A functional role of Rv1738 in Mycobacterium tuberculosis persistence suggested by racemic protein crystallography

Bunker, Richard D.; Mandal, Kalyaneswar; Bashiri, Ghader; Chaston, Jessica J.; Pentelute, Bradley L.; Lott, J. Shaun; Kent, Stephen B. H.; Baker, Edward N.

doi:10.1073/pnas.1422387112

Title: A functional role of Rv1738 in Mycobacterium tuberculosis persistence suggested by racemic protein crystallography

Journal Article · Tue Apr 07 00:00:00 EDT 2015 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1422387112· OSTI ID:1178127

Bunker, Richard D. ^[1]; Mandal, Kalyaneswar ^[2]; Bashiri, Ghader ^[1]; Chaston, Jessica J. ^[1]; Pentelute, Bradley L. ^[2]; Lott, J. Shaun ^[1]; Kent, Stephen B. H. ^[2]; Baker, Edward N. ^[1]

Univ. of Auckland, Auckland (New Zealand)
Univ. of Chicago, Chicago, IL (United States)

Racemic protein crystallography was used to determine the X-ray structure of the predicted Mycobacterium tuberculosis protein Rv1738, which had been completely recalcitrant to crystallization in its natural L-form. Native chemical ligation was used to synthesize both L-protein and D-protein enantiomers of Rv1738. Crystallization of the racemic {D-protein + L-protein} mixture was immediately successful. The resulting crystals diffracted to high resolution and also enabled facile structure determination because of the quantized phases of the data from centrosymmetric crystals. The X-ray structure of Rv1738 revealed striking similarity with bacterial hibernation factors, despite minimal sequence similarity. As a result, we predict that Rv1738, which is highly up-regulated in conditions that mimic the onset of persistence, helps trigger dormancy by association with the bacterial ribosome.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1178127

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, Issue 14; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 36 works

Citation information provided by
Web of Science

References (40)

