7,875
Views
47
CrossRef citations to date
0
Altmetric
Research Paper

SIGMAR1/Sigma-1 receptor ablation impairs autophagosome clearance

ORCID Icon, , & ORCID Icon
Pages 1539-1557 | Received 05 Apr 2018, Accepted 06 Feb 2019, Published online: 14 Mar 2019

References

  • Farre JC, Subramani S. Mechanistic insights into selective autophagy pathways: lessons from yeast. Nat Rev Mol Cell Biol. 2016;17(9):537–552.
  • Ryter SW, Cloonan SM, Choi AM. Autophagy: a critical regulator of cellular metabolism and homeostasis. Mol Cells. 2013;36(1):7–16.
  • Sica V, Galluzzi L, Bravo-San Pedro JM, et al. Organelle-specific initiation of autophagy. Mol Cell. 2015;59(4):522–539.
  • Ashrafi G, Schwarz TL. The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ. 2013;20(1):31–42.
  • Chen Y, Dorn GW 2nd. PINK1-phosphorylated mitofusin 2 is a Parkin receptor for culling damaged mitochondria. Science. 2013;340(6131):471–475.
  • Lazarou M, Sliter DA, Kane LA, et al. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature. 2015;524(7565):309–314.
  • Choi AM, Ryter SW, Levine B. Autophagy in human health and disease. N Engl J Med. 2013;368(19):1845–1846.
  • Garcia-Prat L, Martínez-Vicente M, Perdiguero E, et al. Autophagy maintains stemness by preventing senescence. Nature. 2016;529(7584):37–42.
  • Diao J, Liu R, Rong Y, et al. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature. 2015;520(7548):563–566.
  • Hayashi T, Su TP. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell. 2007;131(3):596–610.
  • Mavlyutov TA, Yang H, Epstein ML, et al. APEX2-enhanced electron microscopy distinguishes sigma-1 receptor localization in the nucleoplasmic reticulum. Oncotarget. 2017;8(31):51317–51330.
  • Mavlyutov TA, Epstein M, Guo LW. Subcellular localization of the sigma-1 receptor in retinal neurons - an electron microscopy study. Sci Rep. 2015;5:10689.
  • Hanner M, Moebius FF, Flandorfer A, et al. Purification, molecular cloning, and expression of the mammalian sigma1-binding site. Proc Natl Acad Sci U S A. 1996;93(15):8072–8077.
  • Kourrich S. Su TP, Fujimoto M, et al. The sigma-1 receptor: roles in neuronal plasticity and disease. Trends Neurosci. 2012;35(12):762–771.
  • Su TP, Hayashi T, Maurice T, et al. The sigma-1 receptor chaperone as an inter-organelle signaling modulator. Trends Pharmacol Sci. 2010;31(12):557–566.
  • Tsai SA, Chuang J-Y, Tsai M-S, et al. Sigma-1 receptor mediates cocaine-induced transcriptional regulation by recruiting chromatin-remodeling factors at the nuclear envelope. Proceedings of the National Academy of Sciences of the United States of America, 2015
  • Mavlyutov TA, Nickells RW, Guo LW. Accelerated retinal ganglion cell death in mice deficient in the sigma-1 receptor. Mol Vis. 2011;17:1034–1043.
  • Yang H, Fu Y, Liu X, et al. Role of the sigma-1 receptor chaperone in rod and cone photoreceptor degenerations in a mouse model of retinitis pigmentosa. Mol Neurodegener. 2017;12(1):68.
  • Luty AA, Kwok JBJ, Dobson-Stone C, et al. Sigma nonopioid intracellular receptor 1 mutations cause frontotemporal lobar degeneration-motor neuron disease. Ann Neurol. 2010;68(5):639–649.
  • Geva M, Kusko R, Soares H, et al. Pridopidine activates neuroprotective pathways impaired in huntington disease. Hum Mol Genet. 2016;25(18):3975–3987.
  • Al-Saif A, Al-Mohanna F, Bohlega S. A mutation in sigma-1 receptor causes juvenile amyotrophic lateral sclerosis. Ann Neurol. 2011;70(6):913–919.
  • Feher A, Juhász A, László A, et al. Association between a variant of the sigma-1 receptor gene and Alzheimer’s disease. Neurosci Lett. 2012;517(2):136–139.
  • Li X, Hu Z, Liu L, et al. A SIGMAR1 splice-site mutation causes distal hereditary motor neuropathy. Neurology. 2015;84(24):2430–2437.
