弓形虫卵囊感染小鼠的急性期与慢性期的脑组织蛋白质组变化

doi:10.11843/j.issn.0366-6964.2022.02.022

Abstract

Abstract: Toxoplasma gondii is an opportunistic pathogen with a worldwide distribution, which can cause fatal encephalitis. Human acute toxoplasmosis is closely related to the contamination of T. gondii oocysts. To explore the pathogenic mechanism of T. gondii oocyst infection on the host and to prevent and control toxoplasmosis, we used iTRAQ to analyze the differential expression of proteins in mouse brain tissue after acute and chronic infection with T. gondii PRU strain oocysts. Compared with the control group, 85 and 51 differentially expressed proteins were identified in the acute and chronic infection, respectively, while 114 proteins were differentially expressed in the chronic versus acute infection. The functional analysis revealed that these differentially expressed proteins are mainly involved in pathways such as immune and metabolic processes. The results of our study provide important data for elucidating the host brain tissue damage and pathogenic mechanism caused by T. gondii oocysts in the acute and chronic infection.

Key words: Toxoplasma gondii, iTRAQ, brain, proteomics, bioinformatic analysis

CLC Number:

S855.9

FU Ming, HE Junjun, ZHU Xingquan, CONG Wei. Proteomic Analysis of Changes in the Mouse Brain Tissue Infected with Toxoplasma gondii Oocysts during the Acute and Chronic Stage[J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(2): 556-566.

