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A Basic Sequence in STIM1 Promotes Ca2+ Influx by Interacting with the C-Terminal Acidic Coiled Coil of Orai1

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    A Basic Sequence in STIM1 Promotes Ca2+ Influx by Interacting with the C-Terminal Acidic Coiled Coil of Orai1
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    Department of Chemistry and Chemical Biology, Cornell University, Ithaca, New York 14853
    *To whom correspondence should be addressed: Department of Chemistry and Chemical Biology, Baker Laboratory, Cornell University, Ithaca, NY 14853-1301. Phone: (607) 255-4095. Fax: (607) 255-4137. E-mail: [email protected]
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    Biochemistry

    Cite this: Biochemistry 2010, 49, 6, 1067–1071
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    https://doi.org/10.1021/bi901936q
    Published January 14, 2010
    Copyright © 2010 American Chemical Society
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    Store-operated Ca2+ entry (SOCE) is a ubiquitous signaling process in eukaryotic cells in which the endoplasmic reticulum (ER)-localized Ca2+ sensor, STIM1, activates the plasma membrane-localized Ca2+ release-activated Ca2+ (CRAC) channel, Orai1, in response to emptying of ER Ca2+ stores. In efforts to understand this activation mechanism, we recently identified an acidic coiled-coil region in the C-terminus of Orai1 that contributes to physical association between these two proteins, as measured by fluorescence resonance energy transfer, and is necessary for Ca2+ influx, as measured by an intracellular Ca2+ indicator. Here, we present evidence that a positively charged sequence of STIM1 in its CRAC channel activating domain, human residues 384−386, is necessary for activation of SOCE, most likely because this sequence interacts directly with the acidic coiled coil of Orai1 to gate Ca2+ influx. We find that mutation to remove positive charges in these residues in STIM1 prevents its stimulated association with wild-type Orai1. However, association does occur between this mutant STIM1 and Orai1 that is mutated to remove negative charges in its C-terminal coiled coil, indicating that other structural features are sufficient for this interaction. Despite this physical association, we find that thapsigargin fails to activate SOCE following coexpression of mutant STIM1 with either wild type or mutant Orai1, implicating STIM1 residues 384−386 in transmission of the Ca2+ gating signal to Orai1 following store depletion.

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    Population distribution of Ca2+ levels in cells expressing mutant and wild-type STIM1 and Orai1 (Figure S1). This material is available free of charge via the Internet at http://pubs.acs.org.

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    This article is cited by 68 publications.

    1. Valerie Walker. The Molecular Biology of Placental Transport of Calcium to the Human Foetus. International Journal of Molecular Sciences 2025, 26 (1) , 383. https://doi.org/10.3390/ijms26010383
    2. Matthias Sallinger, Herwig Grabmayr, Christina Humer, Daniel Bonhenry, Christoph Romanin, Rainer Schindl, Isabella Derler. Activation mechanisms and structural dynamics of STIM proteins. The Journal of Physiology 2024, 602 (8) , 1475-1507. https://doi.org/10.1113/JP283828
