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Title: Characterization of WY 14,643 and its Complex with Aldose Reductase

Abstract

The peroxisome proliferator, WY 14,643 exhibits a pure non-competitive inhibition pattern in the aldehyde reduction and in alcohol oxidation activities of human Aldose reductase (hAR). Fluorescence emission measurements of the equilibrium dissociation constants, Kd, of oxidized (hAR•NADP+) and reduced (hAR•NADPH) holoenzyme complexes display a 2-fold difference between them. Kd values for the dissociation of WY 14,643 from the oxidized (hAR•NADP+•WY 14,643) and reduced (hAR•NADPH•WY 14,643) ternary complexes are comparable to each other. The ternary complex structure of hAR•NADP+•WY 14,643 reveals the first structural evidence of a fibrate class drug binding to hAR. These observations demonstrate how fibrate molecules such as WY 14,643, besides being valued as agonists for PPAR, also inhibit hAR.

Authors:
 [1];  [2];  [3];  [4];  [1];  [3]
  1. UCLA-DOE, Los Angeles, CA (United States)
  2. Univ. of Manchester (United Kingdom)
  3. Youngstown State Univ., OH (United States)
  4. Univ. of Missouri, St. Louis, MO (United States)
Publication Date:
Research Org.:
Stanford Synchrotron Radiation Lab., (SSRL), CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1378554
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Sawaya, Michael R., Verma, Malkhey, Balendiran, Vaishnavi, Rath, Nigam P., Cascio, Duilio, and Balendiran, Ganesaratnam K. Characterization of WY 14,643 and its Complex with Aldose Reductase. United States: N. p., 2016. Web. doi:10.1038/srep34394.
Sawaya, Michael R., Verma, Malkhey, Balendiran, Vaishnavi, Rath, Nigam P., Cascio, Duilio, & Balendiran, Ganesaratnam K. Characterization of WY 14,643 and its Complex with Aldose Reductase. United States. doi:10.1038/srep34394.
Sawaya, Michael R., Verma, Malkhey, Balendiran, Vaishnavi, Rath, Nigam P., Cascio, Duilio, and Balendiran, Ganesaratnam K. Mon . "Characterization of WY 14,643 and its Complex with Aldose Reductase". United States. doi:10.1038/srep34394. https://www.osti.gov/servlets/purl/1378554.
@article{osti_1378554,
title = {Characterization of WY 14,643 and its Complex with Aldose Reductase},
author = {Sawaya, Michael R. and Verma, Malkhey and Balendiran, Vaishnavi and Rath, Nigam P. and Cascio, Duilio and Balendiran, Ganesaratnam K.},
abstractNote = {The peroxisome proliferator, WY 14,643 exhibits a pure non-competitive inhibition pattern in the aldehyde reduction and in alcohol oxidation activities of human Aldose reductase (hAR). Fluorescence emission measurements of the equilibrium dissociation constants, Kd, of oxidized (hAR•NADP+) and reduced (hAR•NADPH) holoenzyme complexes display a 2-fold difference between them. Kd values for the dissociation of WY 14,643 from the oxidized (hAR•NADP+•WY 14,643) and reduced (hAR•NADPH•WY 14,643) ternary complexes are comparable to each other. The ternary complex structure of hAR•NADP+•WY 14,643 reveals the first structural evidence of a fibrate class drug binding to hAR. These observations demonstrate how fibrate molecules such as WY 14,643, besides being valued as agonists for PPAR, also inhibit hAR.},
doi = {10.1038/srep34394},
journal = {Scientific Reports},
number = 1,
volume = 6,
place = {United States},
year = {2016},
month = {10}
}

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Works referenced in this record:

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Aldose reductase expression is induced by hyperglycemia in diabetic nephropathy
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journal, June 2003

