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中国生物工程杂志

CHINA BIOTECHNOLOGY
中国生物工程杂志
中国生物工程杂志  2021, Vol. 41 Issue (7): 81-90    DOI: 10.13523/j.cb.2102035
综述     
病原细菌效应蛋白靶向宿主细胞核研究进展*
袁博鑫1,吴昊1,闫春晓1,路娟娥2,魏振平1,乔建军1,阮海华2,3,**()
1 天津大学化工学院 天津 300072
2 天津商业大学生物技术与食品科学学院 天津 300134
3 天津市食品科学与生物技术重点实验室 天津 300134
Progress of Effector Proteins of Pathogenic Bacteria Invading Host Cell Nucleus
YUAN Bo-xin1,WU Hao1,YAN Chun-xiao1,LU Juan-e2,WEI Zhen-ping1,QIAO Jian-jun1,RUAN Hai-hua2,3,**()
1 School of Chemical Engineering and Technology, Tianjin University, Tianjin 300072, China
2 Tianjin University of Commerce, Tianjin 300134, China
3 Tianjin Key Laboratory of Food Science and Biotechnology, Tianjin　300134, China
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摘要：

细胞核是细胞遗传与代谢的控制中心,调控细胞对外界的响应、代谢、生长和分化等细胞活动。在细菌感染宿主细胞过程中,个别细菌来源的效应蛋白能够靶向进入宿主细胞核,影响细胞核内基因的转录、RNA剪切、DNA修复以及染色质重组等生命活动,将这些能够进入细胞核的细菌效应蛋白称之为核调节蛋白。对病原菌分泌的核调节蛋白进入宿主细胞核的方式,以及不同病原菌的核调节蛋白调控宿主细胞的生命过程进行归纳总结,从而为深入探究病原细菌感染宿主细胞的致病机理提供理论基础。
关键词： 核调节蛋白;  病原细菌;  宿主细胞核    
Abstract:

The nucleus is the control center of cell genetics and metabolism, regulating the cell’s responses to the outside environment, metabolism, growth and differentiation and other cellular activities. Many studies have shown that in the process of bacterial infection into host cells, some effector proteins of pathogenic bacteria enter the nucleus of the host cells, affecting gene transcription, RNA splicing, DNA repair, chromatin remodeling, etc. These nucleus-targeting pathogenic effector proteins are called nucleomodulins. This review summarized the means of these nuclear regulatory proteins entering the host nucleus, aftersecreted by pathogenic bacteria. Importantly, the functions of these nucleomodulins regulating the activities of host cells were elucidated. It provides a theoretical basis to further explore the infection and pathogenic mechanisms of intracellular bacteria on host cells.
Key words: Nucleomodulins    Pathogenic bacteria    Host cell nucleus
收稿日期: 2021-02-28 出版日期: 2021-08-03
ZTFLH:  Q819  
基金资助: * 国家自然科学基金(31870122);天津市自然科学基金资助项目(18JCYBJC96000)
通讯作者: 阮海华     E-mail: ruanhaihua@tjcu.edu.cn
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袁博鑫
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魏振平
乔建军
阮海华

引用本文:

袁博鑫,吴昊,闫春晓,路娟娥,魏振平,乔建军,阮海华. 病原细菌效应蛋白靶向宿主细胞核研究进展*[J]. 中国生物工程杂志, 2021, 41(7): 81-90.

YUAN Bo-xin,WU Hao,YAN Chun-xiao,LU Juan-e,WEI Zhen-ping,QIAO Jian-jun,RUAN Hai-hua. Progress of Effector Proteins of Pathogenic Bacteria Invading Host Cell Nucleus. China Biotechnology, 2021, 41(7): 81-90.

