顶复门原虫感染与宿主细胞自噬相互作用的研究进展

doi:10.12140/j.issn.1000-7423.2021.06.015

中国寄生虫学与寄生虫病杂志 ›› 2021, Vol. 39 ›› Issue (6): 826-831.doi: 10.12140/j.issn.1000-7423.2021.06.015

顶复门原虫感染与宿主细胞自噬相互作用的研究进展

鲁飞(), 卓洵辉, 陆绍红^*()

杭州医学院基础医学与法医学院,杭州 310000

收稿日期:2021-05-24 修回日期:2021-08-09 出版日期:2021-12-30 发布日期:2021-12-13
通讯作者: 陆绍红
作者简介:鲁飞（1996-）,男,硕士研究生,从事弓形虫基因靶向敲除及分子生物学研究。E-mail： 836685633@qq.com
基金资助:
国家自然科学基金(81802037);国家自然科学基金(81871684);浙江省重点研发项目(2019C03057);浙江省基金-青山湖科技城联合基金(LQY19H190002)

Research progress on the interaction between host cell autophagy and apicomplexa protozoa infection

LU Fei(), ZHUO Xun-hui, LU Shao-hong^*()

School of Basic Medical Sciences and Forensic Medicine, Hangzhou Medical College, Hangzhou 310000, China

Received:2021-05-24 Revised:2021-08-09 Online:2021-12-30 Published:2021-12-13
Contact: LU Shao-hong
Supported by:
Natural Science Foundation of China(81802037);National Natural Science Foundation of China(81871684);Key Research and Development Project of Zhejiang Province(2019C03057);Qingshan Lake United Fund of Zhejiang Province(LQY19H190002)

摘要/Abstract

摘要：

细胞自噬是一种保守的、广泛存在于真核生物中的溶酶体依赖性的降解系统,细胞内物质通过该机制运送至溶酶体内进行降解,对处于饥饿、缺氧等应激条件下的细胞生存发挥着重要作用。此外,细胞也可以通过自噬的清除作用消灭外来病原体如寄生虫、病毒等。顶复门原虫是一类专性细胞内寄生原虫,多为人兽共患病病原,对社会公共卫生带来较大的威胁。近年来关于细胞自噬和顶复门原虫之间的相互影响的研究进展主要集中在弓形虫和疟原虫。本文对自噬机制、自噬与重要顶复门原虫感染的相互作用研究进展进行综述。

关键词: 自噬, 顶复门原虫, 刚地弓形虫, 疟原虫

Abstract:

Autophagy is a conserved lysosome-depenendant degradation system widely present in eukaryotes, and intracellular substances are transported to lysosomes for degradation through this mechanism, which plays an important role in cell survival under stress conditions of starvation and hypoxia. In addition, cells can also eliminate foreign pathogens such as parasites and viruses through the clearance action of autophagy. Apicomplexa protozoa are obligatory intracellular parasites, often zoonotic pathogens, posing considerable threats to social development and public health. In recent years, researches on the interaction between autophagy and apicomplexa protozoa mainly focused on Toxoplasma gondii and Plasmodium. In this paper, we reviewed the progress of research on the interaction between autophagy and important Apicomplexa protozoa infection.

Key words: Autophagy, Apicomplexan, Toxoplasma gondii, Plasmodium

中图分类号:

R531

鲁飞, 卓洵辉, 陆绍红. 顶复门原虫感染与宿主细胞自噬相互作用的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2021, 39(6): 826-831.

LU Fei, ZHUO Xun-hui, LU Shao-hong. Research progress on the interaction between host cell autophagy and apicomplexa protozoa infection[J]. Chinese Journal of Parasitology and Parasitic Diseases, 2021, 39(6): 826-831.