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Staurosporine-induced conformational changes of cAMP-dependent protein kinase catalytic subunit explain inhibitory potential
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Cefprozil versus Cefuroxime Axetil in the Treatment of Acute Sinusitis
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PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes
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Equilibrium binding of nicotinamide nucleotides to lactate dehydrogenases
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  • DOI: 10.1042/bj1310719

Fenofibric Acid: In Combination Therapy in the Treatment of Mixed Dyslipidemia
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    Works referencing / citing this record:

    CCDC 1476501: Experimental Crystal Structure Determination: IXIJOQ : ((4-chloro-6-((2,3-dimethylphenyl)amino)pyrimidin-2-yl)sulfanyl)acetic acid
    dataset, April 2016


    The involvement of aldose reductase in diabetic complications
    journal, June 1988

    • Kinoshita, Jin H.; Nishimura, Chihiro
    • Diabetes / Metabolism Reviews, Vol. 4, Issue 4
    • DOI: 10.1002/dmr.5610040403

    Biomolecular Chemistry of Isopropyl Fibrates
    journal, April 2012

    • Balendiran, Ganesaratnam K.; Rath, Niharika; Kotheimer, Amanda
    • Journal of Pharmaceutical Sciences, Vol. 101, Issue 4
    • DOI: 10.1002/jps.23040

    Verification of protein structures: Patterns of nonbonded atomic interactions
    journal, September 1993


    A potent antihypercholesterolemic agent: [4-chloro-6-(2,3-xylidino)-2-pyrimidinylthio]acetic acid (Wy-14643)
    journal, October 1974

    • Santilli, A. A.; Scotese, A. C.; Tomarelli, R. M.
    • Experientia, Vol. 30, Issue 10
    • DOI: 10.1007/bf01923636

    Protection against myocardial ischaemia/reperfusion injury by PPAR–α activation is related to production of nitric oxide and endothelin–1
    journal, January 2006

    • Bulhak, A. A.; Sjöquist, P. -O.; Xu, C. -B.
    • Basic Research in Cardiology, Vol. 101, Issue 3
    • DOI: 10.1007/s00395-005-0580-1

    Fluorescence Quenching to Study Protein-ligand Binding: Common Errors
    journal, December 2009


    In vivo covalent binding of clofibric acid to human plasma proteins and rat liver proteins
    journal, September 1991

    • Sallustio, Benedetta C.; Knights, Kathleen M.; Roberts, Benjamin J.
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    • DOI: 10.1016/0006-2952(91)90454-d

    Le mécanisme de la formation du fructose séminal et du fructose foetal
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    Inhibiting wild-type and C299S mutant AKR1B10; a homologue of aldose reductase upregulated in cancers
    journal, April 2008


    Molecular Mechanism of Peroxisome Proliferator-Activated Receptor α Activation by WY14643: a New Mode of Ligand Recognition and Receptor Stabilization
    journal, August 2013

    • Bernardes, Amanda; Souza, Paulo C. T.; Muniz, João R. C.
    • Journal of Molecular Biology, Vol. 425, Issue 16
    • DOI: 10.1016/j.jmb.2013.05.010

    Fluorescence quenching and ligand binding: A critical discussion of a popular methodology
    journal, July 2011


    The pp60 c-Src inhibitor PP1 is non-competitive against ATP
    journal, January 2003


    Long-term effect of epalrestat on cardiac autonomic neuropathy in subjects with non-insulin dependent diabetes mellitus
    journal, March 1999


    Staurosporine-induced conformational changes of cAMP-dependent protein kinase catalytic subunit explain inhibitory potential
    journal, December 1997


    Crystal Structure of Hck in Complex with a Src Family–Selective Tyrosine Kinase Inhibitor
    journal, May 1999


    The Sorbinil Trap:  A Predicted Dead-End Complex Confirms the Mechanism of Aldose Reductase Inhibition
    journal, August 2000

    • Bohren, Kurt M.; Grimshaw, Charles E.
    • Biochemistry, Vol. 39, Issue 32
    • DOI: 10.1021/bi000789q

