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Calcium binding and allosteric signaling mechanisms for the sarcoplasmic reticulum Ca 2+ ATPase

dc.contributor.authorKekenes‐huskey, Peter M.en_US
dc.contributor.authorMetzger, Vincent T.en_US
dc.contributor.authorGrant, Barry J.en_US
dc.contributor.authorAndrew McCammon, J.en_US
dc.date.accessioned2012-10-02T17:20:19Z
dc.date.available2013-11-04T19:53:16Zen_US
dc.date.issued2012-10en_US
dc.identifier.citationKekenes‐huskey, Peter M. ; Metzger, Vincent T.; Grant, Barry J.; Andrew McCammon, J. (2012). "Calcium binding and allosteric signaling mechanisms for the sarcoplasmic reticulum Ca 2+ ATPase ." Protein Science 21(10): 1429-1443. <http://hdl.handle.net/2027.42/93731>en_US
dc.identifier.issn0961-8368en_US
dc.identifier.issn1469-896Xen_US
dc.identifier.urihttps://hdl.handle.net/2027.42/93731
dc.description.abstractThe sarcoplasmic reticulum Ca 2+ ATPase (SERCA) is a membrane‐bound pump that utilizes ATP to drive calcium ions from the myocyte cytosol against the higher calcium concentration in the sarcoplasmic reticulum. Conformational transitions associated with Ca 2+ ‐binding are important to its catalytic function. We have identified collective motions that partition SERCA crystallographic structures into multiple catalytically‐distinct states using principal component analysis. Using Brownian dynamics simulations, we demonstrate the important contribution of surface‐exposed, polar residues in the diffusional encounter of Ca 2+ . Molecular dynamics simulations indicate the role of Glu309 gating in binding Ca 2+ , as well as subsequent changes in the dynamics of SERCA's cytosolic domains. Together these data provide structural and dynamical insights into a multistep process involving Ca 2+ binding and catalytic transitions.en_US
dc.publisherWiley Subscription Services, Inc., A Wiley Companyen_US
dc.subject.otherMolecular Dynamicsen_US
dc.subject.otherGatingen_US
dc.subject.otherCalcium Bindingen_US
dc.subject.otherSERCAen_US
dc.subject.otherBrownian Dynamicsen_US
dc.titleCalcium binding and allosteric signaling mechanisms for the sarcoplasmic reticulum Ca 2+ ATPaseen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelBiological Chemistryen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, Michigan 48109en_US
dc.contributor.affiliationotherDepartment of Chemistry and Biochemistry, University of California, San Diego, La Jolla, California 92093en_US
dc.contributor.affiliationotherUniversity of California, San Diego, 9500 Gilman Dr., M/C 0365, La Jolla, CA 92093‐0365en_US
dc.contributor.affiliationotherDepartment of Pharmacology, University of California, San Diego, La Jolla, California 92093en_US
dc.identifier.pmid22821874en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/93731/1/2129_ftp.pdf
dc.identifier.doi10.1002/pro.2129en_US
dc.identifier.sourceProtein Scienceen_US
dc.identifier.citedreferenceRostkowski M, Olsson MH, Søndergaard CR, Jensen JH. ( 2011 ) Graphical analysis of pH‐dependent properties of proteins predicted using PROPKA. BMC Struct Biol 11: 6.en_US
dc.identifier.citedreferenceWade RC, Gabdoulline RR, LÃdemann SK, Lounnas V. ( 1998 ) Electrostatic steering and ionic tethering in enzyme‐ligand binding: insights from simulations. Proc Nat Acad Sci 95: 5942 – 5949.en_US
