Chemical modulation of SQSTM1/p62-mediated xenophagy that targets a broad range of pathogenic bacteria

References

• Shaid S, Brandts CH, Serve H, et al. Ubiquitination and selective autophagy. Cell Death Differ. 2013;20(1):21–30.
   PubMed Web of Science ®Google Scholar
• Gatica D, Lahiri V, Klionsky DJ. Cargo recognition and degradation by selective autophagy. Nat Cell Biol. 2018;20(3):233–242.
   PubMed Web of Science ®Google Scholar
• Birgisdottir AB, Lamark T, Johansen T. The LIR motif - crucial for selective autophagy. J Cell Sci. 2013;126(15):3237–3247.
   PubMed Web of Science ®Google Scholar
• Okamoto K. Organellophagy: eliminating cellular building blocks via selective autophagy. J Cell Biol. 2014;205(4):435–445.
   PubMed Web of Science ®Google Scholar
• Anding AL, Baehrecke EH. Cleaning house: selective autophagy of organelles. Dev Cell. 2017;41(1):10–22.
   PubMed Web of Science ®Google Scholar
• Ichimura Y, Waguri S, Sou YS, et al. Phosphorylation of SQSTM1 activates the Keap1-Nrf2 pathway during selective autophagy. Mol Cell. 2013;51(5):618–631.
   PubMed Web of Science ®Google Scholar
• Richter B, Sliter DA, Herhaus L, et al. Phosphorylation of OPTN by TBK1 enhances its binding to Ub chains and promotes selective autophagy of damaged mitochondria. Proc Natl Acad Sci U S A. 2016;113(15):4039–4044.
   PubMed Web of Science ®Google Scholar
• Sorbara MT, Girardin SE. Emerging themes in bacterial autophagy. Curr Opin Microbiol. 2015;23:163–170.
   PubMed Web of Science ®Google Scholar
• Pareja ME, Colombo MI. Autophagic clearance of bacterial pathogens: molecular recognition of intracellular microorganisms. Front Cell Infect Microbiol. 2013;3:54.
   PubMed Web of Science ®Google Scholar
• Ishimura R, Tanaka K, Komatsu M. Dissection of the role of p62/Sqstm1 in activation of Nrf2 during xenophagy. FEBS Lett. 2014;588(5):822–828.
   PubMed Web of Science ®Google Scholar
• Deretic V, Levine B. Autophagy, immunity, and microbial adaptations. Cell Host Microbe. 2009;5(6):527–549.
   PubMed Web of Science ®Google Scholar
• Noda T, Yoshimori T. Molecular basis of canonical and bactericidal autophagy. Int Immunol. 2009;21(11):1199–1204.
   PubMed Web of Science ®Google Scholar
• Levine B, Deretic V. Unveiling the roles of autophagy in innate and adaptive immunity. Nat Rev Immunol. 2007;7(10):767–777.
   PubMed Web of Science ®Google Scholar
• Vergne I, Singh S, Roberts E, et al. Autophagy in immune defense against Mycobacterium tuberculosis. Autophagy. 2006;2(3):175–178.
   PubMed Web of Science ®Google Scholar
• Rogov V, Dotsch V, Johansen T, et al. Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol Cell. 2014;53(2):167–178.
   PubMed Web of Science ®Google Scholar
• Wu Y, Cui J. Selective autophagy regulates innate immunity through cargo receptor network. Adv Exp Med Biol. 2019;1209:145–166.
   PubMed Web of Science ®Google Scholar
• Fracchiolla D, Sawa-Makarska J, Martens S. Beyond Atg8 binding: the role of AIM/LIR motifs in autophagy. Autophagy. 2017;13(5):978–979.
   PubMed Web of Science ®Google Scholar
• Thomas DR, Newton P, Lau N, et al. Interfering with autophagy: the opposing strategies deployed by Legionella pneumophila and Coxiella burnetii effector proteins. Front Cell Infect Microbiol. 2020;10:599762.
