Role of Red-Ox Cycle in Structural Oscillations and Solvation Dynamics in the Mitochondria of a Live Cell

Journal of Physical Chemistry B

Volumn 119, Issue 29, 2015, Pages 8842-8851

  Chattoraj, Shyamtanu ^a   Chowdhury, Rajdeep ^a   Dey, Sumit Kumar ^a   Jana, Siddhartha Sankar ^a   Bhattacharyya, Kankan ^a  

^a DEPARTMENT OF MATERIALS SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; DISEASES; DYNAMICS; FLUORESCENCE; PROBES; SOLVATION;

FLUORESCENCE INTENSITIES; FLUORESCENCE PROBES; HUMAN BREAST CANCER CELLS; MICROENVIRONMENTS; PERIODIC FLUCTUATIONS; SOLVATION DYNAMICS; STRUCTURAL OSCILLATIONS; TIME RESOLVED MICROSCOPY;

CELLS;

COUMARIN DERIVATIVE; N-(4-(7-DIETHYLAMINO-4-METHYLCOUMARIN-3-YL)PHENYL)MALEIMIDE; SOLVENT;

BREAST; BREAST TUMOR; CONFOCAL MICROSCOPY; DRUG EFFECTS; HUMAN; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PERIODICITY; SPECTROSCOPY; TUMOR CELL LINE;

BREAST; BREAST NEOPLASMS; CELL LINE, TUMOR; COUMARINS; HUMANS; MICROSCOPY, CONFOCAL; MITOCHONDRIA; OXIDATION-REDUCTION; PERIODICITY; SOLVENTS; SPECTRUM ANALYSIS;

EID: 84937900639     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp503808z     Document Type: Article

References (66)

