TMBIM6 (transmembrane BAX inhibitor motif containing 6) enhances autophagy through regulation of lysosomal calcium

References

• Wang W, Gao Q, Yang M, et al. Up-regulation of lysosomal TRPML1 channels is essential for lysosomal adaptation to nutrient starvation. Proc Natl Acad Sci U S A. 2015;112:E1373–81.
   PubMed Web of Science ®Google Scholar
• Medina DL, Di Paola S, Peluso I, et al. Lysosomal calcium signalling regulates autophagy through calcineurin and TFEB. Nat Cell Biol. 2015;17:288–299.
   PubMed Web of Science ®Google Scholar
• Sardiello M, Palmieri M, Di Ronza A, et al. A gene network regulating lysosomal biogenesis and function. Science. 2009;325:473–477.
   PubMed Web of Science ®Google Scholar
• Settembre C, Di Malta C, Polito VA, et al. TFEB links autophagy to lysosomal biogenesis. Science. 2011;332:1429–1433.
   PubMed Web of Science ®Google Scholar
• Ferron M, Settembre C, Shimazu J, et al. A RANKL-PKCbeta-TFEB signaling cascade is necessary for lysosomal biogenesis in osteoclasts. Genes Dev. 2013;27:955–969.
   PubMed Web of Science ®Google Scholar
• Settembre C, Zoncu R, Medina DL, et al. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. Embo J. 2012;31:1095–1108.
   PubMed Web of Science ®Google Scholar
• Roczniak-Ferguson A, Petit CS, Froehlich F, et al. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci Signal. 2012;5:ra42.
   PubMed Web of Science ®Google Scholar
• He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet. 2009;43:67–93.
   PubMed Web of Science ®Google Scholar
• Lloyd-Evans E, Platt FM. Lysosomal Ca(2+) homeostasis: role in pathogenesis of lysosomal storage diseases. Cell Calcium. 2011;50:200–205.
   PubMed Web of Science ®Google Scholar
• Garrity AG, Wang W, Collier CM, et al. The endoplasmic reticulum, not the pH gradient, drives calcium refilling of lysosomes. eLife. 2016;5:e15887.
   PubMed Web of Science ®Google Scholar
• Xu Q, Reed JC. Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol Cell. 1998;1:337–346.
   PubMed Web of Science ®Google Scholar
• Chae HJ, Kim HR, Xu C, et al. BI-1 regulates an apoptosis pathway linked to endoplasmic reticulum stress. Mol Cell. 2004;15:355–366.
   PubMed Web of Science ®Google Scholar
• Bultynck G, Kiviluoto S, Henke N, et al. The C terminus of Bax inhibitor-1 forms a Ca2+-permeable channel pore. J Biol Chem. 2012;287:2544–2557.
   PubMed Web of Science ®Google Scholar
• Guo G, Xu M, Chang Y, et al. Ion and pH Sensitivity of a TMBIM Ca(2+) Channel. Structure. 2019;27:1013–21 e3.
   PubMed Web of Science ®Google Scholar
• Chang Y, Bruni R, Kloss B, et al. Structural basis for a pH-sensitive calcium leak across membranes. Science. 2014;344:1131–1135.
   PubMed Web of Science ®Google Scholar
• Kiviluoto S, Schneider L, Luyten T, et al. Bax inhibitor-1 is a novel IP(3) receptor-interacting and -sensitizing protein. Cell Death Dis. 2012;3:e367.
   PubMed Web of Science ®Google Scholar
• Lisbona F, Rojas-Rivera D, Thielen P, et al. BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1alpha. Mol Cell. 2009;33:679–691.
   PubMed Web of Science ®Google Scholar
• Castillo K, Rojas-Rivera D, Lisbona F, et al. BAX inhibitor-1 regulates autophagy by controlling the IRE1alpha branch of the unfolded protein response. Embo J. 2011;30:4465–4478.
   PubMed Web of Science ®Google Scholar
• Sano R, Hou YC, Hedvat M, et al. Endoplasmic reticulum protein BI-1 regulates Ca(2)(+)-mediated bioenergetics to promote autophagy. Genes Dev. 2012;26:1041–1054.
   PubMed Web of Science ®Google Scholar
• Kim HR, Lee GH, Ha KC, et al. Bax Inhibitor-1 Is a pH-dependent regulator of Ca2+ channel activity in the endoplasmic reticulum. J Biol Chem. 2008;283:15946–15955.
   PubMed Web of Science ®Google Scholar
• Lloyd-Evans E, Morgan AJ, He X, et al. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat Med. 2008;14:1247–1255.
   PubMed Web of Science ®Google Scholar
• Morgan AJ, Davis LC, Galione A. Imaging approaches to measuring lysosomal calcium. Methods Cell Biol. 2015;126:159–195.
