Involvement of the TRPML Mucolipin Channels in Viral Infections and Anti-viral Innate Immune Responses

Xu, 2015, Lysosomal physiology., Annu Rev Physiol., 77, 57, 10.1146/annurev-physiol-021014-071649

Venkatachalam, 2015, The role of TRPMLs in endolysosomal trafficking and function., Cell Calcium., 58, 48, 10.1016/j.ceca.2014.10.008

Venkatachalam, 2006, Lysosomal localization of TRPML3 depends on TRPML2 and the mucolipidosis-associated protein TRPML1., J Biol Chem., 281, 17517, 10.1074/jbc.M600807200

Li, 2017, Structural basis of dual Ca(2+)/pH regulation of the endolysosomal TRPML1 channel., Nat Struct Mol Biol., 24, 205, 10.1038/nsmb.3362

Li, 2016, A molecular mechanism to regulate lysosome motility for lysosome positioning and tubulation., Nat Cell Biol., 18, 404, 10.1038/ncb3324

Wang, 2015, Up-regulation of lysosomal TRPML1 channels is essential for lysosomal adaptation to nutrient starvation., Proc Natl Acad Sci USA., 112, E1373, 10.1073/pnas.1419669112

Zhang, 2016, MCOLN1 is a ROS sensor in lysosomes that regulates autophagy., Nat Commun., 7, 10.1038/ncomms12109

Samie, 2013, A TRP channel in the lysosome regulates large particle phagocytosis via focal exocytosis., Dev Cell., 26, 511, 10.1016/j.devcel.2013.08.003

Garrity, 2016, The endoplasmic reticulum, not the pH gradient, drives calcium refilling of lysosomes., Elife., 5, 10.7554/eLife.15887

Falardeau, 2002, Cloning and characterization of the mouse Mcoln1 gene reveals an alternatively spliced transcript not seen in humans., BMC Genomics., 3, 10.1186/1471-2164-3-3

Bassi, 2000, Cloning of the gene encoding a novel integral membrane protein, mucolipidin-and identification of the two major founder mutations causing mucolipidosis type IV., Am J Hum Genet., 67, 1110, 10.1016/S0002-9297(07)62941-3

Bargal, 2000, Identification of the gene causing mucolipidosis type IV., Nat Genet., 26, 118, 10.1038/79095

Sun, 2000, Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel., Hum Mol Genet., 9, 2471, 10.1093/hmg/9.17.2471

Bach, 2001, Mucolipidosis type IV., Mol Genet Metab., 73, 197, 10.1006/mgme.2001.3195

Chen, 2014, A small molecule restores function to TRPML1 mutant isoforms responsible for mucolipidosis type IV., Nat Commun., 5, 10.1038/ncomms5681

Altarescu, 2002, The neurogenetics of mucolipidosis type IV., Neurology., 59, 306, 10.1212/wnl.59.3.306

Tuysuz, 2009, Mucolipidosis type IV in a Turkish boy associated with a novel MCOLN1 mutation., Brain Dev., 31, 702, 10.1016/j.braindev.2008.10.001

AlBakheet, 2013, A novel mutation in a large family causes a unique phenotype of Mucolipidosis IV., Gene., 526, 464, 10.1016/j.gene.2013.04.076

García-Añoveros, 2014, TRPML2 and mucolipin evolution., Handb Exp Pharmacol., 222, 647, 10.1007/978-3-642-54215-2_25

Morelli, 2016, Overexpression of transient receptor potential mucolipin-2 ion channels in gliomas: role in tumor growth and progression., Oncotarget., 7, 43654, 10.18632/oncotarget.9661

Grimm, 2010, Small molecule activators of TRPML3., Chem Biol., 17, 135, 10.1016/j.chembiol.2009.12.016

Nagata, 2008, The varitint-waddler (Va) deafness mutation in TRPML3 generates constitutive, inward rectifying currents and causes cell degeneration., Proc Natl Acad Sci USA., 105, 353, 10.1073/pnas.0707963105

Grimm, 2007, A helix-breaking mutation in TRPML3 leads to constitutive activity underlying deafness in the varitint-waddler mouse., Proc Natl Acad Sci USA., 104, 19583, 10.1073/pnas.0709846104