    3. Hadas Achildiev Cohen, Elia Zomot, Tomer Nataniel, Ruslana Militsin, Raz Palty. The SOAR of STIM1 interacts with plasma membrane lipids to form ER-PM contact sites. Cell Reports 2023, 42 (3) , 112238. https://doi.org/10.1016/j.celrep.2023.112238
    4. Christina Humer, Christoph Romanin, Carmen Höglinger. Highlighting the Multifaceted Role of Orai1 N-Terminal- and Loop Regions for Proper CRAC Channel Functions. Cells 2022, 11 (3) , 371. https://doi.org/10.3390/cells11030371
    5. Stijn van Dorp, Ruoyi Qiu, Ucheor B Choi, Minnie M Wu, Michelle Yen, Michael Kirmiz, Axel T Brunger, Richard S Lewis. Conformational dynamics of auto-inhibition in the ER calcium sensor STIM1. eLife 2021, 10 https://doi.org/10.7554/eLife.66194
    6. Elena Conte, Paola Imbrici, Paola Mantuano, Maria Antonietta Coppola, Giulia Maria Camerino, Annamaria De Luca, Antonella Liantonio. Alteration of STIM1/Orai1-Mediated SOCE in Skeletal Muscle: Impact in Genetic Muscle Diseases and Beyond. Cells 2021, 10 (10) , 2722. https://doi.org/10.3390/cells10102722
    7. Jose Sanchez-Collado, Jose J. Lopez, Isaac Jardin, Gines M. Salido, Juan A. Rosado. Cross-Talk Between the Adenylyl Cyclase/cAMP Pathway and Ca2+ Homeostasis. 2020, 73-116. https://doi.org/10.1007/112_2020_55
    8. Sampath Bhuvaneshwari, Kavitha Sankaranarayanan. Structural and Mechanistic Insights of CRAC Channel as a Drug Target in Autoimmune Disorder. Current Drug Targets 2019, 21 (1) , 55-75. https://doi.org/10.2174/1389450120666190926150258
    9. Victoria Lunz, Christoph Romanin, Irene Frischauf. STIM1 activation of Orai1. Cell Calcium 2019, 77 , 29-38. https://doi.org/10.1016/j.ceca.2018.11.009
    10. M. Bulla, G. Gyimesi, J.H. Kim, R. Bhardwaj, M.A. Hediger, M. Frieden, N. Demaurex. ORAI1 channel gating and selectivity is differentially altered by natural mutations in the first or third transmembrane domain. The Journal of Physiology 2019, 597 (2) , 561-582. https://doi.org/10.1113/JP277079
    11. Sisi Zheng, Guolin Ma, Lian He, Tian Zhang, Jia Li, Xiaoman Yuan, Nhung T. Nguyen, Yun Huang, Xiaoyan Zhang, Ping Gao, Robert Nwokonko, Donald L. Gill, Hao Dong, Yubin Zhou, Youjun Wang, . Identification of molecular determinants that govern distinct STIM2 activation dynamics. PLOS Biology 2018, 16 (11) , e2006898. https://doi.org/10.1371/journal.pbio.2006898
    12. Nhung T. Nguyen, Weidong Han, Wen‐Ming Cao, Youjun Wang, Shufan Wen, Yun Huang, Minyong Li, Lupei Du, Yubin Zhou. Store‐Operated Calcium Entry Mediated by ORAI and STIM. Comprehensive Physiology 2018, 8 (3) , 981-1002. https://doi.org/10.1002/j.2040-4603.2018.tb00032.x
    13. Matthew J. Novello, Jinhui Zhu, Qingping Feng, Mitsuhiko Ikura, Peter B. Stathopulos. Structural elements of stromal interaction molecule function. Cell Calcium 2018, 73 , 88-94. https://doi.org/10.1016/j.ceca.2018.04.006
    14. Nhung T. Nguyen, Weidong Han, Wen‐Ming Cao, Youjun Wang, Shufan Wen, Yun Huang, Minyong Li, Lupei Du, Yubin Zhou. Store‐Operated Calcium Entry Mediated by ORAI and STIM. 2018, 981-1002. https://doi.org/10.1002/cphy.c170031
    15. Jill L. Thompson, Yue Zhao, Peter B. Stathopulos, Alan Grossfield, Trevor J. Shuttleworth. Phosphorylation-mediated structural changes within the SOAR domain of stromal interaction molecule 1 enable specific activation of distinct Orai channels. Journal of Biological Chemistry 2018, 293 (9) , 3145-3155. https://doi.org/10.1074/jbc.M117.819078
