Polymer nanoreactors with dual functionality: Simultaneous detoxification of peroxynitrite and oxygen transport

Langmuir

Volumn 28, Issue 45, 2012, Pages 15889-15899

  Dobrunz, Dominik ^a   Toma, Adriana C ^a   Tanner, Pascal ^a   Pfohl, Thomas ^a   Palivan, Cornelia G ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHANNEL PROTEINS; CONFINED SPACE; CONFORMATIONAL CHANGE; DUAL FUNCTION; ENVIRONMENTAL SCIENCE; MODEL PROTEINS; MULTIFUNCTIONAL SYSTEMS; OXIDATION STATE; OXYGEN TRANSPORT; PEROXYNITRITES; POLYMER MEMBRANE; PROTEIN STRUCTURES;

DETOXIFICATION; FUNCTIONAL POLYMERS; MEDICAL APPLICATIONS; OXYGEN; PROTEINS;

NANOREACTORS;

HEMOGLOBIN; NANOPARTICLE; OXAZOLE DERIVATIVE; OXYGEN; PEROXYNITROUS ACID; POLY(2 METHYL OXAZOLINE) BLOCK POLYDIMETHYLSILOXANE BLOCK POLY(2 METHYL OXAZOLINE); POLY(2-METHYL OXAZOLINE)-BLOCK POLYDIMETHYLSILOXANE-BLOCK-POLY(2-METHYL OXAZOLINE); POLYMER;

ARTICLE; CHEMISTRY; METABOLISM; PARTICLE SIZE; SURFACE PROPERTY;

HEMOGLOBINS; NANOPARTICLES; OXAZOLES; OXYGEN; PARTICLE SIZE; PEROXYNITROUS ACID; POLYMERS; SURFACE PROPERTIES;

EID: 84869005056     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la302724m     Document Type: Article

References (74)