图/表 2

参考文献 55

[1]	Matta SK, Rinkenberger N, Dunay IR, et al. Toxoplasma gondii infection and its implications within the central nervous system[J]. Nat Rev Microbiol, 2021, 19(7): 467-480. doi: 10.1038/s41579-021-00518-7
[2]	Lopez Corcino Y, Gonzalez Ferrer S, Mantilla LE, et al. Toxoplasma gondii induces prolonged host epidermal growth factor receptor signalling to prevent parasite elimination by autophagy: perspectives for in vivo control of the parasite[J]. Cell Microbiol, 2019, 21(10): e13084.
[3]	Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues[J]. Cell, 2011, 147(4): 728-741. doi: 10.1016/j.cell.2011.10.026 pmid: 22078875
[4]	Boya P, Reggiori F, Codogno P. Emerging regulation and functions of autophagy[J]. Nat Cell Biol, 2013, 15(7): 713-720. doi: 10.1038/ncb2788
[5]	Zhang J, Gao DM, Wang XL. Influence of regulation of host cell autophagy on the proliferation of Toxoplasma gondii in host cells[J]. Acta Universitatis Medicinalis Anhui, 2015, 50(3): 290-293. (in Chinese)
	(张婧, 高冬梅, 汪学龙. 调控宿主细胞自噬对弓形虫在宿主细胞内增殖的影响[J]. 安徽医科大学学报, 2015, 50(3): 290-293.)
[6]	Díaz-Troya S, Pérez-Pérez ME, Florencio FJ, et al. The role of TOR in autophagy regulation from yeast to plants and mammals[J]. Autophagy, 2008, 4(7): 851-865. pmid: 18670193
[7]	Hale AN, Ledbetter DJ, Gawriluk TR, et al. Autophagy: regulation and role in development[J]. Autophagy, 2013, 9(7): 951-972. doi: 10.4161/auto.24273
[8]	Nazio F, Strappazzon F, Antonioli M, et al. mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6[J]. Nat Cell Biol, 2013, 15(4): 406-416. doi: 10.1038/ncb2708
[9]	Hosokawa N, Hara T, Kaizuka T, et al. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy[J]. Mol Biol Cell, 2009, 20(7): 1981-1991. doi: 10.1091/mbc.E08-12-1248 pmid: 19211835
[10]	Sasai M, Pradipta A, Yamamoto M. Host immune responses to Toxoplasma gondii[J]. Int Immunol, 2018, 30(3): 113-119. doi: 10.1093/intimm/dxy004 pmid: 29408976
[11]	Montoya JG, Remington JS. Management of Toxoplasma gondii infection during pregnancy[J]. Clin Infect Dis, 2008, 47(4): 554-566. doi: 10.1086/590149 pmid: 18624630
[12]	Su HY, Yang SJ, Peng HJ, et al. Current status of toxoplasmosis misdiagnosis in clinic[J]. Chin J Parasitol Parasit Dis, 2019, 37(3): 342-345. (in Chinese)
	(苏海莹, 杨淑君, 彭鸿娟, 等. 弓形虫病临床误诊现状分析[J]. 中国寄生虫学与寄生虫病杂志, 2019, 37(3): 342-345.)
[13]	Smith NC, Goulart C, Hayward JA, et al. Control of human toxoplasmosis[J]. Int J Parasitol, 2021, 51(2/3): 95-121. doi: 10.1016/j.ijpara.2020.11.001
[14]	Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation[J]. Nature, 2011, 469(7330): 323-335. doi: 10.1038/nature09782
[15]	Wang Y, Weiss LM, Orlofsky A. Host cell autophagy is induced by Toxoplasma gondii and contributes to parasite growth[J]. J Biol Chem, 2009, 284(3): 1694-1701. doi: 10.1074/jbc.M807890200
[16]	Schmid D, Münz C. Innate and adaptive immunity through autophagy[J]. Immunity, 2007, 27(1): 11-21. doi: 10.1016/j.immuni.2007.07.004
[17]	Muniz-Feliciano L, Van Grol J, Portillo JA, et al. Toxoplasma gondii-induced activation of EGFR prevents autophagy protein-mediated killing of the parasite[J]. PLoS Pathog, 2013, 9(12): e1003809. doi: 10.1371/journal.ppat.1003809
[18]	Van Kooten C, Banchereau J. CD40-CD40 ligand[J]. J Leukoc Biol, 2000, 67(1): 2-17. doi: 10.1002/jlb.2000.67.issue-1
[19]	Besteiro S. The role of host autophagy machinery in controlling Toxoplasma infection[J]. Virulence, 2019, 10(1): 438-447. doi: 10.1080/21505594.2018.1518102
[20]	Liu E, Lopez Corcino Y, Portillo JA, et al. Identification of signaling pathways by which CD40 stimulates autophagy and antimicrobial activity against Toxoplasma gondii in macrophages[J]. Infect Immun, 2016, 84(9): 2616-2626. doi: 10.1128/IAI.00101-16
