ORP4L couples IP <subscript>3</subscript> to ITPR1 in control of endoplasmic reticulum calcium release. - OpacWWW

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Tytuł:: ORP4L couples IP 3 to ITPR1 in control of endoplasmic reticulum calcium release.
Autorzy:: Cao X; Department of Biology, Jinan University, Guangzhou, China.
Chen J; Department of Biology, Jinan University, Guangzhou, China.
Li D; Department of Biology, Jinan University, Guangzhou, China.
Xie P; Department of Biology, Jinan University, Guangzhou, China.
Xu M; Department of Biology, Jinan University, Guangzhou, China.
Lin W; Department of Biology, Jinan University, Guangzhou, China.
Li S; Department of Biology, Jinan University, Guangzhou, China.
Pan G; Department of Biology, Jinan University, Guangzhou, China.
Tang Y; Department of Biology, Jinan University, Guangzhou, China.
Xu J; Research Center for Drug Discovery, School of Pharmaceutical Sciences, Sun Yat-sen University, Guangzhou, China.
Olkkonen VM; Minerva Foundation Institute for Medical Research, Biomedicum Helsinki 2U, Helsinki, Finland.
Yan D; Department of Biology, Jinan University, Guangzhou, China.
Zhong W; Department of Biology, Jinan University, Guangzhou, China.
Źródło:: FASEB journal : official publication of the Federation of American Societies for Experimental Biology [FASEB J] 2019 Dec; Vol. 33 (12), pp. 13852-13865. Date of Electronic Publication: 2019 Oct 23.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Publication: 2020- : [Bethesda, Md.] : Hoboken, NJ : Federation of American Societies for Experimental Biology ; Wiley
Original Publication: [Bethesda, Md.] : The Federation, [c1987-
MeSH Terms:: Calcium/*metabolism
Endoplasmic Reticulum/*metabolism
Inositol 1,4,5-Trisphosphate Receptors/*metabolism
Receptors, Steroid/*metabolism
Cell Line, Tumor ; Cell Membrane/metabolism ; Cell Survival/physiology ; Cytosol/metabolism ; Humans ; Inositol 1,4,5-Trisphosphate/metabolism ; Jurkat Cells ; Mitochondria/metabolism ; Oxidative Phosphorylation ; Phospholipase C beta/metabolism
References:: Bagur, R., and Hajnóczky, G. (2017) Intracellular Ca2+ sensing: its role in calcium homeostasis and signaling. Mol. Cell 66, 780-788.
Wang, L., Wagner L. E. II, Alzayady, K. J., and Yule, D. I. (2017) Region-specific proteolysis differentially regulates type 1 inositol 1,4,5-trisphosphate receptor activity. J. Biol. Chem. 292, 11714-11726.
Kuchay, S., Giorgi, C., Simoneschi, D., Pagan, J., Missiroli, S., Saraf, A., Florens, L., Washburn, M. P., Collazo-Lorduy, A., Castillo-Martin, M., Cordon-Cardo, C., Sebti, S. M., Pinton, P., and Pagano, M. (2017) PTEN counteracts FBXL2 to promote IP3R3- and Ca2+-mediated apoptosis limiting tumour growth. Nature 546, 554-558.
Taylor, C. W., and Konieczny, V. (2016) IP3 receptors: take four IP3 to open. Sci. Signal. 9, pe1.
Marchant, J. S., and Taylor, C. W. (1997) Cooperative activation of IP3 receptors by sequential binding of IP3 and Ca2+ safeguards against spontaneous activity. Curr. Biol. 7, 510-518.
Taylor, C. W., Genazzani, A. A., and Morris, S. A. (1999) Expressionof inositol trisphosphate receptors. Cell Calcium 26, 237-251.
Prole, D. L., and Taylor, C. W. (2019) Structure and function of IP3 receptors. Cold Spring Harb. Perspect. Biol. 11, a035063.
Tarasov, A. I., Griffiths, E. J., and Rutter, G. A. (2012) Regulation of ATP production by mitochondrial Ca(2+). Cell Calcium 52, 28-35.
Cárdenas, C., Miller, R. A., Smith, I., Bui, T., Molgó, J., Müller, M., Vais, H., Cheung, K. H., Yang, J., Parker, I., Thompson, C. B., Birnbaum, M. J., Hallows, K. R., and Foskett, J. K. (2010) Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 142, 270-283.