1. Dandan, C.; Tingfei, X.; Jing, B. Biological effects induced by nanosilver particles: in vivo study Biomed. Mater. 2007, 2 (3) S126
2. Slemmer, J. E.; Shacka, J. J.; Sweeney, M. I.; Weber, J. T. Antioxidants and Free Radical Scavengers for the Treatment Of Stroke, Traumatic Brain Injury and Aging Curr. Med. Chem. 2008, 15 (4) 404-414
3. Droege, W. Oxidative Stress. Disease and Cancer; Singh, K. K., Ed.; Imperial College Press: London, 2006; p 885.
4. Torreilles, F.; Salman-Tabcheh, S. d.; Guérin, M.-C.; Torreilles, J. Neurodegenerative disorders: the role of peroxynitrite Brain Res. Rev. 1999, 30 (2) 153-163
5. Li, J.; Su, J.; Li, W.; Liu, W.; Altura, B. T.; Altura, B. M. Peroxynitrite induces apoptosis in canine cerebral vascular muscle cells: possible relation to neurodegenerative diseases and strokes Neurosci. Lett. 2003, 350 (3) 173-177
6. Bouloumié, A.; Bauersachs, J.; Linz, W.; Schölkens, B. A.; Wiemer, G.; Fleming, I.; Busse, R. Endothelial Dysfunction Coincides With an Enhanced Nitric Oxide Synthase Expression and Superoxide Anion Production Hypertension 1997, 30 (4) 934-941
7. Pacher, P.; Beckman, J. S.; Liaudet, L. Nitric Oxide and Peroxynitrite in Health and Disease Physiol. Rev. 2007, 87 (1) 315-424
8. Radi, R.; Peluffo, G.; Alvarez, M. a. N.; Naviliat, M.; Cayota, A. Unraveling peroxynitrite formation in biological systems Free Radical Biol. Med. 2001, 30 (5) 463-488
9. Nauser, T.; Koppenol, W. H. The Rate Constant of the Reaction of Superoxide with Nitrogen Monoxide: Approaching the Diffusion Limit J. Phys. Chem. A 2002, 106 (16) 4084-4086
10. Mésenge, C.; Charriaut-Marlangue, C.; Verrecchia, C.; Allix, M.; Boulu, R. R.; Plotkine, M. Reduction of tyrosine nitration after Nω-nitro-l-arginine-methylester treatment of mice with traumatic brain injury Eur. J. Pharmacol. 1998, 353 (1) 53-57
11. Mihm, M. J.; Bauer, J. A. Peroxynitrite-induced inhibition and nitration of cardiac myofibrillar creatine kinase Biochimie 2002, 84 (10) 1013-1019
12. Stachowiak, O.; Dolder, M.; Wallimann, T.; Richter, C. Mitochondrial Creatine Kinase Is a Prime Target of Peroxynitrite-induced Modification and Inactivation J. Biol. Chem. 1998, 273 (27) 16694-16699
13. Szabo, C.; Ischiropoulos, H.; Radi, R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics Nat. Rev. Drug Discovery 2007, 6 (8) 662-680
14. Dairou, J.; Atmane, N.; Rodrigues-Lima, F.; Dupret, J.-M. Peroxynitrite Irreversibly Inactivates the Human Xenobioticmetabolizing Enzyme Arylamine N-Acetyltransferase 1 (NAT1) in Human Breast Cancer Cells J. Biol. Chem. 2004, 279 (9) 7708-7714
15. Arteel, G. E.; Briviba, K.; Sies, H. Protection against peroxynitrite FEBS Lett. 1999, 445 (2) 226-230
16. Rhee, S. G.; Chae, H. Z.; Kim, K. Peroxiredoxins: A historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling Free Radical Biol. Med. 2005, 38 (12) 1543-1552
17. Wood, Z. A.; Schröder, E.; Robin Harris, J.; Poole, L. B. Structure, mechanism and regulation of peroxiredoxins Trends Biochem. Sci. 2003, 28 (1) 32-40
18. Romero, N.; Radi, R.; Linares, E.; Augusto, O.; Detweiler, C. D.; Mason, R. P.; Denicola, A. Reaction of Human Hemoglobin with Peroxynitrite J. Biol. Chem. 2003, 278 (45) 44049-44057
19. Cohn, S. M. The Current Status of Haemoglobin-based Blood Substitutes Ann. Med. 1997, 29 (5) 371-376
20. Schreiber, G. B.; Busch, M. P.; Kleinman, S. H.; Korelitz, J. J. The Risk of Transfusion-Transmitted Viral Infections N. Engl. J. Med. 1996, 334 (26) 1685-1690
21. Sanders, K. E.; Lo, J.; Sligar, S. G. Intersubunit circular permutation of human hemoglobin Blood 2002, 100 (1) 299-305