Xu, 2007, Activating mutation in a mucolipin transient receptor potential channel leads to melanocyte loss in varitint-waddler mice., Proc Natl Acad Sci USA., 104, 18321, 10.1073/pnas.0709096104

Di Palma, 2002, Mutations in Mcoln3 associated with deafness and pigmentation defects in varitint-waddler (Va) mice., Proc Natl Acad Sci USA., 99, 14994, 10.1073/pnas.222425399

Noben-Trauth, 2011, The TRPML3 channel: from gene to function., Adv Exp Med Biol., 704, 229, 10.1007/978-94-007-0265-3_13

Dong, 2010, PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome., Nat Commun., 1, 10.1038/ncomms1037

Shen, 2012, Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release., Nat Commun., 3, 10.1038/ncomms1735

Zhang, 2012, Phosphoinositide isoforms determine compartment-specific ion channel activity., Proc Natl Acad Sci USA., 109, 11384, 10.1073/pnas.1202194109

Dong, 2008, The type IV mucolipidosis-associated protein TRPML1 is an endolysosomal iron release channel., Nature., 455, 992, 10.1038/nature07311

Raychowdhury, 2004, Molecular pathophysiology of mucolipidosis type IV: pH dysregulation of the mucolipin-1 cation channel., Hum Mol Genet., 13, 617, 10.1093/hmg/ddh067

Plesch, 2018, Selective agonist of TRPML2 reveals direct role in chemokine release from innate immune cells., elife., 7, 10.7554/eLife.39720

Chen, 2017, Small molecules for early endosome-specific patch clamping., Cell Chem Biol., 24, 907, 10.1016/j.chembiol.2017.05.025

Isobe, 2019, PIKfyve accelerates phagosome acidification through activation of TRPML1 while arrests aberrant vacuolation independent of the Ca2+ channel., J Biochem., 165, 75, 10.1093/jb/mvy084

Grimm, 2014, High susceptibility to fatty liver disease in two-pore channel 2-deficient mice., Nat Commun., 5, 10.1038/ncomms5699

Grimm, 2017, From mucolipidosis type IV to Ebola: TRPML and two-pore channels at the crossroads of endo-lysosomal trafficking and disease., Cell Calcium., 67, 148, 10.1016/j.ceca.2017.04.003

Xu, 2015, Organellar channels and transporters., Cell Calcium., 58, 1, 10.1016/j.ceca.2015.02.006

Kiselyov, 2012, The intracellular Ca2+ channels of membrane traffic., Channels (Austin)., 6, 344, 10.4161/chan.21723

Patel, 2015, Evolution of acidic Ca2+ stores and their resident Ca2+-permeable channels., Cell Calcium., 57, 222, 10.1016/j.ceca.2014.12.005

Appelqvist, 2013, The lysosome: from waste bag to potential therapeutic target., J Mol Cell Biol., 5, 214, 10.1093/jmcb/mjt022

Cheng, 2010, Mucolipins: intracellular TRPML1-3 channels., FEBS Lett., 584, 2013, 10.1016/j.febslet.2009.12.056

Cao, 2017, The lysosomal Ca(2+) release channel TRPML1 regulates lysosome size by activating calmodulin., J Biol Chem., 292, 8424, 10.1074/jbc.M116.772160

Thompson, 2007, Lysosomal trafficking functions of mucolipin-1 in murine macrophages., BMC Cell Biol., 8, 10.1186/1471-2121-8-54

Zeevi, 2010, Heteromultimeric TRPML channel assemblies play a crucial role in the regulation of cell viability models and starvation-induced autophagy., J Cell Sci., 123, 3112, 10.1242/jcs.067330

Song, 2006, TRPML cation channels regulate the specialized lysosomal compartment of vertebrate B-lymphocytes., Eur J Cell Biol., 85, 1253, 10.1016/j.ejcb.2006.08.004

Brown, 2001, Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic., J Cell Biol., 154, 1007, 10.1083/jcb.200103107

Naslavsky, 2004, Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements., Mol Biol Cell., 15, 3542, 10.1091/mbc.e04-02-0151

Radhakrishna, 1997, ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway., J Cell Biol., 139, 49, 10.1083/jcb.139.1.49

