Phosphorylation Regulates Mycobacterial Proteasome

Tripti Anandan; Jaeil Han; Heather Baun; Seeta Nyayapathy; Jacob T. Brown; Rebekah L. Dial; Juan A. Moltalvo; Min-Seon Kim; Seung Hwan Yang; Donald R. Ronning; Robert N. Husson; Joowon Suh; Choong-Min Kang

doi:10.1007/s12275-014-4416-2

Articles

Page Path: HOME > J. Microbiol > Volume 52(9); 2014 > Article

Research Support, Non-U.S. Gov't
Phosphorylation Regulates Mycobacterial Proteasome: Tripti Anandan ¹, Jaeil Han ¹, Heather Baun ¹, Seeta Nyayapathy ¹, Jacob T. Brown ², Rebekah L. Dial ², Juan A. Moltalvo ², Min-Seon Kim ¹, Seung Hwan Yang ³, Donald R. Ronning ³, Robert N. Husson ⁴, Joowon Suh ³, Choong-Min Kang ²; Journal of Microbiology 2014;52(9):743-754.
DOI: https://doi.org/10.1007/s12275-014-4416-2
Published online: September 2, 2014

¹Department of Biological Science, Wayne State University, Detroit, MI 48202, USA, ²Department of Biological Sciences, California State University, Stanislaus, Turlock, CA 95382, USA, ³Division of Bioscience and Bioinformatics, Myongji University, Yongin 449-728, Republic of Korea, ⁴Division of Infectious Diseases, Children’s Hospital Boston, Harvard Medical School Boston, MA 02115, USA¹Department of Biological Science, Wayne State University, Detroit, MI 48202, USA, ²Department of Biological Sciences, California State University, Stanislaus, Turlock, CA 95382, USA, ³Division of Bioscience and Bioinformatics, Myongji University, Yongin 449-728, Republic of Korea, ⁴Division of Infectious Diseases, Children’s Hospital Boston, Harvard Medical School Boston, MA 02115, USA

Corresponding author: Joowon Suh , Tel: +82-31-330-6190,
Choong-Min Kang , Tel: +82-31-330-6190,

Received: 15 July 2014 • Revised: 22 July 2014 • Accepted: 23 July 2014

prev next

69 Views
0 Download
14 Crossref
17 Scopus

Full Article

Abstract

Mycobacterium tuberculosis possesses a proteasome system that is required for the microbe to resist elimination by the host immune system. Despite the importance of the proteasome in the pathogenesis of tuberculosis, the molecular mechanisms by which proteasome activity is controlled remain largely unknown. Here, we demonstrate that the α-subunit (PrcA) of the M. tuberculosis proteasome is phosphorylated by the PknB kinase at three threonine residues (T84, T202, and T178) in a sequential manner. Furthermore, the proteasome with phosphorylated PrcA enhances the degradation of Ino1, a known proteasomal substrate, suggesting that PknB regulates the proteolytic activity of the proteasome. Previous studies showed that depletion of the proteasome and the proteasome- associated proteins decreases resistance to reactive nitrogen intermediates (RNIs) but increases resistance to hydrogen peroxide (H2O2). Here we show that PknA phosphorylation of unprocessed proteasome β-subunit (pre-PrcB) and α-subunit reduces the assembly of the proteasome complex and thereby enhances the mycobacterial resistance to H2O2 and that H2O2 stress diminishes the formation of the proteasome complex in a PknA-dependent manner. These findings indicate that phosphorylation of the M. tuberculosis proteasome not only modulates proteolytic activity of the proteasome, but also affects the proteasome complex formation contributing to the survival of M. tuberculosis under oxidative stress conditions.

