Gold nanoparticles regulate tight junctions and improve cetuximab effect in colon cancer cells

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References

• 1. Bobo D, Robinson KJ, Islam J, Thurecht KJ, Corrie SR. Nanoparticle-based medicines: a review of FDA-approved materials and clinical trials to date. Pharm. Res., 33(10), 2373–2387 (2016). • An excellent and extensive review of different types of nanomedicines in clinical trials in recent years.
  Medline CASGoogle Scholar
• 2. Kumar A, Zhang X, Liang X-J. Gold nanoparticles: emerging paradigm for targeted drug delivery system. Biotechnol. Adv., 31(5), 593–606 (2013). • Recent advances in drug delivery approaches with a particular focus on gold nanoparticles, especially for cancer treatment.
  Medline CASGoogle Scholar
• 3. Libutti SK, Paciotti GF, Byrnes AA et al. Phase I and pharmacokinetic studies of CYT-6091, a novel PEGylated colloidal gold-rhTNF. Nanomed. Clin. Cancer Res., 16(24), 6139–6149 (2010).
  Medline CASGoogle Scholar
• 4. Wu D, Wang H, Hou X et al. Effects of gold core size on regulating the performance of doxorubicin-conjugated gold nanoparticles. Nano Res., 11(6), 3396–3410 (2018).
  CASGoogle Scholar
• 5. Connor EE, Mwamuka J, Gole A, Murphy CJ, Wyatt MD. Gold nanoparticles are taken up by human cells but do not cause acute cytotoxicity. Small, 1(3), 325–327 (2005). •• One of the few studies to evaluate the cytotoxicity of uncoated gold nanoparticles reports that they are not inherently toxic to human cells.
  Medline CASGoogle Scholar
• 6. Li C, Li Z, Zhang Y, Fathy AH, Zhou M. The role of the Wnt/β-catenin signaling pathway in the proliferation of gold nanoparticle-treated human periodontal ligament stem cells. Stem Cell Res. Ther., 9, 214 (2018).
  Medline CASGoogle Scholar
• 7. Surapaneni SK, Bashir S, Tikoo K. Gold nanoparticles-induced cytotoxicity in triple negative breast cancer involves different epigenetic alterations depending upon the surface charge. Sci. Reports, 8, 12295 (2018).
  MedlineGoogle Scholar
• 8. Lee E, Jeon H, Lee M et al. Molecular origin of AuNPs-induced cytotoxicity and mechanistic study. Sci. Reports, 9, 2494 (2019).
  Google Scholar
• 9. Lin IC, Liang M, Liu TY, Monteiro MJ, Toth I. Cellular transport pathways of polymer coated gold nanoparticles. Nanomedicine, 8, 8–11 (2012).
  Medline CASGoogle Scholar
• 10. Li CH, Shyu MK, Jhan C et al. Gold nanoparticles increase endothelial paracellular permeability by altering components of endothelial tight junctions, and increase blood–brain barrier permeability in mice. Toxicol. Sci., 148(1), 192–203 (2015).
  Medline CASGoogle Scholar
• 11. Arvizo RR, Saha S, Wang E, Robertson JD, Bhattacharya R, Mukherjee P. Inhibition of tumor growth and metastasis by a self-therapeutic nanoparticle. Proc. Nat. Acad. Sci., 110(17), 6700–6705 (2013). •• Besides characterizing the biological effect of naked gold nanoparticles, it was the first work to show the antitumor effect of these nanoparticles.
  Medline CASGoogle Scholar
• 12. Li W, Li X, Liu S et al. Gold nanoparticles attenuate metastasis by tumor vasculature normalization and epithelial–mesenchymal transition inhibition. Int. J. Nanomed., 12, 3509–3520 (2017).
  Medline CASGoogle Scholar
• 13. Deli MA. Potential use of tight junction modulators to reversibly open membranous barriers and improve drug delivery. Biochim. Biophys. Acta, 1788(4), 892–910 (2009).
  Medline CASGoogle Scholar
• 14. Wang C, Yumul RC, Lin J, Cheng Y, Lieber A, Pun SH. Junction opener protein increases nanoparticle accumulation in solid tumors. J. Control. Rel., 272(9), 16 (2018).
  Google Scholar
• 15. Weinberg RA. The Biology of Cancer. Garland Science, London, UK (2006).
  Google Scholar
• 16. Ratnam M, Hao H, Zheng X et al. Receptor induction and targeted drug delivery: a new anti leukaemia strategy. Expert Opin. Biol. Ther., 3, 563–574 (2003).