dc.identifier.citedreferenceSzabo A, Shoup D, Northrup S, McCammon J. ( 1982 ) Stochastically gated diffusion‐influenced reactions. J Chem Phys 77: 4484 – 4493.en_US
dc.identifier.citedreferenceToyoshima C, Nakasako M, Nomura H, Ogawa H. ( 2000 ) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 —[angst]— resolution. Nature 405: 647 – 655.en_US
dc.identifier.citedreferenceSonntag Y, Musgaard M, Olesen C, Schiott B, Moller JV, Nissen P, Thogersen L. ( 2011 ) Mutual adaptation of a membrane protein and its lipid bilayer during conformational changes. Nat Commun 2: 304.en_US
dc.identifier.citedreferenceLervik A, Bresme F, Kjelstrup S. ( 2012 ) Molecular dynamics simulations of the Ca2+‐pump: a structural analysis. Phys Chem Chem Phy 14: 3543.en_US
dc.identifier.citedreferenceDode L, Vilsen B, Van Baelen K, Wuytack F, Clausen J, Andersen J. ( 2002 ) Dissection of the functional differences between sarco (endo) plasmic reticulum Ca2+‐ATPase (SERCA) 1 and 3 isoforms by steady‐state and transient kinetic analyses. J Biol Chem 277: 45579.en_US
dc.identifier.citedreferenceTzeng S, Kalodimos C. ( 2009 ) Dynamic activation of an allosteric regulatory protein. Nature 462: 368 – 372.en_US
dc.identifier.citedreferenceLi D‐W, Showalter SA, Brüschweiler R. ( 2010 ) Entropy localization in proteins. J Phys Chem B. 114: 16036 – 16044.en_US
dc.identifier.citedreferenceZhang Z, Sumbilla C, Lewis D, Summers S, Klein MG, Inesi G. ( 1995 ) Mutational analysis of the peptide segment linking phosphorylation and Ca(2+)‐binding domains in the sarcoplasmic reticulum Ca(2+)‐ ATPase. J Biol Chem 270: 16283 – 16290.en_US
dc.identifier.citedreferenceMueller B, Zhao M, Negrashov I, Bennett R, Thomas D. ( 2004 ) SERCA structural dynamics induced by ATP and calcium. Biochemistry. 43: 12846 – 12854.en_US
dc.identifier.citedreferenceLenoir G, Jaxel C, Picard M, le Maire M, Champeil P, Falson P. ( 2006 ) Conformational changes in sarcoplasmic reticulum Ca 2+‐ATPase mutants: effect of mutations either at Ca 2+‐Binding Site II or at tryptophan 552 in the cytosolic domain. Biochemistry 45: 5261 – 5270.en_US
dc.identifier.citedreferenceSatoh K, Matsu‐ura T, Enomoto M, Nakamura H, Michikawa T, Mikoshiba K. ( 2011 ) Highly cooperative dependence of sarco/endoplasmic reticulum calcium ATPase (SERCA) 2a pump activity on cytosolic calcium in living cells. J Biol Chem 286: 20591 – 20599.en_US
dc.identifier.citedreferenceObara K, Miyashita N, Xu C, Toyoshima L, Sugita Y, Inesi G, Toyoshima C. ( 2005 ) Structural role of countertransport revealed in Ca2+ pump crystal structure in the absence of Ca2+. Proc Nat Acad Sci 102: 14489 – 14496.en_US
dc.identifier.citedreferenceWeidemüller C, Hauser K. ( 2009 ) Ion transport and energy transduction of P‐type ATPases: implications from electrostatic calculations. Biochim Biophys Acta (BBA) − Bioenerg 1787: 721 – 729.en_US
dc.identifier.citedreferenceHumphrey W, Dalke A, Schulten K. ( 1996 ) VMD: visual molecular dynamics. J Mol Graphics 14: 33 – 38.en_US