   PubMed Web of Science ®Google Scholar
• Kimmey JM, Stallings CL. Bacterial pathogens versus autophagy: implications for therapeutic interventions. Trends Mol Med. 2016;22(12):1060–1076.
   PubMed Web of Science ®Google Scholar
• Campoy E, Colombo MI. Autophagy subversion by bacteria. Curr Top Microbiol Immunol. 2009;335:167–178.
   Web of Science ®Google Scholar
• Yuk JM, Yoshimori T, Jo EK. Autophagy and bacterial infectious diseases. Exp Mol Med. 2012;44(2):99–108.
   PubMed Web of Science ®Google Scholar
• Knodler LA, Celli J. Eating the strangers within: host control of intracellular bacteria via xenophagy. Cell Microbiol. 2011;13(9):1319–1327.
   PubMed Web of Science ®Google Scholar
• Wu YW, Li F. Bacterial interaction with host autophagy. Virulence. 2019;10(1):352–362.
   PubMed Web of Science ®Google Scholar
• Huang J, Brumell JH. Bacteria-autophagy interplay: a battle for survival. Nat Rev Microbiol. 2014;12(2):101–114.
   PubMed Web of Science ®Google Scholar
• Escoll P, Rolando M, Buchrieser C. Modulation of host autophagy during bacterial infection: sabotaging host munitions for pathogen nutrition. Front Immunol. 2016;7:81.
   PubMed Web of Science ®Google Scholar
• Xie Z, Zhang Y, Huang X. Evidence and speculation: the response of Salmonella confronted by autophagy in macrophages. Future Microbiol. 2020;15(13):1277–1286.
   PubMed Web of Science ®Google Scholar
• Ganesan R, Hos NJ, Gutierrez S, et al. Salmonella Typhimurium disrupts Sirt1/AMPK checkpoint control of MTOR to impair autophagy. PLoS Pathog. 2017;13(2):e1006227.
   PubMed Web of Science ®Google Scholar
• Wu S, Shen Y, Zhang S, et al. Salmonella interacts with autophagy to offense or defense. Front Microbiol. 2020;11:721.
   PubMed Web of Science ®Google Scholar
• Jo EK, Yuk JM, Shin DM, et al. Roles of autophagy in elimination of intracellular bacterial pathogens. Front Immunol. 2013;4:97.
   PubMed Web of Science ®Google Scholar
• Manzanillo PS, Ayres JS, Watson RO, et al. The ubiquitin ligase parkin mediates resistance to intracellular pathogens. Nature. 2013;501(7468):512–516.
   PubMed Web of Science ®Google Scholar
• Franco LH, Nair VR, Scharn CR, et al. The ubiquitin ligase Smurf1 functions in selective autophagy of Mycobacterium tuberculosis and anti-tuberculous host defense. Cell Host Microbe. 2017;22(3):421–423.
   PubMed Web of Science ®Google Scholar
• Polajnar M, Dietz MS, Heilemann M, et al. Expanding the host cell ubiquitylation machinery targeting cytosolic Salmonella. EMBO Rep. 2017;18(9):1572–1585.
   PubMed Web of Science ®Google Scholar
• Huett A, Heath RJ, Begun J, et al. The LRR and RING domain protein LRSAM1 is an E3 ligase crucial for ubiquitin-dependent autophagy of intracellular Salmonella Typhimurium. Cell Host Microbe. 2012;12(6):778–790.
   PubMed Web of Science ®Google Scholar
• Noad J, von der Malsburg A, Pathe C, et al. LUBAC-synthesized linear ubiquitin chains restrict cytosol-invading bacteria by activating autophagy and NF-kappaB. Nat Microbiol. 2017;2(7):17063.
   PubMed Web of Science ®Google Scholar
• Slowicka K, van Loo G. Optineurin functions for optimal immunity. Front Immunol. 2018;9:769.
   PubMed Web of Science ®Google Scholar
• Wild P, Farhan H, McEwan DG, et al. Phosphorylation of the autophagy receptor optineurin restricts salmonella growth. Science. 2011;333(6039):228–233.