References 47

[1]	ELSHEIKHA H M, MARRA C M, ZHU X Q. Epidemiology, pathophysiology, diagnosis, and management of cerebral toxoplasmosis[J]. Clin Microbiol Rev, 2021, 34(1):e00115-19.
[2]	ZHOU P, CHEN Z G, LI H L, et al. Toxoplasma gondii infection in humans in China[J]. Parasit Vectors, 2011, 4:165.
[3]	沈继龙, 余莉. 我国弓形虫病流行概况及防治基础研究进展[J]. 中国血吸虫病防治杂志, 2019, 31(1):71-76.SHEN J L, YU L. Prevalence and fundamental researches of prevention and treatment of toxo-plasmosis in China:an overview[J]. Chinese Journal of Schistosomiasis Control, 2019, 31(1):71-76.
[4]	MAHMOUDVAND H, DEZAKI E S, SOLEIMANI S, et al. Seroprevalence and risk factors of Toxoplasma gondii infection among healthy blood donors in south-east of Iran[J]. Parasite Immunol, 2015, 37(7):362-367.
[5]	KRISHNAMURTHY S, KONSTANTINOU E K, YOUNG L H, et al. The human immune response to Toxoplasma:Autophagy versus cell death[J]. PLoS Pathog, 2017, 13(3):e1006176.
[6]	SCHLÜTER D, BARRAGAN A. Advances and challenges in understanding cerebral toxoplasmosis[J]. Front Immunol, 2019, 10:242.
[7]	汪涛, 汤自豪. 弓形虫病:速殖子、包囊和卵囊的传播[J]. 中国人兽共患病学报, 2012, 28(11):1133-1136.WANG T, TANG Z H. Toxoplasmosis:the spread tachyzoites, cysts and oocysts[J]. Chinese Journal of Zoonoses, 2012, 28(11):1133-1136. (in Chinese)
[8]	马巧妮, 王萌, 张海生, 等. 环境中弓形虫卵囊富集及检测技术的研究进展[J]. 中国兽医科学, 2021, 51(3):343-348.MA Q N, WANG M, ZHANG H S, et al. Research progress in enrichment and detection technologies for Toxoplasma gondii in the environment[J]. Chinese Veterinary Science, 2021, 51(3):343-348. (in Chinese)
[9]	GOTTELAND C, GILOT-FROMONT E, AUBERT D, et al. Spatial distribution of Toxoplasma gondii oocysts in soil in a rural area:Influence of cats and land use[J]. Vet Parasitol, 2014, 205(3-4):629-637.
[10]	尹创成, 朱兴全, 袁子国. 水源性弓形虫病的研究进展[J]. 中国畜牧兽医, 2011, 38(4):180-182.YIN C C, ZHU X Q, YUAN Z G. Research progress of water-borne toxoplasmosis[J]. China Animal Husbandry & Veterinary Medicine, 2011, 38(4):180-182. (in Chinese)
[11]	杨俊. 常见食源性寄生虫病的防控措施[J]. 中国畜牧兽医文摘, 2017, 33(9):104-106.YANG J. Prevention and control measures of common food-borne parasitic diseases[J]. China Animal Husbandry and Veterinary Digest, 2017, 33(9):104-106. (in Chinese)
[12]	OPSTEEGH M, MAAS M, SCHARES G, et al. Relationship between seroprevalence in the main livestock species and presence of Toxoplasma gondii in meat (GP/EFSA/BIOHAZ/2013/01) An extensive literature review. Final report[J]. EFSA Support Publicat, 2016, 13(2):996E.
[13]	STELZER S, BASSO W, BENAVIDES SILVÁN J, et al. Toxoplasma gondii infection and toxoplasmosis in farm animals:Risk factors and economic impact[J]. Food Waterborne Parasitol, 2019, 15:e00037.
[14]	PAN M, LYU C, ZHAO J L, et al. Sixty years (1957-2017) of research on toxoplasmosis in China-an overview[J]. Front Microbiol, 2017, 8:1825.
[15]	HE J J, MA J, WANG J L, et al. iTRAQ-based quantitative proteomics analysis identifies host pathways modulated during Toxoplasma gondii infection in swine[J]. Microorganisms, 2020, 8(4):518.
[16]	AEBERSOLD R, MANN M. Mass-spectrometric exploration of proteome structure and function[J]. Nature, 2016, 537(7620):347-355.
[17]	YANG J, DU F, ZHOU X L, et al. Brain proteomic differences between wild-type and CD44- mice induced by chronic Toxoplasma gondii infection[J]. Parasitol Res, 2018, 117(8):2623-2633.
[18]	ZHOU C X, ZHU X Q, ELSHEIKHA H M, et al. Global iTRAQ-based proteomic profiling of Toxoplasma gondii oocysts during sporulation[J]. J Proteom, 2016, 148:12-19.
[19]	WANG Z X, ZHOU C X, ELSHEIKHA H M, et al. Proteomic differences between developmental stages of Toxoplasma gondii revealed by iTRAQ-based quantitative proteomics[J]. Front Microbiol, 2017, 8:985.
[20]	PITTMAN K J, KNOLL L J. Long-term relationships:the complicated interplay between the host and the developmental stages of Toxoplasma gondii during acute and chronic infections[J]. Microbiol Mol Biol Rev, 2015, 79(4):387-401.
[21]	LV L, WANG Y P, FENG W L, et al. iTRAQ-based differential proteomic analysis in Mongolian gerbil brains chronically infected with Toxoplasma gondii[J]. J Proteom, 2017, 160:74-83.
[22]	HE J J, MA J, ELSHEIKHA H M, et al. Proteomic profiling of mouse liver following acute Toxoplasma gondii infection[J]. PLoS One, 2016, 11(3):e0152022.