   PubMed Web of Science ®Google Scholar
• Shen D, Wang X, Li X, et al. Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat Commun. 2012;3:731.
   PubMed Web of Science ®Google Scholar
• Nada S, Hondo A, Kasai A, et al. The novel lipid raft adaptor p18 controls endosome dynamics by anchoring the MEK-ERK pathway to late endosomes. Embo J. 2009;28:477–489.
   PubMed Web of Science ®Google Scholar
• Varnai P, Balla A, Hunyady L, et al. Targeted expression of the inositol 1,4,5-triphosphate receptor (IP3R) ligand-binding domain releases Ca2+ via endogenous IP3R channels. Proc Natl Acad Sci U S A. 2005;102:7859–7864.
   PubMed Web of Science ®Google Scholar
• Suzuki J, Kanemaru K, Ishii K, et al. Imaging intraorganellar Ca2+ at subcellular resolution using CEPIA. Nat Commun. 2014;5:4153.
   PubMed Web of Science ®Google Scholar
• Rosemblit N, Moschella MC, Ondriasova E, et al. Intracellular calcium release channel expression during embryogenesis. Dev Biol. 1999;206:163–177.
   PubMed Web of Science ®Google Scholar
• Ambudkar IS. Polarization of calcium signaling and fluid secretion in salivary gland cells. Curr Med Chem. 2012;19:5774–5781.
   PubMed Web of Science ®Google Scholar
• Subedi KP, Singh TD, Kim JC, et al. Cloning and expression of a new inositol 1,4,5-trisphosphate receptor type 1 splice variant in adult rat atrial myocytes. Cell Mol Biol Lett. 2012;17:124–135.
   PubMed Web of Science ®Google Scholar
• Atakpa P, Thillaiappan NB, Mataragka S, et al. IP3 receptors preferentially associate with ER-lysosome contact sites and selectively deliver Ca(2+) to lysosomes. Cell Rep. 2018;25:3180–93 e7.
   PubMed Web of Science ®Google Scholar
• Pena-Llopis S, Brugarolas J. TFEB, a novel mTORC1 effector implicated in lysosome biogenesis, endocytosis and autophagy. Cell Cycle. 2011;10:3987–3988.
   PubMed Web of Science ®Google Scholar
• Stewart AA, Ingebritsen TS, Manalan A, et al. Discovery of a Ca2+- and calmodulin-dependent protein phosphatase: probable identity with calcineurin (CaM-BP80). FEBS Lett. 1982;137:80–84.
   PubMed Web of Science ®Google Scholar
• Zhang X, Cheng X, Yu L, et al. MCOLN1 is a ROS sensor in lysosomes that regulates autophagy. Nat Commun. 2016;7:12109.
   PubMed Web of Science ®Google Scholar
• Guo S, Liang Y, Murphy SF, et al. A rapid and high content assay that measures cyto-ID-stained autophagic compartments and estimates autophagy flux with potential clinical applications. Autophagy. 2015;11:560–572.
   PubMed Web of Science ®Google Scholar
• Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007;3:452–460.
   PubMed Web of Science ®Google Scholar
• Ni HM, Bockus A, Wozniak AL, et al. Dissecting the dynamic turnover of GFP-LC3 in the autolysosome. Autophagy. 2011;7:188–204.
   PubMed Web of Science ®Google Scholar
• Eskelinen EL. Fine structure of the autophagosome. Methods Mol Biol. 2008;445:11–28.
   PubMedGoogle Scholar
• Korolchuk VI, Saiki S, Lichtenberg M, et al. Lysosomal positioning coordinates cellular nutrient responses. Nat Cell Biol. 2011;13:453–460.
   PubMed Web of Science ®Google Scholar
• Lisak D, Schacht T, Gawlitza A, et al. BAX inhibitor-1 is a Ca(2+) channel critically important for immune cell function and survival. Cell Death Differ. 2016;23:358–368.
   PubMed Web of Science ®Google Scholar
• Kania E, Roest G, Vervliet T, et al. IP3 receptor-mediated calcium signaling and its role in autophagy in cancer. Front Oncol. 2017;7:140.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Sheng X, Meng X, et al. The circular F-actin bundles provide a track for turnaround and bidirectional movement of mitochondria in arabidopsis root hair. PloS One. 2014;9:e91501.
   PubMed Web of Science ®Google Scholar
• Akkerman M, Overdijk EJ, Schel JH, et al. Golgi body motility in the plant cell cortex correlates with actin cytoskeleton organization. Plant Cell Physiol. 2011;52:1844–1855.
   PubMed Web of Science ®Google Scholar
• Lavoie JN, Landry MC, Faure RL, et al. Src-family kinase signaling, actin-mediated membrane trafficking and organellar dynamics in the control of cell fate: lessons to be learned from the adenovirus E4orf4 death factor. Cell Signal. 2010;22:1604–1614.
