Recent:
Thermodynamics and S-Palmitoylation Dependence of Interactions between Human Aquaporin-4 M1 Tetramers in Model Membranes
Jessica D. Carder, Barbara Barile, Krista A. Shisler, Francesco Pisani, Antonio Figeri, K. W. Hipps, Grazia Paola Nicchia, and James A. Brozik
A B S T R A C T:
Aquaporin-4 (AQP4) is a water channel protein found primarily in the central nervous system (CNS) that helps to regulate water–ion homeostasis. AQP4 exists in two major isoforms: M1 and M23. While both isoforms have a homotetrameric quaternary structure and are functionally identical when transporting water, the M23 isoform forms large protein aggregates known as orthogonal arrays of particles (OAPs). In contrast, the M1 isoform creates a peripheral layer around the outside of these OAPs, suggesting a thermodynamically stable interaction between the two. Structurally, the M1 isoform has an N-terminal tail that is 22 amino acids longer than the M23 isoform and contains two solvent-accessible cysteines available for S-palmitoylation at cysteine-13 (Cys-13) and cysteine-17 (Cys-17) in the amino acid sequence. Earlier work suggests that the palmitoylation of these cysteines might aid in regulating AQP4 assemblies. This work discusses the thermodynamic driving forces for M1 protein–protein interactions and how the palmitoylation state of M1 affects them. Using temperature-dependent single-particle tracking, the standard state free energies, enthalpies, and entropies were measured for these interactions. Furthermore, we present a binding model based on measured thermodynamics and a structural modeling study. The results of this study demonstrate that the M1 isoform will associate with itself according to the following expressions: 2[AQP4-M1]4 ↔ [[AQP4-M1]4]2 when palmitoylated and 3[AQP4-M1]4 ↔ [AQP4-M1]4 + [[AQP4-M1]4]2 ↔ [[AQP4-M1]4]3 when depalmitoylated. This is primarily due to a conformational change induced by adding the palmitic acid groups at Cys-13 and Cys-17 in the N-terminal tails of the homotetramers. In addition, a statistical mechanical model was developed to estimate the Gibbs free energy, enthalpy, and entropy for forming dimers and trimers. These results were in good agreement with experimental values.
Publications:
- Jessica D. Carder, Barbara Barile, Krista A. Shisler, Francesco Pisani, Antonio Figeri, K. W. Hipps, Grazia Paola Nicchia, and James A. Brozik. “Thermodynamics and S-Palmitoylation Dependence of Interactions between Human Aquaporin-4 M1 Tetramers in Model Membranes” Journal of Physical Chemistry B, 2024
- Taylor, E. L.; Abounorinejad, F.; Jacobo, E. P.; Dixon, A. D. C.; Lam, K. T.; Brozik, J. A. “Photophysical Rate Constants and Oxygen Dependence for Si and Ge Rhodamine Zwitterions.” The Journal of Physical Chemistry A 2023. DOI: 10.1021/acs.jpca.2c06244.
- Michael J. Martinez, Jessica D. Carder, Evan L. Taylor, Eric P. Jacobo, ChulHee Kang, and J.A. Brozik. “Thermodynamic Driving Forces of Redox Dependant CPR insertion into ER Biomimetic Membranes” Journal of Physical Chemistry B, 2022.
- Jou Chin Chan, Bixia Zhang, Michael Martinez, Balaganesh Kuruba, James Brozik, ChulHee Kang, Xiao Zhang* “Structural Studies of Myceliophthora Thermophila Laccase in the Presence of Deep Eutectic Solvents” Enzyme and Microbial Technology, 2021, Impact Factor = 2.932
- K.-T. Lam, E. L. Taylor, A. J. Thompson, M.-D. Ruepp, M. Lochner, Michael J. Martinez, J. A. Brozik* “Direct Measurement of Single-Molecule Ligand-Receptor Interactions”, Journal of the American Chemical Society, 2020, 124 (36), pp 7791-7802, Impact Factor = 2.991
- Katherine L. Jungjohann*, David R. Wheeler, Ronen Polsky, Susan M. Brozik, James A. Brozik, and Angela R. Rudolph†, “Liquid-Cell Scanning Transmission Electron Microscopy and Fluorescence Correlation Spectroscopy of DNA-Directed Gold Nanoparticle Assemblies”, Micron, 119, pp 54-63, 2019, Impact Factor = 1.527