    Mechanism of Aldose Reductase Inhibition: Binding of NADP+/NADPH and Alrestatin-like Inhibitors
    journal, June 1994

    • Ehrig, Torsten; Bohren, Kurt M.; Prendergast, Franklyn G.
    • Biochemistry, Vol. 33, Issue 23
    • DOI: 10.1021/bi00189a019

    Formation of Polyols by the Lens of the Rat with ‘Sugar’ Cataract
    journal, July 1959


    Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators
    journal, October 1990

    • Issemann, Isabelle; Green, Stephen
    • Nature, Vol. 347, Issue 6294
    • DOI: 10.1038/347645a0

    Assessment of protein models with three-dimensional profiles
    journal, March 1992

    • Lüthy, Roland; Bowie, James U.; Eisenberg, David
    • Nature, Vol. 356, Issue 6364
    • DOI: 10.1038/356083a0

    PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes
    journal, June 2003

    • Mootha, Vamsi K.; Lindgren, Cecilia M.; Eriksson, Karl-Fredrik
    • Nature Genetics, Vol. 34, Issue 3
    • DOI: 10.1038/ng1180

    Equilibrium binding of nicotinamide nucleotides to lactate dehydrogenases
    journal, April 1973

    • Stinson, Robert A.; Holbrook, J. John
    • Biochemical Journal, Vol. 131, Issue 4
    • DOI: 10.1042/bj1310719

    Aldose reductase expression is induced by hyperglycemia in diabetic nephropathy
    journal, July 2001


    The Sorbitol Pathway and the Complications of Diabetes
    journal, April 1973

    • Steinmetz, Philip R.; Balko, Christine; Gabbay, Kenneth H.
    • New England Journal of Medicine, Vol. 288, Issue 16
    • DOI: 10.1056/nejm197304192881609

    Sorbitol, Phosphoinositides, and Sodium-Potassium-ATPase in the Pathogenesis of Diabetic Complications
    journal, March 1987

    • Flier, Jeffrey S.; Underhill, Lisa H.; Greene, Douglas A.
    • New England Journal of Medicine, Vol. 316, Issue 10
    • DOI: 10.1056/nejm198703053161007

    Impaired Mitochondrial Activity in the Insulin-Resistant Offspring of Patients with Type 2 Diabetes
    journal, February 2004

    • Petersen, Kitt Falk; Dufour, Sylvie; Befroy, Douglas
    • New England Journal of Medicine, Vol. 350, Issue 7
    • DOI: 10.1056/nejmoa031314

    Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1
    journal, June 2003

    • Patti, Mary Elizabeth; Butte, Atul J.; Crunkhorn, Sarah
    • Proceedings of the National Academy of Sciences, Vol. 100, Issue 14
    • DOI: 10.1073/pnas.1032913100

    The Role of Cys-298 in Aldose Reductase Function
    journal, November 2010

    • Balendiran, Ganesaratnam K.; Sawaya, Michael R.; Schwarz, Frederick P.
    • Journal of Biological Chemistry, Vol. 286, Issue 8
    • DOI: 10.1074/jbc.m110.154195

    Peroxisome Proliferator-activated Receptor (PPAR) Gene Profiling Uncovers Insulin-like Growth Factor-1 as a PPARα Target Gene in Cardioprotection
    journal, January 2011

    • el Azzouzi, Hamid; Leptidis, Stefanos; Bourajjaj, Meriem
    • Journal of Biological Chemistry, Vol. 286, Issue 16
    • DOI: 10.1074/jbc.m111.220525

    Catalytic Domain Crystal Structure of Protein Kinase C-θ (PKCθ)
    journal, September 2004

    • Xu, Zhang-Bao; Chaudhary, Divya; Olland, Stephane
    • Journal of Biological Chemistry, Vol. 279, Issue 48
    • DOI: 10.1074/jbc.m409216200