1. Ingrosso, F.; Ladanyi, B. M. Intermolecular Structure and Collective Dynamics of Supercritical Fluoroform Studied by Molecular Dynamics Simulations J. Phys. Chem. B 2013, 117, 654-667
2. Pieniazek, P. A.; Lin, Y. S.; Chowdhury, J.; Ladanyi, B. M.; Skinner, J. L. Vibrational Spectroscopy and Dynamics of Water Confined inside Reverse Micelles J. Phys. Chem. B 2009, 113, 15017-15028
3. Milischuk, A. A.; Krewald, V.; Ladanyi, B. M. Water Dynamics in Silica Nanopores: The self-intermediate scattering functions J. Chem. Phys. 2012, 136, 224704-1-10
4. Bagchi, B.; Jana, B. Solvation Dynamics in Dipolar Liquids Chem. Soc. Rev. 2010, 39, 1936-1954
5. Jana, B.; Pal, S.; Bagchi, B. Hydrogen Bond Breaking Mechanism and Water Reorientational Dynamics in the Hydration Layer of Lysozyme J. Phys. Chem. B 2008, 112, 9112-9117
6. Zhang, Z.; Berkowitz, M. L. Orientational Dynamics of Water in Phospholipid Bilayers with Different Hydration Levels J. Phys. Chem. B 2009, 113, 7676-7680
7. Pal, S. K.; Peon, J.; Bagchi, B.; Zewail, A. H. Biological Water: Femtosecond Dynamics of Macromolecular Hydration J. Phys. Chem. B 2002, 106, 12376-12395
8. Bhattacharyya, K.; Bagchi, B. Slow Dynamics of Constrained Water in Complex Geometries J. Phys. Chem. A 2000, 104, 10603-10613
9. Bhattacharyya, K. Nature of Biological Water: A Femtosecond Study Chem. Commun. 2008, 2848-2857
10. Zhong, D.; Pal, S. K.; Zewail, A. H. Biological Water: A Critique Chem. Phys. Lett. 2011, 503, 1-11
11. Jha, A.; Ishii, K.; Udgaonkar, J. B.; Tahara, T.; Krishnamoorthy, G. Exploration of the Correlation between Solvation Dynamics and Internal Dynamics of a Protein Biochemistry 2011, 50, 397-408
12. Andreatta, D.; PérezLustres, J. L.; Kovalenko, S. A.; Ernsting, N. P.; Murphy, C. J.; Coleman, R. S.; Berg, M. A. Power-Law Solvation Dynamics in DNA over Six Decades in Time J. Am. Chem. Soc. 2005, 127, 7270-7271
13. Sen, S.; Andreatta, D.; Ponomarev, S. Y.; Beveridge, D. L.; Berg, M. A. Dynamics of Water and Ions Near DNA: Comparison of Simulation to Time-Resolved Stokes-Shift Experiments J. Am. Chem. Soc. 2009, 131, 1724-1735
14. Pal, N.; Verma, S. D.; Sen, S. Probe Position Dependence of DNA Dynamics: Comparison of the Time-Resolved Stokes Shift of Groove-Bound to Base-Stacked Probes J. Am. Chem. Soc. 2010, 132, 9277-9279
15. Zhang, L.; Kao, Y. T.; Qiu, W.; Wang, L.; Zhong, D. Femtosecond Studies of Tryptophan Fluorescence Dynamics in Proteins: Local Solvation and Electronic Quenching J. Phys. Chem. B 2006, 110, 18097-18103
16. Elf, J.; Li, G. W.; Xie, X. S. Probing Transcription Factor Dynamics at the Single-Molecule Level in a Living Cell Science 2007, 316, 1191-1200
17. Blainey, P. C.; van Oijen, A. M.; Banerjee, A.; Verdine, G. L.; Xie, S. X. A Base-excision DNA-repair Protein Finds Intrahelical Lesion Bases by Fast Sliding in Contact with DNA Proc. Natl. Acad. Sci. U.S.A. 2006, 133, 5752-5757
18. Bagchi, B.; Blainey, P. C.; Xie, X. S. Diffusion Constant of a Nonspecifically Bound Protein Undergoing Curvilinear Motion along DNA J. Phys. Chem. B 2008, 112, 6282-6284
19. He, Y.; Li, Y.; Mukherjee, S.; Wu, Y.; Yan, H.; Lu, H. P. Probing Single-Molecule Enzyme Active-Site Conformational State Intermittent Coherence J. Am. Chem. Soc. 2011, 133, 14389-14395
20. Chen, Y.; Hu, D.; Vorpagel, E. R.; Lu, H. P. Probing Single-Molecule T4 Lysozyme Conformational Dynamics by Intramolecular Fluorescence Energy Transfer J. Phys. Chem. B 2003, 107, 7947-7956
21. Hu, D.; Lu, H. P. Single Molecule Implanting of T4 Lysozyme on Bacterial Cell Surface: Towards Study Single Molecule Enzymatic Reaction in Living Cells Biophys. J. 2004, 87, 656-661
22. Harms, G. S.; Orr, G.; Montal, M.; Thrall, B. D.; Colson, S. D.; Lu, H. P. Probing Conformational Changes of Gramicidin Ion Channels by Single-Molecule Patch-Clamp Fluorescence Microscopy Biophys. J. 2003, 85, 1826-1838
23. Chattoraj, S.; Saha, S.; Jana, S. S.; Bhattacharyya, K. Dynamics of Gene Silencing in a Live Cell: Stochastic Resonance J. Phys. Chem. Lett. 2014, 5, 1012-1016
24. Cai, D.; Hoppe, A. D.; Swanson, J. A.; Verhey, K. J. Kinesin-1 Structural Organization and Conformational Changes Revealed by FRET Stoichiometry in Live Cells J. Cell Biol. 2007, 176, 51-63
