Full Text:   <1467>

Summary:  <455>

CLC number: 

On-line Access: 2022-01-12

Received: 2021-03-21

Revision Accepted: 2021-07-05

Crosschecked: 0000-00-00

Cited: 0

Clicked: 2530

Citations:  Bibtex RefMan EndNote GB/T7714


Qianqian ZHENG


Liangwei DUAN




-   Go to

Article info.
Open peer comments

Journal of Zhejiang University SCIENCE B 2022 Vol.23 No.1 P.19-41


A dynamically evolving war between autophagy and pathogenic microorganisms

Author(s):  Qianqian ZHENG, Liangwei DUAN, Yang ZHANG, Jiaoyang LI, Shiyu ZHANG, Hui WANG

Affiliation(s):  Henan Key Laboratory of Immunology and Targeted Drugs, School of Laboratory Medicine, Xinxiang Medical University, Xinxiang 453003, China; more

Corresponding email(s):   wanghui@xxmu.edu.cn

Key Words:  Autophagy, Pathogenic microorganism, Bacteria, Virus, Fungi, Parasite

Qianqian ZHENG, Liangwei DUAN, Yang ZHANG, Jiaoyang LI, Shiyu ZHANG, Hui WANG. A dynamically evolving war between autophagy and pathogenic microorganisms[J]. Journal of Zhejiang University Science B, 2022, 23(1): 19-41.

@article{title="A dynamically evolving war between autophagy and pathogenic microorganisms",
author="Qianqian ZHENG, Liangwei DUAN, Yang ZHANG, Jiaoyang LI, Shiyu ZHANG, Hui WANG",
journal="Journal of Zhejiang University Science B",
publisher="Zhejiang University Press & Springer",

%0 Journal Article
%T A dynamically evolving war between autophagy and pathogenic microorganisms
%A Qianqian ZHENG
%A Liangwei DUAN
%A Jiaoyang LI
%A Shiyu ZHANG
%J Journal of Zhejiang University SCIENCE B
%V 23
%N 1
%P 19-41
%@ 1673-1581
%D 2022
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2100285

T1 - A dynamically evolving war between autophagy and pathogenic microorganisms
A1 - Qianqian ZHENG
A1 - Liangwei DUAN
A1 - Yang ZHANG
A1 - Jiaoyang LI
A1 - Shiyu ZHANG
A1 - Hui WANG
J0 - Journal of Zhejiang University Science B
VL - 23
IS - 1
SP - 19
EP - 41
%@ 1673-1581
Y1 - 2022
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2100285

autophagy is an intracellular degradation process that maintains cellular homeostasis. It is essential for protecting organisms from environmental stress. autophagy can help the host to eliminate invading pathogens, including bacteria, viruses, fungi, and parasites. However, pathogens have evolved multiple strategies to interfere with autophagic signaling pathways or inhibit the fusion of autophagosomes with lysosomes to form autolysosomes. Moreover, host cell matrix degradation by different types of autophagy can be used for the proliferation and reproduction of pathogens. Thus, determining the roles and mechanisms of autophagy during pathogen infections will promote understanding of the mechanisms of pathogen‍‒‍host interactions and provide new strategies for the treatment of infectious diseases.




Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article


[1]Abdoli A, Alirezaei M, Mehrbod P, et al., 2018. Autophagy: the multi-purpose bridge in viral infections and host cells. Rev Med Virol, 28(4):e1973.

[2]Ahmad L, Mostowy S, Sancho-Shimizu V, 2018. Autophagy-virus interplay: from cell biology to human disease. Front Cell Dev Biol, 6:155.

[3]Allen EA, Amato C, Fortier TM, et al., 2020. A conserved myotubularin-related phosphatase regulates autophagy by maintaining autophagic flux. J Cell Biol, 219(11):e201909073.

[4]Alvarez VE, Kosec G, Sant'Anna C, et al., 2008. Autophagy is involved in nutritional stress response and differentiation in Trypanosoma cruzi. J Biol Chem, 283(6):3454-3464.

[5]Anand PK, Tait SWG, Lamkanfi M, et al., 2011. TLR2 and RIP2 pathways mediate autophagy of Listeria monocytogenes via extracellular signal-regulated kinase (ERK) activation. J Biol Chem, 286(50):42981-42991.

[6]Andriantsitohaina R, Papon N, 2020. Extracellular vesicles: new bullets to fight fungal infections. Trends Cell Biol, 30(8):589-590.

[7]Arasaki K, Mikami Y, Shames SR, et al., 2017. Legionella effector Lpg1137 shuts down ER-mitochondria communication through cleavage of syntaxin 17. Nat Commun, 8:15406.

[8]Attias M, Teixeira DE, Benchimol M, et al., 2020. The life-cycle of Toxoplasma gondii reviewed using animations. Parasit Vectors, 13:588.

[9]Backues SK, Orban DP, Bernard A, et al., 2015. Atg23 and Atg27 act at the early stages of Atg9 trafficking in S. cerevisiae. Traffic, 16(2):172-190.

[10]Bah A, Vergne I, 2017. Macrophage autophagy and bacterial infections. Front Immunol, 8:1483.

[11]Bain JM, Louw J, Lewis LE, et al., 2014. Candida albicans hypha formation and mannan masking of β-glucan inhibit macrophage phagosome maturation. mBio, 5(6):e01874-14.

[12]Barnett TC, Liebl D, Seymour LM, et al., 2013. The globally disseminated M1T1 clone of group A Streptococcus evades autophagy for intracellular replication. Cell Host Microbe, 14(6):675-682.

[13]Bauckman KA, Owusu-Boaitey N, Mysorekar IU, 2015. Selective autophagy: xenophagy. Methods, 75:120-127.

