. 2016;23(5):1799–1809. doi:10.3109/10717544.2015.109905826455787
   PubMed Web of Science ®Google Scholar
• XuY, WuH, HuangJ, et al. Probing and enhancing ligand-mediated active targeting of tumors using sub-5 nm ultrafine iron oxide nanoparticles. Theranostics. 2020;10(6):2479–2494. doi:10.7150/thno.3956032194814
   PubMed Web of Science ®Google Scholar
• WangJ, SuG, YinX, et al. Non-small cell lung cancer-targeted, redox-sensitive lipid-polymer hybrid nanoparticles for the delivery of a second-generation irreversible epidermal growth factor inhibitor-Afatinib: in vitro and in vivo evaluation. Biomed Pharmacother. 2019;120:109493. doi:10.1016/j.biopha.2019.10949331586902
   PubMed Web of Science ®Google Scholar
• WangG, WangZ, LiC, et al. RGD peptide-modified, paclitaxel prodrug-based, dual-drugs loaded, and redox-sensitive lipid-polymer nanoparticles for the enhanced lung cancer therapy. Biomed Pharmacother. 2018;106:275–284. doi:10.1016/j.biopha.2018.06.13729966971
   PubMed Web of Science ®Google Scholar
• CaoC, WangQ, LiuY. Lung cancer combination therapy: doxorubicin and β-elemene co-loaded, pH-sensitive nanostructured lipid carriers. Drug Des Devel Ther. 2019;5(13):1087–1098. doi:10.2147/DDDT.S198003
   Web of Science ®Google Scholar
• WangJ. Combination treatment of cervical cancer using folate-decorated, pH-sensitive, carboplatin and paclitaxel co-loaded lipid-polymer hybrid nanoparticles. Drug Des Devel Ther. 2020;14:823–832. doi:10.2147/DDDT.S235098
   PubMed Web of Science ®Google Scholar
• GaoZ, LiZ, YanJ, WangP. Irinotecan and 5-fluorouracil-co-loaded, hyaluronic acid-modified layer-by-layer nanoparticles for targeted gastric carcinoma therapy. Drug Des Devel Ther. 2017;11:2595–2604. doi:10.2147/DDDT.S140797
   PubMed Web of Science ®Google Scholar
• DuanW, LiuY. Targeted and synergistic therapy for hepatocellular carcinoma: monosaccharide modified lipid nanoparticles for the co-delivery of doxorubicin and sorafenib. Drug Des Devel Ther. 2018;12:2149–2161. doi:10.2147/DDDT.S166402
   PubMed Web of Science ®Google Scholar
• YanJ, WangY, ZhangX, LiuS, TianC, WangH. Targeted nanomedicine for prostate cancer therapy: docetaxel and curcumin co-encapsulated lipid-polymer hybrid nanoparticles for the enhanced anti-tumor activity in vitro and in vivo. Drug Deliv. 2016;23(5):1757–1762. doi:10.3109/10717544.2015.106942326203689
   PubMed Web of Science ®Google Scholar
• HongY, CheS, HuiB, et al. Lung cancer therapy using doxorubicin and curcumin combination: targeted prodrug based, pH sensitive nanomedicine. Biomed Pharmacother. 2019;112:108614. doi:10.1016/j.biopha.2019.10861430798129
   PubMed Web of Science ®Google Scholar
• UdofotO, AfframK, SmithT, et al. Pharmacokinetic, biodistribution and therapeutic efficacy of 5-fluorouracil-loaded pH-sensitive PEGylated liposomal nanoparticles in HCT-116 tumor bearing mouse. J Nat Sci. 2016;2(1):pii: e171.
   PubMedGoogle Scholar
• YuguiF, WangH, SunD, ZhangX. Nasopharyngeal cancer combination chemoradiation therapy based on folic acid modified, gefitinib and yttrium 90 co-loaded, core-shell structured lipid-polymer hybrid nanoparticles. Biomed Pharmacother. 2019;114:108820. doi:10.1016/j.biopha.2019.10882030951947
   PubMed Web of Science ®Google Scholar