A systematic High-Content Screening microscopy approach reveals key roles for Rab33b, OATL1 and Myo6 in nanoparticle trafficking in HeLa cells

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Panarella, Angela ^a,b   Bexiga, Mariana G ^a,c   Galea, George ^a   O'Neill, Elaine D ^a,d   Salvati, Anna ^a,e   Dawson, Kenneth A ^a   Simpson, Jeremy C ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

^b TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d Randox Laboratories Ltd   (United Kingdom)

^e UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY ENDOSOME ANTIGEN 1; LAMP1 PROTEIN, HUMAN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN; MYOSIN HEAVY CHAIN; MYOSIN VI; NANOPARTICLE; RAB PROTEIN; RAB33B PROTEIN, HUMAN; SMALL INTERFERING RNA; VESICULAR TRANSPORT PROTEIN;

CHEMISTRY; CYTOSKELETON; DRUG DELIVERY SYSTEM; HELA CELL LINE; HUMAN; HUMAN GENOME; LYSOSOME; METABOLISM; MICROSCOPY; NANOTECHNOLOGY; PROCEDURES; RNA INTERFERENCE; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CYTOSKELETON; DRUG DELIVERY SYSTEMS; GENOME, HUMAN; HELA CELLS; HUMANS; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MICROSCOPY; MYOSIN HEAVY CHAINS; NANOPARTICLES; NANOTECHNOLOGY; RAB GTP-BINDING PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; VESICULAR TRANSPORT PROTEINS;

EID: 84977555667     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep28865     Document Type: Article

References (46)