[14]Birmingham CL, Smith AC, Bakowski MA, et al., 2006. Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J Biol Chem, 281(16):11374-11383.

[15]Birmingham CL, Canadien V, Gouin E, et al., 2007. Listeria monocytogenes evades killing by autophagy during colonization of host cells. Autophagy, 3(5):442-451.

[16]Cadwell K, 2016. Crosstalk between autophagy and inflammatory signalling pathways: balancing defence and homeostasis. Nat Rev Immunol, 16(11):661-675.

[17]Cardenal-Muñoz E, Arafah S, López-Jiménez AT, et al., 2017. Mycobacterium marinum antagonistically induces an autophagic response while repressing the autophagic flux in a TORC1- and ESX-1-dependent manner. PLoS Pathog, 13(4):e1006344.

[18]Chang TK, Shravage BV, Hayes SD, et al., 2013. Uba1 functions in Atg7- and Atg3-independent autophagy. Nat Cell Biol, 15(9):1067-1078.

[19]Channappanavar R, Zhao JC, Perlman S, 2014. T cell-mediated immune response to respiratory coronaviruses. Immunol Res, 59:118-128.

[20]Chen G, Han Z, Feng D, et al., 2014. A regulatory signaling loop comprising the PGAM5 phosphatase and CK2 controls receptor-mediated mitophagy. Mol Cell, 54(3):362-377.

[21]Chen XJ, Wang K, Xing YL, et al., 2014. Coronavirus membrane-associated papain-like proteases induce autophagy through interacting with Beclin1 to negatively regulate antiviral innate immunity. Protein Cell, 5(12):912-927.

[22]Cheng JL, Fujita A, Yamamoto H, et al., 2014. Yeast and mammalian autophagosomes exhibit distinct phosphatidylinositol 3-phosphate asymmetries. Nat Commun, 5:3207.

[23]Cheng MI, Chen C, Engström P, et al., 2018. Actin-based motility allows Listeria monocytogenes to avoid autophagy in the macrophage cytosol. Cell Microbiol, 20(9):e12854.

[24]Cheng YL, Kuo CF, Lu SL, et al., 2019. Group A streptococcus induces LAPosomes via SLO/β1 integrin/NOX2/ROS pathway in endothelial cells that are ineffective in bacterial killing and suppress xenophagy. mBio, 10(5):e02148-19.

[25]Chew LH, Lu S, Liu X, et al., 2015. Molecular interactions of the Saccharomyces cerevisiae Atg1 complex provide insights into assembly and regulatory mechanisms. Autophagy, 11(6):891-905.

[26]Choi Y, Bowman JW, Jung JU, 2018. Autophagy during viral infection—a double-edged sword. Nat Rev Microbiol, 16(6):341-354.

[27]Choy A, Dancourt J, Mugo B, et al., 2012. The Legionella effector RavZ inhibits host autophagy through irreversible Atg8 deconjugation. Science, 338(6110):1072-1076.

[28]Chun Y, Kim J, 2018. Autophagy: an essential degradation program for cellular homeostasis and life. Cells, 7(12):278.

[29]Coppens I, 2017. How Toxoplasma and malaria parasites defy first, then exploit host autophagic and endocytic pathways for growth. Curr Opin Microbiol, 40:32-39.

[30]Coppens I, dan Dunn J, Romano JD, et al., 2006. Toxoplasma gondii sequesters lysosomes from mammalian hosts in the vacuolar space. Cell, 125(2):261-274.

[31]Coulon PG, Richetta C, Rouers A, et al., 2016. HIV-infected dendritic cells present endogenous MHC class II-restricted antigens to HIV-specific CD4+ T cells. J Immunol, 197(2):517-532.

[32]Dai XF, Zhu ML, 2020. Coupling of ribosome synthesis and translational capacity with cell growth. Trends Biochem Sci, 45(8):681-692.

[33]Deretic V, 2010. Autophagy in infection. Curr Opin Cell Biol, 22(2):252-262.

[34]Deretic V, 2012. Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors. Curr Opin Immunol, 24(1):21-31.

[35]Deretic V, Levine B, 2009. Autophagy, immunity, and microbial adaptations. Cell Host Microbe, 5(6):527-549.

[36]Desai M, Fang R, Sun JR, 2015. The role of autophagy in microbial infection and immunity. Immunotargets Ther, 4:13-26.

[37]Dong B, Liu XH, Lu JP, et al., 2009. MgAtg9 trafficking in Magnaporthe oryzae. Autophagy, 5(7):946-953.

[38]Dortet L, Mostowy S, Louaka AS, et al., 2011. Recruitment of the major vault protein by InlK: a Listeria monocytogenes strategy to avoid autophagy. PLoS Pathog, 7(8):e1002168.

[39]Duan LW, Zheng QQ, Zhang HX, et al., 2020. The SARS-CoV-2 spike glycoprotein biosynthesis, structure, function, and antigenicity: implications for the design of spike-based vaccine immunogens. Front Immunol, 11:576622.

[40]Duhring S, Germerodt S, Skerka C, et al., 2015. Host-pathogen interactions between the human innate immune system and Candida albicans—understanding and modeling defense and evasion strategies. Front Microbiol, 6:625.

[41]Ehlers MRW, 2000. CR3: a general purpose adhesion-recognition receptor essential for innate immunity. Microbes Infect, 2(3):289-294.

[42]Farag NS, Breitinger U, Breitinger HG, et al., 2020. Viroporins and inflammasomes: a key to understand virus-induced inflammation. Int J Biochem Cell Biol, 122:105738.