  • Wang J, Saul A, Roon P, et al. Activation of the molecular chaperone, sigma 1 receptor, preserves cone function in a murine model of inherited retinal degeneration. Proc Natl Acad Sci U S A. 2016;113(26):E3764–72.
  • Watanabe S, Ilieva H, Tamada H, et al. Mitochondria-associated membrane collapse is a common pathomechanism in SIGMAR1- and SOD1-linked ALS. EMBO Mol Med. 2016;8(12):1421–1437.
  • Schmidt HR, Zheng S, Gurpinar E, et al. Crystal structure of the human sigma1 receptor. Nature. 2016;532(7600):527–530.
  • Vollrath JT, Sechi A, Dreser A, et al. Loss of function of the ALS protein SigR1 leads to ER pathology associated with defective autophagy and lipid raft disturbances. Cell Death Dis. 2014;5:e1290.
  • Dreser A, Vollrath JT, Sechi A, et al. The ALS-linked E102Q mutation in sigma receptor-1 leads to ER stress-mediated defects in protein homeostasis and dysregulation of RNA-binding proteins. Cell Death Differ. 2017;24(10):1655–1671.
  • Schrock JM, Spino CM, Longen CG, et al. Sequential cytoprotective responses to Sigma1 ligand-induced endoplasmic reticulum stress. Mol Pharmacol. 2013;84(5):751–762.
  • Kasahara R, Yamamoto N, Suzuki K, et al. The sigma1 receptor regulates accumulation of GM1 ganglioside-enriched autophagosomes in astrocytes. Neuroscience. 2017;340:176–187.
  • Cao L, Walker MP, Vaidya NK, et al. Cocaine-mediated autophagy in astrocytes involves sigma 1 receptor, PI3K, mTOR, Atg5/7, Beclin-1 and induces Type II programed cell death. Mol Neurobiol. 2016;53(7):4417–4430.
  • MacVicar TDB, Mannack LVJC, Lees RM, et al. Targeted siRNA screens identify ER-to-mitochondrial calcium exchange in autophagy and mitophagy responses in RPE1 cells. Int J Mol Sci. 2015;16(6):13356–13380.
  • Yang H, Mavlyutov TA, Guo L-W. An essential role of the sigma-1 receptor in mitophagy and autophagosome-lysosome fusion. Invest Ophthalmol Vis Sci. 2017;58: 1603. abstract (oral presentation).
  • Mavlyutov TA, Yang H, Epstein ML, et al. APEX2-enhanced electron microscopy distinguishes sigma-1 receptor localization in the nucleoplasmic reticulum. Oncotarget. 2017;8(31):51317–51330.
  • Mavlyutov TA, Ruoho AE. Ligand-dependent localization and intracellular stability of sigma-1 receptors in CHO-K1 cells. J Mol Signal. 2007;2:8.
  • Kagan VE, Jiang J, Huang Z, et al. NDPK-D (NM23-H4)-mediated externalization of cardiolipin enables elimination of depolarized mitochondria by mitophagy. Cell Death Differ. 2016;23(7):1140–1151.
  • Geisler S, Holmström KM, Skujat D, et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol. 2010;12(2):119–131.
  • Callegari S, Oeljeklaus S, Warscheid B, et al. Phospho-ubiquitin-PARK2 complex as a marker for mitophagy defects. Autophagy. 2017;13(1):201–211.
  • Nguyen TN, Padman BS, Lazarou M. Deciphering the molecular signals of PINK1/Parkin mitophagy. Trends Cell Biol. 2016;26(10):733–744.
  • Vives-Bauza C, Zhou C, Huang Y, et al. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci U S A. 2010;107(1):378–383.
  • Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell. 2010;140(3):313–326.
  • Yamano K, Matsuda N, Tanaka K. The ubiquitin signal and autophagy: an orchestrated dance leading to mitochondrial degradation. EMBO Rep. 2016;17(3):300–316.
  • Hamasaki M, Furuta N, Matsuda A, et al. Autophagosomes form at ER-mitochondria contact sites. Nature. 2013;495(7441):389–393.
  • Yamamoto A, Tagawa Y, Yoshimori T, et al. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct. 1998;23(1):33–42.
  • Velikkakath AKG, Nishimura T, Oita E, et al. Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol Biol Cell. 2012;23(5):896–909.
  • Wang Y, Li L, Hou C, et al. SNARE-mediated membrane fusion in autophagy. Semin Cell Dev Biol. 2016;60:97–104.