Cárdenas, C., Müller, M., McNeal, A., Lovy, A., Jaňa, F., Bustos, G., Urra, F., Smith, N., Molgó, J., Diehl, J. A., Ridky, T. W., and Foskett, J. K. (2016) Selective vulnerability of cancer cells by inhibition of Ca(2+) transfer from endoplasmic reticulum to mitochondria. Cell Rep. 14, 2313-2324; erratum: 15, 219-220.
Taylor, F. R., Saucier, S. E., Shown, E. P., Parish, E. J., and Kandutsch, A. A. (1984) Correlation between oxysterol binding to a cytosolic binding protein and potency in the repression of hydroxymethylglutaryl coenzyme A reductase. J. Biol. Chem. 259, 12382-12387.
Pietrangelo, A., and Ridgway, N. D. (2018) Bridging the molecular and biological functions of the oxysterol-binding protein family. Cell. Mol. Life Sci. 75, 3079-3098.
Chung, J., Torta, F., Masai, K., Lucast, L., Czapla, H., Tanner, L. B., Narayanaswamy, P., Wenk, M. R., Nakatsu, F., and De Camilli, P. (2015) INTRACELLULAR TRANSPORT. PI4P/phosphatidylserine countertransport at ORP5- and ORP8-mediated ER-plasma membrane contacts. Science 349, 428-432.
Dong, J., Du, X., Wang, H., Wang, J., Lu, C., Chen, X., Zhu, Z., Luo, Z., Yu, L., Brown, A. J., Yang, H., and Wu, J. W. (2019) Allosteric enhancement of ORP1-mediated cholesterol transport by PI (4,5)P2/PI(3,4)P2. Nat. Commun. 10, 829.
Zhong, W., Yi, Q., Xu, B., Li, S., Wang, T., Liu, F., Zhu, B., Hoffmann, P. R., Ji, G., Lei, P., Li, G., Li, J., Li, J., Olkkonen, V. M., and Yan, D. (2016) ORP4L is essential for T-cell acute lymphoblastic leukemia cell survival. Nat. Commun. 7, 12702.
Zhong, W., Pan, G., Wang, L., Li, S., Ou, J., Xu, M., Li, J., Zhu, B., Cao, X., Ma, H., Li, C., Xu, J., Olkkonen, V. M., Staels, B., and Yan, D. (2016) ORP4L facilitates macrophage survival via G-protein-coupled signaling: ORP4L-/- mice display a reduction of atherosclerosis. Circ. Res. 119, 1296-1312.
Charman, M., Colbourne, T. R., Pietrangelo, A., Kreplak, L., and Ridgway, N. D. (2014) Oxysterol-binding protein (OSBP)-related protein 4 (ORP4) is essential for cell proliferation and survival. J. Biol. Chem. 289, 15705-15717.
Burgett, A. W., Poulsen, T. B., Wangkanont, K., Anderson, D. R., Kikuchi, C., Shimada, K., Okubo, S., Fortner, K. C., Mimaki, Y., Kuroda, M., Murphy, J. P., Schwalb, D. J., Petrella, E. C., Cornella-Taracido, I., Schirle, M., Tallarico, J. A., and Shair, M. D. (2011) Natural products reveal cancer cell dependence on oxysterol-binding proteins. Nat. Chem. Biol. 7, 639-647.
Pan, G., Cao, X., Liu, B., Li, C., Li, D., Zheng, J., Lai, C., Olkkonen, V. M., Zhong, W., and Yan, D. (2018) OSBP-related protein 4L promotes phospholipase Cβ3 translocation from the nucleus to the plasma membrane in Jurkat T-cells. J. Biol. Chem. 293, 17430-17441.
Zhong, W., Xu, M., Li, C., Zhu, B., Cao, X., Li, D., Chen, H., Hu, C., Li, R., Luo, C., Pan, G., Zhang, W., Lai, C., Wang, T., Du, X., Chen, H., Xu, G., Olkkonen, V. M., Lei, P., Xu, J., and Yan, D. (2019) ORP4Lextracts and presents PIP2 from plasma membrane for PLCβ3 catalysis: targeting it eradicates leukemia stem cells. Cell Rep. 26, 2166-2177.e9.