链接本文:

https://manu60.magtech.com.cn/biotech/CN/10.13523/j.cb.2102035    或    https://manu60.magtech.com.cn/biotech/CN/Y2021/V41/I7/81

图1  Importin α/Importin β 介导的蛋白质入核机制
Nucleomodulins Organism Function Reference
TRP32 Ehrlichia chaffeensis Binds to the G-enrichment motif of host DNA and regulates transcription of related genes [11-12]
OspF Shigella Inhibits the transcription of immune factors;alters chromatin structure [13, 37]
YopM Yersinia Affects RSK1 levels and inhibits transcription of immune factors, such as IL-10 [15-17, 63]
PPE2 Mycobacterium tuberculosis Acts on macrophages and inhibits the production of NO [20]
CBU1976 Coxiella burnetii Not clear [25]
CBU1524 Coxiella burnetii Inhibits the activation of Caspase-7 and interferes with the process of apoptosis [31]
CBU1314 Coxiella burnetii Interferes with the transcription of host genes [32]
TRP47 Ehrlichia chaffeensis Binds to host GC enrichment motif and regulating transcription of essential genes [44]
TRP120 Ehrlichia chaffeensis Binds to host GC enrichment motif and activates host gene transcription [44-45]
OrfX Listeria monocytogenes Inhibites the expression of RYBP, and decreases the p53 ubiquitination mediated by MDM2 [46]
Nucleomodulins Organism Function Reference
LntA Listeria monocytogenes Targets host chromatin repressor BAHD1 and inhibited interferon gene expression [47, 64]
IpaH9.8 Shigella Interacts with U2AF35 to inhibit the transcription of immune factors [50-51]
SspH1 salmonella typhimurium Inhibits the production of the pro-inflammatory cytokine IL-8 [52]
SINC Chlamydia psittaci Interacts with nucleoporin, nucleofibrillar protein and nucleoendrimal protein [54]
AnkA Anaplasma phagocytophilum Binds to AT-rich motifs and inhibits the expression of CYBB [60-61]
RomA Legionella pneumophila Leads to methylation of histone H3 Lys 14 [60, 65]
Rv3423 Mycobacterium tuberculosis Histone acetyltrans ferases target either H3K9 or H3K14 [66]
SnpL Legionella pneumophila Interacts with SUPT5H and affects RNA polymerase II mediated transcription elongation [62]
Rv1988 Mycobacterium tuberculosis Interacts with host chromatin and affects histone methylation [67]
Rv2966c Mycobacterium tuberculosis Interacts with host chromatin and affects gene expression [68]
LegAS4 Legionella pneumophila Makes H3K4 methylation and up-regulate the transcription of heterosomal rDNA [69, 70]
BtSET bacillus thuringiensis Methylates of H3 Lys 14 and activates ribosomal DNA transcription [70]
AnkX Legionella pneumophila Interacts with PLEKHN1 and is involved in the inflammatory response [71]
AnkH Legionella pneumophila Interacts with LARP7 and affects RNA polymerase II mediated transcription elongation [72]
SP-STP Streptococcus pyogenes Phosphatase, which causes the apoptosis of infected cells [73]
NUE Chlamydia trachomatis Targets host histones modifies chromatin structure [74]
表1  代表性核调节蛋白及其主要功能
图2  志贺氏菌志贺氏菌效应蛋白OspF调控机制
图3  单增李斯特菌效应蛋白LntA调控机制
图4  嗜吞噬细胞无形体效应蛋白AnkA调控机制
[1] Ye B J, Zhou C, Guo H T, et al. Effects of BTK signalling in pathogenic microorganism infections. Journal of Cellular and Molecular Medicine, 2019, 23(10):6522-6529.
doi: 10.1111/jcmm.v23.10
[2] Colonne P M, Winchell C G, Voth D E. Hijacking host cell highways: manipulation of the host actin cytoskeleton by obligate intracellular bacterial pathogens. Frontiers in Cellular and Infection Microbiology, 2016, 6:107-115.