Karacsonyi, 2007, Mucolipin-2 localizes to the Arf6-associated pathway and regulates recycling of GPI-APs., Traffic., 8, 1404, 10.1111/j.1600-0854.2007.00619.x

Kim, 2009, The Ca(2+) channel TRPML3 regulates membrane trafficking and autophagy., Traffic., 10, 1157, 10.1111/j.1600-0854.2009.00924.x

Yamauchi, 2013, Virus entry at a glance., J Cell Sci., 126, 1289, 10.1242/jcs.119685

Cossart, 2014, Endocytosis of viruses and bacteria., Cold Spring Harb Perspect Biol., 6, 10.1101/cshperspect.a016972

Boulant, 2015, Dynamics of virus-receptor interactions in virus binding, signaling, and endocytosis., Viruses., 7, 2794, 10.3390/v7062747

Matlin, 1981, Infectious entry pathway of influenza virus in a canine kidney cell line., J Cell Biol., 91, 601, 10.1083/jcb.91.3.601

Chardonnet, 1970, Early events in the interaction of adenoviruses with HeLa cells. I. Penetration of type 5 and intracellular release of the DNA genome., Virology., 40, 462, 10.1016/0042-6822(70)90189-3

Kartenbeck, 1989, Endocytosis of simian virus 40 into the endoplasmic reticulum., J Cell Biol., 109, 2721, 10.1083/jcb.109.6.2721

Rojek, 2008, Cell entry by human pathogenic arenaviruses., Cell Microbiol., 10, 828, 10.1111/j.1462-5822.2007.01113.x

Nanbo, 2010, Ebolavirus is internalized into host cells via macropinocytosis in a viral glycoprotein-dependent manner., PLoS Pathog., 6, 10.1371/journal.ppat.1001121

Mercer, 2010, Virus entry by endocytosis., Annu Rev Biochem., 79, 803, 10.1146/annurev-biochem-060208-104626

Grant, 2009, Pathways and mechanisms of endocytic recycling., Nat Rev Mol Cell Biol., 10, 597, 10.1038/nrm2755

Zila, 2014, Involvement of microtubular network and its motors in productive endocytic trafficking of mouse polyomavirus., PLoS One., 9, 10.1371/journal.pone.0096922

Mainou, 2012, Transport to late endosomes is required for efficient reovirus infection., J Virol., 86, 8346, 10.1128/JVI.00100-12

Grove, 2011, The cell biology of receptor-mediated virus entry., J Cell Biol., 195, 1071, 10.1083/jcb.201108131

Jae, 2015, Emerging intracellular receptors for hemorrhagic fever viruses., Trends Microbiol., 23, 392, 10.1016/j.tim.2015.04.006

Rinkenberger, 2018, Mucolipin-2 cation channel increases trafficking efficiency of endocytosed viruses., MBio., 9, e2314, 10.1128/mBio.02314-17

Schoggins, 2011, Interferon-stimulated genes and their antiviral effector functions., Curr Opin Virol., 1, 519, 10.1016/j.coviro.2011.10.008

Schoggins, 2014, Interferon-stimulated genes: roles in viral pathogenesis., Curr Opin Virol., 6, 40, 10.1016/j.coviro.2014.03.006

Sun, 2015, Novel role of TRPML2 in the regulation of the innate immune response., J Immunol., 195, 4922, 10.4049/jimmunol.1500163

Lanford, 2006, Genomic response to interferon-alpha in chimpanzees: implications of rapid downregulation for hepatitis C kinetics., Hepatology., 43, 961, 10.1002/hep.21167

Valadez, 2015, PAX5 is the transcriptional activator of mucolipin-2 (MCOLN2) gene., Gene., 555, 194, 10.1016/j.gene.2014.11.003

Cuajungco, 2016, The mucolipin-2 (TRPML2) ion channel: a tissue-specific protein crucial to normal cell function., Pflugers Arch., 468, 177, 10.1007/s00424-015-1732-2

Nelson, 2017, The phosphatidylinositol-3-phosphate 5-kinase inhibitor apilimod blocks filoviral entry and infection., PLoS Negl Trop Dis., 11, 10.1371/journal.pntd.0005540

Galione, 2018, Revealing the secrets of secretion., elife., 7, 10.7554/eLife.43512

Sallusto, 1995, Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products., J Exp Med., 182, 389, 10.1084/jem.182.2.389

