Probing nanoscale self-assembly of nonfluorescent small molecules inside live mammalian cells

ACS Nano

Volumn 7, Issue 10, 2013, Pages 9055-9063

  Gao, Yuan ^a   Berciu, Cristina ^a   Kuang, Yi ^a   Shi, Junfeng ^a   Nicastro, Daniela ^a   Xu, Bing ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

enzyme; intracellular; localization; nanofibers; self assembly; small molecule

Indexed keywords

CELL FRACTIONATION; ENDOPLASMIC RETICULUM; FLUORESCENT IMAGING; INTRACELLULAR; LOCALIZATION; SECRETORY PATHWAYS; SMALL MOLECULES; SUBCELLULAR ORGANELLES;

CELL MEMBRANES; ELECTRON MICROSCOPES; ELECTRON MICROSCOPY; ENZYMES; FLUORESCENCE; NANOFIBERS; PROTEINS; SELF ASSEMBLY;

MOLECULES;

ARTICLE; HELA CELL LINE; HUMAN; MOLECULAR PROBE; NANOTECHNOLOGY; TRANSMISSION ELECTRON MICROSCOPY;

HELA CELLS; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR PROBES; NANOTECHNOLOGY;

EID: 84887003403     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn403664n     Document Type: Article

References (46)

1. Fletcher, D. A.; Mullins, D. Cell Mechanics and the Cytoskeleton Nature 2008, 463, 485-492
2. Spillantini, M. G.; Crowther, R. A.; Jakes, R.; Hasegawa, M.; Goedert, M. Alpha-Synuclein in Filamentous Inclusions of Lewy Bodies From Parkinson's Disease and Dementia with Lewy Bodies Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 6469-6473
3. Pollard, T. D.; Cooper, J. A. Actin, a Central Player in Cell Shape and Movement Science 2009, 326, 1208-1212
4. Perng, M. D.; Cairns, L.; van den Ijssel, P.; Prescott, A.; Hutcheson, A. M.; Quinlan, R. A. Intermediate Filament Interactions Can Be Altered by HSP27 and Alpha B-Crystallin J. Cell Sci. 1999, 112, 2099-2112
5. Rubinsztein, D. C. The Roles of Intracellular Protein-Degradation Pathways in Neurodegeneration Nature 2006, 443, 780-786
6. Yang, Z.; Liang, G.; Guo, Z.; Xu, B. Intracellular Hydrogelation of Small Molecules Inhibits Bacterial Growth Angew. Chem., Int. Ed. 2007, 46, 8216-8219
7. Yang, Z. M.; Xu, K. M.; Guo, Z. F.; Guo, Z. H.; Xu, B. Intracellular Enzymatic Formation of Nanofibers Results in Hydrogelation and Regulated Cell Death Adv. Mater. 2007, 19, 3152-3156
8. Estroff, L. A.; Hamilton, A. D. Water Gelation by Small Organic Molecules Chem. Rev. 2004, 104, 1201-1217
9. Terech, P.; Weiss, R. G. Low Molecular Mass Gelators of Organic Liquids and the Properties of Their Gels Chem. Rev. 1997, 97, 3133-3159
10. Ulijn, R. V.; Smith, A. M. Designing Peptide Based Nanomaterials Chem. Soc. Rev. 2008, 37, 664-675
11. Fischer, P. M.; Krausz, E.; Lane, D. P. Cellular Delivery of Impermeable Effector Molecules in the Form of Conjugates with Peptides Capable of Mediating Membrane Translocation Bioconjugate Chem. 2001, 12, 825-841
12. Zorn, J. A.; Wille, H.; Wolan, D. W.; Wells, J. A. Self-Assembling Small Molecules Form Nanofibers That Bind Procaspase-3 to Promote Activation J. Am. Chem. Soc. 2011, 133, 19630-19633
13. Kuang, Y.; Xu, B. Disruption of the Dynamics of Microtubules and Selective Inhibition of Glioblastoma Cells by Nanofibers of Small Hydrophobic Molecules Angew. Chem., Int. Ed. 2013, 52, 6944-6948
