Tuning the autophagy-inducing activity of lanthanide-based nanocrystals through specific surface-coating peptides
Source abstract
Abstract
The induction of autophagy on exposure of cells to a variety of nanoparticles represents both a safety concern and an application niche for engineered nanomaterials. Here, we show that a short synthetic peptide, RE-1, identified by means of phage display, binds to lanthanide (LN) oxide and upconversion nanocrystals (UCN), forms a stable coating layer on the nanoparticles' surface, and effectively abrogates their autophagy-inducing activity. Furthermore, RE-1 peptide variants exhibit a differentially reduced binding capability, and correspondingly, a varied ability to reduce the autophagic response. We also show that the addition of an arginine-glycine-aspartic acid (RGD) motif to RE-1 enhances autophagy for LN UCN through the interaction with integrins. RE-1 and its variants provide a versatile tool for tuning material-cell interactions to achieve the desired level of autophagy, and may prove useful for the various diagnostic and therapeutic applications of LN-based nanomaterials and nanodevices.
Source: europepmc · Quality: candidate unverified · Source record ↗
Research context
OpenAlex topics: Autophagy in Disease and Therapy · Advanced Proteomics Techniques and Applications · Bacteriophages and microbial interactions
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (47)
Show source-provided references
1. Klionsky, D. J. Autophagy: From phenomenology to molecular understanding in less than a decade. Nature Rev. Mol. Cell Biol. 8, 931–937 (2007).10.1038/nrm2245 ↗
2. Mizushima, N. Autophagy: Process and function. Genes Dev. 21, 2861–2873 (2007).10.1101/gad.1599207 ↗
3. Ravikumar, B. et al. Regulation of mammalian autophagy in physiology and pathophysiology. Phys. Rev. 90, 1383–1435 (2010).
4. Mizushima, N., Levine, B., Cuervo, A. M. & Klionsky, D. J. Autophagy fights disease through cellular self-digestion. Nature 451, 1069–1075 (2008).10.1038/nature06639 ↗
5. Levine, B. Cell biology—autophagy and cancer. Nature 446, 745–747 (2007).10.1038/446745a ↗
6. Pan, T. H., Kondo, S., Le, W. & Jankovic, J. The role of autophagy-lysosome pathway in neurodegeneration associated with Parkinson’s disease. Brain 131, 1969–1978 (2008).10.1093/brain/awm318 ↗
7. Levine, B., Mizushima, N. & Virgin, H. W. Autophagy in immunity and inflammation. Nature 469, 323–335 (2011).10.1038/nature09782 ↗
8. Zabirnyk, O., Yezhelyev, M. & Seleverstov, O. Nanoparticles as a novel class of autophagy activators. Autophagy 3, 278–281 (2007).10.4161/auto.3916 ↗
9. Stern, S. T. et al. Induction of autophagy in porcine kidney cells by quantum dots: a common cellular response to nanomaterials? Toxicol. Sci. 106, 140–152 (2008).10.1093/toxsci/kfn137 ↗
10. Man, N., Yu, L., Yu, S. H. & Wen, L. P. Rare earth oxide nanocrystals as a new class of autophagy inducers. Autophagy 6, 310–311 (2010).10.4161/auto.6.2.11138 ↗
11. Seleverstov, O. et al. Quantum dots for human mesenchymal stem cells labeling. A size-dependent autophagy activation. Nano Lett. 6, 2826–2832 (2006).10.1021/nl0619711 ↗
12. Zhang, Q. et al. Autophagy-mediated chemosensitization in cancer cells by fullerene 60C nanocrystal. Autophagy 5, 1107–1117 (2009).10.4161/auto.5.8.9842 ↗
13. Wei, P. F., Zhang, L., Lu, Y., Man, N. & Wen, L. P. 60C (Nd) nanoparticles enhance chemotherapeutic susceptibility of cancer cells by modulation of autophagy. Nanotechnology 21, 5101–5111 (2010).