Erickson, M. G., Moon, D. L., and Yue, D. T. (2003) DsRed as a potential FRET partner with CFP and GFP. Biophys. J. 85, 599-611.
Sekar, R. B., and Periasamy, A. (2003) Fluorescence resonance energy transfer (FRET) microscopy imaging of live cell protein localizations. J. Cell Biol. 160, 629-633.
Zhong, W., Zhou, Y., Li, S., Zhou, T., Ma, H., Wei, K., Li, H., Olkkonen, V. M., and Yan, D. (2011) OSBP-related protein 7 interacts with GATE-16 and negatively regulates GS28 protein stability. Exp. Cell Res. 317, 2353-2363.
Nagai, T., Ibata, K., Park, E. S., Kubota, M., Mikoshiba, K., and Miyawaki, A. (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90.
Patel, S., Morris, S. A., Adkins, C. E., O'Beirne, G., and Taylor, C. W. (1997) Ca2+-independent inhibition of inositol trisphosphate receptors by calmodulin: redistribution of calmodulin as a possible means of regulating Ca2+ mobilization. Proc. Natl. Acad. Sci. USA 94, 11627-11632.
Song, Y., DiMaio, F., Wang, R. Y., Kim, D., Miles, C., Brunette, T., Thompson, J., and Baker, D. (2013) High-resolution comparative modeling with RosettaCM. Structure 21, 1735-1742.
Raman, S., Vernon, R., Thompson, J., Tyka, M., Sadreyev, R., Pei, J., Kim, D., Kellogg, E., DiMaio, F., Lange, O., Kinch, L., Sheffler, W., Kim, B. H., Das, R., Grishin, N. V., and Baker, D. (2009) Structure prediction for CASP8 with all-atom refinement using Rosetta. Proteins 77 (Suppl 9), 89-99.
des Georges, A., Clarke, O. B., Zalk, R., Yuan, Q., Condon, K. J., Grassucci, R. A., Hendrickson, W. A., Marks, A. R., and Frank, J. (2016) Structural basis for gating and activation of RyR1. Cell 167, 145-157.e17.
Bhanumathy, C., da Fonseca, P. C., Morris, E. P., and Joseph, S. K. (2012) Identification of functionally critical residues in the channel domain of inositol trisphosphate receptors. J. Biol. Chem. 287, 43674-43684.
Massova, I., and Kollman, P. A. (2000) Combined molecular mechanical and continuum solvent approach (MM-PBSA/GBSA) to predict ligand binding. Perspect. Drug Discov. Des. 18, 113-135.
Hou, T., Wang, J., Li, Y., and Wang, W. (2011) Assessing the performance of the MM/PBSA and MM/GBSA methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. J. Chem. Inf. Model. 51, 69-82.
Miller B. R. III, McGee, T. D., Jr., Swails, J. M., Homeyer, N., Gohlke, H., and Roitberg, A. E. (2012) MMPBSA.py:an efficient program for end-state free energy calculations. J. Chem. Theory Comput. 8, 3314-3321.
Kerppola, T. K. (2008) Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells. Annu. Rev. Biophys. 37, 465-487.
Rong, Y. P., Aromolaran, A. S., Bultynck, G., Zhong, F., Li, X., McColl, K., Matsuyama, S., Herlitze, S., Roderick, H. L., Bootman, M. D., Mignery, G. A., Parys, J. B., De Smedt, H., and Distelhorst, C. W. (2008) Targeting Bcl-2-IP3 receptor interaction to reverse Bcl-2′s inhibition of apoptotic calcium signals. Mol. Cell 31, 255-265.
Rong, Y. P., Bultynck, G., Aromolaran, A. S., Zhong, F., Parys, J. B., De Smedt, H., Mignery, G. A., Roderick, H. L., Bootman, M. D., and Distelhorst, C. W. (2009) The BH4 domain of Bcl-2 inhibits ER calcium release and apoptosis by binding the regulatory and coupling domain of the IP3 receptor. Proc. Natl. Acad. Sci. USA 106, 14397-14402.