[43]Farré JC, Subramani S, 2016. Mechanistic insights into selective autophagy pathways: lessons from yeast. Nat Rev Mol Cell Biol, 17(9):537-552.

[44]Feng YC, He D, Yao ZY, et al., 2014. The machinery of macroautophagy. Cell Res, 24(1):24-41.

[45]Fujioka Y, Alam JM, Noshiro D, et al., 2020. Phase separation organizes the site of autophagosome formation. Nature, 578(7794):301-305.

[46]Fung TS, Liu DX, 2019. The ER stress sensor IRE1 and MAP kinase ERK modulate autophagy induction in cells infected with coronavirus infectious bronchitis virus. Virology, 533:34-44.

[47]Gao DM, Zhang J, Zhao J, et al., 2014. Autophagy activated by Toxoplasma gondii infection in turn facilitates Toxoplasma gondii proliferation. Parasitol Res, 113(6):2053-2058.

[48]Gassen NC, Niemeyer D, Muth D, et al., 2019. SKP2 attenuates autophagy through Beclin1-ubiquitination and its inhibition reduces MERS-coronavirus infection. Nat Commun, 10:5770.

[49]Ghartey-Kwansah G, Adu-Nti F, Aboagye B, et al., 2020a. Autophagy in the control and pathogenesis of parasitic infections. Cell Biosci, 10:101.

[50]Ghartey-Kwansah G, Aboagye B, Adu-Nti F, et al., 2020b. Clearing or subverting the enemy: role of autophagy in protozoan infections. Life Sci, 247:117453.

[51]Ghislat G, Lawrence T, 2018. Autophagy in dendritic cells. Cell Mol Immunol, 15(11):944-952.

[52]Glick D, Barth S, Macleod KF, 2010. Autophagy: cellular and molecular mechanisms. J Pathol, 221(1):3-12.

[53]Gluschko A, Herb M, Wiegmann K, et al., 2018. The β2 integrin Mac-1 induces protective LC3-associated phagocytosis of Listeria monocytogenes. Cell Host Microbe, 23(3):324-337.e5.

[54]González A, Hall MN, 2017. Nutrient sensing and TOR signaling in yeast and mammals. EMBO J, 36(4):397-408.

[55]Guardia CM, Tan XF, Lian TF, et al., 2020. Structure of human ATG9A, the only transmembrane protein of the core autophagy machinery. Cell Rep, 31(13):107837.

[56]Gui X, Yang H, Li T, et al., 2019. Autophagy induction via STING trafficking is a primordial function of the cGAS pathway. Nature, 567(7747):262-266.

[57]Guo XZ, Zhang MJ, Zhang XQ, et al., 2017. Porcine epidemic diarrhea virus induces autophagy to benefit its replication. Viruses, 9(3):53.

[58]Halonen SK, Taylor GA, Weiss LM, 2001. Gamma interferon-induced inhibition of Toxoplasma gondii in astrocytes is mediated by IGTP. Infect Immun, 69(9):5573-5576.

[59]Hamasaki M, Furuta N, Matsuda A, et al., 2013. Autophagosomes form at ER-mitochondria contact sites. Nature, 495(7441):389-393.

[60]Harada K, Kotani T, Kirisako H, et al., 2019. Two distinct mechanisms target the autophagy-related E3 complex to the pre-autophagosomal structure. eLife, 8:e43088.

[61]He CC, Song H, Yorimitsu T, et al., 2006. Recruitment of Atg9 to the preautophagosomal structure by Atg11 is essential for selective autophagy in budding yeast. J Cell Biol, 175(6):925-935.

[62]Heckmann BL, Green DR, 2019. LC3-associated phagocytosis at a glance. J Cell Sci, 132(5):jcs222984.

[63]Heckmann BL, Boada-Romero E, Cunha LD, et al., 2017. LC3-associated phagocytosis and inflammation. J Mol Biol, 429(23):3561-3576.

[64]Hu W, Chan H, Lu L, et al., 2020. Autophagy in intracellular bacterial infection. Semin Cell Dev Biol, 101:41-50.

[65]Huett A, Heath RJ, Begun J, et al., 2012. The LRR and RING domain protein LRSAM1 is an E3 ligase crucial for ubiquitin-dependent autophagy of intracellular Salmonella typhimurium. Cell Host Microbe, 12(6):778-790.

[66]Huss A, Derks LAN, Heederik DJJ, et al., 2020. Green waste compost as potential reservoirs of Legionella in the Netherlands. Clin Microbiol Infec, 26(9):1259.e1-1259.e3.

[67]Hytönen J, Haataja S, Gerlach D, et al., 2001. The SpeB virulence factor of Streptococcus pyogenes, a multifunctional secreted and cell surface molecule with strepadhesin, laminin-binding and cysteine protease activity. Mol Microbiol, 39(2):512-519.

[68]Itakura E, Kishi-Itakura C, Mizushima N, 2012. The hairpin-type tail-anchored SNARE syntaxin 17 targets to autophagosomes for fusion with endosomes/lysosomes. Cell, 151(6):1256-1269.

[69]Jaber N, Zong WX, 2013. Class III PI3K Vps34: essential roles in autophagy, endocytosis, and heart and liver function. Ann N Y Acad Sci, 1280(1):48-51.

[70]Jennings E, Thurston TLM, Holden DW, 2017. Salmonella SPI-2 type III secretion system effectors: molecular mechanisms and physiological consequences. Cell Host Microbe, 22(2):217-231.

[71]Joo JH, Dorsey FC, Joshi A, et al., 2011. Hsp90-Cdc37 chaperone complex regulates Ulk1- and Atg13-mediated mitophagy. Mol Cell, 43(4):572-585.

