Identification of a secretory heme‐binding protein from Nocardia seriolae involved in cell apoptosis

Wen, Yiming; Kang, Xu; Li, Zhiyuan; Xia, Liqun; Lu, Yishan

doi:10.1111/jfd.13654

Identification of a secretory heme‐binding protein from Nocardia seriolae involved in cell apoptosis

Journal Article · Tue Jun 07 00:00:00 EDT 2022 · Journal of Fish Diseases

DOI:https://doi.org/10.1111/jfd.13654· OSTI ID:1875945

Wen, Yiming ^[1]; Kang, Xu ^[2]; Li, Zhiyuan ^[2]; ^[1]; Lu, Yishan ^[1]

Fisheries College of Guangdong Ocean University Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture Zhanjiang China, Shenzhen Institute of Guangdong Ocean University Guangdong Provincial Engineering Research Center for Aquatic Animal Health Assessment, Shenzhen Public Service Platform for Evaluation of Marine Economic Animal Seedings Shenzhen China
Fisheries College of Guangdong Ocean University Guangdong Provincial Key Laboratory of Aquatic Animal Disease Control and Healthy Culture Zhanjiang China

Abstract

According to the whole‐genome bioinformatics analysis, a heme‐binding protein from Nocardia seriolae (HBP) was found. HBP was predicted to be a bacterial secretory protein, located at mitochondrial membrane in eukaryotic cells and have a similar protein structure with the heme‐binding protein of Mycobacterium tuberculosis , Rv0203. In this study, HBP was found to be a secretory protein and co‐localized with mitochondria in FHM cells. Quantitative analysis of mitochondrial membrane potential value, caspase‐3 activity, and transcription level of apoptosis‐related genes suggested that overexpression of HBP protein can induce cell apoptosis. In conclusion, HBP was a secretory protein which may target to mitochondria and involve in cell apoptosis in host cells. This research will promote the function study of HBP and deepen the comprehension of the virulence factors and pathogenic mechanisms of N. seriolae .

View Accepted Manuscript (Publisher)

Sponsoring Organization:: USDOE

OSTI ID:: 1875945

Journal Information:: Journal of Fish Diseases, Journal Name: Journal of Fish Diseases Journal Issue: 8 Vol. 45; ISSN 0140-7775

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (42)