- Nathan Turner, Sarah Kim, James Brozik, Matthew Marcus, Sirine Fakra, and Susan Dexhiemer* “EXAFS Spectroscopy of Fractional Mixed-Valence Charge Density Wave Systems, Journal of Physical Chemistry C, Journal of Physical Chemistry C 2019, 123, pp 6162-6189, Impact Factor = 4.484
- Evan L. Taylor†, Kumud R. Poudel, and James A. Brozik* “A Guide to Tracking Single Integral Membrane Proteins and Their Interactions in Supported Lipid Bilayers”, Methods in Molecular Biology, Accepted August 2018, Springer Press, Editor: Jorg Kleinschmidt, Impact Factor = 13.9
- Carlo Barnaba†, Evan Taylor†, and James A. Brozik* “Dissociation Constants of Cytochrome P450 2C9 / Cytochrome P450 Reductase Complexes in a Lipid Bilayer Membrane Depend on NADPH: A Single Protein Tracking Study”, Journal of the American Chemical Society 2017, 139(49), pp 17923-17934. Impact Factor = 13.038
- Carlo Barnaba†, Michael J. Martinez†, Evan Taylor†, Adam O. Barden, and James A. Brozik* “Single Protein Tracking Reveals that NADPH Mediates the Insertion of Cytochrome P450-Reductase into a Biomimetic of the Endoplasmic Reticulum”, Journal of the American Chemical Society 2017, 139(15), pp 5420-5430. Impact Factor = 13.038
- Carlo Barnaba†, Sara C. Humphreys†, Adam O. Barden, Jeffrey P. Jones, and James A. Brozik* “Substrate Dependent Native Luminescence from Cytochromes P450 3A4, 2C9, and P450cam” Journal of Physical Chemistry B, 2016, 120 (12), pp 3038–3047.Impact Factor=3.302
- Emily E. Scott, C. Roland Wolf, Michal Otyepka, Sara C. Humphreys†, James R. Reed, Colin J. Henderson, Lesley A. McLaughlin, Marketa Paloncyova, Veronika Navratilova, Karel Berka, Pavel Anzenbacher, Upendra P. Dahal, Carlo Barnaba†, James A. Brozik, Jeffrey P. Jones, D. Fernando Estrada, Jennifer S. Laurence, Ji Won Park, and Wayne L. Backes “The Role of Protein-Protein and Protein-Membrane Interactions on P450 Function” Drug Metab Dispos2016, 44, pp 576–590. Impact Factor=3.252
- Adam O Barden, Adam S. Goler, Sara C. Humphreys, Samaneh Tabatabaei, Martin Lochner, Marc-David Ruepp, Thomas Jack, Jonathan Simonin, Andrew J. Thompson, Jeffrey P. Jones, and James A. Brozik “Tracking Individual Membrane Proteins and Their Biochemistry: The Power of Direct Observation” Neuropharmacology, 98, 22-30, 2015. Impact Factor=4.819
- Marc-David Ruepp, James A. Brozik, Iwan J.P. de Esch, Richard W. Farndale, Ruth D. Murrell-Lagnado, and Andrew J. Thompson* “A Fluorescent Approach for Identifying P2X1 Ligands” Neuropharmacology,98, 13-21, 2015. Impact Factor=4.819
- Elsa I. Silva-Lopez†, Lance E. Edens†, David J. Keller, and James A. Brozik* “Conditions for Liposome Adsorption and Bilayer Formation on BSA Passivated Solid Supports”, Chemistry and Physics of Lipids, 183, 91-99, 2014. Impact Factor =2.680
- Elsa I. Silva-Lopez†, Adam O. Barden†, and James A. Brozik* “Near Native Binding of a Fluorescent Serotonin Conjugate to Serotonin Type-3 Receptors”, Bioorganic and Medicinal Chemistry Letters, 23(3), 773-775, 2013. Impact Factor = 2.554
- Kumud R. Poudel†, Jeffery P. Jones, and James A. Brozik* “A Guide to Tracking Single Transmembrane Proteins in Supported Lipid Bilayers” Methods in Molecular Biology, Chapter 11, Springer Press, Vol. 974, Editor: Jorg Kleinschmidt, ISBN: 978-1-62703-274-2, Release February 28th, 2013. Impact Factor = 13.9
- Lance E. Edens†, James A. Brozik, and David J. Keller* “Course-Grained Model DNA: Structure, Sequences, Stems, Circles, Hairpins” Journal of Physical Chemistry B, 116(51) 14735-14743, 2012. Impact Factor = 3.603
- Kumud R. Poudel†, David J. Keller, and James A. Brozik* “The Effect of a Phase Transition on Single Molecule Tracks of Annexin V in Cushioned DMPC Assemblies”, Soft Matter, 8, 11285-11293, 2012. Impact Factor = 4.869