[3] Bomberger J M, Ye S Y, Maceachran D P, et al. A Pseudomonas aeruginosa toxin that hijacks the host ubiquitin proteolytic system. PLoS Pathogens, 2011, 7(3):e1001325.
doi: 10.1371/journal.ppat.1001325
[4] Horenkamp F A, Mukherjee S, Alix E, et al. Legionella pneumophila subversion of host vesicular transport by SidC effector proteins. Traffic (Copenhagen, Denmark), 2014, 15(5):488-499.
doi: 10.1111/tra.12158
[5] Wälde S, Kehlenbach R H. The part and the whole: functions of nucleoporins in nucleocytoplasmic transport. Trends in Cell Biology, 2010, 20(8):461-469.
doi: 10.1016/j.tcb.2010.05.001
[6] Miyamoto Y, Yamada K, Yoneda Y. Importin α: a key molecule in nuclear transport and non-transport functions. Journal of Biochemistry, 2016, 160(2):69-75.
doi: 10.1093/jb/mvw036 pmid: 27289017
[7] Miyamoto Y, Boag P R, Hime G R, et al. Regulated nucleocytoplasmic transport during gametogenesis. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, 2012, 1819(6):616-630.
doi: 10.1016/j.bbagrm.2012.01.015
[8] Lowe A R, Tang J H, Yassif J, et al. Importin-beta modulates the permeability of the nuclear pore complex in a Ran-dependent manner. Elife, 2015, 4:e04052.
doi: 10.7554/eLife.04052
[9] Bannister A J, Kouzarides T. Regulation of chromatin by histone modifications. Cell Research, 2011, 21(3):381-395.
doi: 10.1038/cr.2011.22 pmid: 21321607
[10] Bierne H, Cossart P. When bacteria target the nucleus: the emerging family of nucleomodulins. Cellular Microbiology, 2012, 14(5):622-633.
doi: 10.1111/cmi.2012.14.issue-5
[11] Farris T R, Dunphy P S, Zhu B, et al. Ehrlichia chaffeensis TRP32 is a nucleomodulin that directly regulates expression of host genes governing differentiation and proliferation. Infection and Immunity, 2016, 84(11):3182-3194.
doi: 10.1128/IAI.00657-16
[12] Farris T R, Zhu B, Wang J Y, et al. Ehrlichia chaffeensis TRP32 nucleomodulin function and localization is regulated by NEDD4L-mediated ubiquitination. Frontiers in Cellular and Infection Microbiology, 2017, 7:534.
doi: 10.3389/fcimb.2017.00534
[13] Jo K, Kim E J, Yu H J, et al. Host cell nuclear localization of Shigella flexneri effector OspF is facilitated by SUMOylation. Journal of Microbiology and Biotechnology, 2017, 27(3):610-615.
doi: 10.4014/jmb.1611.11066
[14] Navarro L, Alto N M, Dixon J E. Functions of the Yersinia effector proteins in inhibiting host immune responses. Current Opinion in Microbiology, 2005, 8(1):21-27.
pmid: 15694853
[15] Benabdillah R, Jaime Mota L, Lützelschwab S, et al. Identification of a nuclear targeting signal in YopM from Yersinia spp. Microbial Pathogenesis, 2004, 36(5):247-261.
pmid: 15043860
[16] Berneking L, Schnapp M, Rumm A, et al. Immunosuppressive Yersinia effector YopM binds DEAD box helicase DDX3 to control ribosomal S6 kinase in the nucleus of host cells. PLoS Pathogens, 2016, 12(6):e1005660.
doi: 10.1371/journal.ppat.1005660
[17] Kerschen E J, Cohen D A, Kaplan A M, et al. The plague virulence protein YopM targets the innate immune response by causing a global depletion of NK cells. Infection and Immunity, 2004, 72(8):4589-4602.
pmid: 15271919
[18] Fishbein S, van Wyk N, Warren R M, et al. Phylogeny to function: PE/PPE protein evolution and impact on Mycobacterium tuberculosis pathogenicity. Molecular Microbiology, 2015, 96(5):901-916.
doi: 10.1111/mmi.12981 pmid: 25727695
[19] Ahmed A, Das A, Mukhopadhyay S. Immunoregulatory functions and expression patterns of PE/PPE family members: Roles in pathogenicity and impact on anti-tuberculosis vaccine and drug design. IUBMB Life, 2015, 67(6):414-427.
