Transcriptome analysis of <i>Drosophila</i> S2 cells infected by <i>Listeria innocua</i>

WU Kunzhong; LI Rongsong; CAO Yang; HUANG Zhijun; TIAN Ling

doi:10.7671/j.issn.1001-411X.202001023

Journal of South China Agricultural University > 2020 > 41(5): 17-26. > DOI: 10.7671/j.issn.1001-411X.202001023

WU Kunzhong, LI Rongsong, CAO Yang, et al. Transcriptome analysis of Drosophila S2 cells infected by Listeria innocua[J]. Journal of South China Agricultural University, 2020, 41(5): 17-26. DOI: 10.7671/j.issn.1001-411X.202001023

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Transcriptome analysis of Drosophila S2 cells infected by Listeria innocua

College of Animal Science, South China Agricultural University/Guangdong Provincial Key Laboratory of Agro-animal Genomics and Molecular Breeding/Guangdong Provincial Sericulture and Mulberry Engineering Research Center, Guangzhou 510642, China

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Received Date: January 12, 2020
Available Online: May 17, 2023

Graphical Abstract

Abstract

Abstract

Objective
Listeria innocua is a non-pathogenic bacterium from the Listeria genus, which harbors the virulence factors evolved from the same ancestor with the pathogenic bacterium L. monocytogenes. This study aims to investigate the transcriptional variations of host cells after L. innocuainfection, and provide a basis for host regulation and prevention of damage from L. monocytogenes.

Method
We used L. innocua to infect Drosophila melanogaster S2 cells and analyzed the change of gene expression in Drosophila S2 cells by transcriptome sequencing. The differentially expressed genes in Drosophila S2 cells infected by L. innocua was verified by qPCR.

Result
The Toll/Imd signaling pathways were significantly upregulated in Drosophila S2 cells after L. innocua infection for three hours, while the phagosome and Vibrio cholerae infection signaling pathways were significantly downregulated. The antimicrobial peptide genes including DmDef (DmDefensin), DmDro (DmDrosomycin), DmDpt A (DmDptericin A), DmDpt B (DmDptericin B), DmMtk (DmMetchnikowin), DmCec A2 (DmCecropin A2), DmAtt A (DmAttacin A), DmAtt B (DmAttacin B), DmAtt D (DmAttacin D), and DmCec B (DmCecropin B) were significantly induced after L. innocua infection. Among them, the most upregulated gene was DmDef with 9.805 fold change. The qPCR verification results showed that the expressions of DmMtk, DmAtt A, DmDro and DmDef genes were upregulated by 8.180, 7.533, 7.204 and 4.569 fold.

Conclusion
After L. innocua infection, the genes with the most significant change in Drosophila S2 cells are antimicrobial peptide genes. This study offers a comprehensive investigation of gene expression changes in Drosophila S2 cells after L. innocua infection, and provide a reference for revealing the response of host cells evoked by non-pathogenic bacteria as well as interaction studies between bacterial pathogens and hosts.
- Listeria innocua,
- Drosophila S2 cell,
- transcriptome sequencing,
- immunity,
- antimicrobial peptide,
- signaling pathway

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References (43)

