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

doi:10.12140/j.issn.1000-7423.2021.06.015

Abstract

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

CLC Number:

R531

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.

Figures/Tables 2

References 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.
[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.
[4]	Boya P, Reggiori F, Codogno P. Emerging regulation and functions of autophagy[J]. Nat Cell Biol, 2013, 15(7): 713-720.
[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)
[5]	(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.
[7]	Hale AN, Ledbetter DJ, Gawriluk TR, et al. Autophagy: regulation and role in development[J]. Autophagy, 2013, 9(7): 951-972.
[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.
[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.
[10]	Sasai M, Pradipta A, Yamamoto M. Host immune responses to Toxoplasma gondii[J]. Int Immunol, 2018, 30(3): 113-119.
[11]	Montoya JG, Remington JS. Management of Toxoplasma gondii infection during pregnancy[J]. Clin Infect Dis, 2008, 47(4): 554-566.
[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)
[12]	(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.
[14]	Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation[J]. Nature, 2011, 469(7330): 323-335.
[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.
[16]	Schmid D, Münz C. Innate and adaptive immunity through autophagy[J]. Immunity, 2007, 27(1): 11-21.
[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.
[18]	Van Kooten C, Banchereau J. CD40-CD40 ligand[J]. J Leukoc Biol, 2000, 67(1): 2-17.
[19]	Besteiro S. The role of host autophagy machinery in controlling Toxoplasma infection[J]. Virulence, 2019, 10(1): 438-447.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[28]	Kravets E, Degrandi D, Ma Q, et al. Guanylate binding proteins directly attack Toxoplasma gondii via supramolecular complexes[J]. Elife, 2016, 5: e11479.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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)
[39]	(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.
[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.
[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.
[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.
[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)
[46]	(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.
[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.
[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)
[49]	(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.
[51]	Bouzid M, Hunter PR, Chalmers RM, et al. Cryptosporidium pathogenicity and virulence[J]. Clin Microbiol Rev, 2013, 26(1): 115-134.
[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.
[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.
[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.