doi: 10.1002/iub.1387 pmid: 26104967
[20] Bhat K H, Srivastava S, Kotturu S K, et al. The PPE2 protein of Mycobacterium tuberculosis translocates to host nucleus and inhibits nitric oxide production. Scientific Reports, 2017, 7:39706.
doi: 10.1038/srep39706
[21] Bhat K H, Das A, Srikantam A, et al. PPE2 protein of Mycobacterium tuberculosis may inhibit nitric oxide in activated macrophages. Annals of the New York Academy of Sciences, 2013, 1283:97-101.
doi: 10.1111/nyas.12070
[22] Mukhopadhyay S, Ghosh S. Mycobacterium tuberculosis: what is the role of PPE2 during infection. Future Microbiology, 2017, 12(6):457-460.
doi: 10.2217/fmb-2017-0038
[23] Baca O G, Paretsky D. Q fever and Coxiella burnetii: a model for host-parasite interactions. Microbiological Reviews, 1983, 47(2):127-149.
pmid: 6348504
[24] Segal G, Feldman M, Zusman T. The Icm/Dot type-IV secretion systems of Legionella pneumophila and Coxiella burnetii. FEMS Microbiology Reviews, 2005, 29(1):65-81.
pmid: 15652976
[25] Carey K L, Newton H J, Lührmann A, et al. The Coxiella burnetii Dot/Icm system delivers a unique repertoire of type IV effectors into host cells and is required for intracellular replication. PLoS Pathogens, 2011, 7(5):e1002056.
doi: 10.1371/journal.ppat.1002056
[26] Chen C, Banga S, Mertens K, et al. Large-scale identification and translocation of type IV secretion substrates by Coxiella burnetii. PNAS, 2010, 107(50):21755-21760.
doi: 10.1073/pnas.1010485107 pmid: 21098666
[27] Weber M M, Chen C, Rowin K, et al. Identification of Coxiella burnetii type IV secretion substrates required for intracellular replication and Coxiella-containing vacuole formation. Journal of Bacteriology, 2013, 195(17):3914-3924.
pmid: 23813730
[28] Klingenbeck L, Eckart R A, Berens C, et al. The Coxiella burnetii type IV secretion system substrate CaeB inhibits intrinsic apoptosis at the mitochondrial level. Cellular Microbiology, 2013, 15(4):675-687.
doi: 10.1111/cmi.12066 pmid: 23126667
[29] Bisle S, Klingenbeck L, Borges V, et al. The inhibition of the apoptosis pathway by the Coxiella burnetii effector protein CaeA requires the EK repetition motif, but is independent of survivin. Virulence, 2016, 7(4):400-412.
doi: 10.1080/21505594.2016.1139280
[30] Eckart R A, Bisle S, Schulze-Luehrmann J, et al. Antiapoptotic activity of Coxiella burnetii effector protein AnkG is controlled by p32-dependent trafficking. Infection and Immunity, 2014, 82(7):2763-2771.
doi: 10.1128/IAI.01204-13 pmid: 24733095
[31] Schäfer W, Eckart R A, Schmid B, et al. Nuclear trafficking of the anti-apoptotic Coxiella burnetii effector protein AnkG requires binding to p32 and importin-α1. Cellular Microbiology, 2017, 19(1):e12634.
doi: 10.1111/cmi.12634
[32] Weber M M, Faris R, McLachlan J, et al. Modulation of the host transcriptome by Coxiella burnetii nuclear effector Cbu1314. Microbes and Infection, 2016, 18(5):336-345.
doi: 10.1016/j.micinf.2016.01.003 pmid: 26827929
[33] Cossart P, Sansonetti P J. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science (New York, N Y), 2004, 304(5668):242-248.
doi: 10.1126/science.1090124
[34] Venkatesan M M, Goldberg M B, Rose D J, et al. Complete DNA sequence and analysis of the large virulence plasmid of Shigella flexneri. Infection and Immunity, 2001, 69(5):3271-3285.