[72]Kagan JC, Stein MP, Pypaert M, et al., 2004. Legionella subvert the functions of Rab1 and Sec22b to create a replicative organelle. J Exp Med, 199(9):1201-1211.

[73]Kamada Y, Funakoshi T, Shintani T, et al., 2000. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol, 150(6):1507-1513.

[74]Kamber RA, Shoemaker CJ, Denic V, 2015. Receptor-bound targets of selective autophagy use a scaffold protein to activate the Atg1 kinase. Mol Cell, 59(3):372-381.

[75]Kanayama M, Shinohara ML, 2016. Roles of autophagy and autophagy-related proteins in antifungal immunity. Front Immunol, 7:47.

[76]Kanayama M, Inoue M, Danzaki K, et al., 2015. Autophagy enhances NFκB activity in specific tissue macrophages by sequestering A20 to boost antifungal immunity. Nat Commun, 6:5779.

[77]Kandul NP, Zhang T, Hay BA, et al., 2016. Selective removal of deletion-bearing mitochondrial DNA in heteroplasmic Drosophila. Nat Commun, 7:13100.

[78]Kato M, Yang YS, Sutter BM, et al., 2019. Redox state controls phase separation of the yeast ataxin-2 protein via reversible oxidation of its methionine-rich low-complexity domain. Cell, 177(3):711-721.e8.

[79]Kaushik S, Cuervo AM, 2018. The coming of age of chaperone-mediated autophagy. Nat Rev Mol Cell Biol, 19(6):365-381.

[80]Kawabata T, Yoshimori T, 2020. Autophagosome biogenesis and human health. Cell Discov, 6:33.

[81]Kawamata T, Kamada Y, Kabeya Y, et al., 2008. Organization of the pre-autophagosomal structure responsible for autophagosome formation. Mol Biol Cell, 19(5):2039-2050.

[82]Keil E, Höcker R, Schuster M, et al., 2013. Phosphorylation of Atg5 by the Gadd45β‍‍‒‍MEKK4-p38 pathway inhibits autophagy. Cell Death Differ, 20(2):321-332.

[83]Kihara A, Noda T, Ishihara N, et al., 2001. Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol, 152(3):519-530.

[84]Kim J, Kundu M, Viollet B, et al., 2011. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol, 13(2):132-141.

[85]Kim SI, Kim S, Kim E, et al., 2018. Secretion of Salmonella pathogenicity island 1-encoded type III secretion system effectors by outer membrane vesicles in Salmonella enterica serovar typhimurium. Front Microbiol, 9:2810.

[86]Kimmey JM, Stallings CL, 2016. Bacterial pathogens versus autophagy: implications for therapeutic interventions. Trends Mol Med, 22(12):1060-1076.

[87]Kirkin V, Rogov VV, 2019. A diversity of selective autophagy receptors determines the specificity of the autophagy pathway. Mol Cell, 76(2):268-285.

[88]Kishi-Itakura C, Ktistakis NT, Buss F, 2020. Ultrastructural insights into pathogen clearance by autophagy. Traffic, 21(4):310-323.

[89]Kobayashi S, Koujin T, Kojidani T, et al., 2015. BAF is a cytosolic DNA sensor that leads to exogenous DNA avoiding autophagy. Proc Natl Acad Sci USA, 112(22):7027-7032.

[90]Kocaturk NM, Gozuacik D, 2018. Crosstalk between mammalian autophagy and the ubiquitin-proteasome system. Front Cell Dev Biol, 6:128.

[91]Kotani T, Kirisako H, Koizumi M, et al., 2018. The Atg2-Atg18 complex tethers pre-autophagosomal membranes to the endoplasmic reticulum for autophagosome formation. Proc Natl Acad Sci USA, 115(41):10363-10368.

[92]Kourtis N, Tavernarakis N, 2009. Autophagy and cell death in model organisms. Cell Death Differ, 16(1):21-30.

[93]Kumsta C, Chang JT, Schmalz J, et al., 2017. Hormetic heat stress and HSF-1 induce autophagy to improve survival and proteostasis in C. elegans. Nat Commun, 8:14337.

[94]Kyrmizi I, Gresnigt MS, Akoumianaki T, et al., 2013. Corticosteroids block autophagy protein recruitment in Aspergillus fumigatus phagosomes via targeting dectin-1/Syk kinase signaling. J Immunol, 191(3):1287-1299.

[95]Lecuit M, 2020. Listeria monocytogenes, a model in infection biology. Cell Microbiol, 22(4):e13186.

[96]Lee YK, Lee JA, 2016. Role of the mammalian ATG8/LC3 family in autophagy: differential and compensatory roles in the spatiotemporal regulation of autophagy. BMB Rep, 49(8):424-430.

[97]Levine B, 2005. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell, 120(2):159-162.

[98]Levine B, Klionsky DJ, 2004. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell, 6(4):463-477.

[99]Li L, Zhu XM, Su ZZ, et al., 2021. Insights of roles played by septins in pathogenic fungi. Virulence, 12(1):1550-1562.

[100]Li XH, He SK, Ma BY, 2020. Autophagy and autophagy-related proteins in cancer. Mol Cancer, 19:12.

[101]Li XZ, Yan XH, 2019. Sensors for the mTORC1 pathway regulated by amino acids. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 20(9):699-712.

[102]Lin PW, Chu ML, Liu HS, 2021. Autophagy and metabolism. Kaohsiung J Med Sci, 37(1):12-19.

[103]Ling YM, Shaw MH, Ayala C, et al., 2006. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J Exp Med, 203(9):2063-2071.

