High susceptibility to fatty liver disease in two-pore channel 2-deficient mice

Nature Communications - Tập 5 Số 1
Christian Grimm1, Lesca M. Holdt2, Cheng‐Chang Chen1, Sami Hassan1, Christoph Müller3, Simone Jörs4, Hartmut Cuny5,6, Sandra Kissing7, Bernd Schröder7, Elisabeth Butz1, Bernd H. Northoff2, Jan Castonguay8, Christian A. Luber9, Markus Moser10, Saskia Spahn1, Renate Lüllmann‐Rauch11, Christina Fendel12, Norbert Klugbauer8, Oliver Griesbeck13, Albert Haas12, Matthias Mann9, Franz Bracher3, Daniel Teupser2, Paul Säftig7, Martin Biel1, Christian Wahl‐Schott1
1Department of Pharmacy – Center for Drug Research and Center for Integrated Protein Science Munich (CIPSM), Ludwig-Maximilians-Universität München, Germany
2Institute of Laboratory Medicine, University Hospital Munich, Munich, Germany;
3Department of Pharmacy, Ludwig-Maximilians-Universität München, München, Germany
42nd Department of Internal Medicine, Klinikum rechts der Isar, Technical University of Munich, München, Germany
5Department of Pharmacy—Center for Drug Research and Center for Integrated Protein Science Munich (CIPSM), Ludwig-Maximilians-Universität, München, Germany
6Present address: RMIT University, Melbourne, VIC 3001, Australia,
7Institute of Biochemistry, Christian-Albrechts-Universität Kiel, Kiel, Germany.
8Institute for Experimental and Clinical Pharmacology and Toxicology, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany.
9Mann, Matthias / Proteomics and Signal Transduction, Max Planck Institute of Biochemistry, Max Planck Society
10Fässler, Reinhard / Molecular Medicine, Max Planck Institute of Biochemistry, Max Planck Society
11Institute of Anatomy, Christian-Albrechts-Universität Kiel, Kiel, Germany
12Institute for Cell Biology, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany
13Research Group: Cellular Dynamics / Griesbeck, MPI of Neurobiology, Max Planck Society

Tóm tắt

Từ khóa


Tài liệu tham khảo

Min, H. K. et al. Increased hepatic synthesis and dysregulation of cholesterol metabolism is associated with the severity of nonalcoholic fatty liver disease. Cell Metab. 15, 665–674 (2012).

Bhatia, L. S., Curzen, N. P., Calder, P. C. & Byrne, C. D. Non-alcoholic fatty liver disease: a new and important cardiovascular risk factor? Eur. Heart J. 33, 1190–1200 (2012).

Tiniakos, D. G., Vos, M. B. & Brunt, E. M. Nonalcoholic fatty liver disease: pathology and pathogenesis. Annu. Rev. Pathol. 5, 145–171 (2010).

Postic, C. & Girard, J. Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice. J. Clin. Invest. 118, 829–838 (2008).

Browning, J. D. & Horton, J. D. Molecular mediators of hepatic steatosis and liver injury. J. Clin. Invest. 114, 147–152 (2004).

Chen, Y. et al. Inflammatory stress exacerbates hepatic cholesterol accumulation via disrupting cellular cholesterol export. J. Gastroenterol. Hepatol. 27, 974–984 (2012).

Musso, G., Gambino, R. & Cassader, M. Cholesterol metabolism and the pathogenesis of non-alcoholic steatohepatitis. Prog. Lipid Res. 52, 175–191 (2013).

Hendrikx, T., Walenbergh, S. M., Hofker, M. H. & Shiri-Sverdlov, R. Lysosomal cholesterol accumulation: driver on the road to inflammation during atherosclerosis and non-alcoholic steatohepatitis. Obes. Rev. 15, 424–433 (2014).

Cullen, P. J. Endosomal sorting and signalling: an emerging role for sorting nexins. Nat. Rev. Mol. Cell Biol. 9, 574–582 (2008).

Goldstein, J. L. & Brown, M. S. The LDL receptor and the regulation of cellular cholesterol metabolism. J. Cell Sci. Suppl. 3, 131–137 (1985).

Gruenberg, J. Lipids in endocytic membrane transport and sorting. Curr. Opin. Cell Biol. 15, 382–388 (2003).

Luzio, J. P., Parkinson, M. D., Gray, S. R. & Bright, N. A. The delivery of endocytosed cargo to lysosomes. Biochem. Soc. Trans. 37, 1019–1021 (2009).

Luzio, J. P., Gray, S. R. & Bright, N. A. Endosome-lysosome fusion. Biochem. Soc. Trans. 38, 1413–1416 (2010).

