Influence of the Surface Functional Group Density on the Carbon-Nanotube-Induced α-Chymotrypsin Structure and Activity Alterations

ACS Applied Materials and Interfaces

Volumn 7, Issue 33, 2015, Pages 18880-18890

  Zhao, Xingchen ^a   Hao, Fang ^a   Lu, Dawei ^a   Liu, Wei ^b   Zhou, Qunfang ^a   Jiang, Guibin ^a  

^a RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^b CHINESE ACADEMY OF INSPECTION AND QUARANTINE   (China)

Author keywords

carbon nanotubes; enzymatic activity; functionalization density; protein structure; chymotrypsin

Indexed keywords

ATOMIC FORCE MICROSCOPY; CIRCULAR DICHROISM SPECTROSCOPY; DICHROISM; FLUORESCENCE; IONIC STRENGTH; MULTIWALLED CARBON NANOTUBES (MWCN); PROTEINS; SURFACE TREATMENT; YARN;

ALPHA CHYMOTRYPSINS; BIOPHYSICAL ENVIRONMENTS; ENZYMATIC ACTIVITIES; FUNCTIONALIZATIONS; PROTEIN FLUORESCENCE; PROTEIN STRUCTURES; STRUCTURE AND ACTIVITIES; SURFACE FUNCTIONAL GROUPS;

CARBON NANOTUBES;

ALPHA-CHYMOTRYPSIN; CARBON NANOTUBE; CHYMOTRYPSIN;

ATOMIC FORCE MICROSCOPY; BIOCATALYSIS; CHEMISTRY; CIRCULAR DICHROISM; INFRARED SPECTROSCOPY; KINETICS; METABOLISM; OSMOLARITY; PH; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

BIOCATALYSIS; CHYMOTRYPSIN; CIRCULAR DICHROISM; HYDROGEN-ION CONCENTRATION; KINETICS; MICROSCOPY, ATOMIC FORCE; NANOTUBES, CARBON; OSMOLAR CONCENTRATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 84940417000     PISSN: 19448244     EISSN: 19448252     Source Type: Journal    
DOI: 10.1021/acsami.5b05895     Document Type: Article

References (45)