[21]	Pattingre S, Tassa A, Qu X, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy[J]. Cell, 2005, 122(6): 927-939. pmid: 16179260
[22]	Portillo JA, Okenka G, Reed E, et al. The CD40-autophagy pathway is needed for host protection despite IFN-Γ-dependent immunity and CD40 induces autophagy via control of P21 levels[J]. PLoS One, 2010, 5(12): e14472. doi: 10.1371/journal.pone.0014472
[23]	Andrade RM, Wessendarp M, Gubbels MJ, et al. CD40 induces macrophage anti-Toxoplasma gondii activity by triggering autophagy-dependent fusion of pathogen-containing vacuoles and lysosomes[J]. J Clin Invest, 2006, 116(9): 2366-2377. pmid: 16955139
[24]	Martens S, Parvanova I, Zerrahn J, et al. Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases[J]. PLoS Pathog, 2005, 1(3): e24. doi: 10.1371/journal.ppat.0010024
[25]	Ling YM, Shaw MH, Ayala C, et al. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages[J]. J Exp Med, 2006, 203(9): 2063-2071. doi: 10.1084/jem.20061318
[26]	Kim BH, Shenoy AR, Kumar P, et al. IFN-inducible GTPases in host cell defense[J]. Cell Host Microbe, 2012, 12(4): 432-444. doi: 10.1016/j.chom.2012.09.007
[27]	Howard JC, Hunn JP, Steinfeldt T. The IRG protein-based resistance mechanism in mice and its relation to virulence in Toxoplasma gondii[J]. Curr Opin Microbiol, 2011, 14(4): 414-421. doi: 10.1016/j.mib.2011.07.002
[28]	Kravets E, Degrandi D, Ma Q, et al. Guanylate binding proteins directly attack Toxoplasma gondii via supramolecular complexes[J]. Elife, 2016, 5: e11479. doi: 10.7554/eLife.11479
[29]	Zhao Y, Ferguson DJ, Wilson DC, et al. Virulent Toxoplasma gondii evade immunity-related GTPase-mediated parasite vacuole disruption within primed macrophages[J]. J Immunol, 2009, 182(6): 3775-3781. doi: 10.4049/jimmunol.0804190
[30]	Khaminets A, Hunn JP, Könen-Waisman S, et al. Coordinated loading of IRG resistance GTPases on to the Toxoplasma gondii parasitophorous vacuole[J]. Cell Microbiol, 2010, 12(7): 939-961. doi: 10.1111/cmi.2010.12.issue-7
[31]	Fentress SJ, Behnke MS, Dunay IR, et al. Phosphorylation of immunity-related GTPases by a Toxoplasma gondii-secreted kinase promotes macrophage survival and virulence[J]. Cell Host Microbe, 2010, 8(6): 484-495. doi: 10.1016/j.chom.2010.11.005 pmid: 21147463
[32]	Reese ML, Shah N, Boothroyd JC. The Toxoplasma pseudokinase ROP5 is an allosteric inhibitor of the immunity-related GTPases[J]. J Biol Chem, 2014, 289(40): 27849-27858. doi: 10.1074/jbc.M114.567057
[33]	Behnke MS, Fentress SJ, Mashayekhi M, et al. The polymorphic pseudokinase ROP5 controls virulence in Toxoplasma gondii by regulating the active kinase ROP18[J]. PLoS Pathog, 2012, 8(11): e1002992. doi: 10.1371/journal.ppat.1002992
[34]	Portillo JC, Muniz-Feliciano L, Lopez Corcino Y, et al. Toxoplasma gondii induces FAK-Src-STAT3 signaling during infection of host cells that prevents parasite targeting by autophagy[J]. PLoS Pathog, 2017, 13(10): e1006671. doi: 10.1371/journal.ppat.1006671
[35]	Van Grol J, Subauste C, Andrade RM, et al. HIV-1 inhibits autophagy in bystander macrophage/monocytic cells through Src-Akt and STAT3[J]. PLoS One, 2010, 5(7): e11733. doi: 10.1371/journal.pone.0011733
[36]	Biscardi JS, Maa MC, Tice DA, et al. c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function[J]. J Biol Chem, 1999, 274(12): 8335-8343. pmid: 10075741
[37]	Shen S, Niso-Santano M, Adjemian S, et al. Cytoplasmic STAT3 represses autophagy by inhibiting PKR activity[J]. Mol Cell, 2012, 48(5): 667-680. doi: 10.1016/j.molcel.2012.09.013