22. Chang, T. M. S.; Powanda, D.; Yu, W. P. Analysis of Polyethylene-glycol- polylactide Nano-Dimension Artificial Red Blood Cells in Maintaining Systemic Hemoglobin Levels and Prevention of Methemoglobin Formation Artif. Cells, Blood Substitutes, Biotechnol. 2003, 31 (3) 231-247
23. Balasubramanian, V.; Onaca, O.; Enea, R.; Hughes, D. W.; Palivan, C. G. Protein delivery: from conventional drug delivery carriers to polymeric nanoreactors Exp. Opin. Drug Delivery 2010, 7 (1) 63-78
24. Li, S.; Nickels, J.; Palmer, A. F. Liposome-encapsulated actin-hemoglobin (LEAcHb) artificial blood substitutes Biomaterials 2005, 26 (17) 3759-3769
25. Arifin, D. R.; Palmer, A. F. Polymersome Encapsulated Hemoglobin: A Novel Type of Oxygen Carrier Biomacromolecules 2005, 6 (4) 2172-2181
26. Arifin, D. R.; Palmer, A. F. Stability of Liposome Encapsulated Hemoglobin Dispersions Artif. Cells, Blood Substitutes, Biotechnol. 2005, 33 (2) 113-136
27. Yechezkel, B. Liposome application: problems and prospects Curr. Opin. Colloid Interface Sci. 2001, 6 (1) 66-77
28. Sakai, H.; Tomiyama, K.-i.; Sou, K.; Takeoka, S.; Tsuchida, E. Poly(ethylene glycol)-Conjugation and Deoxygenation Enable Long-Term Preservation of Hemoglobin-Vesicles as Oxygen Carriers in a Liquid State Bioconjugate Chem. 2000, 11 (3) 425-432
29. Phillips, W. T.; Klipper, R. W.; Awasthi, V. D.; Rudolph, A. S.; Cliff, R.; Kwasiborski, V.; Goins, B. A. Polyethylene Glycol-Modified Liposome-Encapsulated Hemoglobin: A Long Circulating Red Cell Substitute J. Pharmacol. Exp. Ther. 1999, 288 (2) 665-670
30. Centis, V.; Proulx, P.; Vermette, P. PEGylated liposomes encapsulating human hemoglobin enhance oxygen transfer and cell proliferation while decreasing cell hypoxia in fibrin Biochem. Eng. J. 2011, 55 (3) 162-168
31. Rameez, S.; Guzman, N.; Banerjee, U.; Fontes, J.; Paulaitis, M. E.; Palmer, A. F.; Patel, R. P.; Honavar, J. Encapsulation of hemoglobin inside liposomes surface conjugated with poly(ethylene glycol) attenuates their reactions with gaseous ligands and regulates nitric oxide dependent vasodilation Biotechnol. Prog. 2012, 28 (3) 636-645
32. Bermudez, H.; Brannan, A. K.; Hammer, D. A.; Bates, F. S.; Discher, D. E. Molecular Weight Dependence of Polymersome Membrane Structure, Elasticity, and Stability Macromolecules 2002, 35 (21) 8203-8208
33. Rameez, S.; Alosta, H.; Palmer, A. F. Biocompatible and Biodegradable Polymersome Encapsulated Hemoglobin: A Potential Oxygen Carrier Bioconjugate Chem. 2008, 19 (5) 1025-1032
34. Zhao, J.; Liu, C.-S.; Yuan, Y.; Tao, X.-Y.; Shan, X.-Q.; Sheng, Y.; Wu, F. Preparation of hemoglobin-loaded nano-sized particles with porous structure as oxygen carriers Biomaterials 2007, 28 (7) 1414-1422
35. Hunt, J. A.; Lee, J.; Groves, J. T. Amphiphilic peroxynitrite decomposition catalysts in liposomal assemblies Chem. Biol. 1997, 4 (11) 845-858
36. Tanner, P.; Egli, S.; Balasubramanian, V.; Onaca, O.; Palivan, C. G.; Meier, W. Can polymeric vesicles that confine enzymatic reactions act as simplified organelles? FEBS Lett. 2011, 585 (11) 1699-1706
37. van Dongen, S. F. M.; Nallani, M.; Cornelissen, J. J. L. M.; Nolte, R. J. M.; van Hest, J. C. M. A Three-Enzyme Cascade Reaction through Positional Assembly of Enzymes in a Polymersome Nanoreactor Chem.-Eur. J. 2009, 15 (5) 1107-1114
38. Axthelm, F.; Casse, O.; Koppenol, W. H.; Nauser, T.; Meier, W.; Palivan, C. G. Antioxidant Nanoreactor Based on Superoxide Dismutase Encapsulated in Superoxide-Permeable Vesicles J. Phys. Chem. B 2008, 112 (28) 8211-8217