  Medline CASGoogle Scholar
• 17. Belting M, Sandgren S, Wittrup A. Nuclear delivery of macromolecules: barriers and carriers. Adv. Drug Deliv. Rev., 57(4), 505–527 (2005).
  Medline CASGoogle Scholar
• 18. Hymel D, Peterson BR. Synthetic cell surface receptors for delivery of therapeutics and probes. Adv. Drug Deliv. Rev., 64, 797–810 (2012).
  Medline CASGoogle Scholar
• 19. Fornasier G, Francescon S, Baldo SFP. An update of efficacy and safety of cetuximab in metastatic colorectal cancer: a narrative review. Adv. Ther., 35(10), 1497–1509 (2018).
  MedlineGoogle Scholar
• 20. García-Fernández L, Garcia-Pardo J, Tort O et al. Conserved effects and altered trafficking of cetuximab antibodies conjugated to gold nanoparticles with precise control of their number and orientation. Nanoscale, 9(18), 6111–6121 (2017).
  Medline CASGoogle Scholar
• 21. Khan JA, Kudgus RA, Szabolcs A et al. Designing nanoconjugates to effectively target pancreatic cancer cells in vitro and in vivo. PLoS ONE, 6(6), e20347 (2011).
  Medline CASGoogle Scholar
• 22. Kao H-W, Lin Y-Y, Chen C-C et al. Biological characterization of cetuximab conjugated gold nanoparticles in a tumor animal model. Nanotechnology, 25(29), 295102 (2014).
  MedlineGoogle Scholar
• 23. Berger C, Madshus IH, Stang E. Cetuximab in combination with anti-human IgG antibodies efficiently down-regulates the EGF receptor by micropinocytosis. Exp. Cell Res., 318(20), 2578–2591 (2012).
  Medline CASGoogle Scholar
• 24. Kimling J, Maier M, Okenve B, Kotaidis V, Ballot H, Plech A. Turkevich method for gold nanoparticle synthesis revisited. J. Phys. Chem. B, 110(32), 15700–15707 (2006).
  Medline CASGoogle Scholar
• 25. Leve F, de Souza W, Morgado-Díaz JA. A cross-link between protein kinase A and Rho-family GTPases signaling mediates cell–cell adhesion and actin cytoskeleton organization in epithelial cancer cells. J. Pharmacol. Exp. Ther., 327(3), 777–788 (2008).
  Medline CASGoogle Scholar
• 26. Jonitz-Heincke A, Tillmann J, Ostermann M et al. Label-free monitoring of uptake and toxicity of endoprosthetic wear particles in human cell cultures. Int. J. Mol. Sci., 19(11), pii:E3486 (2018).
  Google Scholar
• 27. Ivanov AI, Hunt D, Utech M, Nusrat A, Parkos CA. Differential roles for actin polymerization and a myosin II motor in assembly of the epithelial apical junctional complex. Mol. Biol. Cell., 16(6), 2636–2650 (2005).
  Medline CASGoogle Scholar
• 28. Zinser-Sierra JW, Rodríguez-Ramírez S, Villalobos-Valencia R, Ramírez-Márquez M. Use of bevacizumab in metastatic colorectal cancer report from the Mexican opinion and analysis forum on colorectal cancer treatment with bevacizumab (September 2009). Drugs RD, 11(2), 101–111 (2011).
  MedlineGoogle Scholar
• 29. Gehren AS, Rocha MR, de Souza WF, Morgado-Díaz JA. Alterations of the apical junctional complex and actin cytoskeleton and their role in colorectal cancer progression. Tissue Barriers, 3, e1017688 (2015).
  MedlineGoogle Scholar
• 30. Beyer I, Rensburg R, Strauss R et al. Epithelial junction opener JO-1 improves monoclonal antibody therapy of cancer. Cancer Res., 71(22), 7080–7090 (2011).
  Medline CASGoogle Scholar
• 31. Schlinkert P, Casals E, Boyles M et al. The oxidative potential of differently charged silver and gold nanoparticles on three human lung epithelial cell types. J. Nanobiotechnol., 13, 1 (2015).
  MedlineGoogle Scholar
• 32. Lin IC, Liang MT, Liu TY, Ziora ZM, Monteiro MJ, Toth I. Interaction of densely polymer-coated gold nanoparticles with epithelial caco-2 monolayers. Biomacromolecules, 12, 1339–1348 (2011). •• The authors investigate how different coatings on gold nanoparticles of different sizes influence the loss of Caco-2 cells epithelial barrier.