    WY 14,643 inhibits human aldose reductase activity
    journal, January 2006

    • Klemin, Sara; Calvo, Richard Y.; Bond, Stephanie
    • Journal of Enzyme Inhibition and Medicinal Chemistry, Vol. 21, Issue 5
    • DOI: 10.1080/14756360600720887

    PROCHECK: a program to check the stereochemical quality of protein structures
    journal, April 1993

    • Laskowski, R. A.; MacArthur, M. W.; Moss, D. S.
    • Journal of Applied Crystallography, Vol. 26, Issue 2
    • DOI: 10.1107/s0021889892009944

    Fenofibric acid
    journal, January 2005

    • Rath, Nigam P.; Haq, Wahajul; Balendiran, Ganesaratnam K.
    • Acta Crystallographica Section C Crystal Structure Communications, Vol. 61, Issue 2
    • DOI: 10.1107/s0108270104032573

    A short history of SHELX
    journal, December 2007

    • Sheldrick, George M.
    • Acta Crystallographica Section A Foundations of Crystallography, Vol. 64, Issue 1, p. 112-122
    • DOI: 10.1107/s0108767307043930

    Coot model-building tools for molecular graphics
    journal, November 2004

    • Emsley, Paul; Cowtan, Kevin
    • Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
    • DOI: 10.1107/s0907444904019158

    XDS
    journal, January 2010

    • Kabsch, Wolfgang
    • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2
    • DOI: 10.1107/s0907444909047337

    Overview of the CCP 4 suite and current developments
    journal, March 2011

    • Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D.
    • Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
    • DOI: 10.1107/s0907444910045749

    Data processing and analysis with the autoPROC toolbox
    journal, March 2011

    • Vonrhein, Clemens; Flensburg, Claus; Keller, Peter
    • Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4
    • DOI: 10.1107/s0907444911007773

    How good are my data and what is the resolution?
    journal, June 2013

    • Evans, Philip R.; Murshudov, Garib N.
    • Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7
    • DOI: 10.1107/s0907444913000061

    2.2 Å refined crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MnATP and a peptide inhibitor
    journal, May 1993

    • Zheng, J.; Trafny, E. A.; Knighton, D. R.
    • Acta Crystallographica Section D Biological Crystallography, Vol. 49, Issue 3
    • DOI: 10.1107/s0907444993000423

    Refinement of Macromolecular Structures by the Maximum-Likelihood Method
    journal, May 1997

    • Murshudov, G. N.; Vagin, A. A.; Dodson, E. J.
    • Acta Crystallographica Section D Biological Crystallography, Vol. 53, Issue 3
    • DOI: 10.1107/s0907444996012255

    An Evaluation of Charge Effects on the Quenching of Tryptophan Fluorescence in Small Peptides by Iodide ion
    journal, July 1985


    STUDIES OF THE EFFICIENCY and MECHANISM OF FLUORESCENCE QUENCHING REACTIONS USING ACRYLAMIDE and SUCCINIMIDE AS QUENCHERS
    journal, July 1987


    Three hypolipidemic drugs increase hepatic palmitoyl-coenzyme A oxidation in the rat
    journal, August 1977


    The Mechanisms of Action of PPARs
    journal, February 2002


    Abnormal Cardiac and Skeletal Muscle Energy Metabolism in Patients With Type 2 Diabetes
    journal, June 2003


    Structural and Functional Consequences of Mitochondrial Biogenesis in Human Adipocytes in Vitro
    journal, December 2005

    • Bogacka, Iwona; Ukropcova, Barbara; McNeil, Michele
    • The Journal of Clinical Endocrinology & Metabolism, Vol. 90, Issue 12
    • DOI: 10.1210/jc.2005-1024

    Cefprozil versus Cefuroxime Axetil in the Treatment of Acute Sinusitis
    journal, January 1998


    Acyl Glucuronides Revisited: Is the Glucuronidation Proces a Toxification as Well as a Detoxification Mechanism?
    journal, January 1992