Saftig, P. & Klumperman, J. Lysosome biogenesis and lysosomal membrane proteins: trafficking meets function. Nat. Rev. Mol. Cell Biol. 10, 623–635 (2009).

Wenk, M. R. & De Camilli, P. Protein-lipid interactions and phosphoinositide metabolism in membrane traffic: insights from vesicle recycling in nerve terminals. Proc. Natl Acad. Sci. USA 101, 8262–8269 (2004).

Ruas, M. et al. Purified TPC isoforms form NAADP receptors with distinct roles for Ca(2+) signaling and endolysosomal trafficking. Curr. Biol. 20, 703–709 (2010).

Wang, X. et al. TPC proteins are phosphoinositide-activated sodium-selective ion channels in endosomes and lysosomes. Cell 151, 372–383 (2012).

Calcraft, P. J. et al. NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459, 596–600 (2009).

Rietdorf, K. et al. Two-pore channels form homo- and heterodimers. J. Biol. Chem. 286, 37058–37062 (2011).

Cang, C. et al. mTOR regulates lysosomal ATP-sensitive two-pore Na+ channels to adapt to metabolic state. Cell 152, 778–790 (2013).

Schieder, M., Rötzer, K., Brüggemann, A., Biel, M. & Wahl-Schott, C. A. Characterization of two-pore channel 2 (TPCN2)-mediated Ca2+ currents in isolated lysosomes. J. Biol. Chem. 285, 21219–21222 (2010a).

Schieder, M., Rötzer, K., Brüggemann, A., Biel, M. & Wahl-Schott, C. Planar patch clamp approach to characterize ionic currents from intact lysosomes. Sci. Signal. 3, pl3 (2010b).

Morgan, A. J. & Galione, A. Two-pore channels (TPCs): current controversies. Bioessays 36, 173–183 (2014).

Jha, A., Ahuja, M., Patel, S., Brailoiu, E. & Muallem, S. Convergent regulation of the lysosomal two-pore channel-2 by Mg2+, NAADP, PI(3,5)P2 and multiple protein kinases. EMBO J. 33, 501–511 (2014).

Pitt, S. J. et al. TPC2 is a novel NAADP-sensitive Ca2+ release channel, operating as a dual sensor of luminal pH and Ca2+. J. Biol. Chem. 285, 35039–35046 (2010).

Zong, X. et al. The two-pore channel TPCN2 mediates NAADP-dependent Ca(2+)-release from lysosomal stores. Pflugers Arch. 458, 891–899 (2009).

Miedel, M. T. et al. Membrane traffic and turnover in TRP-ML1-deficient cells: a revised model for mucolipidosis type IV pathogenesis. J. Exp. Med. 205, 1477–1490 (2008).

Curcio-Morelli, C. et al. Functional multimerization of mucolipin channel proteins. J. Cell. Physiol. 222, 328–335 (2010).

Carpenter, G. & Cohen, S. 125I-labeled human epidermal growth factor. Binding, internalization, and degradation in human fibroblasts. J. Cell Biol. 71, 159–171 (1976).

Morgan, A. J., Platt, F. M., Lloyd-Evans, E. & Galione, A. Molecular mechanisms of endolysosomal Ca2+ signalling in health and disease. Biochem. J. 439, 349–374 (2011).

Martina, J. A., Lelouvier, B. & Puertollano, R. The calcium channel mucolipin-3 is a novel regulator of trafficking along the endosomal pathway. Traffic 10, 1143–1156 (2009).

Hay, J. C. Calcium: a fundamental regulator of intracellular membrane fusion? EMBO Rep. 8, 236–240 (2007).

Pryor, P. R., Mullock, B. M., Bright, N. A., Gray, S. R. & Luzio, J. P. The role of intraorganellar Ca(2+) in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. J. Cell Biol. 149, 1053–1062 (2000).

Wong, C. O., Li, R., Montell, C. & Venkatachalam, K. Drosophila TRPML is required for TORC1 activation. Curr. Biol. 22, 1616–1621 (2012).

Moreno, S. N. & Zhong, L. Acidocalcisomes in Toxoplasma gondii tachyzoites. Biochem. J. 313, 655–659 (1996).

Dong, X. P. et al. PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat. Commun. 1, 38 (2010).

Peet, D. J. et al. Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR alpha. Cell 93, 693–704 (1998).

Osono, Y., Woollett, L. A., Herz, J. & Dietschy, J. M. Role of the low density lipoprotein receptor in the flux of cholesterol through the plasma and across the tissues of the mouse. J. Clin. Invest. 95, 1124–1132 (1995).