  Medline CASGoogle Scholar
• 33. Runkle EA, Mu D. Tight junction proteins: from barrier to tumorigenesis. Cancer Lett., 337(1), 41–48 (2013).
  Medline CASGoogle Scholar
• 34. Kotelevets L, Chastre E, Desmaële D, Couvreur P. Nanotechnologies for the treatment of colon cancer: from old drugs to new hope. Int. J. Pharm., 514(1), 24–40 (2016). • A very detailed review on therapy in colon cancer and how the approach of nanomedicine may circumvent the mechanisms of drug resistance.
  Medline CASGoogle Scholar
• 35. Cui L, Her S, Dunne M et al. Significant radiation enhancement effects by gold nanoparticles in combination with cisplatin in triple negative breast cancer cells and tumor xenografts. Radiat. Res., 187(2), 147–160 (2017).
  Medline CASGoogle Scholar
• 36. Patra CR, Bhattacharya R, Wang E et al. Targeted delivery of gemcitabine to pancreatic adenocarcinoma using cetuximab as a targeting agent. Cancer Res., 68(6), 1970–1978 (2008).
  Medline CASGoogle Scholar
• 37. Lee CS, Kim H, Yu J et al. Doxorubicin-loaded oligonucleotide conjugated gold nanoparticles: a promising in vivo drug delivery system for colorectal cancer therapy. Eur. J. Med. Chem., 142, 416–423 (2017).
  Medline CASGoogle Scholar
• 38. Coluccia D, Figueiredo CA, Wu MY et al. Enhancing glioblastoma treatment using cisplatin–gold-nanoparticle conjugates and targeted delivery with magnetic resonance-guided focused ultrasound. Nanomedicine, 14(4), 1137–1148 (2018).
  Medline CASGoogle Scholar
• 39. Misale S, Yaeger R, Hobor S et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature, 486(7404), 532–536 (2012).
  Medline CASGoogle Scholar
• 40. Dunn EF, Iida M, Myers RA et al. Dasatinib sensitizes KRAS mutant colorectal tumors to cetuximab. Oncogene, 30(5), 561–574 (2011).
  Medline CASGoogle Scholar
• 41. Li X, Lu Y, Pan T, Fan Z. Roles of autophagy in cetuximab-mediated cancer therapy against EGFR. Autophagy, 6, 1066–1077 (2010).
  Medline CASGoogle Scholar
• 42. Kumar SS, Price TJ, Mohyieldin O, Borg M, Townsend A, Hardingham JE. KRAS G13D mutation and sensitivity to cetuximab or panitumumab in a colorectal cancer cell line model. Gastrointest. Cancer Res., 7(1), 23–26 (2014).
  MedlineGoogle Scholar
• 43. Singh AB, Harris RC. Epidermal growth factor receptor activation differentially regulates claudin expression and enhances transepithelial resistance in Madin–Darby canine kidney cells. J. Biol. Chem., 279(5), 3543–3552 (2004).
  Medline CASGoogle Scholar
• 44. Rübsam M, Mertz AS, Kubo A et al. E-cadherin integrates mechanotransduction and EGFR signaling to control junctional tissue polarization and tight junction positioning. Nat. Commun., 8, 1250 (2017).
  MedlineGoogle Scholar
• 45. Nakamoto K, Nagahara H, Maeda K et al. Expression of E-cadherin and KRAS mutation may serve as biomarkers of cetuximab-based therapy in metastatic colorectal cancer. Oncol. Lett., 5(4), 1295–1300 (2013).
  Medline CASGoogle Scholar
• 46. Qian Y, Qiu M, Wu Q et al. Enhanced cytotoxic activity of cetuximab in EGFR-positive lung cancer by conjugating with gold nanoparticles. Sci. Rep., 4, 7490 (2014). •• The authors show that conjugation of cetuximab with gold nanoparticles enhances the cytotoxicity of lung cancer both in vitro and in vivo.
  Medline CASGoogle Scholar
• 47. Bhattacharyya S, Bhattacharya R, Curley S, McNiven MA, Mukherjee P. Nanoconjugation modulates the trafficking and mechanism of antibody induced receptor endocytosis. Proc. Nat. Acad. Sci., 107(33), 14541 (2010).
  Medline CASGoogle Scholar
• 48. Ahmed M, Pan DW, Davis ME. Lack of in vivo antibody dependent cellular cytotoxicity with antibody containing gold nanoparticles. Bioconjugate Chem., 26(5), 812–816 (2015).
  Medline CASGoogle Scholar