pmid: 11292750
[35] Zurawski D V, Mitsuhata C, Mumy K L, et al. OspF and OspC1 are Shigella flexneri type III secretion system effectors that are required for postinvasion aspects of virulence. Infection and Immunity, 2006, 74(10):5964-5976.
pmid: 16988276
[36] Zurawski D V, Mumy K L, Faherty C S, et al. Shigella flexneri type III secretion system effectors OspB and OspF target the nucleus to downregulate the host inflammatory response via interactions with retinoblastoma protein. Molecular Microbiology, 2009, 71(2):350-368.
doi: 10.1111/j.1365-2958.2008.06524.x pmid: 19017275
[37] Zhao H M, Zhang Y, Wu P J, et al. The Shigella type three secretion system effector OspF invades host nucleus by binding host importin α1. World Journal of Microbiology and Biotechnology, 2019, 35(5):71-81.
doi: 10.1007/s11274-019-2635-8
[38] Newton I L G, Woyke T, Auchtung T A, et al. The Calyptogena magnifica chemoautotrophic symbiont genome. Science, 2007, 315(5814):998-1000.
pmid: 17303757
[39] Dunphy P S, Luo T, McBride J W. Ehrlichia moonlighting effectors and interkingdom interactions with the mononuclear phagocyte. Microbes and Infection, 2013, 15(14-15):1005-1016.
doi: 10.1016/j.micinf.2013.09.011 pmid: 24141087
[40] Zhu B, Kuriakose J A, Luo T, et al. Ehrlichia chaffeensis TRP120 binds a G+C-rich motif in host cell DNA and exhibits eukaryotic transcriptional activator function. Infection and Immunity, 2011, 79(11):4370-4381.
doi: 10.1128/IAI.05422-11
[41] Saijo Y, Schulze-Lefert P. Manipulation of the eukaryotic transcriptional machinery by bacterial pathogens. Cell Host & Microbe, 2008, 4(2):96-99.
[42] Lukas J, Mazna P, Valenta T, et al. Dazap2 modulates transcription driven by the Wnt effector TCF-4. Nucleic Acids Research, 2009, 37(9):3007-3020.
doi: 10.1093/nar/gkp179 pmid: 19304756
[43] Luo T, McBride J W. Ehrlichia chaffeensis TRP32 interacts with host cell targets that influence intracellular survival. Infection and Immunity, 2012, 80(7):2297-2306.
doi: 10.1128/IAI.00154-12
[44] Kibler C E, Milligan S L, Farris T R, et al. Ehrlichia chaffeensis TRP47 enters the nucleus via a MYND-binding domain-dependent mechanism and predominantly binds enhancers of host genes associated with signal transduction, cytoskeletal organization, and immune response. PLoS One, 2018, 13(11):e0205983.
doi: 10.1371/journal.pone.0205983
[45] Klema V J, Sepuru K M, Füllbrunn N, et al. Ehrlichia chaffeensis TRP120 nucleomodulin binds DNA with disordered tandem repeat domain. PLoS One, 2018, 13(4):e0194891.
doi: 10.1371/journal.pone.0194891
[46] Prokop A, Gouin E, Villiers V, et al. OrfX, a nucleomodulin required for Listeria monocytogenes virulence. MBio, 2017, 8(5):e01550.
[47] Lebreton A, Job V, Ragon M, et al. Structural basis for the inhibition of the chromatin repressor BAHD1 by the bacterial nucleomodulin LntA. MBio, 2014, 5(1):e00775-e00713.
[48] Bierne H, Tham T N, Batsche E, et al. Human BAHD1 promotes heterochromatic gene silencing. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(33):13826-13831.