[104]Liu D, Wu H, Wang CG, et al., 2019. STING directly activates autophagy to tune the innate immune response. Cell Death Differ, 26(9):1735-1749.

[105]Liu TB, Liu XH, Lu JP, et al., 2010. The cysteine protease MoAtg4 interacts with MoAtg8 and is required for differentiation and pathogenesis in Magnaporthe oryzae. Autophagy, 6(1):74-85.

[106]Liu XH, Lin FC, 2008. Investigation of the biological roles of autophagy in appressorium morphogenesis in Magnaporthe oryzae. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 9(10):793-796.

[107]Liu XH, Gao HM, Xu F, et al., 2012. Autophagy vitalizes the pathogenicity of pathogenic fungi. Autophagy, 8(10):1415-1425.

[108]Liu XH, Zhao YH, Zhu XM, et al., 2017. Autophagy-related protein MoAtg14 is involved in differentiation, development and pathogenicity in the rice blast fungus Magnaporthe oryzae. Sci Rep, 7:40018.

[109]Loewith R, Jacinto E, Wullschleger S, et al., 2002. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol Cell, 10(3):457-468.

[110]Loi M, Müller A, Steinbach K, et al., 2016. Macroautophagy proteins control MHC class I levels on dendritic cells and shape anti-viral CD8+ T cell responses. Cell Rep, 15(5):1076-1087.

[111]Lu SL, Kuo CF, Chen HW, et al., 2015. Insufficient acidification of autophagosomes facilitates group A streptococcus survival and growth in endothelial cells. mBio, 6(5):e01435-15.

[112]Lv YX, Fang L, Ding PS, et al., 2019. PI3K/Akt-Beclin1 signaling pathway positively regulates phagocytosis and negatively mediates NF-‍κB-dependent inflammation in Staphylococcus aureus-infected macrophages. Biochem Biophys Res Commun, 510(2):284-289.

[113]Ma J, Underhill DM, 2013. β‍-glucan signaling connects phagocytosis to autophagy. Glycobiology, 23(9):1047-1051.

[114]Ma J, Becker C, Lowell CA, et al., 2012. Dectin-1-triggered recruitment of light chain 3 protein to phagosomes facilitates major histocompatibility complex class II presentation of fungal-derived antigens. J Biol Chem, 287(41):34149-34156.

[115]Maier HJ, Cottam EM, Stevenson-Leggett P, et al., 2013. Visualizing the autophagy pathway in avian cells and its application to studying infectious bronchitis virus. Autophagy, 9(4):496-509.

[116]Maphasa RE, Meyer M, Dube A, 2021. The macrophage response to Mycobacterium tuberculosis and opportunities for autophagy inducing nanomedicines for tuberculosis therapy. Front Cell Infect Microbiol, 10:618414.

[117]Martens S, Parvanova I, Zerrahn J, et al., 2005. Disruption of Toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog, 1(3):e24.

[118]Martinez J, Almendinger J, Oberst A, et al., 2011. Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells. Proc Natl Acad Sci USA, 108(42):17396-17401.

[119]Martinez J, Malireddi RKS, Lu Q, et al., 2015. Molecular characterization of LC3-associated phagocytosis reveals distinct roles for Rubicon, NOX2 and autophagy proteins. Nat Cell Biol, 17(7):893-906.

[120]Matscheko N, Mayrhofer P, Rao YJ, et al., 2019. Atg11 tethers Atg9 vesicles to initiate selective autophagy. PLoS Biol, 17(7):e3000377.

[121]Matsunaga K, Morita E, Saitoh T, et al., 2010. Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J Cell Biol, 190(4):511-521.

[122]Melzer T, Duffy A, Weiss LM, et al., 2008. The gamma interferon (IFN-γ)-inducible GTP-binding protein IGTP is necessary for Toxoplasma vacuolar disruption and induces parasite egression in IFN-‍γ‍-stimulated astrocytes. Infect Immun, 76(11):4883-4894.

[123]Mestre MB, Colombo MI, 2012. cAMP and EPAC are key players in the regulation of the signal transduction pathway involved in the α-hemolysin autophagic response. PLoS Pathog, 8(5):e1002664.

[124]Mestre MB, Fader CM, Sola C, et al., 2010. α‍-Hemolysin is required for the activation of the autophagic pathway in Staphylococcus aureus infected cells. Autophagy, 6(1):110-125.

[125]Mijaljica D, Prescott M, Devenish RJ, 2011. Microautophagy in mammalian cells: revisiting a 40-year-old conundrum. Autophagy, 7(7):673-682.

[126]Min JS, Kim DE, Jin YH, et al., 2020. Kurarinone inhibits HCoV-OC43 infection by impairing the virus-induced autophagic flux in MRC-5 human lung cells. J Clin Med, 9(7):2230.

[127]Miramón P, Dunker C, Windecker H, et al., 2012. Cellular responses of Candida albicans to phagocytosis and the extracellular activities of neutrophils are critical to counteract carbohydrate starvation, oxidative and nitrosative stress. PLoS ONE, 7(12):e52850.

[128]Mitchell G, Ge L, Huang QY, et al., 2015. Avoidance of autophagy mediated by PlcA or ActA is required for Listeria monocytogenes growth in macrophages. Infect Immun, 83(5):2175-2184.

[129]Mizushima N, Komatsu M, 2011. Autophagy: renovation of cells and tissues. Cell, 147(4):728-741.

[130]Mogensen TH, Paludan SR, 2001. Molecular pathways in virus-induced cytokine production. Microbiol Mol Biol Rev, 65(1):131-150.

[131]Mostowy S, 2013. Autophagy and bacterial clearance: a not so clear picture. Cell Microbiol, 15(3):395-402.