    16. Jing-hong Yao, Zi-jian Liu, Jian-hua Yi, Jun Wang, Ya-nan Liu. Hepatitis B Virus X Protein Upregulates Intracellular Calcium Signaling by Binding C-terminal of Orail Protein. Current Medical Science 2018, 38 (1) , 26-34. https://doi.org/10.1007/s11596-018-1843-z
    17. Marek K. Korzeniowski, Eva Wisniewski, Barbara Baird, David A. Holowka, Tamas Balla. Molecular anatomy of the early events in STIM1 activation – oligomerization or conformational change?. Journal of Cell Science 2017, 130 (17) , 2821-2832. https://doi.org/10.1242/jcs.205583
    18. Raz Palty, Zhu Fu, Ehud Y. Isacoff. Sequential Steps of CRAC Channel Activation. Cell Reports 2017, 19 (9) , 1929-1939. https://doi.org/10.1016/j.celrep.2017.05.025
    19. Jonathan Pacheco, Laura Dominguez, A. Bohórquez-Hernández, Alexander Asanov, Luis Vaca. A cholesterol-binding domain in STIM1 modulates STIM1-Orai1 physical and functional interactions. Scientific Reports 2016, 6 (1) https://doi.org/10.1038/srep29634
    20. David Holowka, Marcus Wilkes, Christopher Stefan, Barbara Baird. Roles for Ca2+ mobilization and its regulation in mast cell functions: recent progress. Biochemical Society Transactions 2016, 44 (2) , 505-509. https://doi.org/10.1042/BST20150273
    21. Isabella Derler, Isaac Jardin, Christoph Romanin. Molecular mechanisms of STIM/Orai communication. American Journal of Physiology-Cell Physiology 2016, 310 (8) , C643-C662. https://doi.org/10.1152/ajpcell.00007.2016
    22. Irene Frischauf, Marc Fahrner, Isaac Jardín, Christoph Romanin. The STIM1: Orai Interaction. 2016, 25-46. https://doi.org/10.1007/978-3-319-26974-0_2
    23. Marek K. Korzeniowski, Barbara Baird, David Holowka, . STIM1 activation is regulated by a 14 amino acid sequence adjacent to the CRAC activation domain. AIMS Biophysics 2016, 3 (1) , 99-118. https://doi.org/10.3934/biophy.2016.1.99
    24. Guolin Ma, Ming Wei, Lian He, Chongxu Liu, Bo Wu, Shenyuan L. Zhang, Ji Jing, Xiaowen Liang, Alessandro Senes, Peng Tan, Siwei Li, Aomin Sun, Yunchen Bi, Ling Zhong, Hongjiang Si, Yuequan Shen, Minyong Li, Mi-Sun Lee, Weibin Zhou, Junfeng Wang, Youjun Wang, Yubin Zhou. Inside-out Ca2+ signalling prompted by STIM1 conformational switch. Nature Communications 2015, 6 (1) https://doi.org/10.1038/ncomms8826
    25. Rodrigo S. Lacruz, Stefan Feske. Diseases caused by mutations in ORAI1 and STIM1. Annals of the New York Academy of Sciences 2015, 1356 (1) , 45-79. https://doi.org/10.1111/nyas.12938
    26. Murali Prakriya, Richard S. Lewis. Store-Operated Calcium Channels. Physiological Reviews 2015, 95 (4) , 1383-1436. https://doi.org/10.1152/physrev.00020.2014
    27. Raz Palty, Cherise Stanley, Ehud Y Isacoff. Critical role for Orai1 C-terminal domain and TM4 in CRAC channel gating. Cell Research 2015, 25 (8) , 963-980. https://doi.org/10.1038/cr.2015.80
    28. Anshul Rana, Michelle Yen, Amir Masoud Sadaghiani, Seth Malmersjö, Chan Young Park, Ricardo E. Dolmetsch, Richard S. Lewis. Alternative splicing converts STIM2 from an activator to an inhibitor of store-operated calcium channels. Journal of Cell Biology 2015, 209 (5) , 653-670. https://doi.org/10.1083/jcb.201412060
    29. Leidamarie Tirado-Lee, Megumi Yamashita, Murali Prakriya, . Conformational Changes in the Orai1 C-Terminus Evoked by STIM1 Binding. PLOS ONE 2015, 10 (6) , e0128622. https://doi.org/10.1371/journal.pone.0128622