Zhang, M. et al. Cessation of rapid late endosomal tubulovesicular trafficking in Niemann-Pick type C1 disease. Proc. Natl Acad. Sci. USA 98, 4466–4471 (2001).

Soyombo, A. A. et al. TRP-ML1 regulates lysosomal pH and acidic lysosomal lipid hydrolytic activity. J. Biol. Chem. 281, 7294–7301 (2006).

Lloyd-Evans, E. et al. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 14, 1247–1255 (2008).

Shen, D. et al. Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat. Commun. 3, 731 (2012).

Soccio, R. E. & Breslow, J. L. Intracellular cholesterol transport. Arterioscler. Thromb. Vasc. Biol. 24, 1150–1160 (2004).

Martin, S. & Parton, R. G. Lipid droplets: a unified view of a dynamic organelle. Nat. Rev. Mol. Cell Biol. 7, 373–378 (2006).

Alrefai, W. A. & Gill, R. K. Bile acid transporters: structure, function, regulation and pathophysiological implications. Pharm. Res. 24, 1803–1823 (2007).

Eden, E. R., White, I. J., Tsapara, A. & Futter, C. E. Membrane contacts between endosomes and ER provide sites for PTP1B-epidermal growth factor receptor interaction. Nat. Cell Biol. 12, 267–272 (2010).

van der Kant, R., Zondervan, I., Janssen, L. & Neefjes, J. Cholesterol-binding molecules MLN64 and ORP1L mark distinct late endosomes with transporters ABCA3 and NPC1. J. Lipid Res. 54, 2153–2165 (2013).

Friedman, J. R., Dibenedetto, J. R., West, M., Rowland, A. A. & Voeltz, G. K. Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature. Mol. Biol. Cell 24, 1030–1040 (2013).

Hölttä-Vuori, M. & Ikonen, E. Endosomal cholesterol traffic: vesicular and non-vesicular mechanisms meet. Biochem. Soc. Trans. 34, 392–394 (2006).

Du, X. & Yang, H. Endosomal cholesterol trafficking: protein factors at a glance. Acta Biochim. Biophys. Sin. (Shanghai) 45, 11–17 (2013).

Antonin, W. et al. A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function. EMBO J. 19, 6453–6464 (2000).

Mullock, B. M. et al. Syntaxin 7 is localized to late endosome compartments, associates with Vamp 8, and is required for late endosome-lysosome fusion. Mol. Biol. Cell 11, 3137–3153 (2000).

Prekeris, R., Yang, B., Oorschot, V., Klumperman, J. & Scheller, R. H. Differential Roles of Syntaxin 7 and Syntaxin 8 in endosomal trafficking. Mol. Biol. Cell 10, 3891–3908 (1999).

Rosenbaum, A. I. & Maxfield, F. R. Niemann-Pick type C disease: molecular mechanisms and potential therapeutic approaches. J. Neurochem. 116, 789–795 (2011).

Schenkman, J. B. & Cinti, D. L. Preparation of microsomes with calcium. Methods Enzymol. 52, 83–89 (1978).

Steinberg, B. E. et al. A cation counterflux supports lysosomal acidification. J. Cell Biol. 189, 1171–1186 (2010).

Grimm, C., Jörs, S., Guo, Z., Obukhov, A. G. & Heller, S. Constitutive activity of TRPML2 and TRPML3 channels versus activation by low extracellular sodium and small molecules. J. Biol. Chem. 287, 22701–22708 (2012).

Schröder, J. et al. Deficiency of the tetraspanin CD63 associated with kidney pathology but normal lysosomal function. Mol. Cell Biol. 29, 1083–1094 (2009).

Teupser, D., Persky, A. D. & Breslow, J. L. Induction of atherosclerosis by low-fat, semisynthetic diets in LDL receptor-deficient C57BL/6J and FVB/NJ mice: comparison of lesions of the aortic root, brachiocephalic artery, and whole aorta (en face measurement). Arterioscler. Thromb. Vasc. Biol. 23, 1907–1913 (2003).

Holdt, L. M., Thiery, J., Breslow, J. L. & Teupser, D. Increased ADAM17 mRNA expression and activity is associated with atherosclerosis resistance in LDL-receptor deficient mice. Arterioscler. Thromb. Vasc. Biol. 28, 1097–1103 (2008).

Holdt, L. M. et al. Alu elements in ANRIL non-coding RNA at chromosome 9p21 modulate atherogenic cell functions through trans-regulation of gene networks. PLoS Genet. 9, e1003588 (2013).