1. Ferrari M. Cancer nanotechnology: opportunities and challenges. Nature Reviews. Cancer 5, 161-171, doi: 10.1038/nrc1566 (2005
2. Dawidczyk C. M, et al. State-of-The-Art in design rules for drug delivery platforms: lessons learned from FDA-Approved nanomedicines. Journal of Controlled Release: Official Journal of the Controlled Release Society 187, 133-144, doi: 10.1016/j. jconrel.2014.05.036 (2014
3. Moghimi S. M, Hunter A. C, & Andresen T. L. Factors controlling nanoparticle pharmacokinetics: an integrated analysis and perspective. Annual Review of Pharmacology and Toxicology 52, 481-503, doi: 10.1146/annurev-pharmtox-010611-134623 (2012
4. Tarrago-Trani M. T, & Storrie B. Alternate routes for drug delivery to the cell interior: pathways to the Golgi apparatus and endoplasmic reticulum. Advanced Drug Delivery Reviews 59, 782-797, doi: 10.1016/j.addr.2007.06.006 (2007
5. Nel A. E, et al. Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater. 8, 543-557, doi: 10.1038/.nmat2442 (2009
6. Monopoli M. P, Aberg C, Salvati A, & Dawson K. A. Biomolecular coronas provide the biological identity of nanosized materials. Nature Nanotechnology 7, 779-786, doi: 10.1038/nnano.2012.207 (2012
7. dos Santos T, Varela J, Lynch I, Salvati A, & Dawson K. A. Effects of transport inhibitors on the cellular uptake of carboxylated polystyrene nanoparticles in different cell lines. PloS One 6, e24438, doi: 10.1371/journal.pone.0024438 (2011
8. Sahay G, Alakhova D. Y, & Kabanov A. V. Endocytosis of nanomedicines. Journal of Controlled Release: Official Journal of the Controlled Release Society 145, 182-195, doi: 10.1016/j.jconrel.2010.01.036 (2010
9. Vercauteren D, et al. The use of inhibitors to study endocytic pathways of gene carriers: optimization and pitfalls. Molecular Therapy: The Journal of the American Society of Gene Therapy 18, 561-569, doi: 10.1038/mt.2009.281 (2010
10. Collinet C, et al. Systems survey of endocytosis by multiparametric image analysis. Nature 464, 243-249, doi: 10.1038/nature08779 (2010
11. Simpson J. C, et al. Genome-wide RNAi screening identifies human proteins with a regulatory function in the early secretory pathway. Nature Cell Biology 14, 764-774, doi: 10.1038/ncb2510 (2012
12. Brayden D. J, Cryan S. A, Dawson K. A, O'Brien P. J, & Simpson J. C. High-content analysis for drug delivery and nanoparticle applications. Drug Discovery Today 20, 942-957, doi: 10.1016/j.drudis.2015.04.001 (2015
13. Kozik P, et al. A human genome-wide screen for regulators of clathrin-coated vesicle formation reveals an unexpected role for the V-ATPase. Nature Cell Biology 15 50-60, doi: 10.1038/ncb2652 (2013
14. Sahay G, et al. Efficiency of siRNA delivery by lipid nanoparticles is limited by endocytic recycling. Nature Biotechnology 31, 653-658, doi: 10.1038/nbt.2614 (2013
15. Gilleron J, et al. Image-based analysis of lipid nanoparticle-mediated siRNA delivery, intracellular trafficking and endosomal escape. Nature Biotechnology 31, 638-646, doi: 10.1038/nbt.2612 (2013
16. Kim J. A, Aberg C, Salvati A, & Dawson K. A. Role of cell cycle on the cellular uptake and dilution of nanoparticles in a cell population. Nature Nanotechnology 7, 62-68, doi: 10.1038/nnano.2011.191 (2012
17. Yacobi N. R, et al. Mechanisms of alveolar epithelial translocation of a defined population of nanoparticles. American Journal of Respiratory Cell and Molecular Biology 42, 604-614, doi: 10.1165/rcmb.2009-0138OC (2010
18. Anguissola S, Garry D, Salvati A, O'Brien P. J, & Dawson K. A. High content analysis provides mechanistic insights on the pathways of toxicity induced by amine-modified polystyrene nanoparticles. PloS One 9, e108025, doi: 10.1371/journal.pone.0108025 (2014
19. Monopoli M. P, et al. Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. Journal of the American Chemical Society 133, 2525-2534, doi: 10.1021/ja107583h (2011
20. Nance E. A, et al. A dense poly (ethylene glycol) coating improves penetration of large polymeric nanoparticles within brain tissue. Science Translational Medicine 4 149ra119, doi: 10.1126/scitranslmed.3003594 (2012
21. Salvati A, et al. Experimental and theoretical comparison of intracellular import of polymeric nanoparticles and small molecules: toward models of uptake kinetics. Nanomedicine: Nanotechnology, Biology, and Medicine 7, 818-826, doi: 10.1016/j.nano.2011.03.005 (2011
22. Wang F, et al. Time resolved study of cell death mechanisms induced by amine-modified polystyrene nanoparticles. Nanoscale 5, 10868-10876, doi: 10.1039/c3nr03249c (2013
