Coxiella burnetii effector CvpE maintains biogenesis of Coxiella-containing vacuoles by suppressing lysosome tubulation through binding PI(3)P and perturbing PIKfyve activity on lysosomes

References

• Eldin C, Mélenotte C, Mediannikov O, et al. From Q fever to coxiella burnetii infection: a paradigm change. Clin Microbiol Rev. 2017 Jan;30(1):115–17. doi: 10.1128/CMR.00045-16
   PubMed Web of Science ®Google Scholar
• Maurin M, Raoult D. Q fever. Clin Microbiol Rev. 1999 Oct;12(4):518–553. doi: 10.1128/CMR.12.4.518
   PubMed Web of Science ®Google Scholar
• Padmanabhan B, Fielden LF, Hachani A, et al. Biogenesis of the spacious coxiella-Containing vacuole depends on host transcription factors TFEB and TFE3. Infect Immun. 2020 Feb 20;88(3). doi: 10.1128/IAI.00534-19
   PubMed Web of Science ®Google Scholar
• Heinzen RA, Scidmore MA, Rockey DD, et al. Differential interaction with endocytic and exocytic pathways distinguish parasitophorous vacuoles of coxiella burnetii and chlamydia trachomatis. Infect Immun. 1996 Mar;64(3):796–809. doi: 10.1128/iai.64.3.796-809.1996
   PubMed Web of Science ®Google Scholar
• Miller HE, Hoyt FH, Heinzen RA, et al. Replication of coxiella burnetii in a lysosome-like vacuole does not require lysosomal hydrolases. Infect Immun. 2019 Nov;87(11). doi: 10.1128/IAI.00493-19
   PubMed Web of Science ®Google Scholar
• Samanta D, Clemente TM, Schuler BE, et al. Coxiella burnetii Type 4B secretion system-dependent manipulation of endolysosomal maturation is required for bacterial growth. PLOS Pathog. 2019 Dec;15(12):e1007855. doi: 10.1371/journal.ppat.1007855
   PubMed Web of Science ®Google Scholar
• Martinez E, Allombert J, Cantet F, et al. Coxiella burnetii effector CvpB modulates phosphoinositide metabolism for optimal vacuole development. Proc Natl Acad Sci USA. 2016 Jun 7;113(23):E3260–9. doi: 10.1073/pnas.1522811113
   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. doi: 10.3389/fcimb.2020.599762
   PubMed Web of Science ®Google Scholar
• Newton HJ, Kohler LJ, McDonough JA, et al. A screen of coxiella burnetii mutants reveals important roles for Dot/Icm effectors and host autophagy in vacuole biogenesis. PLOS Pathog. 2014 Jul;10(7):e1004286. doi: 10.1371/journal.ppat.1004286
   PubMed Web of Science ®Google Scholar
• Siadous FA, Cantet F, Van Schaik E, et al. Coxiella effector protein CvpF subverts RAB26-dependent autophagy to promote vacuole biogenesis and virulence. Autophagy. 2021 Mar;17(3):706–722. doi: 10.1080/15548627.2020.1728098
   PubMed Web of Science ®Google Scholar
• Ballabio A, Bonifacino JS. Lysosomes as dynamic regulators of cell and organismal homeostasis. Nat Rev Mol Cell Biol. 2020 Feb;21(2):101–118. doi: 10.1038/s41580-019-0185-4
   PubMed Web of Science ®Google Scholar
• de Araujo, MEG, Liebscher G, Hess MW, et al. Lysosomal size matters. Traffic. 2020 Jan;21(1):60–75. doi: 10.1111/tra.12714
   PubMed Web of Science ®Google Scholar
• Huotari J, Helenius A. Endosome maturation. Embo J. 2011 Aug 31;30(17):3481–3500. doi: 10.1038/emboj.2011.286
   PubMed Web of Science ®Google Scholar
• Jahn R, Fasshauer D. Molecular machines governing exocytosis of synaptic vesicles. Nature. 2012 Oct 11;490(7419):201–207. doi: 10.1038/nature11320
   PubMed Web of Science ®Google Scholar
• Baker RW, Hughson FM. Chaperoning SNARE assembly and disassembly. Nat Rev Mol Cell Biol. 2016 Aug;17(8):465–479. doi: 10.1038/nrm.2016.65
   PubMed Web of Science ®Google Scholar
• Chen Y, Yu L. Recent progress in autophagic lysosome reformation. Traffic. 2017 Jun;18(6):358–361. doi: 10.1111/tra.12484
   PubMed Web of Science ®Google Scholar
• Saric A, Hipolito VE, Kay JG, et al. mTOR controls lysosome tubulation and antigen presentation in macrophages and dendritic cells. Mol Biol Cell. [2016 Jan 15];27(2):321–333. doi: 10.1091/mbc.e15-05-0272
   PubMed Web of Science ®Google Scholar
• Saffi GT, Botelho RJ. Lysosome fission: planning for an exit. Trends Cell Biol. 2019 Aug;29(8):635–646. doi: 10.1016/j.tcb.2019.05.003
   PubMed Web of Science ®Google Scholar