   PubMed Web of Science ®Google Scholar
• Lopez Romo A, Quiros R. Appropriate use of antibiotics: an unmet need. Ther Adv Urol. 2019;11:1756287219832174.
   Web of Science ®Google Scholar
• Fair RJ, Tor Y. Antibiotics and bacterial resistance in the 21st century. Perspect Medicin Chem. 2014;6:25–64.
   PubMedGoogle Scholar
• Aslam B, Wang W, Arshad MI, et al. Antibiotic resistance: a rundown of a global crisis. Infect Drug Resist. 2018;11:1645–1658.
   PubMed Web of Science ®Google Scholar
• Fauconnier A, Nagel TE, Fauconnier C, et al. The unique role that WHO could play in implementing phage therapy to combat the global antibiotic resistance crisis. Front Microbiol. 2020;11:1982.
   PubMedGoogle Scholar
• Mendelson M. Practical solutions to the antibiotic resistance crisis. S Afr Med J. 2015;105(5):413.
   PubMed Web of Science ®Google Scholar
• Kaufmann SHE, Dorhoi A, Hotchkiss RS, et al. Host-directed therapies for bacterial and viral infections. Nat Rev Drug Discov. 2018;17(1):35–56.
   PubMed Web of Science ®Google Scholar
• Tobin DM. Host-directed therapies for tuberculosis. Csh Perspect Med. 2015;5:a021196.
   Google Scholar
• Andersson AM, Andersson B, Lorell C, et al. Autophagy induction targeting MTORC1 enhances Mycobacterium tuberculosis replication in HIV co-infected human macrophages. Sci Rep. 2016;6(1):28171.
   PubMedGoogle Scholar
• Zullo AJ, Jurcic Smith KL, Lee S. Mammalian target of Rapamycin inhibition and mycobacterial survival are uncoupled in murine macrophages. BMC Biochem. 2014;15(1):4.
   PubMedGoogle Scholar
• Singhal A, Jie L, Kumar P, et al. Metformin as adjunct antituberculosis therapy. Sci Transl Med. 2014;6(263):263ra159.
   PubMed Web of Science ®Google Scholar
• Yang CS, Kim JJ, Lee HM, et al. The AMPK-PPARGC1A pathway is required for antimicrobial host defense through activation of autophagy. Autophagy. 2014;10(5):785–802.
   PubMed Web of Science ®Google Scholar
• Cheng CY, Gutierrez NM, Marzuki MB, et al. Host sirtuin 1 regulates mycobacterial immunopathogenesis and represents a therapeutic target against tuberculosis. Sci Immunol. 2017;2(9). DOI:10.1126/sciimmunol.aaj1789.
   Google Scholar
• Chiu HC, Kulp SK, Soni S, et al. Eradication of intracellular Salmonella enterica serovar typhimurium with a small-molecule, host cell-directed agent. Antimicrob Agents Chemother. 2009;53(12):5236–5244.
   PubMed Web of Science ®Google Scholar
• Nagy TA, Quintana JLJ, Reens AL, et al. Autophagy induction by a small molecule inhibits Salmonella survival in macrophages and mice. Antimicrob Agents Chemother. 2019;63(12). DOI:10.1128/AAC.01536-19.
   PubMedGoogle Scholar
• Tasaki T, Sriram SM, Park KS, et al. The N-end rule pathway. Annu Rev Biochem. 2012;81(1):261–289.
   PubMedGoogle Scholar
• Varshavsky A. N-degron and C-degron pathways of protein degradation. Proc Natl Acad Sci U S A. 2019;116(2):358–366.
   PubMed Web of Science ®Google Scholar
• Kwon YT, Kashina AS, Davydov IV, et al. An essential role of N-terminal arginylation in cardiovascular development. Science. 2002;297(5578):96–99.
   PubMed Web of Science ®Google Scholar
• Sriram SM, Kwon YT. The molecular principles of N-end rule recognition. Nat Struct Mol Biol.2010;17(10):1164–1165.