- Kumud R. Poudel†, David J. Keller, and James A. Brozik* “Single Particle Tracking Reveals Corralling of a Transmembrane Protein in a Double-Cushioned Bilayer Assembly” Langmuir, 27(1), 320-327, 2011. Impact Factor = 4.269
- Christopher M. Hartshorn†, Cayla M. Jewett§, and James A. Brozik* “Molecular Effects of a Nanocrystalline Quartz Support Upon Planar Lipid Bilayers” Langmuir, 26(4), 2609-2617, 2010. Impact Factor = 4.269
- Ryan W. Davis†, Adrean Flores§, Todd Barrick§, Jason M. Cox†, Susan M. Brozik, Gabriel P. Lopez, and James A. Brozik* “Nanoporous Microbead Supported Bilayers: Stability, Physical Characterization, and Incorporation of Functional Transmembrane Proteins” Langmuir 23, 3864-3872, 2007. Impact Factor = 4.269
- Theodore P. Ortiz†, Jason A. Marshall‡, Lauren A. Meyer§, Ryan W. Davis†, Jed C. Macosko‡, David J. Keller, and James A. Brozik* “Stepping Statistics of Single HIV-1 Reverse Transcriptase Molecules During DNA Polymerization”. Journal of Physical Chemistry B 109 (33), 16127 – 16131, 2005. Impact Factor = 3.603
- David J. Keller* and James A. Brozik, “Framework Model for DNA Polymerases”. Biochemistry 44 (18), 6877 – 6888, 2005. Impact Factor = 3.226
- James A. Brozik* and G. A. Crosby* “Photochemical Reactions of Rhodium(III) Diimine Complexes in Solid Glycerol Matrices. Ligand-Field Influences on Activation Energies”. Coordination Chemical Reviews 249 (13-14), 1310 – 1315, 2005. Impact Factor = 10.018
- Hialong Lu†, Jed C. Macosko‡, James A. Brozik, and David J. Keller* “Motor Forces of HIV Reverse Transcriptase Closing of the Fingers Domain Generates Motor Forces in the HIV Reverse Transcriptase”. Journal of Biological Chemistry 279, 54529-54532, 2004. Impact Factor = 5.3128
- Ryan W. Davis†, Elizabeth L. Patrick§, Lauren A. Meyer§, Theodore P. Ortiz†, Jason A. Marshall‡, David J. Keller, Susan M. Brozik, and James A. Brozik* “The Thermodynamic Properties of Single Ion Channel Formation: Gramicidin”. Journal of Physical Chemistry B, 108, 15364-15369, 2004. Impact Factor = 3.603
- Theodore P. Ortiz†, Jason A. Marshall‡, Luke A. Emmert‡, Jing Yang†, Wonsook Choi†, Alison L. Costello† and James A. Brozik* “The Transient Mixed-Valence Character of Re(I)4(CO)12(4,4’-Bpy)4Cl4”, Inorganic Chemistry, 43(1), 132-141, 2004. Impact Factor = 4.326
- Luke A. Emmert‡, Wonsook Choi†, Jason A. Marshall‡, Jing Yang†, Lauren A. Meyer§, and James A. Brozik* “The Excited State Symmetry Characteristics of Platinum Phenylacetylene Compounds”, Journal of Physical Chemistry A, 107, 11340-11346, 2003. Impact Factor = 2.732
- Elizabeth L. Patrick§, Chad J. Ray§, Grant D. Meyer§, Theodore P. Ortiz†, Jason A. Marshall‡, Melissa A. Summers§, John W. Kenney, III and James A. Brozik* “Non-Localized Ligand-to-Metal Charge Transfer Excited States in (Cp)2Ti(IV)(NCS)2” Journal of the American Chemical Society, 125(18), 5461-5470, 2003. Impact Factor = 9.023
- Joe Ritter*, James A. Brozik, Luke Emmert‡, Mike Fallbach†, Rodney Bradford, Don Leo, and Ken Meissner, “Novel Photomechanical Actuators”, SPIE, August 2003. Impact Factor = 0.822
- Joe Ritter*, James A. Brozik “Novel Combined Cis-Trans / Twisted Intermolecular Charge Transfer (CCT-TICT) Actuated Adaptive Optics” MHPCC/AFRL Application Briefs, 40-41, 2003.
- Joe Ritter*, James A. Brozik, Luke Emmert‡, Mike Fallbach†, Rodney Bradford, Don Leo, and Ken Meissner “Novel Active Optics with 1023 Photomechanical Acuators” MHPCC/AFRL Application Briefs, 38-39, 2003.
- G. D. Meyer§, T. P. Ortiz†, A. L. Costello†, J. W. Kenney, III and J. A. Brozik* “A Simple Fiber-Optic Coupled Luminescence Cryostat” Review of Scientific Instruments, 73(12), 4369-4374, 2002. Impact Factor = 1.598
- Joe Ritter*, James A. Brozik, James Newhouse, and David Keller “Novel Laser Actuated Optically Addressable Adaptive Optics”, MHPCC/AFRL Application Briefs, 2002.