[49] Lebreton A, Cossart P, Bierne H. Bacteria tune interferon responses by playing with chromatin. Virulence, 2012, 3(1):87-91.
doi: 10.4161/viru.3.1.18531 pmid: 22286704
[50] Toyotome T, Suzuki T, Kuwae A, et al. Shigella protein IpaH(9.8) is secreted from bacteria within mammalian cells and transported to the nucleus. The Journal of Biological Chemistry, 2001, 276(34):32071-32079.
doi: 10.1074/jbc.M101882200
[51] Okuda J, Toyotome T, Kataoka N, et al. Shigella effector IpaH9.8 binds to a splicing factor U2AF35 to modulate host immune responses. Biochemical and Biophysical Research Communications, 2005, 333(2):531-539.
pmid: 15950937
[52] Haraga A, Miller S I. A Salmonella enterica serovar typhimurium translocated leucine-rich repeat effector protein inhibits NF-kappa B-dependent gene expression. Infection and Immunity, 2003, 71(7):4052-4058.
doi: 10.1128/IAI.71.7.4052-4058.2003
[53] Vivoda M, Cirković I, Aleksić D, et al. Biology and intracellular life of chlamydia. Medicinski Pregled, 2011, 64(11-12):561-564.
pmid: 22369000
[54] Mojica S A, Hovis K M, Frieman M B, et al. SINC, a type III secreted protein of Chlamydia psittaci, targets the inner nuclear membrane of infected cells and uninfected neighbors. Molecular Biology of the Cell, 2015, 26(10):1918-1934.
doi: 10.1091/mbc.E14-11-1530
[55] Hänsch S, Spona D, Murra G, et al. Chlamydia-induced curvature of the host-cell plasma membrane is required for infection. PNAS, 2020, 117(5):2634-2644.
doi: 10.1073/pnas.1911528117
[56] Woldehiwet Z. The natural history of Anaplasma phagocytophilum. Veterinary Parasitology, 2010, 167(2-4):108-122.
doi: 10.1016/j.vetpar.2009.09.013 pmid: 19811878
[57] Rikihisa Y. Mechanisms of obligatory intracellular infection with Anaplasma phagocytophilum. Clinical Microbiology Reviews, 2011, 24(3):469-489.
doi: 10.1128/CMR.00064-10 pmid: 21734244
[58] Garyu J W A, Choi K S, Grab D J, et al. Defective phagocytosis in Anaplasma phagocytophilum-infected neutrophils. Infection and Immunity, 2005, 73(2):1187-1190.
doi: 10.1128/IAI.73.2.1187-1190.2005
[59] Rennoll-Bankert K E, Garcia-Garcia J C, Sinclair S H, et al. Chromatin-bound bacterial effector ankyrin a recruits histone deacetylase 1 and modifies host gene expression. Cellular Microbiology, 2015, 17(11):1640-1652.
doi: 10.1111/cmi.12461 pmid: 25996657
[60] Garcia-Garcia J C, Rennoll-Bankert K E, Pelly S, et al. Silencing of host cell CYBB gene expression by the nuclear effector AnkA of the intracellular pathogen Anaplasma phagocytophilum. Infection and Immunity, 2009, 77(6):2385-2391.
doi: 10.1128/IAI.00023-09 pmid: 19307214
[61] Dumler J S, Sinclair S H, Pappas-Brown V, et al. Genome-wide Anaplasma phagocytophilum AnkA-DNA interactions are enriched in intergenic regions and gene promoters and correlate with infection-induced differential gene expression. Frontiers in Cellular and Infection Microbiology, 2016, 6:97.
[62] Schuelein R, Spencer H, Dagley L F, et al. Targeting of RNA Polymerase II by a nuclear Legionella pneumophila Dot/Icm effector SnpL. Cellular Microbiology, 2018, 20(9):e12852.
doi: 10.1111/cmi.v20.9
[63] Wei C W, Wang Y, Du Z M, et al. The Yersinia type III secretion effector YopM is an E3 ubiquitin ligase that induced necrotic cell death by targeting NLRP3. Cell Death & Disease, 2016, 7(12):e2519.