1. Ursini, C. L.; Cavallo, D.; Fresegna, A. M.; Ciervo, A.; Maiello, R.; Buresti, G.; Casciardi, S.; Tombolini, F.; Bellucci, S.; Iavicoli, S. Comparative Cyto-Genotoxicity Assessment of Functionalized and Pristine Multiwalled Carbon Nanotubes on Human Lung Epithelial Cells Toxicol. In Vitro 2012, 26 (6) 831-840 10.1016/j.tiv.2012.05.001
2. Bussy, C.; Pinault, M.; Cambedouzou, J.; Landry, M. J.; Jegou, P.; Mayne-L'hermite, M.; Launois, P.; Boczkowski, J.; Lanone, S. Critical Role of Surface Chemical Modifications Induced by Length Shortening on Multi-Walled Carbon Nanotubes-Induced Toxicity Part. Fibre Toxicol. 2012, 9, 46 10.1186/1743-8977-9-46
3. Wang, G.; Zhang, J. P.; Dewilde, A. H.; Pal, A. K.; Bello, D.; Therrien, J. M.; Braunhut, S. J.; Marx, K. A. Understanding and Correcting for Carbon Nanotube Interferences with a Commercial LDH Cytotoxicity Assay Toxicology 2012, 299 (2-3) 99-111 10.1016/j.tox.2012.05.012
4. Boczkowski, J.; Lanone, S. Respiratory Toxicities of Nanomaterials-A Focus on Carbon Nanotubes Adv. Drug Delivery Rev. 2012, 64 (15) 1694-1699 10.1016/j.addr.2012.05.011
5. Wang, X.; Xia, T. A.; Ntim, S. A.; Ji, Z. X.; George, S.; Meng, H. A.; Zhang, H. Y.; Castranova, V.; Mitra, S.; Nel, A. E. Quantitative Techniques for Assessing and Controlling the Dispersion and Biological Effects of Multiwalled Carbon Nanotubes in Mammalian Tissue Culture Cells ACS Nano 2010, 4 (12) 7241-7252 10.1021/nn102112b
6. Møller, P.; Christophersen, D. V.; Jensen, D. M.; Kermanizadeh, A.; Roursgaard, M.; Jacobsen, N. R.; Hemmingsen, J. G.; Danielsen, P. H.; Cao, Y.; Jantzen, K.; Klingberg, H.; Hersoug, L.-G.; Loft, S. Role of Oxidative Stress in Carbon Nanotube-Generated Health Effects Arch. Toxicol. 2014, 88 (11) 1939-1964 10.1007/s00204-014-1356-x
7. Xu, J. G.; Alexander, D. B.; Futakuchi, M.; Numano, T.; Fukamachi, K.; Suzui, M.; Omori, T.; Kanno, J.; Hirose, A.; Tsuda, H. Size- and Shape-Dependent Pleural Translocation, Deposition, Fibrogenesis, and Mesothelial Proliferation by Multiwalled Carbon Nanotubes Cancer Sci. 2014, 105 (7) 763-769 10.1111/cas.12437
8. Zhao, X.; Liu, R. Recent Progress and Perspectives on the Toxicity of Carbon Nanotubes at Organism, Organ, Cell, and Biomacromolecule Levels Environ. Int. 2012, 40, 244-255 10.1016/j.envint.2011.12.003
9. Song, M. Y.; Wang, F. B.; Zeng, L. Z.; Yin, J. F.; Wang, H. L.; Jiang, G. B. Co-exposure of Carboxyl-Functionalized Single-Walled Carbon Nanotubes and 17 alpha-Ethinylestradiol in Cultured Cells: Effects on Bioactivity and Cytotoxicity Environ. Sci. Technol. 2014, 48 (23) 13978-13984 10.1021/es504216a
10. Antonelli, A.; Serafini, S.; Menotta, M.; Sfara, C.; Pierige, F.; Giorgi, L.; Ambrosi, G.; Rossi, L.; Magnani, M. Improved Cellular Uptake of Functionalized Single-Walled Carbon Nanotubes Nanotechnology 2010, 21 (42) 425101 10.1088/0957-4484/21/42/425101
11. Luan, B.; Zhou, R. Nanopore-Based Sensors for Detecting Toxicity of a Carbon Nanotube to Proteins J. Phys. Chem. Lett. 2012, 3 (17) 2337-2341 10.1021/jz3007832
12. Ali-Boucetta, H.; Kostarelos, K. Carbon Nanotubes in Medicine & Biology-Therapy and Diagnostics Preface Adv. Drug Delivery Rev. 2013, 65 (15) 1897-1898 10.1016/j.addr.2013.11.002
13. Ali-Boucetta, H.; Kostarelos, K. Pharmacology of Carbon Nanotubes: Toxicokinetics, Excretion and Tissue Accumulation Adv. Drug Delivery Rev. 2013, 65 (15) 2111-2119 10.1016/j.addr.2013.10.004