- Joe Ritter*, James A. Brozik, James Newhouse, and Debi G. Evans “Novel Ultra-Lightweight Space Telescopes Using Optically Active Polymer “Membrane Mirror Shape Control”, MHPCC/AFRL Application Briefs, 2001.
- S. L. Dexheimer*, A. D. Van Pelt, J. A. Brozik, B. I. Swanson, “Dynamics of the formation of the self-trapped exciton in the MX complex PtBr(en)”, Synthetic Metals, 116 (#1-3), 393-396, 2001. Impact Factor = 1.871
- S. L. Dexheimer*, A. D. Van Pelt, J. A. Brozik, B. I. Swanson, “Fetmosecond Vibrational Dynamics of Self-Trapping in a Quasi-One-Dimensional System”, Physical Review Letters, 84 (19), 4425-4428, 2000. Impact Factor = 7.328
- S. L. Dexheimer*, A. D. Van Pelt, J. A. Brozik, B. I. Swanson, “Ultrafast vibrational dynamics in a quasi-one-dimensional system: Femtosecond impulsive excitation of the PtBr(ethylenediamine) mixed-valence linear chain complex”, Journal of Physical Chemistry A, 104(18), 4308-4313, 2000. Impact Factor = 2.732
- J. A. Brozik*, B. L. Scott, B. I. Swanson, “Preparation and Spectroscopic Characterization of [Pt(en)2I2][Pt(CN)4]: A New Quasi-One Dimensional Mixed Valence Chain Material in a Completely Ordered Lattice”, Journal of Physical Chemistry B, 103, 10566-10571, 1999. Impact Factor = 3.603
- J. A. Brozik*, B. L. Scott, B. I. Swanson, “Synthetic Control of Intrinsic Ground State Defects in a Mixed Valence Quasi-One-Dimensional Pt Halide Chain”, Inorganica Chimica ACTA, 294, 275-280, 1999. Impact Factor = 1.899
- B. I. Swanson*, J. A. Brozik, S. P. Love, G. Strouse, A. P. Shreve, M. Salkola, W. Wen-Zheng, and A. R. Bishop, “Vibrational Self-Focusing: The Observation of Intrinsically Localized Modes in a Discrete Quasi-1-D Material”, Physical Review Letters, 82 (16), 3288-3291, 1999. Impact Factor = 7.328
- J. A. Brozik and G. A. Crosby*, “Activation Energies for Photochemical Reactions of Rhodium(III) Tris(Diimine) Complexes in Solid Matrices at Low Temperature: Part I”, Journal of Physical Chemistry A, 102 (1), 45-50 (1998). Impact Factor = 2.732
- J. A. Brozik and G. A. Crosby*, “Thermal Redistribution of Excited State Energy from a 3pp* Term to a Nearby Chemically Reactive 3dd level in [Rh(III)(NN)3](PF6)3 Complexes”, Chemical Physics Letters 255, 445-450 (1996). Impact Factor = 2.229
- D. R. Striplin, J. A. Brozik, G. A. Crosby*, “Assignment of the Luminescing States of [Au(I)Ir(I)Cl(CO)(m-dppm)2][PF6], Chemical Physics Letters 231, 159-163 (1994). Impact Factor = 2.229
- H. Miki, M. Shimada, T. Azumi*, J. A. Brozik, G. A. Crosby*, “Effect of Ligand-Field Strength on the Radiative Properties of the Ligand-Localized 3pp* State of Rhodium Complexes with 1,10-Phenanthroline”, Journal of Physical Chemistry 97, 11175-11179 (1993). Impact Factor = 2.732
- J. P. Peterson, D. B. Horsley, J. A. Brozik, R. D. Rogers*, “Anticancer Agent Development. 4. X-ray Crystal Structure and Intermolecular Crystal Lattice Interactions of Methyl trans-4,5- dihydro-4-acetoylmethyl-5-(3,4,5-trimethoxyphenyl)-2-(3,4-methylenedioxyphenyl)-3-furancarbozylate”, Journal of Crystallographic and Spectroscopic Research 20, 47-52 (1990). Impact Factor = 0.341
- J. P. Peterson, D. B. Horsley, J. A. Brozik, R. D. Rogers*, “Platelet Activating Factor Antagonist Design. 3. X-ray Crystal Structure and Intermolecular Crystal Lattice Interactions of Methyl-trans-4,5-dihydro-2,5-bis(3,4-methylenedioxyphenyl)-3-furancarbozylate”, Acta Crystallographica, C45, 1164-1167 (1989). Impact Factor = 0.492