[38]	Sobolewska A, Gajewska M, Zarzyńska J, et al. IGF-I, EGF, and sex steroids regulate autophagy in bovine mammary epithelial cells via the mTOR pathway[J]. Eur J Cell Biol, 2009, 88(2): 117-130. doi: 10.1016/j.ejcb.2008.09.004 pmid: 19013662
[39]	Yan AX, Zou Y, Li JJ, et al. Research advance on molecular mechanism of gliding motility, invasion and egress in Apicomplexa[J]. Chin Trop Med, 2018, 18(9): 950-954. (in Chinese)
	(闫爱霞, 邹洋, 李晶晶, 等. 顶复门原虫运动、入侵和逸出相关分子机制研究进展[J]. 中国热带医学, 2018, 18(9): 950-954.)
[40]	WHO. Malaria Report 2020[R]. Geneva: WHO, 2021.
[41]	Agop-Nersesian C, Niklaus L, Wacker R, et al. Host cell cytosolic immune response during Plasmodium liver stage development[J]. FEMS Microbiol Rev, 2018, 42(3): 324-334. doi: 10.1093/femsre/fuy007 pmid: 29529207
[42]	Thieleke-Matos C, Lopes Da Silva M, Cabrita-Santos L, et al. Host cell autophagy contributes to Plasmodium liver development[J]. Cell Microbiol, 2016, 18(3): 437-450. doi: 10.1111/cmi.12524 pmid: 26399761
[43]	Schmuckli-Maurer J, Reber V, Wacker R, et al. Inverted recruitment of autophagy proteins to the Plasmodium berghei parasitophorous vacuole membrane[J]. PLoS One, 2017, 12(8): e0183797. doi: 10.1371/journal.pone.0183797
[44]	Prado M, Eickel N, De Niz M, et al. Long-term live imaging reveals cytosolic immune responses of host hepatocytes against Plasmodium infection and parasite escape mechanisms[J]. Autophagy, 2015, 11(9): 1561-1579. doi: 10.1080/15548627.2015.1067361
[45]	Joy S, Thirunavukkarasu L, Agrawal P, et al. Basal and starvation-induced autophagy mediates parasite survival during intraerythrocytic stages of Plasmodium falciparum[J]. Cell Death Discov, 2018, 4: 43.
[46]	Lin JN, Zhang MY, Lv ZY. Autophagy and parasitic protozoa[J]. J Trop Med, 2017, 17(9): 1258-1262. (in Chinese)
	(林锦娜, 张梦颖, 吕志跃. 自噬与寄生性原虫[J]. 热带医学杂志, 2017, 17(9): 1258-1262.)
[47]	Mueller AK, Labaied M, Kappe SH, et al. Genetically modified Plasmodium parasites as a protective experimental malaria vaccine[J]. Nature, 2005, 433(7022): 164-167. doi: 10.1038/nature03188
[48]	Real E, Rodrigues L, Cabal GG, et al. Plasmodium UIS3 sequesters host LC3 to avoid elimination by autophagy in hepatocytes[J]. Nat Microbiol, 2018, 3(1): 17-25. doi: 10.1038/s41564-017-0054-x
[49]	Li Z, Zou Y, Jia YG, et al. Current advance of autophagy in Plasmodium and Toxoplasma[J]. Chin Trop Med, 2018, 18(9): 944-949. (in Chinese)
	(李缜, 邹洋, 贾永根, 等. 疟原虫和弓形虫的自噬作用研究进展[J]. 中国热带医学, 2018, 18(9): 944-949.)
[50]	Tomlins AM, Ben-Rached F, Williams RA, et al. Plasmodium falciparum ATG8 implicated in both autophagy and apicoplast formation[J]. Autophagy, 2013, 9(10): 1540-1552. doi: 10.4161/auto.25832 pmid: 24025672
[51]	Bouzid M, Hunter PR, Chalmers RM, et al. Cryptosporidium pathogenicity and virulence[J]. Clin Microbiol Rev, 2013, 26(1): 115-134. doi: 10.1128/CMR.00076-12 pmid: 23297262
[52]	Priyamvada S, Jayawardena D, Bhalala J, et al. Cryptosporidium parvum infection induces autophagy in intestinal epithelial cells[J]. Cell Microbiol, 2020: e13298.
[53]	Blake DP, Worthing K, Jenkins MC. Exploring Eimeria genomes to understand population biology: recent progress and future opportunities[J]. Genes (Basel), 2020, 11(9): 1103. doi: 10.3390/genes11091103
[54]	Qi N, Liao S, Abuzeid AMI, et al. The effect of autophagy on the survival and invasive activity of Eimeria tenella sporozoites[J]. Sci Rep, 2019, 9(1): 5835. doi: 10.1038/s41598-019-41947-y
[55]	Qi N, Liao S, Mohiuddin M, et al. Autophagy induced by monensin serves as a mechanism for programmed death in Eimeria tenella[J]. Vet Parasitol, 2020, 287: 109181. doi: 10.1016/j.vetpar.2020.109181