25. Verbrugge, S.; Lechner, B.; Woehlke, G.; Peterman, E. J. Alternating-site Mechanism of Kinesin-1 Characterized by Single-molecule FRET using Fluorescent ATP Analogues Biophys. J. 2009, 97, 173-182
26. Verbrugge, S.; Lansky, Z.; Peterman, E. J. Kinesin's Step Dissected with Single-motor FRET Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 17741-17746
27. Maurer, S. P.; Fourniol, F. J.; Bohner, G.; Moores, C. A.; Surrey, T. EBs Recognize a Nucleotide-Dependent Structural Cap at Growing Microtubule Ends Cell 2012, 149, 371-382
28. Maurer, S. P.; Bieling, P.; Cope, J.; Hoenger, A.; Surrey, T. GTPγS Microtubules Mimic the Growing Microtubule End Structure Recognized by End-Binding Proteins (EBs) Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 3988-3993
29. Aon, M. A.; Roussel, M. R.; Cortassa, S.; Rourke, B. O.; Murray, D. B.; Beckmann, M.; Lloyd, D. The Scale-Free Dynamics of Eukaryotic Cells PLoS One 2008, 3, e3624-1-e3624-12
30. Longtin, A.; Bulsara, A.; Moss, F. Time-Interval Sequences in Bistable Systems and the Noise-Induced Transmission of Information by Sensory Neurons Phys. Rev. Lett. 1991, 67, 656-659
31. Domke, J.; Parak, W. J.; George, M.; Gaub, H. E.; Radmacher, M. Mapping the Mechanical Pulse of Single Cardiomyocytes with the Atomic Force Microscope Eur. Biophys. J. 1999, 28, 179-186
32. Maksym, G. N.; Fabry, B.; Butler, J. P.; Navajas, D.; Tschumperlin, D. J.; Laporte, J. D.; Fredberg, J. J. Mechanical Properties of Cultured Human Airway Smooth Muscle Cells from 0.05 to 0.4 Hz J. Appl. Physiol. 2000, 89, 1619-1632
33. Domnisoru, C.; Kinkhabwala, A. A.; Tank, D. W. Membrane Potential Dynamics of Grid Cells Nature 2013, 495, 199-204
34. Chapman, C. A.; Lacaille, J. C. Intrinsic Theta-Frequency Membrane Potential Oscillations in Hippocampal CA1 Interneurons of Stratum Lacunosum-Moleculare J. Neurophysiol. 1999, 81, 1296-1307
35. Atwater, I.; Dawson, C. M.; Scott, A.; Eddlestone, G.; Rojas, E. The Nature of the Oscillatory Behavior in Electrical Activity for Pancreatic β-Cell. In Biochemistry Biophysics of the Pancreatic-β-Cell; Georg Thieme Verlag: New York, 1980; pp 100-107.
36. Olsen, L. F.; Andersen, A. Z.; Lunding, A.; Brasen, J. C.; Poulsen, A. K. Regulation of Glycolytic Oscillations by Mitochondrial and Plasma Membrane H+-ATPases Biophys. J. 2009, 96, 3850-3861
37. Torres, A. G.; Gait, M. J. Exploiting Cell Surface Thiols to Enhance Cellular Uptake Trends Biotechnol. 2012, 30, 185-190
38. Ghosh, S.; Chattoraj, S.; Bhattacharyya, K. Solvation Dynamics and Intermittent Oscillation of Cell Membrane: Live Chinese Hamster Ovary Cell J. Phys. Chem. B 2014, 118, 2949-2956
39. Friedman, J. R.; Nunnari, J. Mitochondrial Form and Function Nature 2014, 505, 335-343
40. Aon, M. A.; Cortassa, S.; Maack, C.; Rourke, B. O. Sequential Opening of Mitochondrial Ion Channels as a Function of Glutathione Redox Thiol Status J. Biol. Chem. 2007, 282, 21889-21900
41. Sevier, C. S.; Kaiser, C. A. Formation and Transfer of Disulphide Bonds in Living Cells Nat. Rev. Molecular Cell Biol. 2002, 3, 836-847
42. Collins, Y.; Chouchani, E. T.; James, A. M.; Menger, K. E.; Cochemé, H. M.; Murphy, M. P. Mitochondrial Redox Signaling at a Glance J. Cell Sci. 2012, 125, 801-806
43. Aon, M. A.; Cortassa, S.; Rourke, B. O. The Fundamental Organization of Cardiac Mitochondria as a Network of Coupled Oscillators Biophys. J. 2006, 91, 4317-4327
44. Lin, T. K.; Hughes, G.; Muratovska, A.; Blaikie, F. H.; Brookes, P. S.; Usmar, V. D.; Smith, R. A. J.; Murphy, M. P. Specific Modification of Mitochondrial Protein Thiols in Response to Oxidative Stress J. Biol. Chem. 2002, 277, 17048-17056
45. James, A. M.; Collins, Y.; Logan, A.; Murphy, M. P. Mitochondrial Oxidative Stress and The metabolic syndrome Trends Endocrinol. Metab. 2012, 23, 429-434
46. Hurd, T. R.; Filipovska, A.; Costa, N. J.; Dahm, C. C.; Murphy, M. P. Disulphide Formation on Mitochondrial Protein Thiols Biochem. Soc. Trans. 2005, 33, 1390-1393
47. Wong, H. L.; Liebler, D. C. Mitochondrial Protein Targets of Thiol-Reactive Electrophiles Chem. Res. Toxicol. 2008, 21, 796-804