14. Liu, H. L. et al. A functionalized single-walled carbon nanotube-induced autophagic cell death in human lung cells through Akt-TSC2-mTOR signaling. Cell Death Dis. 2, 159–165 (2011).10.1038/cddis.2011.27 ↗
15. Chen, Y., Yang, L., Feng, C. & Wen, L. P. Nano neodymium oxide induces massive vacuolization and autophagic cell death in non-small cell lung cancer NCI-H460 cells. Biochem. Biophys. Res. Commun. 337, 52–60 (2005).10.1016/j.bbrc.2005.09.018 ↗
16. Yu, L., Lu, Y., Yu, S. H. & Wen, L. P. Rare earth oxide nanocrystals induce autophagy in HeLa cells. Small 5, 2784–2787 (2009).10.1002/smll.200901714 ↗
17. Zhang, Y., Yu, C., Huang, G., Wang, C. & Wen, L. P. Nano rare-earth oxides induced size-dependent vacuolization: An independent pathway from autophagy. Int. J. Nanomed. 5, 601–609 (2010).10.2147/IJN.S11513 ↗
18. Li, C. G. et al. PAMAM nanoparticles promote acute lung injury by inducing autophagic cell death through the Akt-TSC2-mTOR signaling pathway. J. Mol. Cell Biol. 1, 37–45 (2009).10.1093/jmcb/mjp002 ↗
19. Li, J. J., Hartono, D., Ong, C. N., Bay, B. H. & Yung, L. Y. Autophagy and oxidative stress associated with gold nanoparticles. Biomaterials 31, 5996–6003 (2010).10.1016/j.biomaterials.2010.04.014 ↗
20. Wu, Y. N. et al. The selective growth inhibition of oral cancer by iron core–gold shell nanoparticles through mitochondria-mediated autophagy. Biomaterials 32, 4565–4573 (2011).10.1016/j.biomaterials.2011.03.006 ↗
21. Ma, X. W. et al. Gold nanoparticles induce autophagosome accumulation through size-dependent nanoparticle uptake and lysosome impairment. ACS Nano 5, 8629–8639 (2011).10.1021/nn202155y ↗
22. Yu, J. X. & Li, T. H. Distinct biological effects of different nanoparticles commonly used in cosmetics and medicine coatings. Cell Biosci. 1, 19–27 (2011).10.1186/2045-3701-1-19 ↗
23. Stern, S. T. & Johnson, D. N. Role for nanomaterial–autophagy interaction in neurodegenerative disease. Autophagy 4, 1097–1100 (2008).10.4161/auto.7142 ↗
24. Li, H. Y., Li, Y. H., Jiao, J. & Hu, H. M. Alpha–alumina nanoparticles induce efficient autophagy-dependent cross-presentation and potent antitumour response. Nature Nanotech. 6, 645–650 (2011).10.1038/nnano.2011.153 ↗
25. Verma, A. & Stellacci, F. Effect of surface properties on nanoparticle–cell interactions. Small 6, 12–21 (2010).10.1002/smll.200901158 ↗
26. Nel, A. E. et al. Understanding biophysicochemical interactions at the nano-bio interface. Nature Mater. 8, 543–557 (2009).10.1038/nmat2442 ↗
27. Dutta, D. et al. Adsorbed proteins influence the biological activity and molecular targeting of nanomaterials. Toxicol. Sci. 100, 303–315 (2007).10.1093/toxsci/kfm217 ↗
28. Bakota, E. L., Aulisa, L., Tsyboulski, D. A., Weisman, R. B. & Hartgerink, J. D. Multidomain peptides as single-walled carbon nanotube surfactants in cell culture. Biomacromolecules 10, 2201–2206 (2009).10.1021/bm900382a ↗
29. Whaley, S. R., English, D. S., Hu, E. L., Barbara, P. F. & Belcher, A. M. Selection of peptides with semiconductor binding specificity for directed nanocrystal assembly. Nature 405, 665–668 (2000).10.1038/35015043 ↗