[132]Nakagawa I, Amano A, Mizushima N, et al., 2004. Autophagy defends cells against invading group A Streptococcus. Science, 306(5698):1037-1040.

[133]Narendra D, Tanaka A, Suen DF, et al., 2008. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol, 183(5):795-803.

[134]Neumann Y, Bruns SA, Rohde M, et al., 2016. Intracellular Staphylococcus aureus eludes selective autophagy by activating a host cell kinase. Autophagy, 12(11):2069-2084.

[135]Nicola AM, Albuquerque P, Martinez LR, et al., 2012. Macrophage autophagy in immunity to Cryptococcus neoformans and Candida albicans. Infect Immun, 80(9):3065-3076.

[136]Noad J, von der Malsburg A, Pathe C, et al., 2017. LUBAC-synthesized linear ubiquitin chains restrict cytosol-invading bacteria by activating autophagy and NF-κB. Nat Microbiol, 2(7):17063.

[137]Obara K, Ohsumi Y, 2011. PtdIns 3-kinase orchestrates autophagosome formation in yeast. J Lipids, 2011:498768.

[138]Ogawa M, Mimuro H, Yoshikawa Y, et al., 2011. Manipulation of autophagy by bacteria for their own benefit. Microbiol Immunol, 55(7):459-471.

[139]Öhman T, Teirilä L, Lahesmaa-Korpinen AM, et al., 2014. Dectin-1 pathway activates robust autophagy-dependent unconventional protein secretion in human macrophages. J Immunol, 192(12):5952-5962.

[140]Ohshima J, Lee Y, Sasai M, et al., 2014. Role of mouse and human autophagy proteins in IFN-‍γ‍-induced cell-autonomous responses against Toxoplasma gondii. J Immunol, 192(7):3328-3335.

[141]Okamoto S, Nagase S, 2018. Pathogenic mechanisms of invasive group a Streptococcus infections by influenza virus-group A Streptococcus superinfection. Microbiol Immunol, 62(3):141-149.

[142]Orvedahl A, Levine B, 2008. Viral evasion of autophagy. Autophagy, 4(3):280-285.

[143]Otto M, 2014. Staphylococcus aureus toxins. Curr Opin Microbiol, 17:32-37.

[144]Pauwels AM, Trost M, Beyaert R, et al., 2017. Patterns, receptors, and signals: regulation of phagosome maturation. Trends Immunol, 38(6):407-422.

[145]Ploen D, Hildt E, 2015. Hepatitis C virus comes for dinner: how the hepatitis C virus interferes with autophagy. World J Gastroenterol, 21(28):8492-8507.

[146]Polajnar M, Dietz MS, Heilemann M, et al., 2017. Expanding the host cell ubiquitylation machinery targeting cytosolic Salmonella. EMBO Rep, 18(9):1572-1585.

[147]Portes J, Barrias E, Travassos R, et al., 2020. Toxoplasma gondii mechanisms of entry into host cells. Front Cell Infect Microbiol, 10:294.

[148]Prentice E, Jerome WG, Yoshimori T, et al., 2004a. Coronavirus replication complex formation utilizes components of cellular autophagy. J Biol Chem, 279(11):10136-10141.

[149]Prentice E, McAuliffe J, Lu XT, et al., 2004b. Identification and characterization of severe acute respiratory syndrome coronavirus replicase proteins. J Virol, 78(18):9977-9986.

[150]Py BF, Lipinski MM, Yuan JY, 2007. Autophagy limits Listeria monocytogenes intracellular growth in the early phase of primary infection. Autophagy, 3(2):117-125.

[151]Queval CJ, Brosch R, Simeone R, 2017. The macrophage: a disputed fortress in the battle against Mycobacterium tuberculosis. Front Microbiol, 8:2284.

[152]Raught B, Gingras AC, Sonenberg N, 2001. The target of rapamycin (TOR) proteins. Proc Natl Acad Sci USA, 98(13):7037-7044.

[153]Ravenhill BJ, Boyle KB, von Muhlinen N, et al., 2019. The cargo receptor NDP52 initiates selective autophagy by recruiting the ULK complex to cytosol-invading bacteria. Mol Cell, 74(2):320-329.e6.

[154]Reggiori F, Tucker KA, Stromhaug PE, et al., 2004. The Atg1-Atg13 complex regulates Atg9 and Atg23 retrieval transport from the pre-autophagosomal structure. Dev Cell, 6(1):79-90.

[155]Reggiori F, Monastyrska I, Shintani T, et al., 2005a. The actin cytoskeleton is required for selective types of autophagy, but not nonspecific autophagy, in the yeast Saccharomyces cerevisiae. Mol Biol Cell, 16(12):5843-5856.

[156]Reggiori F, Shintani T, Chong H, et al., 2005b. Atg9 cycles between mitochondria and the pre-autophagosomal structure in yeasts. Autophagy, 1(2):101-109.

[157]Reggiori F, Monastyrska I, Verheije MH, et al., 2010. Coronaviruses hijack the LC3-I-positive edemosomes, ER-derived vesicles exporting short-lived ERAD regulators, for replication. Cell Host Microbe, 7(6):500-508.

[158]Reggiori F, Komatsu M, Finley K, et al., 2012. Autophagy: more than a nonselective pathway. Int J Cell Biol, 2012:219625.

[159]Richards AL, Jackson WT, 2012. Intracellular vesicle acidification promotes maturation of infectious poliovirus particles. PLoS Pathog, 8(11):e1003046.

[160]Romano PS, Arboit MA, Vázquez CL, et al., 2009. The autophagic pathway is a key component in the lysosomal dependent entry of Trypanosoma cruzi into the host cell. Autophagy, 5(1):6-18.