14. Sacchetti, C.; Motamedchaboki, K.; Magrini, A.; Palmieri, G.; Mattei, M.; Bernardini, S.; Rosato, N.; Bottini, N.; Bottini, M. Surface Polyethylene Glycol Conformation Influences the Protein Corona of Polyethylene Glycol-Modified Single-Walled Carbon Nanotubes: Potential Implications on Biological Performance ACS Nano 2013, 7 (3) 1974-1989 10.1021/nn400409h
15. Skakalova, V.; Dettlaff-Weglikowska, U.; Roth, S. Gamma-Irradiated and Functionalized Single Wall Nanotubes Diamond Relat. Mater. 2004, 13 (2) 296-298 10.1016/j.diamond.2003.11.003
16. Zhao, X. C.; Liu, R. T.; Chi, Z. X.; Teng, Y.; Qin, P. F. New Insights into the Behavior of Bovine Serum Albumin Adsorbed onto Carbon Nanotubes: Comprehensive Spectroscopic Studies J. Phys. Chem. B 2010, 114 (16) 5625-5631 10.1021/jp100903x
17. Ohshima, H. Henry's Function for Electrophoresis of a Cylindrical Colloidal Particle J. Colloid Interface Sci. 1996, 180 (1) 299-301 10.1006/jcis.1996.0305
18. Gu, Q.; Kenny, J. E. Improvement of Inner Filter Effect Correction Based on Determination of Effective Geometric Parameters Using a Conventional Fluorimeter Anal. Chem. 2009, 81 (1) 420-426 10.1021/ac801676j
19. Cheng, X. X.; Lui, Y.; Zhou, B.; Xiao, X. H.; Liu, Y. Probing the Binding Sites and the Effect of Berbamine on the Structure of Bovine Serum Albumin Spectrochim. Acta, Part A 2009, 72 (5) 922-928 10.1016/j.saa.2008.12.003
20. Hu, Y. J.; Liu, Y.; Xiao, X. H. Investigation of the Interaction between Berberine and Human Serum Albumin Biomacromolecules 2009, 10 (3) 517-521 10.1021/bm801120k
21. Greenfield, N. J. Using Circular Dichroism Spectra to Estimate Protein Secondary Structure Nat. Protoc. 2007, 1 (6) 2876-2890 10.1038/nprot.2006.202
22. Rubinow, S. I.; Lebowitz, J. L. Time-Dependent Michaelis-Menten Kinetics for an Enzyme-Substrate-Inhibitor System J. Am. Chem. Soc. 1970, 92 (13) 3888-3893 10.1021/ja00716a009
23. Cornish-Bowden, A.; Eisenthal, R. Statistical Considerations in Estimation of Enzyme Kinetic-Parameters by Direct Linear Plot and Other Methods Biochem. J. 1974, 139 (3) 721-730 10.1042/bj1390721
24. Guo, J. X.; Li, Y. G.; Wu, S. W.; Li, W. X. The Effects of Gamma-Irradiation Dose on Chemical Modification of Multi-Walled Carbon Nanotubes Nanotechnology 2005, 16 (10) 2385-2388 10.1088/0957-4484/16/10/065
25. Karajanagi, S. S.; Vertegel, A. A.; Kane, R. S.; Dordick, J. S. Structure and Function of Enzymes Adsorbed onto Single-Walled Carbon Nanotubes Langmuir 2004, 20 (26) 11594-11599 10.1021/la047994h
26. Ge, C.; Du, J.; Zhao, L.; Wang, L.; Liu, Y.; Li, D.; Yang, Y.; Zhou, R.; Zhao, Y.; Chai, Z.; Chen, C. Binding of Blood Proteins to Carbon Nanotubes Reduces Cytotoxicity Proc. Natl. Acad. Sci. U. S. A. 2011, 108 (41) 16968-16973 10.1073/pnas.1105270108
27. Yonamine, Y.; Yoshimatsu, K.; Lee, S.-H.; Hoshino, Y.; Okahata, Y.; Shea, K. J. Polymer Nanoparticle-Protein Interface. Evaluation of the Contribution of Positively Charged Functional Groups to Protein Affinity ACS Appl. Mater. Interfaces 2013, 5 (2) 374-379 10.1021/am302404q
28. Ball, E. G. The Composition of Pancreatic Juice and Blood Serum as Influenced by the Injection of Acid and Base J. Biol. Chem. 1930, 86 (2) 0433-0448
29. Sun, X.; Feng, Z.; Hou, T.; Li, Y. Mechanism of Graphene Oxide as an Enzyme Inhibitor from Molecular Dynamics Simulations ACS Appl. Mater. Interfaces 2014, 6 (10) 7153-7163 10.1021/am500167c
30. Subramanyam, R.; Gollapudi, A.; Bonigala, P.; Chinnaboina, M.; Amooru, D. G. Betulinic Acid Binding to Human Serum Albumin: A Study of Protein Conformation and Binding Affinity J. Photochem. Photobiol., B 2009, 94 (1) 8-12 10.1016/j.jphotobiol.2008.09.002