  • Stoka V, Turk V, Turk B. Lysosomal cathepsins and their regulation in aging and neurodegeneration. Ageing Res Rev. 2016;32:22–37.
  • Liu R, Zhi X, Zhong Q. ATG14 controls SNARE-mediated autophagosome fusion with a lysosome. Autophagy. 2015;11(5):847–849.
  • Shyu YJ, Hiatt SM, Duren HM, et al. Visualization of protein interactions in living Caenorhabditis elegans using bimolecular fluorescence complementation analysis. Nat Protoc. 2008;3(4):588–596.
  • Padman BS, Bach M, Lucarelli G, et al. The protonophore CCCP interferes with lysosomal degradation of autophagic cargo in yeast and mammalian cells. Autophagy. 2013;9(11):1862–1875.
  • Li L, Zhong Q. Autophagosome-lysosome fusion: pIs to the rescue. Embo J. 2016;35(17):1845–1847.
  • Nguyen L, Lucke-Wold BP, Mookerjee SA, et al. Role of sigma-1 receptors in neurodegenerative diseases. J Pharmacol Sci. 2015;127(1):17–29.
  • Mavlyutov TA, Guo LW. Peeking into sigma-1 receptor functions through the retina. Adv Exp Med Biol. 2017;964:285–297.
  • Su TP, Su T-C, Nakamura Y, et al. The Sigma-1 receptor as a pluripotent modulator in living systems. Trends Pharmacol Sci. 2016;37(4):262–278.
  • Kim FJ, Kovalyshyn I, Burgman M, et al. Sigma 1 receptor modulation of G-protein-coupled receptor signaling: potentiation of opioid transduction independent from receptor binding. Mol Pharmacol. 2010;77(4):695–703.
  • Miyagawa K, Oe S, Honma Y, et al. Lipid-induced endoplasmic reticulum stress impairs selective autophagy at the step of autophagosome-lysosome fusion in hepatocytes. Am J Pathol. 2016;186(7):1861–1873.
  • Wu Z, Bowen WD. Role of sigma-1 receptor C-terminal segment in inositol 1,4,5-trisphosphate receptor activation: constitutive enhancement of calcium signaling in MCF-7 tumor cells. J Biol Chem. 2008;283(42):28198–28215.
  • Mavylutov T, Chen X, Guo L, et al. APEX2- tagging of Sigma 1-receptor indicates subcellular protein topology with cytosolic N-terminus and ER luminal C-terminus. Protein Cell. 2018;9(8):733–737.
  • Chu UB, Ruoho AE. Biochemical pharmacology of the sigma-1 receptor. Mol Pharmacol. 2016;89(1):142–153.
  • Ramirez-Peinado S, León-Annicchiarico CL, Galindo-Moreno J, et al. Glucose-starved cells do not engage in prosurvival autophagy. J Biol Chem. 2013;288(42):30387–30398.
  • Ni HM, Bockus A, Wozniak AL, et al. Dissecting the dynamic turnover of GFP-LC3 in the autolysosome. Autophagy. 2011;7(2):188–204.
  • Cayouette M, Whitmore AV, Jeffery G, et al. Asymmetric segregation of Numb in retinal development and the influence of the pigmented epithelium. J Neurosci. 2001;21(15):5643–5651.
  • Cai Q, Zakaria HM, Simone A, et al. Spatial parkin translocation and degradation of damaged mitochondria via mitophagy in live cortical neurons. Curr Biol. 2012;22(6):545–552.
  • Chu UB, Mavlyutov TA, Chu M-L, et al. The Sigma-2 receptor and progesterone receptor membrane component 1 are different binding sites derived from independent genes. EBioMedicine. 2015;2(11):1806–1813.
  • Sanjana NE, Shalem O, Zhang F. Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods. 2014;11(8):783–784.
  • Kearns NA, Genga RM, Enuameh MS, et al. Cas9 effector-mediated regulation of transcription and differentiation in human pluripotent stem cells. Development. 2014;141(1):219–223.
  • Lu Y, Hao B-X, Graeff R, et al. Two pore channel 2 (TPC2) inhibits autophagosomal-lysosomal fusion by alkalinizing lysosomal pH. J Biol Chem. 2013;288(33):24247–24263.
  • Bardet PL, Kolahgar G, Mynett A, et al. A fluorescent reporter of caspase activity for live imaging. Proc Natl Acad Sci U S A. 2008;105(37):13901–13905.