MartIn-Fontecha, 2003, Regulation of dendritic cell migration to the draining lymph node: impact on T lymphocyte traffic and priming., J Exp Med., 198, 615, 10.1084/jem.20030448

Weber, 2013, Interstitial dendritic cell guidance by haptotactic chemokine gradients., Science., 339, 328, 10.1126/science.1228456

Bretou, 2017, Lysosome signaling controls the migration of dendritic cells., Sci Immunol., 2, 10.1126/sciimmunol.aak9573

Settembre, 2012, A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB., EMBO J., 31, 1095, 10.1038/emboj.2012.32

Medina, 2015, Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB., Nat Cell Biol., 17, 288, 10.1038/ncb3114

Visvikis, 2014, Innate host defense requires TFEB-mediated transcription of cytoprotective and antimicrobial genes., Immunity., 40, 896, 10.1016/j.immuni.2014.05.002

Samie, 2015, The transcription factor TFEB acts as a molecular switch that regulates exogenous antigen-presentation pathways., Nat Immunol., 16, 729, 10.1038/ni.3196

Sardiello, 2009, A gene network regulating lysosomal biogenesis and function., Science., 325, 473, 10.1126/science.1174447

Settembre, 2011, TFEB links autophagy to lysosomal biogenesis., Science., 332, 1429, 10.1126/science.1204592

Beutler, 2006, Genetic analysis of host resistance: toll-like receptor signaling and immunity at large., Annu Rev Immunol., 24, 353, 10.1146/annurev.immunol.24.021605.090552

Kaisho, 2006, Toll-like receptor function and signaling., J Allergy Clin Immunol., 117, 979, 10.1016/j.jaci.2006.02.023

Kawai, 2010, The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors., Nat Immunol., 11, 373, 10.1038/ni.1863

Gasteiger, 2017, Cellular innate immunity: an old game with new players., J Innate Immun., 9, 111, 10.1159/000453397

Li, 2015, Mucolipin 1 positively regulates TLR7 responses in dendritic cells by facilitating RNA transportation to lysosomes., Int Immunol., 27, 83, 10.1093/intimm/dxu086

Ma, 2018, Mechanisms by which dendritic cells present tumor microparticle antigens to CD8(+) T cells., Cancer Immunol Res., 6, 1057, 10.1158/2326-6066.CIR-17-0716

Wende, 1999, Organization of the leukocyte receptor cluster (LRC) on human chromosome 19q13.4., Mamm Genome., 10, 154, 10.1007/s003359900961

Billadeau, 2002, ITAMs versus ITIMs: striking a balance during cell regulation., J Clin Invest., 109, 161, 10.1172/JCI14843

Bastidas-Legarda, 2019, Conserved and variable natural killer cell receptors: diverse approaches to viral infections., Immunology., 156, 319, 10.1111/imm.13039

Pisegna, 2004, p38 MAPK activation controls the TLR3-mediated up-regulation of cytotoxicity and cytokine production in human NK cells., Blood., 104, 4157, 10.1182/blood-2004-05-1860

Sivori, 2004, CpG and double-stranded RNA trigger human NK cells by Toll-like receptors: induction of cytokine release and cytotoxicity against tumors and dendritic cells., Proc Natl Acad Sci USA., 101, 10116, 10.1073/pnas.0403744101

Adib-Conquy, 2014, TLR-mediated activation of NK cells and their role in bacterial/viral immune responses in mammals., Immunol Cell Biol., 92, 256, 10.1038/icb.2013.99

Goodridge, 2019, Remodeling of secretory lysosomes during education tunes functional potential in NK cells., Nat Commun., 10, 10.1038/s41467-019-08384-x

Clement, , Role of the mucolipin calcium channel family in vescicular trafficking anf natural killer cell function., Proceedings of the 18th Meeting of the Society for Natural Immunity (NK2019); Sept 30–Oct 3 Luxembourg, abstract n.17.

Miao, 2015, A TRP channel senses lysosome neutralization by pathogens to trigger their expulsion., Cell., 161, 1306, 10.1016/j.cell.2015.05.009

Paul, 2016, Autophagy and mammalian virus: roles in immune response, viral replications and beyond., Adv Virus Rev., 95, 149, 10.1016/bs.aivir.2016.02.002