Selective Desulfurization of Cysteine in the Presence of Cys(Acm) in Polypeptides Obtained by Native Chemical Ligation Pentelute, Brad L.; Kent, Stephen B. H. Organic Letters, Vol. 9, Issue 4 https://doi.org/10.1021/ol0630144	journal	February 2007
The structure of a centrosymmetric protein crystal Zawadzke, Laura E.; Berg, Jeremy M. Proteins: Structure, Function, and Genetics, Vol. 16, Issue 3 https://doi.org/10.1002/prot.340160308	journal	July 1993
Nonreplicating Persistence of Mycobacterium Tuberculosis Wayne, Lawrence G.; Sohaskey, Charles D. Annual Review of Microbiology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev.micro.55.1.139	journal	October 2001
Traitement statistique des erreurs dans la determination des structures cristallines Luzzati, V. Acta Crystallographica, Vol. 5, Issue 6 https://doi.org/10.1107/S0365110X52002161	journal	November 1952
PHENIX: a comprehensive Python-based system for macromolecular structure solution. Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.45787	text	January 2010
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6 https://doi.org/10.1007/s00775-020-01814-y	journal	August 2020
Protein synthesis is shutdown in dormant Mycobacterium tuberculosis and is reversed by oxygen or heat shock Hu, Yan Min; Butcher, Philip D.; Sole, Kath FEMS Microbiology Letters, Vol. 158, Issue 1 https://doi.org/10.1111/j.1574-6968.1998.tb12813.x	journal	January 1998
Solution structure of the E. coli ribosome hibernation promoting factor HPF: Implications for the relationship between structure and function Sato, Akiko; Watanabe, Takumi; Maki, Yasushi Biochemical and Biophysical Research Communications, Vol. 389, Issue 4 https://doi.org/10.1016/j.bbrc.2009.09.022	journal	November 2009
Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Krissinel, E.; Henrick, K. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904026460	journal	November 2004
Genes required for mycobacterial growth defined by high density mutagenesis: Genes required for mycobacterial growth Sassetti, Christopher M.; Boyd, Dana H.; Rubin, Eric J. Molecular Microbiology, Vol. 48, Issue 1 https://doi.org/10.1046/j.1365-2958.2003.03425.x	journal	March 2003
Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding -crystallin Sherman, D. R.; Voskuil, M.; Schnappinger, D. Proceedings of the National Academy of Sciences, Vol. 98, Issue 13 https://doi.org/10.1073/pnas.121172498	journal	June 2001
The Dormancy Regulator DosR Controls Ribosome Stability in Hypoxic Mycobacteria Trauner, Andrej; Lougheed, Kathryn E. A.; Bennett, Mark H. Journal of Biological Chemistry, Vol. 287, Issue 28 https://doi.org/10.1074/jbc.M112.364851	journal	April 2012
Total chemical synthesis of proteins Kent, Stephen B. H. Chem. Soc. Rev., Vol. 38, Issue 2 https://doi.org/10.1039/b700141j	journal	January 2009
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/s0907444910007493	journal	March 2010
Ribosome-associated factor Y adopts a fold resembling a double-stranded RNA binding domain scaffold: Solution structure of ribosome associated factor Y Ye, Keqiong; Serganov, Alexander; Hu, Weidong European Journal of Biochemistry, Vol. 269, Issue 21 https://doi.org/10.1046/j.1432-1033.2002.03222.x	journal	October 2002
Protein crystallization by surface entropy reduction: optimization of the SER strategy Cooper, David R.; Boczek, Tomasz; Grelewska, Katarzyna Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 5 https://doi.org/10.1107/S0907444907010931	journal	April 2007
The Growing Burden of Tuberculosis: Global Trends and Interactions With the HIV Epidemic Corbett, Elizabeth L.; Watt, Catherine J.; Walker, Neff Archives of Internal Medicine, Vol. 163, Issue 9 https://doi.org/10.1001/archinte.163.9.1009	journal	May 2003
Solution structure of the ribosome-associated cold shock response protein Yfia of Escherichia coli Rak, Alexey; Kalinin, Alexander; Shcherbakov, Dmitry Biochemical and Biophysical Research Communications, Vol. 299, Issue 5 https://doi.org/10.1016/S0006-291X(02)02721-3	journal	December 2002
Mycobacterial persistence requires the utilization of host cholesterol Pandey, A. K.; Sassetti, C. M. Proceedings of the National Academy of Sciences, Vol. 105, Issue 11 https://doi.org/10.1073/pnas.0711159105	journal	March 2008
Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis: DosR and the M. tuberculosis hypoxic response Park, Heui-Dong; Guinn, Kristi M.; Harrell, Maria I. Molecular Microbiology, Vol. 48, Issue 3 https://doi.org/10.1046/j.1365-2958.2003.03474.x	journal	April 2003
Crystal Enigma Mackay, Alan L. Nature, Vol. 342, Issue 6246 https://doi.org/10.1038/342133a0	journal	November 1989
How Hibernation Factors RMF, HPF, and YfiA Turn Off Protein Synthesis Polikanov, Y. S.; Blaha, G. M.; Steitz, T. A. Science, Vol. 336, Issue 6083 https://doi.org/10.1126/science.1218538	journal	May 2012
A flexible and economical medium-throughput strategy for protein production and crystallization Moreland, Nicole; Ashton, Rachael; Baker, Heather M. Acta Crystallographica Section D Biological Crystallography, Vol. 61, Issue 10 https://doi.org/10.1107/S0907444905023590	journal	September 2005
PARP1 exhibits enhanced association and catalytic efficiency with γH2A.X-nucleosome Sharma, Deepti; De Falco, Louis; Padavattan, Sivaraman Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-13641-0	journal	December 2019
Racemic crystallography-Easy crystals and easy structures: What's not to like? Matthews, Brian W. Protein Science, Vol. 18, Issue 6 https://doi.org/10.1002/pro.125	journal	June 2009
Synthesis of Peptides and Proteins without Cysteine Residues by Native Chemical Ligation Combined with Desulfurization Yan, Liang Z.; Dawson, Philip E. Journal of the American Chemical Society, Vol. 123, Issue 4 https://doi.org/10.1021/ja003265m	journal	January 2001
Synthesis of proteins by native chemical ligation Dawson, P.; Muir, T.; Clark-Lewis, I. Science, Vol. 266, Issue 5186 https://doi.org/10.1126/science.7973629	journal	November 1994
Cavin1 intrinsically disordered domains are essential for fuzzy electrostatic interactions and caveola formation Tillu, Vikas A.; Rae, James; Gao, Ya Nature Communications, Vol. 12, Issue 1 https://doi.org/10.1038/s41467-021-21035-4	journal	February 2021
Crystallographic ab initio protein structure solution below atomic resolution Rodríguez, Dayté D.; Grosse, Christian; Himmel, Sebastian Nature Methods, Vol. 6, Issue 9 https://doi.org/10.1038/nmeth.1365	journal	August 2009
Racemic Protein Crystallography Yeates, Todd O.; Kent, Stephen B. H. Annual Review of Biophysics, Vol. 41, Issue 1 https://doi.org/10.1146/annurev-biophys-050511-102333	journal	June 2012
Why protein crystals favour some space-groups over others Wukovitz, Stephanie W.; Yeates, Todd O. Nature Structural & Molecular Biology, Vol. 2, Issue 12 https://doi.org/10.1038/nsb1295-1062	journal	December 1995
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Structural basis for the control of translation initiation during stress Vila-Sanjurjo, Antón; Schuwirth, Barbara-S; Hau, Cathy W. Nature Structural & Molecular Biology, Vol. 11, Issue 11 https://doi.org/10.1038/nsmb850	journal	October 2004
Inhibition of Respiration by Nitric Oxide Induces a Mycobacterium tuberculosis Dormancy Program Voskuil, Martin I.; Schnappinger, Dirk; Visconti, Kevin C. Journal of Experimental Medicine, Vol. 198, Issue 5 https://doi.org/10.1084/jem.20030205	journal	September 2003
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Structure of Vibrio cholerae ribosome hibernation promoting factor De Bari, Heather; Berry, Edward A. Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 69, Issue 3 https://doi.org/10.1107/S1744309113000961	journal	February 2013
The Buccaneer software for automated model building. 1. Tracing protein chains Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 9 https://doi.org/10.1107/s0907444906022116	journal	August 2006
The Pfam protein families database Finn, Robert D.; Mistry, Jaina; Tate, John Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp985	journal	November 2009
Mechanisms of latency in Mycobacterium tuberculosis Parrish, Nikki M.; Dick, James D.; Bishai, William R. Trends in Microbiology, Vol. 6, Issue 3 https://doi.org/10.1016/S0966-842X(98)01216-5	journal	March 1998
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007