References

[1]	李翠云. 单核细胞李斯特菌研究近况[J]. 中国热带医学, 2010, 10(1): 120-122.
[2]	蔡雪薛. 单核细胞增生李斯特菌毒力相关基因的筛选鉴定及其功能研究[D]. 扬州: 扬州大学, 2017.
[3]	VÁZQUEZ-BOLAND J A, DOMÍNGUEZ-BERNAL G, GONZÁLEZ-ZORN B, et al. Pathogenicity islands and virulence evolution in Listeria[J]. Microbes Infect, 2001, 3(7): 571-584. doi: 10.1016/S1286-4579(01)01413-7
[4]	GAILLARD J L, BERCHE P, SANSONETTI P. Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes[J]. Infect Immun, 1986, 52(1): 50-55. doi: 10.1128/IAI.52.1.50-55.1986
[5]	陈健舜, 江玲丽, 方维焕. 李斯特菌毒力因子及其进化[J]. 微生物学报, 2007(4): 738-742. doi: 10.3321/j.issn:0001-6209.2007.04.035
[6]	ORSI R H, WIEDMANN M. Characteristics and distribution of Listeriaspp., including Listeria species newly described since 2009[J]. Appl Microbiol Biotechnol, 2016, 100(12): 5273-5287. doi: 10.1007/s00253-016-7552-2
[7]	JUNTTILA J R, NIEMELÄ S I, HIRN J. Minimum growth temperatures of Listeria monocytogenes and non‐haemolytic Listeria[J]. J Appl Bacteriol, 1988, 65(4): 321-327. doi: 10.1111/j.1365-2672.1988.tb01898.x
[8]	王旭. 基于比较基因组学和转录组学技术揭示单增李斯特菌毒力因子的研究[D]. 上海: 上海海洋大学, 2016.
[9]	杜秀嫒. 李斯特菌致病性的研究及部分基因的功能分析[D]. 兰州: 甘肃农业大学, 2018.
[10]	SCALLAN E, HOEKSTRA R M, ANGULO F J, et al. Foodborne illness acquired in the United States: Major pathogens[J]. Emerg Infect Dis, 2011, 17(1): 7-15. doi: 10.3201/eid1701.P11101
[11]	LI W, BAI L, FU P, et al. The epidemiology of Listeria monocytogenes in China[J]. Foodborne Pathog Dis, 2018, 15(8): 459-466. doi: 10.1089/fpd.2017.2409
[12]	郎需龙, 王兴龙. 李斯特菌毒力因子及其调控机制的研究进展[J]. 中国畜牧兽医, 2011, 38(3): 195-198.
[13]	ALVAREZ-DOMINGUEZ C, ROBERTS R, STAHL P D. Internalized Listeria monocytogenes modulates intracellular trafficking and delays maturation of the phagosome[J]. J Cell Sci, 1997, 110(Pt 6): 731-743.
[14]	MARQUIS H, GOLDFINE H, PORTNOY D A. Proteolytic pathways of activation and degradation of a bacterial phospholipase C during intracellular infection by Listeria monocytogenes[J]. J Cell Biol, 1997, 137(6): 1381-1392. doi: 10.1083/jcb.137.6.1381
[15]	PIZARRO-CERDÁ J, COSSART P. Subversion of cellular functions by Listeria monocytogenes[J]. J Pathol, 2006, 208(2): 215-223. doi: 10.1002/path.1888
[16]	KOCKS C, GOUIN E, TABOURET M, et al. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein[J]. Cell, 1992, 68(3): 521-531.
[17]	COSSART P, TOLEDO-ARANA A. Listeria monocytogenes, a unique model in infection biology: An overview[J]. Microbes Infect, 2008, 10(9): 1041-1050. doi: 10.1016/j.micinf.2008.07.043
[18]	CHONG R, SWISS R, BRIONES G, et al. Regulatory mimicry in Listeria monocytogenes actin-based motility[J]. Cell Host Microbe, 2009, 6(3): 268-278. doi: 10.1016/j.chom.2009.08.006
[19]	DEN BAKKER H C, CUMMINGS C A, FERREIRA V, et al. Comparative genomics of the bacterial genus Listeria: Genome evolution is characterized by limited gene acquisition and limited gene loss[J]. BMC Genomics, 2010, 11(1): 688. doi: 10.1186/1471-2164-11-688
[20]	MILILLO S R, FRIEDLY E C, SALDIVAR J C, et al. A Review of the ecology, genomics, and stress response of Listeria innocua and Listeria monocytogenes[J]. Crit Rev Food Sci Nutr, 2012, 52(8): 712-725. doi: 10.1080/10408398.2010.507909
[21]	JOHNSON J, JINNEMAN K, STELMA G, et al. Natural atypical Listeria innocua strains with Listeria monocytogenes pathogenicity island 1 genes[J]. Appl Environ Microbiol, 2004, 7(7): 4256-4266.
[22]	MOURA A, DISSON O, LAVINA M, et al. Atypical hemolytic Listeria innocua isolates are virulent, albeit less than Listeria monocytogenes[J]. Infect Immun, 2019, 87(4): e00758-18.