   PubMed Web of Science ®Google Scholar
• Lee GH, Ahn T, Kim DS, et al. Bax inhibitor 1 increases cell adhesion through actin polymerization: involvement of calcium and actin binding. Mol Cell Biol. 2010;30:1800–1813.
   PubMed Web of Science ®Google Scholar
• Lee GH, Lee HY, Li B, et al. Bax inhibitor-1-mediated inhibition of mitochondrial Ca2+ intake regulates mitochondrial permeability transition pore opening and cell death. Sci Rep. 2014;4:5194.
   PubMed Web of Science ®Google Scholar
• Xu G, Wang S, Han S, et al. Plant Bax Inhibitor-1 interacts with ATG6 to regulate autophagy and programmed cell death. Autophagy. 2017;13:1161–1175.
   PubMed Web of Science ®Google Scholar
• Yadav RK, Lee GH, Lee HY, et al. TMBIM6 (transmembrane BAX inhibitor motif containing 6) enhances autophagy and reduces renal dysfunction in a cyclosporine A-induced nephrotoxicity model. Autophagy. 2015;11:1760–1774.
   PubMed Web of Science ®Google Scholar
• Lee GH, Kim DS, Kim HT, et al. Enhanced lysosomal activity is involved in Bax inhibitor-1-induced regulation of the endoplasmic reticulum (ER) stress response and cell death against ER stress: involvement of vacuolar H+-ATPase (V-ATPase). J Biol Chem. 2011;286:24743–24753.
   PubMed Web of Science ®Google Scholar
• Lee GH, Yan C, Shin SJ, et al. BAX inhibitor-1 enhances cancer metastasis by altering glucose metabolism and activating the sodium-hydrogen exchanger: the alteration of mitochondrial function. Oncogene. 2010;29:2130–2141.
   PubMed Web of Science ®Google Scholar
• Churchill GC, Okada Y, Thomas JM, et al. NAADP mobilizes Ca(2+) from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell. 2002;111:703–708.
   PubMed Web of Science ®Google Scholar
• Seo SU, Woo SM, Lee HS, et al. mTORC1/2 inhibitor and curcumin induce apoptosis through lysosomal membrane permeabilization-mediated autophagy. Oncogene. 2018;37(38):5205–5220.
   Web of Science ®Google Scholar
• Pena-Llopis S, Vega-Rubin-de-Celis S, Schwartz JC, et al. Regulation of TFEB and V-ATPases by mTORC1. Embo J. 2011;30:3242–3258.
   PubMed Web of Science ®Google Scholar
• Kim JH, Lee ER, Jeon K, et al. Role of BI-1 (TEGT)-mediated ERK1/2 activation in mitochondria-mediated apoptosis and splenomegaly in BI-1 transgenic mice. Biochim Biophys Acta. 2012;1823:876–888.
   PubMed Web of Science ®Google Scholar
• Lee GH, Kim HR, Chae HJ. Bax inhibitor-1 regulates the expression of P450 2E1 through enhanced lysosome activity. Int J Biochem Cell Biol. 2012;44:600–611.
   PubMed Web of Science ®Google Scholar
• Park KH, Kim BJ, Kang J, et al. Ca2+ signaling tools acquired from prostasomes are required for progesterone-induced sperm motility. Sci Signal. 2011;4:ra31.
   PubMed Web of Science ®Google Scholar
• Nishida Y, Arakawa S, Fujitani K, et al. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature. 2009;461:654–658.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yamamoto A, Matsui M, et al. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell. 2004;15:1101–1111.
   PubMed Web of Science ®Google Scholar
• He C, Bassik MC, Moresi V, et al. Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature. 2012;481:511–515.
   PubMed Web of Science ®Google Scholar
• Parkhitko A, Myachina F, Morrison TA, et al. Tumorigenesis in tuberous sclerosis complex is autophagy and p62/sequestosome 1 (SQSTM1)-dependent. Proc Natl Acad Sci U S A. 2011;108:12455–12460.
   PubMed Web of Science ®Google Scholar
• Lackner C, Gogg-Kamerer M, Zatloukal K, et al. Ballooned hepatocytes in steatohepatitis: the value of keratin immunohistochemistry for diagnosis. J Hepatol. 2008;48:821–828.
   PubMed Web of Science ®Google Scholar
• Ragazzoni Y, Desideri M, Gabellini C, et al. The thiazole derivative CPTH6 impairs autophagy. Cell Death Dis. 2013;4:e524.
   PubMed Web of Science ®Google Scholar
• Lingwood D, Simons K. Detergent resistance as a tool in membrane research. Nat Protoc. 2007;2:2159–2165.
   PubMed Web of Science ®Google Scholar