• Cerny J, Feng Y, Yu A, et al. The small chemical vacuolin-1 inhibits Ca(2+)-dependent lysosomal exocytosis but not cell resealing. EMBO Rep. 2004 Sep;5(9):883–888. doi: 10.1038/sj.embor.7400243
   PubMed Web of Science ®Google Scholar
• Cao Q, Yang Y, Zhong XZ, et al. The lysosomal Ca(2+) release channel TRPML1 regulates lysosome size by activating calmodulin. J Biol Chem. 2017 May 19;292(20):8424–8435. doi: 10.1074/jbc.M116.772160
   PubMed Web of Science ®Google Scholar
• Latomanski EA, Newton P, Khoo CA, et al. The effector Cig57 hijacks FCHO-mediated vesicular trafficking to facilitate intracellular replication of coxiella burnetii. PLOS Pathog. 2016 Dec;12(12):e1006101. doi: 10.1371/journal.ppat.1006101
   PubMed Web of Science ®Google Scholar
• Larson CL, Beare PA, Howe D, et al. Coxiella burnetii effector protein subverts clathrin-mediated vesicular trafficking for pathogen vacuole biogenesis. Proc Natl Acad Sci USA. 2013 Dec 3;110(49):E4770–9. doi: 10.1073/pnas.1309195110
   PubMed Web of Science ®Google Scholar
• Fu M, Zhang J, Zhao M, et al. Coxiella burnetii plasmid effector B promotes LC3-II accumulation and contributes to bacterial virulence in a SCID mouse Model. Infect Immun. 2022 Jun 16;90(6):e0001622. doi: 10.1128/iai.00016-22
   PubMed Web of Science ®Google Scholar
• Larson CL, Beare PA, Voth DE, et al. Coxiella burnetii effector proteins that localize to the parasitophorous vacuole membrane promote intracellular replication. Infect Immun. 2015 Feb;83(2):661–670. doi: 10.1128/IAI.02763-14
   PubMed Web of Science ®Google Scholar
• Fu M, Liu Y, Wang G, et al. A protein–protein interaction map reveals that the coxiella burnetii effector CirB inhibits host proteasome activity. PLOS Pathog. 2022 Jul;18(7):e1010660. doi: 10.1371/journal.ppat.1010660
   PubMed Web of Science ®Google Scholar
• Zhang Y, Fu J, Liu S, et al. Coxiella burnetii inhibits host immunity by a protein phosphatase adapted from glycolysis. Proc Natl Acad Sci USA. 2022 Jan 4;119(1). doi: 10.1073/pnas.2110877119
   Web of Science ®Google Scholar
• Harrison RE, Bucci C, Vieira OV, et al. Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol. 2003 Sep;23(18):6494–6506. doi: 10.1128/MCB.23.18.6494-6506.2003
   PubMed Web of Science ®Google Scholar
• Seto S, Tsujimura K, Koide Y. Rab GTPases regulating phagosome maturation are differentially recruited to mycobacterial phagosomes. Traffic. 2011 Apr;12(4):407–420. doi: 10.1111/j.1600-0854.2011.01165.x
   PubMed Web of Science ®Google Scholar
• Johansson M, Lehto M, Tanhuanpää K, et al. The oxysterol-binding protein homologue ORP1L interacts with Rab7 and alters functional properties of late endocytic compartments. Mol Biol Cell. 2005 Dec;16(12):5480–5492. doi: 10.1091/mbc.e05-03-0189
   PubMed Web of Science ®Google Scholar
• Schröder B, Wrocklage C, Pan C, et al. Integral and associated lysosomal membrane proteins. Traffic. 2007 Dec;8(12):1676–1686. doi: 10.1111/j.1600-0854.2007.00643.x
   PubMed Web of Science ®Google Scholar
• Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem. 2003;72(1):395–447. doi: 10.1146/annurev.biochem.72.121801.161800
   PubMed Web of Science ®Google Scholar
• Durchfort N, Verhoef S, Vaughn MB, et al. The enlarged lysosomes in beige j cells result from decreased lysosome fission and not increased lysosome fusion. Traffic. 2012 Jan;13(1):108–119. doi: 10.1111/j.1600-0854.2011.01300.x
   PubMed Web of Science ®Google Scholar
• Li X, Rydzewski N, Hider A, et al. A molecular mechanism to regulate lysosome motility for lysosome positioning and tubulation. Nat Cell Biol. 2016 Apr;18(4):404–417. doi: 10.1038/ncb3324
   PubMed Web of Science ®Google Scholar
• Fine M, Schmiege P, Li X. Structural basis for PtdInsP2-mediated human TRPML1 regulation. Nat Commun. 2018 Oct 10;9(1):4192. doi: 10.1038/s41467-018-06493-7
   PubMedGoogle Scholar
• Zhao Y, Araki S, Wu J, et al. An expanded palette of genetically encoded Ca(2)(+) indicators. Science. 2011 Sep 30;333(6051):1888–1891. doi: 10.1126/science.1208592
   PubMed Web of Science ®Google Scholar