Genomic characterization of Nocardia seriolae strains isolated from diseased fish Han, Hyun‐Ja; Kwak, Min‐Jung; Ha, Sung‐min MicrobiologyOpen, Vol. 8, Issue 3 https://doi.org/10.1002/mbo3.656	journal	May 2018
Another formula for calculating the gene change rate in real-time RT-PCR Chang, Shujian; Chen, Weichang; Yang, Jicheng Molecular Biology Reports, Vol. 36, Issue 8 https://doi.org/10.1007/s11033‐008‐9430‐1	journal	December 2008
Heme, iron, and the mitochondrial decay of ageing Atamna, Hani Ageing Research Reviews, Vol. 3, Issue 3 https://doi.org/10.1016/j.arr.2004.02.002	journal	July 2004
Structural and functional diversity of transient heme binding to bacterial proteins Brewitz, Hans Henning; Hagelueken, Gregor; Imhof, Diana Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1861, Issue 3 https://doi.org/10.1016/j.bbagen.2016.12.021	journal	March 2017
The role of mitochondria in cellular iron–sulfur protein biogenesis and iron metabolism Lill, Roland; Hoffmann, Bastian; Molik, Sabine Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1823, Issue 9 https://doi.org/10.1016/j.bbamcr.2012.05.009	journal	September 2012
Diverse structural approaches to haem appropriation by pathogenic bacteria Hare, Stephen A. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1865, Issue 4 https://doi.org/10.1016/j.bbapap.2017.01.006	journal	April 2017
Iron in Infection and Immunity Cassat, James E.; Skaar, Eric P. Cell Host & Microbe, Vol. 13, Issue 5 https://doi.org/10.1016/j.chom.2013.04.010	journal	May 2013
Drug targeting of heme proteins in Mycobacterium tuberculosis McLean, Kirsty J.; Munro, Andrew W. Drug Discovery Today, Vol. 22, Issue 3 https://doi.org/10.1016/j.drudis.2016.11.004	journal	March 2017
Immune responses to live and inactivated Nocardia seriolae and protective effect of recombinant interferon gamma (rIFN γ) against nocardiosis in ginbuna crucian carp, Carassius auratus langsdorfii Nayak, Sukanta Kumar; Shibasaki, Yasuhiro; Nakanishi, Teruyuki Fish & Shellfish Immunology, Vol. 39, Issue 2 https://doi.org/10.1016/j.fsi.2014.05.015	journal	August 2014
Th2 immune response by the iron-regulated protein HupB of Mycobacterium tuberculosis Choudhury, Mitali; Virivinti, Jahnavi; Kandi, Subhakar Indian Journal of Tuberculosis, Vol. 69, Issue 1 https://doi.org/10.1016/j.ijtb.2021.04.011	journal	January 2022
‘Ride on the ferrous wheel’ – The cycle of iron in macrophages in health and disease Nairz, Manfred; Schroll, Andrea; Demetz, Egon Immunobiology, Vol. 220, Issue 2 https://doi.org/10.1016/j.imbio.2014.09.010	journal	February 2015
Macrophages and Iron Metabolism Soares, Miguel P.; Hamza, Iqbal Immunity, Vol. 44, Issue 3 https://doi.org/10.1016/j.immuni.2016.02.016	journal	March 2016
The Crystal Structure of the Secreted Dimeric Form of the Hemophore HasA Reveals a Domain Swapping with an Exchanged Heme Ligand Czjzek, Mirjam; Létoffé, Sylvie; Wandersman, Cécile Journal of Molecular Biology, Vol. 365, Issue 4 https://doi.org/10.1016/j.jmb.2006.10.063	journal	January 2007
Heme Synthesis and Acquisition in Bacterial Pathogens Choby, Jacob E.; Skaar, Eric P. Journal of Molecular Biology, Vol. 428, Issue 17 https://doi.org/10.1016/j.jmb.2016.03.018	journal	August 2016
Iron in infection and immunity Nairz, Manfred; Weiss, Günter Molecular Aspects of Medicine, Vol. 75 https://doi.org/10.1016/j.mam.2020.100864	journal	October 2020
Mycobacterium tuberculosis-induced apoptotic neutrophils trigger a pro-inflammatory response in macrophages through release of heat shock protein 72, acting in synergy with the bacteria Persson, Y. Alexander Z.; Blomgran-Julinder, Robert; Rahman, Sayma Microbes and Infection, Vol. 10, Issue 3 https://doi.org/10.1016/j.micinf.2007.11.007	journal	March 2008