[23]	FERNANDES S, BRILHANTE-SIMÕES P, COUTINHO T, et al. Comparison of indirect and modified agglutination tests for detection of antibodies to Toxoplasma gondii in domestic cats[J]. J Vet Diagnost Investigat, 2019, 31(5):774-777.
[24]	STAGGS S E, SEE M J, DUBEY J P, et al. Obtaining highly purified Toxoplasma gondii oocysts by a discontinuous cesium chloride gradient[J]. J Visual Experim, 2009, 33:e1402.
[25]	HU R S, HE J J, ELSHEIKHA H M, et al. Transcriptomic profiling of mouse brain during acute and chronic infections by Toxoplasma gondii oocysts[J]. Front Microbiol, 2020, 11:570903.
[26]	ZHOU D H, ZHAO F R, HUANG S Y, et al. Changes in the proteomic profiles of mouse brain after infection with cyst-forming Toxoplasma gondii[J]. Parasit Vectors, 2013, 6:96.
[27]	ZHOU C X, XIE S C, LI M Y, et al. Analysis of the serum peptidome associated with Toxoplasma gondii infection[J]. J Proteom, 2020, 222:103805.
[28]	CHEN X Q, ELSHEIKHA H M, HU R S, et al. Hepatic metabolomics investigation in acute and chronic murine toxoplasmosis[J]. Front Cell Infect Microbiol, 2018, 8:189.
[29]	ZHOU C X, CONG W, CHEN X Q, et al. Serum Metabolic profiling of oocyst-induced Toxoplasma gondii acute and chronic infections in mice using mass-spectrometry[J]. Front Microbiol, 2018, 8:2612.
[30]	MA J, CHEN T, WU S F, et al. iProX:an integrated proteome resource[J]. Nucleic Acids Res, 2019, 47(D1):D1211-D1217.
[31]	SOTO A S, FENOY I M, SANCHEZ V R, et al. Toxoplasma gondii serine-protease inhibitor-1:A new adjuvant candidate for asthma therapy[J]. PLoS One, 2017, 12(10):e0187002.
[32]	SUZUKI Y, ORELLANA M A, SCHREIBER R D, et al. Interferon-gamma:the major mediator of resistance against Toxoplasma gondii[J]. Science, 1988, 240(4851):516-518.
[33]	SASAI M, PRADIPTA A, YAMAMOTO M. Host immune responses to Toxoplasma gondii[J]. Int Immunol, 2018, 30(3):113-119.
[34]	MACMICKING J D. Interferon-inducible effector mechanisms in cell-autonomous immunity[J]. Nat Rev Immunol, 2012, 12(5):367-382.
[35]	STEFFENS N, BEUTER-GUNIA C, KRAVETS E, et al. Essential role of mGBP7 for survival of Toxoplasma gondii infection[J]. mBio, 2020, 11(1):e02993-19.
[36]	DEGRANDI D, KRAVETS E, KONERMANN C, et al. Murine guanylate binding protein 2(mGBP2) controls Toxoplasma gondii replication[J]. Proc Natl Acad Sci U S A, 2013, 110(1):294-299.
[37]	KRAVETS E, DEGRANDI D, MA Q J, et al. Guanylate binding proteins directly attack Toxoplasma gondii via supramolecular complexes[J]. eLife, 2016, 5:e11479.
[38]	SELLECK E M, FENTRESS S J, BEATTY W L, et al. Guanylate-binding protein 1(Gbp1) contributes to cell-autonomous immunity against Toxoplasma gondii[J]. PLoS Pathog, 2013, 9(4):e1003320.
[39]	CAI Y, LEE J, WANG W, et al. Effect of Cd2+ on muscle type of creatine kinase:Inhibition kinetics integrating computational simulations[J]. Int J Biol Macromol, 2016, 83:233-241.
[40]	LI Q J, FAN S, LI X Y, et al. Insights into the phosphoryl transfer mechanism of human ubiquitous mitochondrial creatine kinase[J]. Sci Rep, 2016, 6:38088.
[41]	周永华, 范红结, 张英,等. 慢性弓形虫感染大鼠海马蛋白质组的研究[J]. 中国寄生虫学与寄生虫病杂志, 2013, 31(6):454-457.ZHOU Y H, FAN H J, ZHANG Y, et al. Proteomic study of the hippocampus tissue from rats with chronic Toxoplasma gondii infection[J]. Chinese Journal of Parasitology and Parasitic Diseases, 2013, 31(6):454-457. (in Chinese)
[42]	ZHUANG G Z, KEELER B, GRANT J, et al. Carbonic anhydrase-8 regulates inflammatory pain by inhibiting the ITPR1-cytosolic free calcium pathway[J]. PLoS One, 2015, 10(3):e0118273.
[43]	NAST R, CHOEPAK T, LVDER C G K. Epigenetic control of IFN-γ host responses during infection with Toxoplasma gondii[J]. Front Immunol, 2020, 11:581241.
[44]	LANG C, HILDEBRANDT A, BRAND F, et al. Impaired chromatin remodelling at STAT1-regulated promoters leads to global unresponsiveness of Toxoplasma gondii-infected macrophages to IFN-γ[J]. PLoS Pathog, 2012, 8(1):e1002483.
[45]	SEDWICK C. Tuning up STAT1[J]. PLoS Biol, 2015, 13(7):e1002201.
[46]	GAY G, BRAUN L, BRENIER-PINCHART M P, et al. Toxoplasma gondii TgIST co-opts host chromatin repressors dampening STAT1-dependent gene regulation and IFN-γ-mediated host defenses[J]. J Exp Mede, 2016, 213(9):1779-1798.
[47]	OLIAS P, ETHERIDGE R D, ZHANG Y, et al. Toxoplasma effector recruits the Mi-2/NuRD complex to repress STAT1 transcription and block IFN-γ-dependent gene expression[J]. Cell Host Micr, 2016, 20(1):72-82.