14. Kumar, R. K.; Yu, X. X.; Patil, A.; Li, M.; Mann, S. Cytoskeletal-like Supramolecular Assembly and Nanoparticle-Based Motors in a Model Protocell Angew. Chem., Int. Ed. 2011, 50, 9343-9347
15. Gao, Y.; Shi, J. F.; Yuan, D.; Xu, B. Imaging Enzyme-Triggered Self-Assembly of Small Molecules Inside Live Cells Nat. Commun. 2012, 3, 1033
16. Sameiro, M.; Goncalves, T. Fluorescent Labeling of Biomolecules with Organic Probes Chem. Rev. 2009, 109, 190-212
17. Zimmer, M. Green Fluorescent Protein (GFP): Applications, Structure, and Related Photophysical Behavior Chem. Rev. 2002, 102, 759-781
18. Medintz, I. L.; Uyeda, H. T.; Goldman, E. R.; Mattoussi, H. Quantum Dot Bioconjugates for Imaging, Labelling and Sensing Nat. Mater. 2005, 4, 435-446
19. Resch-Genger, U.; Grabolle, M.; Cavaliere-Jaricot, S.; Nitschke, R.; Nann, T. Quantum Dots versus Organic Dyes as Fluorescent Labels Nat. Methods 2008, 5, 763-775
20. Wang, K.; Rodgers, M. E.; Toptygin, D.; Munsen, V. A.; Brand, L. Fluorescence Study of the Multiple Binding Equilibria of the Galactose Repressor Biochemistry 1998, 37, 41-50
21. Taniguchi, Y.; Choi, P. J.; Li, G. W.; Chen, H. Y.; Babu, M.; Hearn, J.; Emili, A.; Xie, X. S. Quantifying E-coli Proteome and Transcriptome with Single-Molecule Sensitivity in Single Cells Science 2010, 329, 533-538
22. Freudiger, C. W.; Min, W.; Saar, B. G.; Lu, S.; Holtom, G. R.; He, C. W.; Tsai, J. C.; Kang, J. X.; Xie, X. S. Label-Free Biomedical Imaging with High Sensitivity by Stimulated Raman Scattering Microscopy Science 2008, 322, 1857-1861
23. Channon, K. J.; Devlin, G. L.; MacPhee, C. E. Efficient Energy Transfer within Self-Assembling Peptide Fibers: A Route to Light-Harvesting Nanomaterials J. Am. Chem. Soc. 2009, 131, 12520-12521
24. Chen, L.; Revel, S.; Morris, K.; Adams, D. J. Energy Transfer in Self-Assembled Dipeptide Hydrogels Chem. Commun. 2010, 46, 4267-4269
25. Yang, Z.; Liang, G.; Xu, B. Enzymatic Hydrogelation of Small Molecules Acc. Chem. Res. 2008, 41, 315-326
26. Li, J. Y.; Gao, Y.; Kuang, Y.; Shi, J. F.; Du, X. W.; Zhou, J.; Wang, H. M.; Yang, Z. M.; Xu, B. Dephosphorylation of D-Peptide Derivatives to Form Biofunctional, Supramolecular Nanofibers/Hydrogels and Their Potential Applications for Intracellular Imaging and Intratumoral Chemotherapy J. Am. Chem. Soc. 2013, 135, 9907-9914
27. Li, J. Y.; Kuang, Y.; Gao, Y.; Du, X. W.; Shi, J. F.; Xu, B. D-Amino Acids Boost the Selectivity and Confer Supramolecular Hydrogels of a Nonsteroidal Anti-Inflammatory Drug (NSAID) J. Am. Chem. Soc. 2013, 135, 542-545
28. Li, J. Y.; Kuang, Y.; Shi, J. F.; Gao, Y.; Zhou, J.; Xu, B. The Conjugation of Non-steroidal Anti-inflammatory Drugs (NSAID) to Small Peptides for Generating Multifunctional Supramolecular Nanofibers/Hydrogels Beilstein J. Org. Chem. 2013, 9, 908-917
29. Li, J. Y.; Li, X. M.; Kuang, Y.; Gao, Y.; Du, X. W.; Shi, J. F.; Xu, B. Self-delivery Multifunctional Anti-HIV Hydrogels for Sustained Release Adv. Healthc. Mater. 2013, DOI: 10.1002/adhm.201300041