39. Kumar, M.; Grzelakowski, M.; Zilles, J.; Clark, M.; Meier, W. Highly permeable polymeric membranes based on the incorporation of the functional water channel protein Aquaporin Z Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (52) 20719-20724
40. Brož, P.; Benito, S. M.; Saw, C.; Burger, P.; Heider, H.; Pfisterer, M.; Marsch, S.; Meier, W.; Hunziker, P. Cell targeting by a generic receptor-targeted polymer nanocontainer platform J. Controlled Release 2005, 102 (2) 475-488
41. Graff, A.; Fraysse-Ailhas, C.; Palivan, C. G.; Grzelakowski, M.; Friedrich, T.; Vebert, C.; Gescheidt, G.; Meier, W. Amphiphilic Copolymer Membranes Promote NADH:Ubiquinone Oxidoreductase Activity: Towards an Electron-Transfer Nanodevice Macromol. Chem. Phys. 2010, 211 (2) 229-238
42. Nardin, C.; Thoeni, S.; Widmer, J.; Winterhalter, M.; Meier, W. Nanoreactors based on (polymerized) ABA-triblock copolymer vesicles Chem. Commun. 2000, 15, 1433-1434
43. Graff, A.; Sauer, M.; Van Gelder, P.; Meier, W. Virus-assisted loading of polymer nanocontainer Proc. Natl. Acad. Sci. 2002, 99 (8) 5064-5068
44. Prilipov, A.; S. P., P.; Gelder, P. Van; Rosenbusch, J. P.; Koebnik, R. FEMS Microbiol. Lett. 1998, 163, 65-72
45. Grzelakowski, M.; Onaca, O.; Rigler, P.; Kumar, M.; Meier, W. Immobilized Protein-Polymer Nanoreactors Small 2009, 5 (22) 2545-2548
46. Uppu, R. M.; Pryor, W. A. Synthesis of Peroxynitrite in a Two-Phase System Using Isoamyl Nitrite and Hydrogen Peroxide Anal. Biochem. 1996, 236 (2) 242-249
47. Sun, J.; Huang, Y.; Shi, Q.; Chen, X.; Jing, X. Oxygen Carrier Based on Hemoglobin/Poly(l -lysine)- block -poly(l -phenylalanine) Vesicles Langmuir 2009, 25 (24) 13726-13729
48. Dhont, J. K. G. An introduction to Dynamics of Colloids. Elsevier: Amsterdam, 1996; pp 147-149.
49. Onaca, O.; Hughes, D. W.; Balasubramanian, V.; Grzelakowski, M.; Meier, W.; Palivan, C. G. SOD Antioxidant Nanoreactors: Influence of Block Copolymer Composition on the Nanoreactor Efficiency Macromol. Biosci. 2010, 10 (5) 531-538
50. Nardin, C.; Hirt, T.; Leukel, J.; Meier, W. Polymerized ABA Triblock Copolymer Vesicles Langmuir 1999, 16 (3) 1035-1041
51. Rigler, P.; Meier, W. Encapsulation of Fluorescent Molecules by Functionalized Polymeric Nanocontainers: Investigation by Confocal Fluorescence Imaging and Fluorescence Correlation Spectroscopy J. Am. Chem. Soc. 2005, 128 (1) 367-373
52. Wohland, T.; Rigler, R.; Vogel, H. The Standard Deviation in Fluorescence Correlation Spectroscopy Biophys. J. 2001, 80 (6) 2987-2999
53. Arosio, D.; Kwansa, H. E.; Gering, H.; Piszczek, G.; Bucci, E. Static and dynamic light scattering approach to the hydration of hemoglobin and its supertetramers in the presence of osmolites Biopolymers 2002, 63 (1) 1-11
54. Tsuruga, M.; Matsuoka, A.; Hachimori, A.; Sugawara, Y.; Shikama, K. The Molecular Mechanism of Autoxidation for Human Oxyhemoglobin J. Biol. Chem. 1998, 273 (15) 8607-8615
55. Zhang, X.; Liu, C.; Yuan, Y.; Shan, X.; Sheng, Y.; Xu, F. Reduction and suppression of methemoglobin loaded in the polymeric nanoparticles intended for blood substitutes J. Biomed. Mater. Res., Part B 2008, 87B (2) 354-363
56. Exner, M.; Herold, S. Kinetic and Mechanistic Studies of the Peroxynitrite-Mediated Oxidation of Oxymyoglobin and Oxyhemoglobin Chem. Res. Toxicol. 2000, 13 (4) 287-293
57. Ascenzi, P.; Marinis, E. D.; Masi, A. d.; Ciaccio, C.; Coletta, M. Peroxynitrite scavenging by ferryl sperm whale myoglobin and human hemoglobin Biochem. Biophys. Res. Commun. 2009, 390 (1) 27-31