Proteomic Analysis of Changes in the Mouse Brain Tissue Infected with Toxoplasma gondii Oocysts during the Acute and Chronic Stage

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

References 47

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	ZHANG Ying, SONG Chunlian, ZHANG Ying, SHEN Hong, SHU Xianghua, YANG Honggui. Study on the Damage of Blood-brain Barrier by Tight Junction Protein Mediated by MMP-9 in Pseudorabies Virus-infected Mice [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(5): 2186-2194.
[2]	ZHANG Xinrui, FU Yu, YANG Zhuo, SHEN Wenjuan, TAO Jinzhong. Study of Early Pregnancy Diagnostic Proteins in Dairy Cows [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(2): 451-460.
[3]	YAO Ying, ZHOU Yingcong, DU Peiyan, LI Yijuan, QIAN Wenjie, LI Liuyang, YU Zhipeng, CUI Yan, YU Sijiu, FAN Jiangfeng. Proteomic Analysis of Yak Serum During Pregnancy Based on TMT Technology [J]. Acta Veterinaria et Zootechnica Sinica, 2024, 55(1): 192-206.
[4]	SUN Xiaojing, ZHANG Lei, TIAN Tian, MA Xi, YAO Jia, WANG Yang. Unravelling Toxoplasma Treatment: Conventional Drugs toward Nanomedicine [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(5): 1834-1844.
[5]	HE Wenfeng, LI Chen, CHANG Hongtao, LI Longxi, CHEN Jing, YANG Guoqing, LIU Huimin. Screening and Identifying of Host Proteins that Inhibit Pseudorabies Virus Replication [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(3): 1177-1186.
[6]	HU Xiyi, WANG Hui, LI Fukuan, WANG Zhennan, HAN Chengquan, CHU Meiqiang, YANG Yan, Lü Shenjin. Research Progress on the Regulation of Intestinal Flora on Abnormal Behavior of Maternal Separation in Offspring [J]. Acta Veterinaria et Zootechnica Sinica, 2023, 54(11): 4514-4525.
[7]	REN Yu, YAN Wenquan, DING Yuezhu, HU Mengxue, ZHOU Jielong, WU Peifu, CHEN Fenfen, LIU Lili. VPS28 Regulates Milk Protein Synthesis in Bovine Mammary Epithelial Cells through Ubiquitination Signaling Pathway [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(8): 2558-2567.
[8]	YAN Shuo, ZHAO Shanshan, ZHU Zhendong, PAN Qingjie, DONG Huansheng. Study on Nuclear-plasma Transporter KPNA4 of Sheep Sperm Cell [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(7): 2194-2201.
[9]	CHEN Huixian, CHEN Yajie, WANG Xianmei, WANG Lifang, LIU Qun, LIU Jing. Identification of the Cross-reacting Antigen MIC17A of Toxoplasma gondii and Neospora caninum and the Study of Its Cross-immune Protective Efficacy in Mice [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(7): 2300-2306.
[10]	ZHANG Meng, WANG Weiran, FENG Chen, ZHANG Yi, ZHANG Qian, MU Xiang. The Effect of Leonurus artemisia Decoction on the Active Factors of Complement and Coagulation Cascade Pathway Based on Proteomics in vitro [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(6): 1934-1944.
[11]	QI Mengfan, XIE Su, GAO Ruonan, SUN Yishan, SUN Xiaomei, HE Junfei, LU Huiwen, LU Shihao, CHEN Xin, LI Qingchun, HUANG Tao. Identification of Differentially Expressed Proteins in Blood of Sows at Early Pregnancy [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(4): 1109-1121.
[12]	ZOU Ronghua, WU Xiaoni, CHEN Qiwei, GONG Xiaowei, WANG Yanping, ZHENG Fuying, CHU Yuefeng. Effect of Enolase on Riemerella anatipestifer Invading Duck Brain Microvascular Endothelial Cells [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(12): 4389-4397.
[13]	YANG Zhiqing, ZHANG Haoquan, XIAN Runxi, LI Xinran. Effects of P7C3-A20 on Apoptosis and Oxidation of PC12 Cells in Traumatic Brain Injury [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(12): 4429-4438.
[14]	ZHENG Xiaonan, LI Tingting, WANG Jinlei, ZHENG Wenbin, ZHU Xingquan. Research Progress on Biological Functions of Dense Granule Proteins of Toxoplasma gondii [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(10): 3345-3357.
[15]	WANG Pei, WANG Meng, LI Tingting, ZHENG Xiaonan, LIANG Qinli, CHEN Xiaoqing. Generation and Basic Functional Characterization of Four Hypothetical Protein Genes Deletion Strains of Toxoplasma gondii [J]. Acta Veterinaria et Zootechnica Sinica, 2022, 53(10): 3598-3608.