   PubMed Web of Science ®Google Scholar
• Sriram SM, Kim BY, Kwon YT. The N-end rule pathway: emerging functions and molecular principles of substrate recognition. Nat Rev Mol Cell Biol. 2011;12(11):735–747.
   PubMed Web of Science ®Google Scholar
• Yoo YD, Mun SR, Ji CH, et al. N-terminal arginylation generates a bimodal degron that modulates autophagic proteolysis. Proc Natl Acad Sci U S A. 2018;115(12):E2716–E24.
   PubMed Web of Science ®Google Scholar
• Cha-Molstad H, Sung KS, Hwang J, et al. Amino-terminal arginylation targets endoplasmic reticulum chaperone BiP for autophagy through SQSTM1 binding. Nat Cell Biol. 2015;17(7):917–929.
   PubMed Web of Science ®Google Scholar
• Cha-Molstad H, Yu JE, Feng Z, et al. p62/SQSTM1/Sequestosome-1 is an N-recognin of the N-end rule pathway which modulates autophagosome biogenesis. Nat Commun. 2017;8(1):102.
   PubMedGoogle Scholar
• Ji CH, Kim HY, Heo AJ, et al. The N-degron pathway mediates ER-phagy. Mol Cell. 2019;75(5):1058–72 e9.
   PubMed Web of Science ®Google Scholar
• Ciuffa R, Lamark T, Tarafder AK, et al. The selective autophagy receptor p62 forms a flexible filamentous helical scaffold. Cell Rep. 2015;11(5):748–758.
   PubMed Web of Science ®Google Scholar
• Wurzer B, Zaffagnini G, Fracchiolla D, et al. Oligomerization of p62 allows for selection of ubiquitinated cargo and isolation membrane during selective autophagy. Elife. 2015;4:e08941.
   PubMed Web of Science ®Google Scholar
• Rangaraju S, Verrier JD, Madorsky I, et al. Rapamycin activates autophagy and improves myelination in explant cultures from neuropathic mice. J Neurosci. 2010;30(34):11388–11397.
   PubMed Web of Science ®Google Scholar
• Rubinsztein DC, Nixon RA. Rapamycin induces autophagic flux in neurons. Proc Natl Acad Sci U S A. 2010;107(49):E181. author reply E2.
   PubMed Web of Science ®Google Scholar
• Gutierrez MG, Master SS, Singh SB, et al. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell. 2004;119(6):753–766.
   PubMed Web of Science ®Google Scholar
• Mayer-Barber KD, Barber DL. Innate and Adaptive Cellular Immune Responses to Mycobacterium tuberculosis Infection. Cold Spring Harb Perspect Med. 2015;5(12). DOI:10.1101/cshperspect.a018424
   PubMedGoogle Scholar
• Yoshikai Y. Immunological protection against Mycobacterium tuberculosis infection. Crit Rev Immunol. 2006;26(6):515–526.
   PubMed Web of Science ®Google Scholar
• Kraft C, Peter M, Hofmann K. Selective autophagy: ubiquitin-mediated recognition and beyond. Nat Cell Biol. 2010;12(9):836–841.
   PubMed Web of Science ®Google Scholar
• Zaffagnini G, Martens S. Mechanisms of Selective Autophagy. J Mol Biol. 2016;428(9):1714–1724.
   PubMed Web of Science ®Google Scholar
• Ammanathan V, Mishra P, Chavalmane AK, et al. Restriction of intracellular Salmonella replication by restoring TFEB-mediated xenophagy. Autophagy. 2020;16(9):1584–1597.
   PubMed Web of Science ®Google Scholar
• Liu W, Zhuang J, Jiang Y, et al. Toll-like receptor signalling cross-activates the autophagic pathway to restrict Salmonella Typhimurium growth in macrophages. Cell Microbiol. 2019;21(12):e13095.
   PubMed Web of Science ®Google Scholar
• Fujita N, Morita E, Itoh T, et al. Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin. J Cell Biol. 2013;203(1):115–128.