dc.identifier.citedreferenceBrooks BR, Brooks CL III, Mackerell AD Jr, Nilsson L, Petrella RJ, Roux B, Won Y, Archontis G, Bartels C, Boresch S, Caflisch A, Caves L, Cui Q, Dinner AR, Feig M, Fischer S, Gao J, Hodoscek M, Im W, Kuczera K, Lazaridis T, Ma J, Ovchinnikov V, Paci E, Pastor RW, Post CB, Pu JZ, Schaefer M, Tidor B, Venable RM, Woodcock HL, Wu X, Yang W, York DM, Karplus M. ( 2009 ) CHARMM: the biomolecular simulation program. J Comput Chem 30: 1545 – 1614.en_US
dc.identifier.citedreferencePhillips J, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel R, Kale L, Schulten K. ( 2005 ) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781 – 1802.en_US
dc.identifier.citedreferenceDarden T, York D, Pedersen L. ( 1993 ) Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems. J Chem Phys. 98: 10089 – 10092.en_US
dc.identifier.citedreferenceWang Y, Harrison CB, Schulten K, McCammon JA. ( 2011 ) Implementation of Accelerated Molecular Dynamics in NAMD. Comput Sci Discovery. 4: 015002 – 015012.en_US
dc.identifier.citedreferenceGrant BJ, Rodrigues APC, ElSawy KM, McCammon J, Caves LSD. ( 2006 ) Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics 22: 2695 – 2696.en_US
dc.identifier.citedreferenceDurrant J, de Oliveira C, McCammon J. ( 2011 ) POVME: an algorithm for measuring binding‐pocket volumes. J Mol Graphics Modell. 29: 773 – 776.en_US
dc.identifier.citedreferenceHuber GA, McCammon JA. ( 2010 ) Browndye: a software package for Brownian dynamics. Comput Phys Commun 181: 1896 – 1905.en_US
dc.identifier.citedreferenceDolinsky TJ, Czodrowski P, Li J, Nielsen JE, Jensen JH, Klebe G, Baker NA. ( 2007 ) PDB 2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucl Acid Res 35: W522 – W525.en_US
dc.identifier.citedreferenceBaker NA. ( 2001 ) Electrostatics of nanosystems: application to micro‐tubules and the ribosome. Proc Nat Acad Sci 98: 10037 – 10041.en_US
dc.identifier.citedreferenceNorthrup S, Allison S, McCammon J. ( 1984 ) Brownian dynamics simulation of diffusion‐influenced bimolecular reactions. J Chem Phys 80: 1517 – 1526.en_US
dc.identifier.citedreferenceYu H, Noskov S, Roux B. ( 2010 ) Two mechanisms of ion selectivity in protein binding sites. Proc Nat Acad Sci 107: 20329.en_US
dc.identifier.citedreferenceToyoshima C. ( 2008 ) Structural aspects of ion pumping by Ca2+‐ATPase of sarcoplasmic reticulum. Arch Biochem Biophys 476: 3 – 11.en_US
dc.identifier.citedreferenceWinters D, Autry J, Svensson B, Thomas D. ( 2008 ) Interdomain fluorescence resonance energy transfer in SERCA probed by cyan‐fluorescent protein fused to the actuator domain. Biochemistry 47: 4246 – 4256.en_US
dc.identifier.citedreferenceLewis S, Thomas D. ( 1992 ) Resolved conformational states of spin‐labeled calcium‐ATPase during the enzymic cycle. Biochemistry 31: 7381 – 7389.en_US
dc.identifier.citedreferenceToyoshima CC, Asahi MM, Sugita YY, Khanna RR, Tsuda TT, MacLennan DHD. ( 2003 ) Modeling of the inhibitory interaction of phospholamban with the Ca2+ ATPase. Proc Nat Acad Sci 100: 467 – 472.en_US
dc.identifier.citedreferenceToyoshima C, Inesi G. ( 2004 ) Structural basis of ion pumping by CA(2+)‐ATpase of the sarcoplasmic reticulum. Annu Rev Biochem 73: 269 – 292.en_US