顶复门原虫感染与宿主细胞自噬相互作用的研究进展

Research progress on the interaction between host cell autophagy and apicomplexa protozoa infection

RichHTML

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

图/表 2

参考文献 55

相关文章 15

编辑推荐

Metrics

本文评价

[1]	薛羽珊, 林萍, 程训佳, 冯萌. 慢性弓形虫感染对宿主中枢神经系统的损伤及其作用机制[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(5): 527-531.
[2]	姜文静, 孟雅莉, 赵利娜, 王春苗, 张晓磊. 刚地弓形虫棒状体蛋白18和膜表面抗原30复合核酸疫苗对小鼠的免疫保护作用[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(5): 532-538.
[3]	郭帅, 何彪, 高源利, 范永铃, 朱锋, 丁艳, 刘太平, 徐文岳. 鼠疟原虫感染大鼠和小鼠的种特异性分析[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(5): 539-545.
[4]	周瑞敏, 纪鹏慧, 李素华, 杨成运, 刘颖, 钱丹, 邓艳, 鲁德领, 赵玉玲, 赵东阳, 张红卫. 河南省自赤道几内亚输入的恶性疟原虫抗药性基因多态性分析[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(5): 593-600.
[5]	梁柯嘉, 刘聪, 李彦霖, 李小鸽, 刘彦, 李贞魁. 疟原虫有性阶段转录调控的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(5): 619-624.
[6]	丁红芸, 董莹, 徐艳春, 邓艳, 刘言, 吴静, 陈梦妮, 张苍林. 云南省输入性间日疟原虫多药抗性蛋白1基因突变多态性分析[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(4): 404-411.
[7]	赵紫琪, 吕芳丽. 蒿甲醚脂质体体外抑制刚地弓形虫增殖作用的研究[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(4): 446-451.
[8]	张驰, 陈嘉婷, 辛紫萱, 杨莉莉, 杨梓瀚, 彭鸿娟. 弓形虫慢性感染小鼠脑转录组分析及与抑郁相关的犬尿氨酸通路的验证[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(3): 270-278.
[9]	徐少杰, 陈绅波, 陈军虎. 恶性疟原虫重复散布家族基因转录调控的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(3): 374-379.
[10]	杜鹃, 李佳, 吴迪, 余琦, 张玮, 白如念, 郭俊林, 刘庆斌, 雷琪莉, 谷传慧, 王萌, 赵浩军. 2022年北京市犬猫刚地弓形虫感染血清流行病学调查[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(3): 389-392.
[11]	孙军. 疟原虫色素形成的生物学意义[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(2): 209-212.
[12]	李美, 肖宁, 夏志贵. 基于无性期18S rDNA特异性引物检测5种疟原虫qPCR的建立和应用[J]. 中国寄生虫学与寄生虫病杂志, 2023, 41(1): 36-43.
[13]	李佳铭, 王艺璇, 杨宁爱, 马慧慧, 兰敏, 刘春兰, 赵志军. 刚地弓形虫ROP16蛋白对MH-S细胞极化和凋亡的影响及其相关机制[J]. 中国寄生虫学与寄生虫病杂志, 2022, 40(5): 579-586.
[14]	邹伟浩, 吴蔚玲, 廖远鹏, 陈敏, 彭鸿娟. 刚地弓形虫抗缓殖子期抗原1单克隆抗体的制备与应用[J]. 中国寄生虫学与寄生虫病杂志, 2022, 40(5): 587-593.
[15]	代莉莎, 张丽新, 尹昆. 刚地弓形虫诱导宿主精神行为障碍的研究进展[J]. 中国寄生虫学与寄生虫病杂志, 2022, 40(5): 642-646.