    30. Mate Maus, Amit Jairaman, Peter B. Stathopulos, Martin Muik, Marc Fahrner, Carl Weidinger, Melina Benson, Sebastian Fuchs, Stephan Ehl, Christoph Romanin, Mitsuhiko Ikura, Murali Prakriya, Stefan Feske. Missense mutation in immunodeficient patients shows the multifunctional roles of coiled-coil domain 3 (CC3) in STIM1 activation. Proceedings of the National Academy of Sciences 2015, 112 (19) , 6206-6211. https://doi.org/10.1073/pnas.1418852112
    31. Jill L. Thompson, Trevor J. Shuttleworth. Anchoring protein AKAP79‐mediated PKA phosphorylation of STIM1 determines selective activation of the ARC channel, a store‐independent Orai channel. The Journal of Physiology 2015, 593 (3) , 559-572. https://doi.org/10.1113/jphysiol.2014.284182
    32. Colin A. Leech, Richard F. Kopp, Louis H. Philipson, Michael W. Roe. β Cell Store-Operated Ion Channels. 2015, 337-368. https://doi.org/10.1007/978-94-007-6686-0_40
    33. Anna Amcheslavsky, Mona L. Wood, Andriy V. Yeromin, Ian Parker, J. Alfredo Freites, Douglas J. Tobias, Michael D. Cahalan. Molecular Biophysics of Orai Store-Operated Ca2+ Channels. Biophysical Journal 2015, 108 (2) , 237-246. https://doi.org/10.1016/j.bpj.2014.11.3473
    34. Ann Hye-Ryong Shim, Leidamarie Tirado-Lee, Murali Prakriya. Structural and Functional Mechanisms of CRAC Channel Regulation. Journal of Molecular Biology 2015, 427 (1) , 77-93. https://doi.org/10.1016/j.jmb.2014.09.021
    35. Eunan Hendron, Xizhuo Wang, Yandong Zhou, Xiangyu Cai, Jun-Ichi Goto, Katsuhiko Mikoshiba, Yoshihiro Baba, Tomohiro Kurosaki, Youjun Wang, Donald L. Gill. Potent functional uncoupling between STIM1 and Orai1 by dimeric 2-aminodiphenyl borinate analogs. Cell Calcium 2014, 56 (6) , 482-492. https://doi.org/10.1016/j.ceca.2014.10.005
    36. Xizhuo Wang, Youjun Wang, Yandong Zhou, Eunan Hendron, Salvatore Mancarella, Mark D Andrake, Brad S Rothberg, Jonathan Soboloff, Donald L Gill. Distinct Orai-coupling domains in STIM1 and STIM2 define the Orai-activating site. Nature Communications 2014, 5 (1) https://doi.org/10.1038/ncomms4183
    37. Doriana Misceo, Asbjørn Holmgren, William E. Louch, Pål A. Holme, Masahiro Mizobuchi, Raul J. Morales, André Maues De Paula, Asbjørg Stray-Pedersen, Robert Lyle, Bjørn Dalhus, Geir Christensen, Helge Stormorken, Geir E. Tjønnfjord, Eirik Frengen. A Dominant STIM1 Mutation Causes Stormorken Syndrome. Human Mutation 2014, 35 (5) , 556-564. https://doi.org/10.1002/humu.22544
    38. Vasyl Nesin, Graham Wiley, Maria Kousi, E-Ching Ong, Thomas Lehmann, David J. Nicholl, Mohnish Suri, Nortina Shahrizaila, Nicholas Katsanis, Patrick M. Gaffney, Klaas J. Wierenga, Leonidas Tsiokas. Activating mutations in STIM1 and ORAI1 cause overlapping syndromes of tubular myopathy and congenital miosis. Proceedings of the National Academy of Sciences 2014, 111 (11) , 4197-4202. https://doi.org/10.1073/pnas.1312520111
    39. Colin A. Leech, Richard F. Kopp, Louis H. Philipson, Michael Wm. Roe. Beta Cell Store-Operated Ion Channels. 2014, 1-31. https://doi.org/10.1007/978-94-007-6884-0_40-2
    40. Peter B. Stathopulos, Rainer Schindl, Marc Fahrner, Le Zheng, Geneviève M. Gasmi-Seabrook, Martin Muik, Christoph Romanin, Mitsuhiko Ikura. STIM1/Orai1 coiled-coil interplay in the regulation of store-operated calcium entry. Nature Communications 2013, 4 (1) https://doi.org/10.1038/ncomms3963