48. Aon, M. A.; Cortassa, S.; Rourke, B. O. Mitochondrial Oscillations in Physiology and Pathophysiology Adv. Exp. Med. Biol. 2008, 641, 98-117
49. Kurz, F. T.; Aon, M. A.; Rourke, B. O.; Armoundas, A. A. Spatio-temporal Oscillations of Individual Mitochondria in Cardiac Myocytes Reveal Modulation of Synchronized Mitochondrial Clusters Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 14315-14320
50. Griffiths, E. J.; Rutter, G. A.; Griffiths, E. J.; Rutter, G. A. Mitochondrial Calcium as a Key Regulator of Mitochondrial ATP Production in Mammalian Cells Biochim. Biophys. Acta 2009, 1787, 1324-1333
51. Cortassa, S.; Aon, M. A.; Winslow, R. L.; Rourke, B. O. A Mitochondrial Oscillator Dependent on Reactive Oxygen Species Biophys. J. 2004, 87, 2060-2073
52. Al-Mehdi, A. B.; Pastukh, V. M.; Swiger, B. M.; Reed, D. J.; Patel, M. R.; Bardwell, G. C.; Pastukh, V. V.; Alexeyev, M. F.; Gillespie, M. N. Peri-nuclear Mitochondrial Clustering Creates an Oxidant-Rich Nuclear Domain Required for Hypoxia-Induced Transcription Sci. Signal. 2012, 5, ra47
53. Hamacher-Brady, A.; Stein, H. A.; Turschner, S.; Toegel, I.; Mora, R.; Jennewein, N.; Efferth, T.; Eils, R.; Brady, N. R. Artesunate Activates Mitochondrial Apoptosis in Breast Cancer Cells via Iron-catalyzed Lysosomal Reactive Oxygen Species Production J. Biol. Chem. 2011, 286, 6587-6601
54. Esposti, M. D.; Hatzinisiriou, I.; McLennan, H.; Ralph, S. Bcl-2 and Mitochondrial Oxygen Radicals J. Biol. Chem. 1999, 274, 29831-29837
55. Vives-Bauza, C.; Zhou, C.; Huang, Y.; Cui, M.; de Vries, R. L. A.; Kim, J.; May, J.; Tocilescu, M. A.; Liu, W.; Ko, H. S.; Magrané, J.; Moore, D. J.; Dawson, V. L.; Grailhe, R.; Dawson, T. M.; Li, C.; Tieu, K.; Przedborski, S. PINK1-dependent Recruitment of Park into Mitochondria in Mitophagy Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 378-383
56. Yee, K. S.; Wilkinson, S.; James, J.; Ryan, K. M.; Vousden, K. H. PUMA- and Bax-Induced Autophagy Contributes to Apoptosis Cell Death Differ. 2009, 16, 1135-1145
57. Wu, L.; Li, Z.; Zhang, Y.; Zhang, P.; Zhu, X.; Huang, J.; Ma, T.; Lu, T.; Song, Q.; Li, Q.; Guo, Y.; Tang, J.; Ma, D.; Chen, K. H.; Qiu, X. Adenovirus-expressed Human Hyperplasia Suppressor Gene Induces Apoptosis in Cancer Cells Mol. Cancer Ther. 2008, 7, 222-232
58. Thomas, W. D.; Zhang, X. D.; Franco, A. V.; Nguyen, T.; Hersey, P. TNF-Related Apoptosis-Inducing Ligand-Induced Apoptosis of Melanoma Is Associated with Changes in Mitochondrial Membrane Potential and Peri-nuclear Clustering of Mitochondria J. Immunol. 2000, 165, 5612-5620
59. Chowdhury, R.; Chattoraj, S.; Sen Mojumdar, S.; Bhattacharyya, K. FRET between a Donor and an Acceptor Covalently Bound to Human Serum Albumin in Native and Non-native states Phys. Chem. Chem. Phys. 2013, 15, 16286-16293
60. Chowdhury, R.; Jana, B.; Saha, A.; Ghosh, S.; Bhattacharyya, K. Confocal Microscopy of Cytoplasmic Lipid Droplets in a Live Cancer Cell: Number, Polarity, Diffusion and Solvation Dynamics Med. Chem. Commun. 2014, 5, 536-539
61. Hess, S. T.; Sheets, E. D.; Wagenknecht-Wiesner, A.; Heikal-Simultaneous, A. A. Quantitative Analysis of the Fluorescence Properties of Intrinsically Fluorescent Proteins in Living Cells Biophys. J. 2003, 85, 2566-2580
62. Fisz, J. J. Fluorescence Polarization Spectroscopy at Combined High-Aperture Excitation and Detection: Application to One-Photon-Excitation Fluorescence Microscopy J. Phys. Chem. A 2007, 111, 8606-8621
63. Petrasek, Z.; Schwille, P. Precise Measurement of Diffusion Coefficients using Scanning Fluorescence Correlation Spectroscopy Biophys. J. 2008, 94, 1437-1448
64. Maroncelli, M.; Fleming, G. R. Picosecond Solvation Dynamics of Coumarin 153: The Importance of Molecular Aspects of Solvation J. Chem. Phys. 1987, 86, 6221-6239
65. Fee, R. S.; Maroncelli, M. Estimating the Time-zero Spectrum in Time-resolved Emission Measurements of Solvation Dynamics Chem. Phys. 1994, 183, 235-247
66. Chowdhury, R.; Sen Mojumdar, S.; Chattoraj, S.; Bhattacharyya, K. Effect of Ionic Liquid on the Native and Denatured State of a Protein Covalently Attached to a Probe: Solvation Dynamics Study J. Chem. Phys. 2012, 137, 055104-1-055104-8