30. Smith, C. Two Microscopes are Better Than One Nature 2012, 492, 293-297
31. Vembar, S. S.; Brodsky, J. L. One Step at a Time: Endoplasmic Reticulum-Associated Degradation Nat. Rev. Mol. Cell Biol. 2008, 9, 944-957
32. Zhang, Y.; Kuang, Y.; Gao, Y.; Xu, B. Versatile Small-Molecule Motifs for Self-Assembly in Water and the Formation of Biofunctional Supramolecular Hydrogels Langmuir 2010, 27, 529-537
33. Gao, Y.; Kuang, Y.; Guo, Z. F.; Guo, Z. H.; Krauss, I. J.; Xu, B. Enzyme-Instructed Molecular Self-Assembly Confers Nanofibers and a Supramolecular Hydrogel of Taxol Derivative J. Am. Chem. Soc. 2009, 131, 13576-13577
34. Alberts, B.; Johnson, A.; Lewis, J.; Raff, M.; Roberts, K.; Walter, P. Molecular Biology of the Cell, 4 th ed.; Garland Science: New York, 2002.
35. Mendez, A. J. Cholesterol Efflux Mediated by Apolipoproteins is an Active Cellular Process Distinct from Efflux Mediated by Passive Diffusion J. Lipid Res. 1997, 38, 1807-1821
36. Dopp, E.; von Recklinghausen, U.; Hartmann, L. M.; Stueckradt, I.; Pollok, I.; Rabieh, S.; Hao, L.; Nussler, A.; Katier, C.; Hirner, A. V. et al. Subcellular Distribution of Inorganic and Methylated Arsenic Compounds in Human Urothelial Cells and Human Hepatocytes Drug Metab. Dispos. 2008, 36, 971-979
37. Frado, L. L.; Craig, R. Electron-Microscopy of the Actin-Myosin Head Complex in the Presence of ATP J. Mol. Biol. 1992, 223, 391-397
38. Nowak, A. P.; Breedveld, V.; Pakstis, L.; Ozbas, B.; Pine, D. J.; Pochan, D.; Deming, T. J. Rapidly Recovering Hydrogel Scaffolds from Self-Assembling Diblock Copolypeptide Amphiphiles Nature 2002, 417, 424-428
39. Levine, B.; Kroemer, G. Autophagy in the Pathogenesis of Disease Cell 2008, 132, 27-42
40. Liang, G. L.; Ren, H. J.; Rao, J. H. A Biocompatible Condensation Reaction for Controlled Assembly of Nanostructures in Living Cells Nat. Chem. 2009, 2, 54-60
41. Huc, I.; Lehn, J. M. Virtual Combinatorial Libraries: Dynamic Generation of Molecular and Supramolecular Diversity by Self-Assembly Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 2106-2110
42. Lehn, J. M. Perspectives in Supramolecular Chemistry-from Molecular Recognition towards Molecular Information-Processing and Self-Organization Angew. Chem., Int. Ed. 1990, 29, 1304-1319
43. Whitesides, G. M.; Mathias, J. P.; Seto, C. T. Molecular Self-Assembly and Nanochemistry-A Chemical Strategy for the Synthesis of Nanostructures Science 1991, 254, 1312-1319
44. Balch, W. E.; Morimoto, R. I.; Dillin, A.; Kelly, J. W. Adapting proteostasis for disease intervention Science 2008, 319, 916-919
45. Lee, Y.; Ishii, T.; Kim, H. J.; Nishiyama, N.; Hayakawa, Y.; Itaka, K.; Kataoka, K. Efficient Delivery of Bioactive Antibodies into the Cytoplasm of Living Cells by Charge-Conversional Polyion Complex Micelles Angew. Chem., Int. Ed. 2010, 49, 2552-2555
46. Mastronarde, D. N. Automated Electron Microscope Tomography Using Robust Prediction of Specimen Movements J. Struct. Biol. 2005, 152, 36-51