    41. Robert Hooper, Elsie Samakai, Joseph Kedra, Jonathan Soboloff. Multifaceted roles of STIM proteins. Pflügers Archiv - European Journal of Physiology 2013, 465 (10) , 1383-1396. https://doi.org/10.1007/s00424-013-1270-8
    42. Jill L Thompson, Trevor J Shuttleworth. Exploring the unique features of the ARC channel, a Store-independent Orai channel. Channels 2013, 7 (5) , 364-373. https://doi.org/10.4161/chan.26156
    43. Marc Fahrner, Isabella Derler, Isaac Jardin, Christoph Romanin. The STIM1/Orai signaling machinery. Channels 2013, 7 (5) , 330-343. https://doi.org/10.4161/chan.26742
    44. Patrick J. Shaw, Bin Qu, Markus Hoth, Stefan Feske. Molecular regulation of CRAC channels and their role in lymphocyte function. Cellular and Molecular Life Sciences 2013, 70 (15) , 2637-2656. https://doi.org/10.1007/s00018-012-1175-2
    45. Jill L. Thompson, Trevor J. Shuttleworth. Molecular basis of activation of the arachidonate‐regulated Ca 2+ (ARC) channel, a store‐independent Orai channel, by plasma membrane STIM1. The Journal of Physiology 2013, 591 (14) , 3507-3523. https://doi.org/10.1113/jphysiol.2013.256784
    46. Brad S. Rothberg, Youjun Wang, Donald L. Gill. Orai Channel Pore Properties and Gating by STIM: Implications from the Orai Crystal Structure. Science Signaling 2013, 6 (267) https://doi.org/10.1126/scisignal.2003971
    47. Murali Prakriya. Store-Operated Orai Channels. 2013, 1-32. https://doi.org/10.1016/B978-0-12-407870-3.00001-9
    48. Aparna Gudlur, Yubin Zhou, Patrick G. Hogan. STIM–ORAI Interactions That Control the CRAC Channel. 2013, 33-58. https://doi.org/10.1016/B978-0-12-407870-3.00002-0
    49. Fang Yu, Lu Sun, Satanay Hubrack, Senthil Selvaraj, Khaled Machaca. Intramolecular shielding maintains STIM1 in an inactive conformation. Journal of Cell Science 2013, 22 https://doi.org/10.1242/jcs.117200
    50. Martin Muik, Rainer Schindl, Marc Fahrner, Christoph Romanin. Ca2+ release-activated Ca2+ (CRAC) current, structure, and function. Cellular and Molecular Life Sciences 2012, 69 (24) , 4163-4176. https://doi.org/10.1007/s00018-012-1072-8
    51. Jonathan Soboloff, Brad S. Rothberg, Muniswamy Madesh, Donald L. Gill. STIM proteins: dynamic calcium signal transducers. Nature Reviews Molecular Cell Biology 2012, 13 (9) , 549-565. https://doi.org/10.1038/nrm3414
    52. Xue Yang, Hao Jin, Xiangyu Cai, Siwei Li, Yuequan Shen. Structural and mechanistic insights into the activation of Stromal interaction molecule 1 (STIM1). Proceedings of the National Academy of Sciences 2012, 109 (15) , 5657-5662. https://doi.org/10.1073/pnas.1118947109
    53. Wei-Wei Shen, Nicolas Demaurex. Morphological and functional aspects of STIM1-dependent assembly and disassembly of store-operated calcium entry complexes. Biochemical Society Transactions 2012, 40 (1) , 112-118. https://doi.org/10.1042/BST20110620
    54. Rainer Schindl, Marc Fahrner, Martin Muik, Christoph Romanin. The STIM-Orai Pathway. 2012, 45-56. https://doi.org/10.1007/978-3-7091-0962-5_4
    55. Isabella Derler, Josef Madl, Gerhard Schütz, Christoph Romanin. Structure, Regulation and Biophysics of ICRAC, STIM/Orai1. 2012, 383-410. https://doi.org/10.1007/978-94-007-2888-2_16
    56. Salvatore Mancarella, Youjun Wang, Xiaoxiang Deng, Gavin Landesberg, Rosario Scalia, Reynold A. Panettieri, Karthik Mallilankaraman, Xiang D. Tang, Muniswamy Madesh, Donald L. Gill. Hypoxia-induced Acidosis Uncouples the STIM-Orai Calcium Signaling Complex. Journal of Biological Chemistry 2011, 286 (52) , 44788-44798. https://doi.org/10.1074/jbc.M111.303081