• Di Paolo G, De Camilli P. Phosphoinositides in cell regulation and membrane dynamics. Nature. 2006 Oct 12;443(7112):651–657. doi: 10.1038/nature05185
   PubMed Web of Science ®Google Scholar
• Ikonomov OC, Sbrissa D, Shisheva A. Mammalian cell morphology and endocytic membrane homeostasis require enzymatically active phosphoinositide 5-kinase PIKfyve. J Biol Chem. 2001 Jul 13;276(28):26141–26147. doi: 10.1074/jbc.M101722200
   PubMed Web of Science ®Google Scholar
• McCartney AJ, Zolov SN, Kauffman EJ, et al. Activity-dependent PI(3,5)P2 synthesis controls AMPA receptor trafficking during synaptic depression. Proc Natl Acad Sci USA. 2014 Nov 11;111(45):E4896–905. doi: 10.1073/pnas.1411117111
   PubMed Web of Science ®Google Scholar
• Ho CY, Alghamdi TA, Botelho RJ. Phosphatidylinositol-3,5-bisphosphate: no longer the poor PIP2. Traffic. 2012 Jan;13(1):1–8. doi: 10.1111/j.1600-0854.2011.01246.x
   PubMed Web of Science ®Google Scholar
• Carey KL, Newton HJ, Luhrmann A, et al. The Coxiella burnetii Dot/Icm system delivers a unique repertoire of type IV effectors into host cells and is required for intracellular replication. PLOS Pathog. 2011 May;7(5):e1002056. doi: 10.1371/journal.ppat.1002056
   PubMed Web of Science ®Google Scholar
• Lifshitz Z, Burstein D, Peeri M, et al. Computational modeling and experimental validation of the legionella and coxiella virulence-related type-IVB secretion signal. Proc Natl Acad Sci USA. 2013 Feb 19;110(8):E707–15. doi: 10.1073/pnas.1215278110
   PubMed Web of Science ®Google Scholar
• McCartney AJ, Zhang Y, Weisman LS. Phosphatidylinositol 3,5-bisphosphate: low abundance, high significance. BioEssays. 2014 Jan;36(1):52–64. doi: 10.1002/bies.201300012
   PubMed Web of Science ®Google Scholar
• Chen Q, She J, Zeng W, et al. Structure of mammalian endolysosomal TRPML1 channel in nanodiscs. Nature. 2017 Oct 19;550(7676):415–418. doi: 10.1038/nature24035
   PubMed Web of Science ®Google Scholar
• Dong XP, Shen D, Wang X, et al. PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat Commun. 2010 Jul 13;1(1):38. doi: 10.1038/ncomms1037
   PubMedGoogle Scholar
• Hirschi M, Herzik Jr MA Jr., Wie J, et al. Cryo-electron microscopy structure of the lysosomal calcium-permeable channel TRPML3. Nature. 2017 Oct 19];550(7676):411–414. doi: 10.1038/nature24055
   PubMed Web of Science ®Google Scholar
• Latomanski EA, Newton HJ. Interaction between autophagic vesicles and the Coxiella-containing vacuole requires CLTC (clathrin heavy chain). Autophagy. 2018;14(10):1710–1725. doi: 10.1080/15548627.2018.1483806
   PubMed Web of Science ®Google Scholar
• Larson CL, Sandoz KM, Cockrell DC, et al. Noncanonical inhibition of mTORC1 by coxiella burnetii promotes replication within a phagolysosome-like vacuole. MBio. 2019 Feb 5;10(1). doi: 10.1128/mBio.02816-18
   PubMed Web of Science ®Google Scholar
• Ledvina HE, Kelly KA, Eshraghi A, et al. A phosphatidylinositol 3-kinase effector alters phagosomal maturation to promote intracellular growth of Francisella. Cell Host Microbe. 2018 Aug 8;24(2):285–295.e8. doi: 10.1016/j.chom.2018.07.003
   PubMed Web of Science ®Google Scholar
• Yu L, Zhang X, Yang Y, et al. Small-molecule activation of lysosomal TRP channels ameliorates duchenne muscular dystrophy in mouse models. Sci Adv. 2020 Feb;6(6):eaaz2736. doi: 10.1126/sciadv.aaz2736
   PubMed Web of Science ®Google Scholar
• Nakamura S, Shigeyama S, Minami S, et al. LC3 lipidation is essential for TFEB activation during the lysosomal damage response to kidney injury. Nat Cell Biol. 2020 Oct;22(10):1252–1263. doi: 10.1038/s41556-020-00583-9
   PubMed Web of Science ®Google Scholar
• Qi J, Xing Y, Liu Y, et al. MCOLN1/TRPML1 finely controls oncogenic autophagy in cancer by mediating zinc influx. Autophagy. 2021 Dec;17(12):4401–4422. doi: 10.1080/15548627.2021.1917132
   PubMed Web of Science ®Google Scholar
• Li M, Zhang WK, Benvin NM, et al. Structural basis of dual Ca(2+)/pH regulation of the endolysosomal TRPML1 channel. Nat Struct Mol Biol. 2017 Mar;24(3):205–213. doi: 10.1038/nsmb.3362
   PubMed Web of Science ®Google Scholar