58. Torres Filho, I. P.; Terner, J.; Pittman, R. N.; Proffitt, E.; Ward, K. R. Measurement of hemoglobin oxygen saturation using Raman microspectroscopy and 532-nm excitation J. Appl. Physiol. 2008, 104 (6) 1809-1817
59. Gaoshan Shen Gaoshan, S.; Tiarrxiu Yan Tiarrxiu, Y.; Huaimin Gu Huaimin, G.; Huajian Wei Huajian, W. Micro-Raman Spectroscopy Monitor Methemoglobin Induced by Sodium Nitrite in Whole Blood COR Conf. Proc. 2008, 1476-1479
60. Spiro, T. G. Biological Applications of Resonance Raman Spectroscopy: Haem Proteins Proc. R. Soc. London, Ser. A 1975, 345 (1640) 89-105
61. Spiro, T. G.; Strekas, T. C. Resonance Raman Spectra of Hemoglobin and Cytochrome c: Inverse Polarization and Vibronic Scattering Proc. Natl. Acad. Sci. U.S.A. 1972, 69 (9) 2622-2626
62. Nagatomo, S.; Nagai, M.; Kitagawa, T. A New Way To Understand Quaternary Structure Changes of Hemoglobin upon Ligand Binding On the Basis of UV-Resonance Raman Evaluation of Intersubunit Interactions J. Am. Chem. Soc. 2011, 133 (26) 10101-10110
63. Yamamoto, T.; Palmer, G.; Gill, D.; Salmeen, I. T.; Rimai, L. The Valence and Spin State of Iron in Oxyhemoglobin as Inferred from Resonance Raman Spectroscopy J. Biol. Chem. 1973, 248 (14) 5211-5213
64. McCool, B. A.; Cashon, R.; Karles, G.; DeSisto, W. J. Silica encapsulated hemoglobin and myoglobin powders prepared by an aqueous fast-freezing technique J. Non-Cryst. Solids 2004, 333 (2) 143-149
65. Masayoshi Matsui, A. N.; Akiko, T.; Kenji, K.; Naoki, M. In Situ Observation of Reduction Behavior of Hemoglobin Molecules Adsorbed on Glass Surface IEICE Trans. 89-C 2006, 12, 1741-1745
66. Xu, H.; Bjerneld, E. J.; Käll, M.; Börjesson, L. Spectroscopy of Single Hemoglobin Molecules by Surface Enhanced Raman Scattering Phys. Rev. Lett. 1999, 83 (21) 4357-4360
67. Herold, S. Kinetic and spectroscopic characterization of an intermediate peroxynitrite complex in the nitrogen monoxide induced oxidation of oxyhemoglobin1 Reprinted in its entirety from vol. 439 (1998) 85-88 because of errors explained on p. 80.1 FEBS Lett. 1999, 443 (1) 81-84
68. Li, D.-J.; Luo, H.; Wang, L.-L.; Zou, G.-L. Potential of Peroxynitrite to Promote the Conversion of Oxyhemoglobin to Methemoglobin Acta Biochim. Biophys. Sin. 2004, 36 (2) 87-92
69. Romero, N.; Denicola, A.; Radi, R. Red blood cells in the metabolism of nitric oxide-derived peroxynitrite IUBMB Life 2006, 58 (10) 572-580
70. Chang, T. M. S. Blood replacement with nanobiotechnologically engineered hemoglobin and hemoglobin nanocapsules Wiley Interdiscip. Rev.: Nanomed. Nanobiotechnol. 2010, 2 (4) 418-430
71. Faivre, B, M. P.; Labrude, P; Vigneron, C., Hemoglobin autooxidation/oxidation mechanisms and methemoglobin prevention or reduction processes in the bloodstream. Literature review and outline of autooxidation reaction Artif. Cells, Blood Substitutes, Immobilization Biotechnol. 1998, 26, 17-26
72. Abe, K.; Sugita, Y. Properties of Cytochrome b5, and Methemoglobin Reduction in Human Erythrocytes Eur. J. Biochem. 1979, 101 (2) 423-428
73. Sakai, H.; Sato, A.; Masuda, K.; Takeoka, S.; Tsuchida, E. Encapsulation of Concentrated Hemoglobin Solution in Phospholipid Vesicles Retards the Reaction with NO, but Not CO, by Intracellular Diffusion Barrier J. Biol. Chem. 2008, 283 (3) 1508-1517
74. Tanner, P.; Onaca, O.; Balasubramanian, V.; Meier, W.; Palivan, C. G. Enzymatic Cascade Reactions inside Polymeric Nanocontainers: A Means to Combat Oxidative Stress Chem.-Eur. J. 2011, 17 (16) 4552-4560