Siderophores: Importance in bacterial pathogenesis and applications in medicine and industry Khasheii, Behnoush; Mahmoodi, Pezhman; Mohammadzadeh, Abdolmajid Microbiological Research, Vol. 250 https://doi.org/10.1016/j.micres.2021.126790	journal	September 2021
Proteome-scale identification and characterization of mitochondria targeting proteins of Mycobacterium avium subspecies paratuberculosis: Potential virulence factors modulating host mitochondrial function Rana, Aarti; Kumar, Devender; Rub, Abdur Mitochondrion, Vol. 23 https://doi.org/10.1016/j.mito.2015.05.005	journal	July 2015
Structural basis for haem piracy from host haemopexin by Haemophilus influenzae Zambolin, Silvia; Clantin, Bernard; Chami, Mohamed Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11590	journal	May 2016
Cytochrome c: functions beyond respiration Ow, Yong-Ling P.; Green, Douglas R.; Hao, Zhenyue Nature Reviews Molecular Cell Biology, Vol. 9, Issue 7 https://doi.org/10.1038/nrm2434	journal	July 2008
Interactions between bacterial pathogens and mitochondrial cell death pathways Rudel, Thomas; Kepp, Oliver; Kozjak-Pavlovic, Vera Nature Reviews Microbiology, Vol. 8, Issue 10 https://doi.org/10.1038/nrmicro2421	journal	September 2010
Discovery and characterization of a unique mycobacterial heme acquisition system Tullius, M. V.; Harmston, C. A.; Owens, C. P. Proceedings of the National Academy of Sciences, Vol. 108, Issue 12 https://doi.org/10.1073/pnas.1009516108	journal	March 2011
Human mitochondrial holocytochrome c synthase’s heme binding, maturation determinants, and complex formation with cytochrome c San Francisco, Brian; Bretsnyder, Eric C.; Kranz, Robert G. Proceedings of the National Academy of Sciences, Vol. 110, Issue 9 https://doi.org/10.1073/pnas.1213897109	journal	November 2012
Role of the Iron Axial Ligands of Heme Carrier HasA in Heme Uptake and Release Caillet-Saguy, Célia; Piccioli, Mario; Turano, Paola Journal of Biological Chemistry, Vol. 287, Issue 32 https://doi.org/10.1074/jbc.M112.366385	journal	August 2012
The Mycobacterium tuberculosis Secreted Protein Rv0203 Transfers Heme to Membrane Proteins MmpL3 and MmpL11 Owens, Cedric P.; Chim, Nicholas; Graves, Amanda B. Journal of Biological Chemistry, Vol. 288, Issue 30 https://doi.org/10.1074/jbc.M113.453076	journal	July 2013
The Role of Iron and Siderophores in Infection, and the Development of Siderophore Antibiotics Page, Malcom G. P. Clinical Infectious Diseases, Vol. 69, Issue Supplement_7 https://doi.org/10.1093/cid/ciz825	journal	November 2019
Nocardia salmonicida nom. rev., a fish pathogen Isik, Kamil; Chun, Jongsik; Hah, Yung Chil International Journal of Systematic and Evolutionary Microbiology, Vol. 49, Issue 2 https://doi.org/10.1099/00207713‐49‐2‐833	journal	April 1999
The type III secretion system of Vibrio alginolyticus induces rapid apoptosis, cell rounding and osmotic lysis of fish cells Zhao, Zhe; Chen, Chang; Hu, Chao-Qun Microbiology, Vol. 156, Issue 9 https://doi.org/10.1099/mic.0.040626‐0	journal	September 2010
Study on the pathogenicity of Nocardia asteroides to the Formosa snakehead, Channa maculata (Lacepede), and largemouth bass, Micropterus salmoides (Lacepede) Chen, S. -C. Journal of Fish Diseases, Vol. 15, Issue 1 https://doi.org/10.1111/j.1365‐2761.1992.tb00635.x	journal	January 1992
A Permanent cell line from the Fathead Minnow (Pimephales Promelas)* Gravell, Maneth; Malsberger, R. G. Annals of the New York Academy of Sciences, Vol. 126, Issue 1 https://doi.org/10.1111/j.1749‐6632.1965.tb14302.x	journal	August 1965