[161]Rudkin FM, Bain JM, Walls C, et al., 2013. Altered dynamics of Candida albicans phagocytosis by macrophages and PMNs when both phagocyte subsets are present. mBio, 4(6):e00810-13.

[162]Rudnicka W, Kaczmarek M, Szeliga J, et al., 1997. The host response to Listeria monocytogenes mutants defective in genes encoding phospholipases C (plcA, plcB) and actin assembly (actA). Microbiol Immunol, 41(11):847-853.

[163]Ruland J, Hartjes L, 2019. CARD‒BCL-10‒MALT1 signalling in protective and pathological immunity. Nat Rev Immunol, 19(2):118-134.

[164]Sakurai A, Maruyama F, Funao J, et al., 2010. Specific behavior of intracellular Streptococcus pyogenes that has undergone autophagic degradation is associated with bacterial streptolysin O and host small G proteins Rab5 and Rab7. J Biol Chem, 285(29):22666-22675.

[165]Salassa BN, Romano PS, 2019. Autophagy: a necessary process during the Trypanosoma cruzi life-cycle. Virulence, 10(1):460-469.

[166]Salazar F, Brown GD, 2018. Antifungal innate immunity: a perspective from the last 10 years. J Innate Immun, 10(5-6): 373-397.

[167]Sanjuan MA, Dillon CP, Tait SWG, et al., 2007. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature, 450(7173):1253-1257.

[168]Sasai M, Yamamoto M, 2019. Innate, adaptive, and cell-autonomous immunity against Toxoplasma gondii infection. Exp Mol Med, 51(12):1-10.

[169]Schille S, Crauwels P, Bohn R, et al., 2018. LC3-associated phagocytosis in microbial pathogenesis. Int J Med Microbiol, 308(1):228-236.

[170]Schnaith A, Kashkar H, Leggio SA, et al., 2007. Staphylococcus aureus subvert autophagy for induction of caspase-independent host cell death. J Biol Chem, 282(4):2695-2706.

[171]Schneider M, Ackermann K, Stuart M, et al., 2012. Severe acute respiratory syndrome coronavirus replication is severely impaired by MG132 due to proteasome-independent inhibition of m-calpain. J Virol, 86(18):10112-10122.

[172]Schuck S, 2020. Microautophagy-distinct molecular mechanisms handle cargoes of many sizes. J Cell Sci, 133(17):jcs246322.

[173]Scott SV, Guan J, Hutchins MU, et al., 2001. Cvt19 is a receptor for the cytoplasm-to-vacuole targeting pathway. Mol Cell, 7(6):1131-1141.

[174]Sekito T, Kawamata T, Ichikawa R, et al., 2009. Atg17 recruits Atg9 to organize the pre-autophagosomal structure. Genes Cells, 14(5):525-538.

[175]Shi CS, Kehrl JH, 2008. MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages. J Biol Chem, 283(48):33175-33182.

[176]Shintani T, Klionsky DJ, 2004a. Autophagy in health and disease: a double-edged sword. Science, 306(5698):990-995.

[177]Shintani T, Klionsky DJ, 2004b. Cargo proteins facilitate the formation of transport vesicles in the cytoplasm to vacuole targeting pathway. J Biol Chem, 279(29):29889-29894.

[178]Shroff A, Sequeira R, Patel V, et al., 2018. Knockout of autophagy gene, ATG5 in mice vaginal cells abrogates cytokine response and pathogen clearance during vaginal infection of Candida albicans. Cell Immunol, 324:59-73.

[179]Smeekens SP, Malireddi RK, Plantinga TS, et al., 2014. Autophagy is redundant for the host defense against systemic Candida albicans infections. Eur J Clin Microbiol Infect Dis, 33(5):711-722.

[180]Snijder EJ, van der Meer Y, Zevenhoven-Dobbe J, et al., 2006. Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J Virol, 80(12):5927-5940.

[181]Stévenin V, Chang YY, le Toquin Y, et al., 2019. Dynamic growth and shrinkage of the Salmonella-containing vacuole determines the intracellular pathogen niche. Cell Rep, 29(12):3958-3973.e7.

[182]Subauste CS, 2019. Interplay between Toxoplasma gondii, autophagy, and autophagy proteins. Front Cell Infect Microbiol, 9:139.

[183]Sudhakar P, Jacomin AC, Hautefort I, et al., 2019. Targeted interplay between bacterial pathogens and host autophagy. Autophagy, 15(9):1620-1633.

[184]Tam JM, Mansour MK, Khan NS, et al., 2014. Dectin-1-dependent LC3 recruitment to phagosomes enhances fungicidal activity in macrophages. J Infect Dis, 210(11):1844-1854.

[185]Tang J, Lin GX, Langdon WY, et al., 2018. Regulation of C-type lectin receptor-mediated antifungal immunity. Front Immunol, 9:123.

[186]Tanida I, Ueno T, Kominami E, 2008. LC3 and autophagy. Methods Mol Biol, 445:77-88.

[187]Tekirdag K, Cuervo AM, 2018. Chaperone-mediated autophagy and endosomal microautophagy: jointed by a chaperone. J Biol Chem, 293(15):5414-5424.

[188]Thurston TLM, Wandel MP, von Muhlinen N, et al., 2012. Galectin 8 targets damaged vesicles for autophagy to defend cells against bacterial invasion. Nature, 482(7385):414-418.

[189]Tian XJ, Gala U, Zhang YP, et al., 2015. A voltage-gated calcium channel regulates lysosomal fusion with endosomes and autophagosomes and is required for neuronal homeostasis. PLoS Biol, 13(3):e1002103.