    57. Wei-Wei Shen, Maud Frieden, Nicolas Demaurex. Local Cytosolic Ca2+ Elevations Are Required for Stromal Interaction Molecule 1 (STIM1) De-oligomerization and Termination of Store-operated Ca2+ Entry. Journal of Biological Chemistry 2011, 286 (42) , 36448-36459. https://doi.org/10.1074/jbc.M111.269415
    58. Wei‐Wei Shen, Maud Frieden, Nicolas Demaurex. Remodelling of the endoplasmic reticulum during store‐operated calcium entry. Biology of the Cell 2011, 103 (8) , 365-380. https://doi.org/10.1042/BC20100152
    59. Nathaniel Calloway, Tristan Owens, Kathryn Corwith, William Rodgers, David Holowka, Barbara Baird. Stimulated association of STIM1 and Orai1 is regulated by the balance of PtdIns(4,5) P 2 between distinct membrane pools. Journal of Cell Science 2011, 124 (15) , 2602-2610. https://doi.org/10.1242/jcs.084178
    60. Silvia Carrasco, Tobias Meyer. STIM Proteins and the Endoplasmic Reticulum-Plasma Membrane Junctions. Annual Review of Biochemistry 2011, 80 (1) , 973-1000. https://doi.org/10.1146/annurev-biochem-061609-165311
    61. Elizabeth Pham, Evan Mills, Kevin Truong. A Synthetic Photoactivated Protein to Generate Local or Global Ca2+ Signals. Chemistry & Biology 2011, 18 (7) , 880-890. https://doi.org/10.1016/j.chembiol.2011.04.014
    62. Martin Muik, Marc Fahrner, Rainer Schindl, Peter Stathopulos, Irene Frischauf, Isabella Derler, Peter Plenk, Barbara Lackner, Klaus Groschner, Mitsuhiko Ikura, Christoph Romanin. STIM1 couples to ORAI1 via an intramolecular transition into an extended conformation. The EMBO Journal 2011, 30 (9) , 1678-1689. https://doi.org/10.1038/emboj.2011.79
    63. Sean R. Collins, Tobias Meyer. Evolutionary origins of STIM1 and STIM2 within ancient Ca2+ signaling systems. Trends in Cell Biology 2011, 21 (4) , 202-211. https://doi.org/10.1016/j.tcb.2011.01.002
    64. Justyna Ciolek, Arhamatoulaye Maïga, Elodie Marcon, Denis Servent, Nicolas Gilles. Pharmacological characterization of zinc and copper interaction with the human alpha1A-adrenoceptor. European Journal of Pharmacology 2011, 655 (1-3) , 1-8. https://doi.org/10.1016/j.ejphar.2010.12.042
    65. Hong-Tao Ma, Michael A. Beaven. Regulators of Ca2+ Signaling in Mast Cells: Potential Targets for Treatment of Mast Cell-Related Diseases?. 2011, 62-90. https://doi.org/10.1007/978-1-4419-9533-9_5
    66. Marek K. Korzeniowski, Isabel Martín Manjarrés, Peter Varnai, Tamas Balla. Activation of STIM1-Orai1 Involves an Intramolecular Switching Mechanism. Science Signaling 2010, 3 (148) https://doi.org/10.1126/scisignal.2001122
    67. Youjun Wang, Xiaoxiang Deng, Donald L. Gill. Calcium Signaling by STIM and Orai: Intimate Coupling Details Revealed. Science Signaling 2010, 3 (148) https://doi.org/10.1126/scisignal.3148pe42
    68. J. Joe Hull, Jae Min Lee, Shogo Matsumoto. Functional role of STIM1 and Orai1 in silkmoth ( Bombyx mori ) sex pheromone production. Communicative & Integrative Biology 2010, 3 (3) , 240-242. https://doi.org/10.4161/cib.3.3.11394
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    Biochemistry

    Cite this: Biochemistry 2010, 49, 6, 1067–1071
    Click to copy citationCitation copied!
    https://doi.org/10.1021/bi901936q
    Published January 14, 2010
    Copyright © 2010 American Chemical Society
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