Cited By (5)

Novel protein science enabled by total chemical synthesis Kent, Stephen B. H. Protein Science, Vol. 28, Issue 2 https://doi.org/10.1002/pro.3533	journal	December 2018
Traceless β-mercaptan-assisted activation of valinyl benzimidazolinones in peptide ligations Wang, Yinglu; Han, Lin; Yuan, Ning Chemical Science, Vol. 9, Issue 7 https://doi.org/10.1039/c7sc04148a	journal	January 2018
Regulation of Three Virulence Strategies of Mycobacterium tuberculosis: A Success Story Zondervan, Niels; van Dam, Jesse; Schaap, Peter International Journal of Molecular Sciences, Vol. 19, Issue 2 https://doi.org/10.3390/ijms19020347	journal	January 2018
Mycobacterial Dormancy Systems and Host Responses in Tuberculosis Peddireddy, Vidyullatha; Doddam, Sankara Narayana; Ahmed, Niyaz Frontiers in Immunology, Vol. 8 https://doi.org/10.3389/fimmu.2017.00084	journal	February 2017
Racemic crystal structures of peptide toxins, GsMTx4 prepared by protein total synthesis Qu, Qian; Gao, Shuai; Li, Yi-Ming Journal of Peptide Science, Vol. 24, Issue 8-9 https://doi.org/10.1002/psc.3112	journal	July 2018

Similar Records

Potent 1,2,4-Triazino[5,6 b ]indole-3-thioether Inhibitors of the Kanamycin Resistance Enzyme Eis from Mycobacterium tuberculosis

Journal Article · Fri Mar 30 00:00:00 EDT 2018 · ACS Infectious Diseases · OSTI ID:1178127

Ngo, Huy X.; Green, Keith D.; Gajadeera, Chathurada S.; +8 more

Racemic crystallography of synthetic protein enantiomers used to determine the X-ray structure of plectasin by direct methods

Journal Article · Tue Jun 30 00:00:00 EDT 2009 · Protein Sci. · OSTI ID:1178127

Mandal, Kalyaneswar; Pentelute, Brad L; Tereshko, Valentina; +4 more

Mycobacterium tuberculosis Universal Stress Protein Rv2623 Regulates Bacillary Growth by ATP Binding: Requirement for Establishing Chronic Persistent Infection

Journal Article · Thu Jan 01 00:00:00 EST 2009 · PLoS Pathogens · OSTI ID:1178127

Drumm, J; Mi, K; Bilder, P; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
racemic protein crystallography
Mycobacterium tuberculosis
ribosome binding
dormancy
protein structure

Title: A functional role of Rv1738 in Mycobacterium tuberculosis persistence suggested by racemic protein crystallography

Citation Formats

References (40)

Cited By (5)

Similar Records

Related Subjects