   PubMed Web of Science ®Google Scholar
• Ponpuak M, Deretic V. Autophagy and p62/sequestosome 1 generate neo-antimicrobial peptides (cryptides) from cytosolic proteins. Autophagy. 2011;7(3):336–337.
   PubMed Web of Science ®Google Scholar
• Watson RO, Manzanillo PS, Cox JS. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell. 2012;150(4):803–815.
   PubMed Web of Science ®Google Scholar
• Pilli M, Arko-Mensah J, Ponpuak M, et al. TBK-1 promotes autophagy-mediated antimicrobial defense by controlling autophagosome maturation. Immunity. 2012;37(2):223–234.
   PubMed Web of Science ®Google Scholar
• Birmingham CL, Smith AC, Bakowski MA, et al. Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J Biol Chem. 2006;281(16):11374–11383.
   PubMed Web of Science ®Google Scholar
• Huang J, Brumell JH. Autophagy in immunity against intracellular bacteria. Curr Top Microbiol Immunol. 2009;335:189–215.
   PubMed Web of Science ®Google Scholar
• Wang L, Yan J, Niu H, et al. Autophagy and ubiquitination in Salmonella infection and the related inflammatory responses. Front Cell Infect Microbiol. 2018;8:78.
   PubMed Web of Science ®Google Scholar
• VanderVen BC, Huang L, Rohde KH, et al. The minimal unit of infection: Mycobacterium tuberculosis in the macrophage. Microbiol Spectr. 2016;4(6). DOI:10.1128/microbiolspec.TBTB2-0025-2016.
   PubMedGoogle Scholar
• Russell DG. Mycobacterium tuberculosis and the intimate discourse of a chronic infection. Immunol Rev. 2011;240(1):252–268.
   PubMed Web of Science ®Google Scholar
• Augenstreich J, Briken V. Host cell targets of released lipid and secreted protein effectors of Mycobacterium tuberculosis. Front Cell Infect Microbiol. 2020;10:595029.
   PubMed Web of Science ®Google Scholar
• Fredlund J, Enninga J. Cytoplasmic access by intracellular bacterial pathogens. Trends Microbiol. 2014;22(3):128–137.
   PubMed Web of Science ®Google Scholar
• Zhang R, Varela M, Vallentgoed W, et al. The selective autophagy receptors Optineurin and SQSTM1 are both required for zebrafish host resistance to mycobacterial infection. PLoS Pathog. 2019;15(2):e1007329.
   PubMed Web of Science ®Google Scholar
• Tattoli I, Sorbara MT, Philpott DJ, et al. Bacterial autophagy: the trigger, the target and the timing. Autophagy. 2012;8(12):1848–1850.
   PubMed Web of Science ®Google Scholar
• Cemma M, Kim PK, Brumell JH. The ubiquitin-binding adaptor proteins p62/SQSTM1 and NDP52 are recruited independently to bacteria-associated microdomains to target Salmonella to the autophagy pathway. Autophagy. 2011;7(3):341–345.
   PubMed Web of Science ®Google Scholar
• Mahairas GG, Sabo PJ, Hickey MJ, et al. Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J Bacteriol. 1996;178(5):1274–1282.
   PubMed Web of Science ®Google Scholar
• Kim YS, Silwal P, Kim SY, et al. Autophagy-activating strategies to promote innate defense against mycobacteria. Exp Mol Med. 2019;51:1–10.
   Web of Science ®Google Scholar
• Paik S, Kim JK, Chung C, et al. Autophagy: a new strategy for host-directed therapy of tuberculosis. Virulence. 2019;10(1):448–459.
   PubMed Web of Science ®Google Scholar
• Kiran D, Podell BK, Chambers M, et al. Host-directed therapy targeting the Mycobacterium tuberculosis granuloma: a review. Semin Immunopathol. 2016;38(2):167–183.
   PubMed Web of Science ®Google Scholar
• Ran FA, Hsu PD, Wright J, et al. Genome engineering using the CRISPR-Cas9 system. Nat Protoc. 2013;8(11):2281–2308.
   PubMed Web of Science ®Google Scholar