[190]Towers CG, Thorburn A, 2016. Therapeutic targeting of autophagy. EBioMedicine, 14:15-23.

[191]Upadhyay S, Philips JA, 2019. LC3-associated phagocytosis: host defense and microbial response. Curr Opin Immunol, 60:81-90.

[192]Vita GM, de Simone G, Leboffe L, et al., 2020. Human serum albumin binds streptolysin O (SLO) toxin produced by group a Streptococcus and inhibits its cytotoxic and hemolytic effects. Front Immunol, 11:507092.

[193]Wang Y, Qin ZH, 2013. Coordination of autophagy with other cellular activities. Acta Pharmacol Sin, 34(5):585-594.

[194]Wang YB, Weiss LM, Orlofsky A, 2009. Host cell autophagy is induced by Toxoplasma gondii and contributes to parasite growth. J Biol Chem, 284(3):1694-1701.

[195]Wen N, Lv Q, Du ZG, 2020. MicroRNAs involved in drug resistance of breast cancer by regulating autophagy. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 21(9):690-702.

[196]Wieczorek M, Abualrous ET, Sticht J, et al., 2017. Major histocompatibility complex (MHC) class I and MHC class II proteins: conformational plasticity in antigen presentation. Front Immunol, 8:292.

[197]Wu MY, Lu JH, 2019. Autophagy and macrophage functions: inflammatory response and phagocytosis. Cells, 9(1):70.

[198]Xie ZP, Nair U, Klionsky DJ, 2008. Atg8 controls phagophore expansion during autophagosome formation. Mol Biol Cell, 19(8):3290-3298.

[199]Xiong QH, Yang M, Li P, et al., 2019. Bacteria exploit autophagy for their own benefit. Infect Drug Resist, 12:3205-3215.

[200]Yamamoto H, Kakuta S, Watanabe TM, et al., 2012. Atg9 vesicles are an important membrane source during early steps of autophagosome formation. J Cell Biol, 198(2):219-233.

[201]Yamasaki A, Watanabe Y, Adachi W, et al., 2016. Structural basis for receptor-mediated selective autophagy of aminopeptidase I aggregates. Cell Rep, 16(1):19-27.

[202]Yang YS, Kato M, Wu X, et al., 2019. Yeast ataxin-2 forms an intracellular condensate required for the inhibition of TORC1 signaling during respiratory growth. Cell, 177(3): 697-710.e17.

[203]Yi XH, Zhang B, Fu YR, et al., 2020. STAT1 and its related molecules as potential biomarkers in Mycobacterium tuberculosis infection. J Cell Mol Med, 24(5):2866-2878.

[204]Yin ZY, Pascual C, Klionsky DJ, 2016. Autophagy: machinery and regulation. Microb Cell, 3(12):588-596.

[205]Yin ZY, Liu X, Ariosa A, et al., 2019. Psp2, a novel regulator of autophagy that promotes autophagy-related protein translation. Cell Res, 29(12):994-1008.

[206]Yorimitsu T, Klionsky DJ, 2005. Autophagy: molecular machinery for self-eating. Cell Death Differ, 12(S2):‍1542-1552.

[207]Yoshikawa Y, Ogawa M, Hain T, et al., 2009. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat Cell Biol, 11(10):1233-1240.

[208]Yu ZQ, Sun LL, Jiang ZD, et al., 2020. Atg38-Atg8 interaction in fission yeast establishes a positive feedback loop to promote autophagy. Autophagy, 16(11):2036-2051.

[209]Yuan WP, Strømhaug PE, Dunn WA, 1999. Glucose-induced autophagy of peroxisomes in Pichia pastoris requires a unique E1-like protein. Mol Biol Cell, 10(5):1353-1366.

[210]Zachari M, Ganley IG, 2017. The mammalian ULK1 complex and autophagy initiation. Essays Biochem, 61(6):585-596.

[211]Zare-Bidaki M, Hakimi H, Abdollahi SH, et al., 2014. TLR4 in toxoplasmosis; friends or foe? Microb Pathog, 69-70:28-32.

[212]Zhai WJ, Wu FJ, Zhang YY, et al., 2019. The immune escape mechanisms of Mycobacterium tuberculosis. Int J Mol Sci, 20(2):340.

[213]Zhang XW, Bai XC, Chen ZJ, 2020. Structures and mechanisms in the cGAS-STING innate immunity pathway. Immunity, 53(1):43-53.

[214]Zhao MM, Wang RS, Zhou YL, et al., 2020. Emerging relationship between RNA helicases and autophagy. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 21(10):767-778.

[215]Zhao ZJ, Thackray LB, Miller BC, et al., 2007. Coronavirus replication does not require the autophagy gene ATG5. Autophagy, 3(6):581-585.

[216]Zhao ZJ, Fux B, Goodwin M, et al., 2008. Autophagosome-independent essential function for the autophagy protein Atg5 in cellular immunity to intracellular pathogens. Cell Host Microbe, 4(5):458-469.

[217]Zhu LQ, Mou CX, Yang X, et al., 2016. Mitophagy in TGEV infection counteracts oxidative stress and apoptosis. Oncotarget, 7(19):27122-27141.

[218]Zhu XM, Li L, Wu M, et al., 2019. Current opinions on autophagy in pathogenicity of fungi. Virulence, 10(1):481-489.

[219]Zientara-Rytter K, Subramani S, 2020. Mechanistic insights into the role of Atg11 in selective autophagy. J Mol Biol, 432(1):104-122.

Open peer comments: Debate/Discuss/Question/Opinion


Please provide your name, email address and a comment

Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - 2022 Journal of Zhejiang University-SCIENCE