Identification of a mitochondrial‐targeting secretory protein from Nocardia seriolae which induces apoptosis in fathead minnow cells Chen, Jianlin; Xia, Liqun; Wang, Wenji Journal of Fish Diseases, Vol. 42, Issue 11 https://doi.org/10.1111/jfd.13062	journal	September 2019
Identification of a secreted superoxide dismutase (SOD) from Nocardia seriolae which induces apoptosis in fathead minnow (FHM) cells Hou, Suying; Wang, Wenji; Chen, Guoquan Journal of Fish Diseases, Vol. 44, Issue 1 https://doi.org/10.1111/jfd.13268	journal	September 2020
Characterization and function study of a glutamyl endopeptidase homolog from Nocardia seriolae Wang, Wenji; Hou, Suying; Chen, Guoquan Journal of Fish Diseases, Vol. 44, Issue 6 https://doi.org/10.1111/jfd.13311	journal	November 2020
A review on the pathogenic bacterium Nocardia seriolae : aetiology, pathogenesis, diagnosis and vaccine development Liu, Yansheng; Chen, Guoquan; Xia, Liqun Reviews in Aquaculture https://doi.org/10.1111/raq.12691	journal	May 2022
Draft Genome Sequence of Nocardia seriolae ZJ0503, a Fish Pathogen Isolated from Trachinotus ovatus in China Xia, Liqun; Cai, Jia; Wang, Bei Genome Announcements, Vol. 3, Issue 1 https://doi.org/10.1128/genomeA.01223‐14	journal	February 2015
Extracellular Heme Uptake and the Challenge of Bacterial Cell Membranes Huang, Weiliang; Wilks, Angela Annual Review of Biochemistry, Vol. 86, Issue 1 https://doi.org/10.1146/annurev‐biochem‐060815‐014214	journal	June 2017
Analysis of the complete genome sequence of Nocardia seriolae UTF1, the causative agent of fish nocardiosis: The first reference genome sequence of the fish pathogenic Nocardia species Yasuike, Motoshige; Nishiki, Issei; Iwasaki, Yuki PLOS ONE, Vol. 12, Issue 3 https://doi.org/10.1371/journal.pone.0173198	journal	March 2017
Function and Characterization of an Alanine Dehydrogenase Homolog From Nocardia seriolae Chen, Guoquan; Tan, Ziyang; Liu, Yansheng Frontiers in Veterinary Science, Vol. 8 https://doi.org/10.3389/fvets.2021.801990	journal	January 2022
From Synthesis to Utilization: The Ins and Outs of Mitochondrial Heme Swenson, Samantha A.; Moore, Courtney M.; Marcero, Jason R. Cells, Vol. 9, Issue 3 https://doi.org/10.3390/cells9030579	journal	February 2020
miR-145 suppresses the proliferation, invasion and migration of NSCLC cells by regulating the BAX/BCL-2 ratio and the caspase-3 cascade Pan, Yi; Ye, Conglin; Tian, Qingshan Oncology Letters https://doi.org/10.3892/ol.2018.7863	journal	January 2018
Development of a Loop-Mediated Isothermal Amplification Assay for Rapid Detection of Nocardia salmonicida, the Causative Agent of Nocardiosis in Fish Xia, Liqun; Zhang, Honglian; Lu, Yishan Journal of Microbiology and Biotechnology, Vol. 25, Issue 3 https://doi.org/10.4014/jmb.1406.06052	journal	March 2015
Nocardia seriolae, a causative agent of systematic granuloma in spotted butterfish, Scatophagus argus, Linn [English] Pei-Chi, Wang; Ming-An, Tsai; Yu-Chi, Liang African Journal of Microbiology Research, Vol. 8, Issue 38 https://doi.org/10.5897/AJMR2014.6874	journal	September 2014

Similar Records

Zearalenone induces apoptosis of rat Sertoli cells through Fas‐Fas ligand and mitochondrial pathway

Journal Article · Mon Dec 31 23:00:00 EST 2018 · Environmental Toxicology · OSTI ID:1489294

Oxidative phosphorylation-dependent regulation of cancer cell apoptosis in response to anticancer agents

Journal Article · Wed Nov 04 23:00:00 EST 2015 · Cell Death and Disease · OSTI ID:1239287

BCL-2 proteins and apoptosis: Recent insights and unknowns

Journal Article · Tue May 15 00:00:00 EDT 2018 · Biochemical and Biophysical Research Communications · OSTI ID:23125228

Identification of a secretory heme‐binding protein from Nocardia seriolae involved in cell apoptosis

Citation Formats

References (42)

Similar Records

Related Subjects