31. Zhao, X.; Lu, D.; Hao, F.; Liu, R. Exploring the Diameter and Surface Dependent Conformational Changes in Carbon Nanotube-Protein Corona and the Related Cytotoxicity J. Hazard. Mater. 2015, 292 (0) 98-107 10.1016/j.jhazmat.2015.03.023
32. Li, S.; Aphale, A. N.; Macwan, I. G.; Patra, P. K.; Gonzalez, W. G.; Miksovska, J.; Leblanc, R. M. Graphene Oxide as a Quencher for Fluorescent Assay of Amino Acids, Peptides, and Proteins ACS Appl. Mater. Interfaces 2012, 4 (12) 7069-7075 10.1021/am302704a
33. Bourassa, P.; Kanakis, C. D.; Tarantilis, P.; Pollissiou, M. G.; Tajmir-Riahi, H. A. Resveratrol, Genistein, and Curcumin Bind Bovine Serum Albumin J. Phys. Chem. B 2010, 114 (9) 3348-3354 10.1021/jp9115996
34. Liu, Y.; Ji, F.; Liu, R. The Interaction of Bovine Serum Albumin with Doxorubicin-Loaded Superparamagnetic Iron Oxide Nanoparticles: Spectroscope and Molecular Modelling Identification Nanotoxicology 2013, 7 (1) 97-104 10.3109/17435390.2011.634079
35. Nepal, D.; Geckeler, K. E. Proteins and Carbon Nanotubes: Close Encounter in Water Small 2007, 3 (7) 1259-1265 10.1002/smll.200600511
36. Mu, Q. X.; Liu, W.; Xing, Y. H.; Zhou, H. Y.; Li, Z. W.; Zhang, Y.; Ji, L. H.; Wang, F.; Si, Z. K.; Zhang, B.; Yan, B. Protein Binding by Functionalized Multiwalled Carbon Nanotubes is Governed by the Surface Chemistry of Both Parties and the Nanotube Diameter J. Phys. Chem. C 2008, 112 (9) 3300-3307 10.1021/jp710541j
37. Zhong, J.; Song, L.; Meng, J.; Gao, B.; Chu, W. S.; Xu, H. Y.; Luo, Y.; Guo, J. H.; Marcelli, A.; Xie, S. S.; Wu, Z. Y. Bio-Nano Interaction of Proteins Adsorbed on Single-Walled Carbon Nanotubes Carbon 2009, 47 (4) 967-973 10.1016/j.carbon.2008.11.051
38. Charbonneau, D.; Beauregard, M.; Tajmir-Riahi, H. A. Structural Analysis of Human Serum Albumin Complexes with Cationic Lipids J. Phys. Chem. B 2009, 113 (6) 1777-1784 10.1021/jp8092012
39. Zhao, X.; Liu, R.; Teng, Y.; Liu, X. The Interaction between Ag+ and Bovine Serum Albumin: A Spectroscopic Investigation Sci. Total Environ. 2011, 409 (5) 892-897 10.1016/j.scitotenv.2010.11.004
40. Zhao, X.; Sheng, F.; Zheng, J.; Liu, R. Composition and Stability of Anthocyanins from Purple Solanum tuberosum and Their Protective Influence on Cr(VI) Targeted to Bovine Serum Albumin J. Agric. Food Chem. 2011, 59 (14) 7902-7909 10.1021/jf2011408
41. De Diego, T.; Lozano, P.; Gmouh, S.; Vaultier, M.; Iborra, J. L. Fluorescence and CD Spectroscopic Analysis of the alpha-Chymotrypsin Stabilization by the Ionic Liquid, 1-Ethyl-3-Methylimidazolium Bis [(Trifluoromethyl) Sulfonyl] Amide Biotechnol. Bioeng. 2004, 88 (7) 916-924 10.1002/bit.20330
42. Sandanaraj, B. S.; Vutukuri, D. R.; Simard, J. M.; Klaikherd, A.; Hong, R.; Rotello, V. M.; Thayumanavan, S. Noncovalent Modification of Chymotrypsin Surface Using an Amphiphilic Polymer Scaffold: Implications in Modulating Protein Function J. Am. Chem. Soc. 2005, 127 (30) 10693-10698 10.1021/ja051947+
43. De, M.; Chou, S. S.; Dravid, V. P. Graphene Oxide as an Enzyme Inhibitor: Modulation of Activity of α-Chymotrypsin J. Am. Chem. Soc. 2011, 133 (44) 17524-17527 10.1021/ja208427j
44. Roy, R.; Sandanaraj, B. S.; Klaikherd, A.; Thayumanavan, S. Tuning Substrate Selectivity of a Cationic Enzyme Using Cationic Polymers Langmuir 2006, 22 (18) 7695-7700 10.1021/la060496j
45. Zhang, B.; Xing, Y.; Li, Z.; Zhou, H.; Mu, Q.; Yan, B. Functionalized Carbon Nanotubes Specifically Bind to alpha-Chymotrypsin's Catalytic Site and Regulate Its Enzymatic Function Nano Lett. 2009, 9 (6) 2280-2284 10.1021/nl900437n