30. Naik, R. R., Stringer, S. J., Agarwal, G., Jones, S. E. & Stone, M. O. Biomimetic synthesis and patterning of silver nanoparticles. Nature Mater. 1, 169–172 (2002).10.1038/nmat758 ↗
31. Wang, S. Q. et al. Peptides with selective affinity for carbon nanotubes. Nature Mater. 2, 196–200 (2003).10.1038/nmat833 ↗
32. Kriplani, U. & Kay, B. K. Selecting peptides for use in nanoscale materials using phage-displayed combinatorial peptide libraries. Curr. Opin. Biotechnol. 16, 470–475 (2005).10.1016/j.copbio.2005.07.001 ↗
33. Lee, S. W., Mao, C., Flynn, C. E. & Belcher, A. M. Ordering of quantum dots using genetically engineered viruses. Science 296, 892–895 (2002).10.1126/science.1068054 ↗
34. Chen, H. B., Su, X., Neoh, K. G. & Choe, W. S. Probing the interaction between peptides and metal oxides using point mutants of a TiO2-binding peptide. Langmuir 24, 6852–6857 (2008).10.1021/la800314p ↗
35. Goede, K., Busch, P. & Grundmann, M. Binding specificity of a peptide on semiconductor surfaces. Nano Lett. 4, 2115–2120 (2004).10.1021/nl048829p ↗
36. Cho, N. H. et al. A multifunctional core–shell nanoparticle for dendritic cell-based cancer immunotherapy. Nature Nanotech. 6, 675–682 (2011).10.1038/nnano.2011.149 ↗
37. Barth, S., Glick, D. & Macleod, K. F. Autophagy: Assays and artifacts. J. Pathol. 221, 117–24 (2010).10.1002/path.2694 ↗
38. Xiong, L., Yang, T., Yang, Y., Xu, C. & Li, F. Long-term in vivo biodistribution imaging and toxicity of polyacrylic acid-coated upconversion nanophosphors. Biomaterials 31, 7078–7085 (2010).10.1016/j.biomaterials.2010.05.065 ↗
39. Abdul, J. R. & Zhang, Y. Biocompatibility of silica coated NaYF4 upconversion fluorescent nanocrystals. Biomaterials 29, 4122–4128 (2008).10.1016/j.biomaterials.2008.07.012 ↗
40. Johnson-Lyles, D. N. et al. Fullerenol cytotoxicity in kidney cells is associated with cytoskeleton disruption, autophagic vacuole accumulation, and mitochondrial dysfunction. Toxicol. Appl. Pharmacol. 248, 249–58 (2010).10.1016/j.taap.2010.08.008 ↗
41. Monick, M. M. et al. Identification of an autophagy defect in smokers’ alveolar macrophages. J. Immunol. 185, 5425–35 (2010).10.4049/jimmunol.1001603 ↗
42. Cho, E. C., Zhang, Q. & Xia, Y. N. The effect of sedimentation and diffusion on cellular uptake of gold nanoparticles. Nature Nanotech. 6, 385–391 (2011).10.1038/nnano.2011.58 ↗
43. Chen, K. & Chen, X. Y. Integrin targeted delivery of chemotherapeutics. Theranostics 1, 189–200 (2011).10.7150/thno/v01p0189 ↗
44. Van Vlerken, L. E., Vyas, T. K. & Amiji, M. M. Poly(ethylene glycol)-modified nanocarriers for tumor-targeted and intracellular delivery. Pharmaceutical Res. 24, 1405–1414 (2007).10.1007/s11095-007-9284-6 ↗
45. Xie, J., Xu, C., Kohler, N., Hou, Y. & Sun, S. Controlled PEGylation of monodisperse Fe3O4 nanoparticles for reduced non-specific uptake by macrophage cells. Adv. Mater. 19, 3163–3166 (2007).10.1002/adma.200701975 ↗
46. Bretscher, M. S. Endocytosis and recycling of the fibronectin receptor in CHO cells. EMBO J. 8, 1341–1348 (1989).10.1002/j.1460-2075.1989.tb03514.x ↗
47. Zhang, Y. & Li, Z. Q. An efficient and user-friendly method for the synthesis of hexagonal-phase NaYF4:Yb, Er/Tm nanocrystals with controllable shape and upconversion fluorescence. Nanotechnology 19, 606–610 (2008).