dc.identifier.citedreferenceRensen, TL‐MlS, Ller JVM, Nissen P. ( 2004 ) Phosphoryl transfer and calcium ion occlusion in the calcium pump. Science. 304: 1672 – 1675.en_US
dc.identifier.citedreferenceZhang Z, Lewis D, Strock C, Inesi G, Nakasako M, Nomura H, Toyoshima C. ( 2000 ) Detailed characterization of the cooperative mechanism of Ca 2+binding and catalytic activation in the Ca 2+transport (SERCA) ATPase. Biochemistry 39: 8758 – 8767.en_US
dc.identifier.citedreferenceHuang Y, Li H, Bu Y. ( 2009 ) Molecular dynamics simulation exploration of cooperative migration mechanism of calcium ions in sarcoplasmic reticulum Ca 2+‐ATPase. J Comput Chem 30: 2136 – 2145.en_US
dc.identifier.citedreferenceInesi G, Lewis D, Toyoshima C, Hirata A, de Meis L. ( 2008 ) Conformational fluctuations of the Ca2+‐ATPase in the native membrane environment. J Biol Chem 283: 1189.en_US
dc.identifier.citedreferenceLee A, East J. ( 2001 ) What the structure of a calcium pump tells us about its mechanism. Biochem J 356: 665.en_US
dc.identifier.citedreferenceEinholm AP. ( 2004 ) Importance of transmembrane segment M1 of the sarcoplasmic reticulum Ca2+‐ATPase in Ca2+ occlusion and phospho‐enzyme processing. J Biol Chem 279: 15888 – 15896.en_US
dc.identifier.citedreferenceZhang Z, Toyoshima C. ( 2001 ) The role of the M6–M7 Loop (L67) in stabilization of the phosphorylation and Ca2+ binding domains of the sarcoplasmic reticulum Ca2+‐ATPase (SERCA). J Biol Chem 276: 15232 – 15239.en_US
dc.identifier.citedreferenceMusgaard M, Thogersen L, Schiott B, Tajkhorshid E. ( 2012 ) Tracing cytoplasmic Ca2+ ion and water access points in the Ca2+‐ATPase. Biophys J 102: 268 – 277.en_US
dc.identifier.citedreferenceCosta V, Carloni P. ( 2003 ) Calcium, binding to the transmembrane domain of the sarcoplasmic reticulum Ca2+‐ATPase: insights from molecular modeling. ProtStruct Funct Bioinformatics 50: 104 – 113.en_US
dc.identifier.citedreferenceSugita Y, Ikeguchi M, Toyoshima C. ( 2010 ) Relationship between Ca2+‐affinity and shielding of bulk water in the Ca2+‐pump from molecular dynamics simulations. Proc Nat Acad Sci 107: 21465 – 21469.en_US
dc.identifier.citedreferenceSugita Y, Miyashita N, Ikeguchi M, Kidera A, Toyoshima C. ( 2005 ) Protonation of the acidic residues in the transmembrane cation‐binding sites of the Ca2+ pump. J Am Chem Soc 127: 6150 – 6151.en_US
dc.identifier.citedreferenceEspinoza‐Fonseca LM, Thomas DD. ( 2011 ) Atomic‐level characterization of the activation mechanism of SERCA by calcium. PLoS ONE. 6: e26936.en_US
dc.identifier.citedreferenceInesi G, Kurzmack M, Coan C, Lewis DE. ( 1980 ) Cooperative calcium binding and ATPase activation in sarcoplasmic reticulum vesicles. J Biol Chem 255: 3025 – 3031.en_US
dc.identifier.citedreferenceInesi G, Ma H, Lewis D, Xu C. ( 2004 ) Ca2+ occlusion and gating function of Glu309 in the ADP‐fluoroaluminate analog of the Ca2+‐ ATPase phosphoenzyme intermediate. J Biol Chem 279: 31629.en_US
dc.identifier.citedreferenceSorensen TLT, Dupont YY, Vilsen BB, Andersen JPJ. ( 2000 ) Fast kinetic analysis of conformational changes in mutants of the Ca(2+)‐ ATPase of sarcoplasmic reticulum. J Biol Chem 275: 5400 – 5408.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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