[64] Lebreton A, Lakisic G, Job V, et al. A bacterial protein targets the BAHD1 chromatin complex to stimulate type III interferon response. Science, 2011, 331(6022):1319-1321.
doi: 10.1126/science.1200120 pmid: 21252314
[65] Rolando M, Sanulli S, Rusniok C, et al. Legionella pneumophila effector RomA uniquely modifies host chromatin to repress gene expression and promote intracellular bacterial replication. Cell Host & Microbe, 2013, 13(4):395-405.
[66] Jose L, Ramachandran R, Bhagavat R, et al. Hypothetical protein Rv3423.1 of Mycobacterium tuberculosis is a histone acetyltransferase. The FEBS Journal, 2016, 283(2):265-281.
doi: 10.1111/febs.13566
[67] Yaseen I, Kaur P, Nandicoori V K, et al. Mycobacteria modulate host epigenetic machinery by Rv1988 methylation of a non-tail arginine of histone H3. Nature Communications, 2015, 6:8922.
doi: 10.1038/ncomms9922
[68] Sharma G, Upadhyay S, Srilalitha M, et al. The interaction of mycobacterial protein Rv2966c with host chromatin is mediated through non-CpG methylation and histone H3/H4 binding. Nucleic Acids Research, 2015, 43(8):3922-3937.
doi: 10.1093/nar/gkv261
[69] Son J, Jo C H, Murugan R N, et al. Crystal structure of Legionella pneumophila type IV secretion system effector LegAS4. Biochemical and Biophysical Research Communications, 2015, 465(4):817-824.
doi: 10.1016/j.bbrc.2015.08.094
[70] Li T, Lu Q H, Wang G L, et al. SET-domain bacterial effectors target heterochromatin protein 1 to activate host rDNA transcription. EMBO Reports, 2013, 14(8):733-740.
doi: 10.1038/embor.2013.86
[71] Yu X B, Noll R R, Romero Dueñas B P, et al. Legionella effector AnkX interacts with host nuclear protein PLEKHN1. BMC Microbiology, 2018, 18(1):5-14.
doi: 10.1186/s12866-017-1147-7
[72] von Dwingelo J, Chung I Y W, Price C T, et al. Interaction of the ankyrin H core effector of Legionella with the host LARP7 component of the 7SK snRNP complex. mBio, 2019, 10(4):e01942.
[73] Agarwal S, Agarwal S, Jin H, et al. Serine/threonine phosphatase (SP-STP), secreted from Streptococcus pyogenes, is a pro-apoptotic protein. Journal of Biological Chemistry, 2012, 287(12):9147-9167.
doi: 10.1074/jbc.M111.316554
[74] Pennini M E, Perrinet S, Dautry-Varsat A, et al. Histone methylation by NUE, a novel nuclear effector of the intracellular pathogen Chlamydia trachomatis. PLoS Pathogens, 2010, 6(7):e1000995.
doi: 10.1371/journal.ppat.1000995
[1] 高兴 王景林. 基因芯片技术在病原细菌检测中的应用[J]. 中国生物工程杂志, 2010, 30(02): 100-104.
[2] 吕军鸿, 张广民. 植物抗细菌基因工程策略与应用[J]. 中国生物工程杂志, 2002, 22(4): 29-33.
[3] 鲁国东, 黄大年. 植物病原菌无毒基因分离及特性的研究进展[J]. 中国生物工程杂志, 1994, 14(4): 37-41.
[4] 黄文晋, 崔晓江, 彭学贤. 抗细菌植物基因工程进展[J]. 中国生物工程杂志, 1993, 13(6): 17-19.
[5] 莽克强. 植物基因工程进展[J]. 中国生物工程杂志, 1993, 13(5): 1-8.
[6] 张朝华, 张志雍, 葛起新. DNA探针在检测和鉴定植物病原细菌中的应用[J]. 中国生物工程杂志, 1992, 12(3): 42-46.
[7] 张朝华, 张志雍, 葛起新. DNA探针在检测和鉴定植物病原细菌中的应用[J]. 中国生物工程杂志, 1992, 12(3): 42-46.
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