[23]	NYHAN L, JOHNSON N, BEGLEY M, et al. Comparison of predicted and impedance determined growth of Listeria innocua in complex food matrices[J]. Food Microbiol, 2020, 87: 103381. doi: 10.1016/j.fm.2019.103381
[24]	SORRENTINO E, TREMONTE P, SUCCI M, et al. Detection of antilisterial activity of 3-phenyllactic acid using Listeria innocua as a model[J]. Front Microbiol, 2018, 9: 1373.
[25]	TREMONTE P, SUCCI M, COPPOLA R, et al. Homology-based modeling of universal stress protein from Listeria innocua up-regulated under acid stress conditions[J]. Front Microbiol, 2016, 7: 1998.
[26]	YILDIRIM Z, YERLIKAYA S, ÖNCÜL N, et al. Inhibitory effect of lactococcin BZ against Listeria innocua and indigenous microbiota of fresh beef[J]. Food Technol Biotechnol, 2016, 54(3): 317-323.
[27]	LIU D. Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen[J]. J Med Microbiol, 2006, 55(6): 645-659. doi: 10.1099/jmm.0.46495-0
[28]	刘甜, 罗开珺. 果蝇Toll和Imd信号通路中的功能结构域[J]. 环境昆虫学报, 2011, 33(3): 388-395. doi: 10.3969/j.issn.1674-0858.2011.03.015
[29]	STUART L M, EZEKOWITZ R A. Phagocytosis and comparative innate immunity: Learning on the fly[J]. Nat Rev Immunol, 2008, 8(2): 131-141. doi: 10.1038/nri2240
[30]	TANJI T, HU X, WEBER A N R, et al. Toll and Imd pathways synergistically activate an innate immune response in Drosophila melanogaster[J]. Mol Cell Biol, 2007, 27(12): 4578-4588. doi: 10.1128/MCB.01814-06
[31]	VODOVAR N, VINALS M, LIEHL P, et al. Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species[J]. Proc Natl Acad Sci USA, 2005, 102(32): 11414-11419. doi: 10.1073/pnas.0502240102
[32]	TZOU P, REICHHART J M, LEMAITRE B. Constitutive expression of a single antimicrobial peptide can restore wild-type resistance to infection in immunodeficient Drosophila mutants[J]. Proc Natl Acad Sci USA, 2002, 99(4): 2152-2157. doi: 10.1073/pnas.042411999
[33]	GOTTAR M, GOBERT V, MICHEL T, et al. The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein[J]. Nature, 2002, 416(6881): 640-644.
[34]	陈康康, 吕志强. 昆虫肽聚糖识别蛋白研究进展[J]. 昆虫学报, 2014, 57(8): 969-978.
[35]	IATSENKO I, KONDO S, MENGIN-LECREULX D, et al. PGRP-SD, an extracellular pattern-recognition receptor, enhances peptidoglycan-mediated activation of the Drosophila Imd pathway[J]. Immunity, 2016, 45(5): 1013-1023. doi: 10.1016/j.immuni.2016.10.029
[36]	LEMAITRE B, REICHHART J M, HOFFMANN J A. Drosophila host defense: Differential induction of antimicrobial peptide genes after infection by various classes of microorganisms[J]. Proc Natl Acad Sci USA, 1997, 94(26): 14614-14619. doi: 10.1073/pnas.94.26.14614
[37]	IMLER J, BULET P. Antimicrobial peptides in Drosophila: Structures, activities and gene regulation[J]. Chem Immunol Allergy, 2005, 86: 86648.
[38]	程廷才, 王根洪, 李娟, 等. 昆虫抗菌肽基因表达调控机理[J]. 蚕学通讯, 2004, 24(3): 20-26. doi: 10.3969/j.issn.1006-0561.2004.03.008
[39]	HANSON M A, DOSTÁLOVÁ A, CERONI C, et al. Synergy and remarkable specificity of antimicrobial peptides in vivo using a systematic knockout approach[J]. eLife, 2019, 8: 44341.
[40]	ALLAN A K, DU J, DAVIES S A, et al. Genome-wide survey of V-ATPase genes in Drosophila reveals a conserved renal phenotype for lethal alleles[J]. Physiol Genomics, 2005, 22(2): 128-138. doi: 10.1152/physiolgenomics.00233.2004
[41]	游海燕, 邓云, 覃文新. V-ATPases的功能及其抑制剂研究进展[J]. 生命科学, 2009, 21(4): 499-503.
[42]	HOLLIDAY L S. Vacuolar H⁺-ATPase: An essential multitasking enzyme in physiology and pathophysiology[J]. New J Sci, 2014, 2014: 1-21.
[43]	谭炳乾, 何启盖, 肖军, 等. 单核细胞增多性李斯特菌hlyA基因序列及溶血素活性测定[J]. 中国兽医学报, 2009, 29(2): 161-165.

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Transcriptome analysis of Drosophila S2 cells infected by Listeria innocua

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