23. Lesniak A, et al. Nanoparticle adhesion to the cell membrane and its effect on nanoparticle uptake efficiency. Journal of the American Chemical Society 135, 1438-1444, doi: 10.1021/ja309812z (2013
24. Rejman J, Bragonzi A, & Conese M. Role of clathrin- and caveolae-mediated endocytosis in gene transfer mediated by lipo- and polyplexes. Molecular Therapy: The Journal of the American Society of Gene Therapy 12, 468-474, doi: 10.1016/j.ymthe.2005.03.038 (2005
25. Chappie J. S, & Dyda F. Building a fission machine-structural insights into dynamin assembly and activation. Journal of Cell Science 126, 2773-2784, doi: 10.1242/jcs.108845 (2013
26. Gratton S. E, et al. The effect of particle design on cellular internalization pathways. Proceedings of the National Academy of Sciences of the United States of America 105, 11613-11618, doi: 10.1073/pnas.0801763105 (2008
27. Harush-Frenkel O, Debotton N, Benita S, & Altschuler Y. Targeting of nanoparticles to the clathrin-mediated endocytic pathway. Biochemical and Biophysical Research Communications 353, 26-32, doi: 10.1016/j.bbrc.2006.11.135 (2007
28. Piper R. C, Dikic I, & Lukacs G. L. Ubiquitin-dependent sorting in endocytosis. Cold Spring Harbor Perspectives in Biology 6, doi: 10.1101/cshperspect.a016808 (2014
29. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nature Reviews. Molecular Cell Biology 10, 513-525, doi: 10.1038/.nrm2728 (2009
30. Sandin P, Fitzpatrick L. W, Simpson J. C, & Dawson K. A. High-Speed Imaging of Rab Family Small GTPases Reveals Rare Events in Nanoparticle Trafficking in Living Cells. ACS Nano 6, 1513-1521 (2012
31. Singan V. R, Jones T. R, Curran K. M, & Simpson J. C. Dual channel rank-based intensity weighting for quantitative colocalization of microscopy images. BMC Bioinformatics 12, 407, doi: 10.1186/1471-2105-12-407 (2011
32. Starr T, Sun Y, Wilkins N, & Storrie B. Rab33b and Rab6 are functionally overlapping regulators of Golgi homeostasis and trafficking. Traffic 11, 626-636, doi: 10.1111/j.1600-0854.2010.01051.x (2010
33. Yang Z, & Klionsky D. J. Mammalian autophagy: core molecular machinery and signaling regulation. Current Opinion in Cell Biology 22, 124-131, doi: 10.1016/j.ceb.2009.11.014 (2010
34. Itoh T, et al. Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Molecular Biology of the Cell 19, 2916-2925, doi: 10.1091/mbc.E07-12-1231 (2008
35. Itoh T, Kanno E, Uemura T, Waguri S, & Fukuda M. OATL1, a novel autophagosome-resident Rab33B-GAP, regulates autophagosomal maturation. The Journal of Cell Biology 192, 839-853, doi: 10.1083/jcb.201008107 (2011
36. Bexiga M. G, et al. Cationic nanoparticles induce caspase 3-, 7- and 9-mediated cytotoxicity in a human astrocytoma cell line. Nanotoxicology 5, 557-567, doi: 10.3109/17435390.2010.539713 (2011
37. Hyttinen J. M, Niittykoski M, Salminen A, & Kaarniranta K. Maturation of autophagosomes and endosomes: a key role for Rab7. Biochimica et Biophysica Acta 1833, 503-510, doi: 10.1016/j.bbamcr.2012.11.018 (2013
38. Tumbarello D. A, Kendrick-Jones J, & Buss F. Myosin VI and its cargo adaptors - linking endocytosis and autophagy. Journal of Cell Science 126, 2561-2570, doi: 10.1242/jcs.095554 (2013
39. Zoncu R, et al. A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes. Cell 136 1110-1121, doi: 10.1016/j.cell.2009.01.032 (2009
40. Spudich G, et al. Myosin VI targeting to clathrin-coated structures and dimerization is mediated by binding to Disabled-2 and PtdIns (4, 5)P2. Nature Cell Biology 9, 176-183, doi: 10.1038/ncb1531 (2007
41. Tumbarello D. A, et al. Autophagy receptors link myosin VI to autophagosomes to mediate Tom1-dependent autophagosome maturation and fusion with the lysosome. Nature Cell Biology 14, 1024-1035, doi: 10.1038/ncb2589 (2012
42. Thurston T. L, Ryzhakov G, Bloor S, von Muhlinen N, & Randow F. The TBK1 adaptor and autophagy receptor NDP52 restricts the proliferation of ubiquitin-coated bacteria. Nature Immunology 10, 1215-1221, doi: 10.1038/ni.1800 (2009
43. Wild P, et al. Phosphorylation of the autophagy receptor optineurin restricts Salmonella growth. Science 333, 228-233, doi: 10.1126/.science.1205405 (2011
44. Galea G, & Simpson J. C. High-content screening and analysis of the Golgi complex. Methods in Cell Biology 118, 281-295, doi: 10.1016/B978-0-12-417164-0.00017-3 (2013
45. Dejgaard S. Y, et al. Rab18 and Rab43 have key roles in ER-Golgi trafficking. Journal of Cell Science 121, 2768-2781, doi: 10.1242/.jcs.021808 (2008
46. Singan V. R, & Simpson J. C. Implementation of the Rank-Weighted Co-localization (RWC) algorithm in multiple image analysis platforms for quantitative analysis of microscopy images. Source Code for Biology and Medicine 11, 2, doi: 10.1186/s13029-016-0048-8 (2016