Keywords: Mycobacterium tuberculosis;proteasome;phosphorylation

Figure & Data

References

Citations

Citations to this article as recorded by

Phosphoproteome modulation by nucleoside diphosphate kinase affects photosynthesis & stress tolerance of Nostoc PCC 7120
Anurag Kirti, Hema Rajaram
Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics.2025; 1873(1): 141054. CrossRef
Gene Regulatory Mechanism of Mycobacterium Tuberculosis during Dormancy
Yiduo Liu, Han Li, Dejia Dai, Jiakang He, Zhengmin Liang
Current Issues in Molecular Biology.2024; 46(6): 5825. CrossRef
Comprehensive essentiality analysis of the Mycobacterium kansasii genome by saturation transposon mutagenesis and deep sequencing
Keith Levendosky, Niklas Janisch, Luis E. N. Quadri, Sabine Ehrt
mBio.2023;[Epub] CrossRef
Nitrate-nitrite fate and oxygen sensing in dormant Mycobacterium tuberculosis: A bioinorganic approach highlighting the importance of transition metals
Eduardo H.S. Sousa, Marta S.P. Carepo, José J.G. Moura
Coordination Chemistry Reviews.2020; 423: 213476. CrossRef
The Mycobacterium tuberculosis Pup-proteasome system regulates nitrate metabolism through an essential protein quality control pathway
Samuel H. Becker, Jordan B. Jastrab, Avantika Dhabaria, Catherine T. Chaton, Jeffrey S. Rush, Konstantin V. Korotkov, Beatrix Ueberheide, K. Heran Darwin
Proceedings of the National Academy of Sciences.2019; 116(8): 3202. CrossRef
PknG supports mycobacterial adaptation in acidic environment
Ruchi Paroha, Rashmi Chourasia, Rajesh Mondal, Shivendra K. Chaurasiya
Molecular and Cellular Biochemistry.2018; 443(1-2): 69. CrossRef
Bacterial Proteasomes: Mechanistic and Functional Insights
Samuel H. Becker, K. Heran Darwin
Microbiology and Molecular Biology Reviews.2017;[Epub] CrossRef
How to control an intracellular proteolytic system: Coordinated regulatory switches in the mycobacterial Pup-proteasome system
Eyal Gur, Maayan Korman, Nir Hecht, Ofir Regev, Shai Schlussel, Nimrod Silberberg, Yifat Elharar
Biochimica et Biophysica Acta (BBA) - Molecular Cell Research.2017; 1864(12): 2253. CrossRef
Epigenetic Phosphorylation Control of Mycobacterium tuberculosis Infection and Persistence
Melissa Richard-Greenblatt, Yossef Av-Gay, William R. Jacobs Jr., Helen McShane, Valerie Mizrahi, Ian M. Orme
Microbiology Spectrum.2017;[Epub] CrossRef
Prokaryotic Ubiquitin-Like Protein and Its Ligase/Deligase Enyzmes
Cyrille L. Delley, Andreas U. Müller, Michal Ziemski, Eilika Weber-Ban
Journal of Molecular Biology.2017; 429(22): 3486. CrossRef
Phosphorylation Modulates Catalytic Activity of Mycobacterial Sirtuins
Ghanshyam S. Yadav, Sandeep K. Ravala, Neha Malhotra, Pradip K. Chakraborti
Frontiers in Microbiology.2016;[Epub] CrossRef
Pupylation-dependent and -independent proteasomal degradation in mycobacteria
Frank Imkamp, Michal Ziemski, Eilika Weber-Ban
Biomolecular Concepts.2015; 6(4): 285. CrossRef
Age-related changes in the proteostasis network in the brain of the naked mole-rat: Implications promoting healthy longevity
Judy C. Triplett, Antonella Tramutola, Aaron Swomley, Jessime Kirk, Kelly Grimes, Kaitilyn Lewis, Miranda Orr, Karl Rodriguez, Jian Cai, Jon B. Klein, Marzia Perluigi, Rochelle Buffenstein, D. Allan Butterfield
Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease.2015; 1852(10): 2213. CrossRef
Bacterial Proteasome Activator Bpa (Rv3780) Is a Novel Ring-Shaped Interactor of the Mycobacterial Proteasome
Cyrille L. Delley, Juerg Laederach, Michal Ziemski, Marcel Bolten, Daniel Boehringer, Eilika Weber-Ban, Riccardo Manganelli
PLoS ONE.2014; 9(12): e114348. CrossRef

Cite this Article

Cite this Article: export Copy Download Format; Close

Download Citation

Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.

Format:

RIS — For EndNote, ProCite, RefWorks, and most other reference management software
BibTeX — For JabRef, BibDesk, and other BibTeX-specific software

Include:

Citation for the content below
Citation and abstract for the content below

Phosphorylation Regulates Mycobacterial Proteasome

J. Microbiol. 2014;52(9):743-754. Published online September 2, 2014

DOI: https://doi.org/10.1007/s12275-014-4416-2

Related articles