Baughman, J. M., Perocchi, F., Girgis, H. S., Plovanich, M., Belcher-Timme, C. A., Sancak, Y., Bao, X. R., Strittmatter, L., Goldberger, O., Bogorad, R. L., Koteliansky, V., and Mootha, V. K. (2011) Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 476, 341-345.
De Stefani, D., Raffaello, A., Teardo, E., Szabò, I., and Rizzuto, R. (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476, 336-340.
Foskett, J. K., and Philipson, B. (2015) The mitochondrial Ca(2+) uniporter complex. J. Mol. Cell. Cardiol. 78, 3-8.
Harrington, J. L., and Murphy, E. (2015) The mitochondrial calcium uniporter: mice can live and die without it. J. Mol. Cell. Cardiol. 78, 46-53.
Hajnóczky, G., Robb-Gaspers, L. D., Seitz M. B., and Thomas A. P. (1995) Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82, 415-424.
Putney, J. W., and Bird, G. S. (2008) Cytoplasmic calcium oscillations and store-operated calcium influx. J. Physiol. 586, 3055-3059.
Schug, Z. T., and Joseph, S. K. (2006) The role of the S4-S5 linker and C-terminal tail in inositol 1,4,5-trisphosphate receptor function. J. Biol. Chem. 281, 24431-24440.
Loewen, C. J., Roy, A., and Levine, T. P. (2003) A conserved ER targeting motif in three families of lipid binding proteins and in Opi1p binds VAP. EMBO J. 22, 2025-2035.
Gamper, N., and Shapiro, M. S. (2007) Target-specific PIP(2) signalling: how might it work? J. Physiol. 582, 967-975.
Levine, T., and Loewen, C. (2006) Inter-organelle membrane contact sites: through a glass, darkly. Curr. Opin. Cell Biol. 18, 371-378.
Wu, M. M., Buchanan, J., Luik, R. M., and Lewis, R. S. (2006) Ca2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J. Cell Biol. 174, 803-813.
Luik, R. M., Wu, M. M., Buchanan, J., and Lewis, R. S. (2006) The elementary unit of store-operated Ca2+ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J. Cell Biol. 174, 815-825.
Toulmay, A., and Prinz, W. A. (2011) Lipid transfer and signaling at organelle contact sites: the tip of the iceberg. Curr. Opin. Cell Biol. 23, 458-463.
Jamecna, D., Polidori, J., Mesmin, B., Dezi, M., Levy, D., Bigay, J., and Antonny, B. (2019) An intrinsically disordered region in OSBP acts as an entropic barrier to control protein dynamics and orientation at membrane contact sites. Dev. Cell 49, 220-234.e8.
Allbritton, N. L., Meyer, T., and Stryer, L. (1992) Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258, 1812-1815.
Dickinson, G. D., Ellefsen, K. L., Dawson, S. P., Pearson, J. E., and Parker, I. (2016) Hindered cytoplasmic diffusion of inositol trisphosphate restricts its cellular range of action. Sci. Signal. 9, ra108.
Contributed Indexing:: Keywords: Ca2+ signaling; T-ALL cells; bioenergetics
Substance Nomenclature:: 0 (ITPR1 protein, human)
0 (Inositol 1,4,5-Trisphosphate Receptors)
0 (Receptors, Steroid)
0 (oxysterol binding protein)
85166-31-0 (Inositol 1,4,5-Trisphosphate)
EC 3.1.4.11 (Phospholipase C beta)
SY7Q814VUP (Calcium)
Entry Date(s):: Date Created: 20191026 Date Completed: 20200608 Latest Revision: 20220623
Update Code:: 20240104
DOI:: 10.1096/fj.201900933RR
PMID:: 31648575
: Czasopismo naukowe

Oxysterol-binding protein-related protein (ORP) 4L acts as a scaffold protein assembling CD3-ε, G-α q/11 , and PLC-β3 into a complex at the plasma membrane that mediates inositol (1,4,5)-trisphosphate (IP 3 )-induced endoplasmic reticulum (ER) Ca 2+ release and oxidative phosphorylation in T-cell acute lymphoblastic leukemia cells. Here, we offer new evidence that ORP4L interacts with the carboxyl terminus of the IP 3 receptor type 1 (ITPR1) in Jurkat T cells. ORP4L enables IP 3 binding to ITPR1; a truncated construct that lacks the ITPR1-binding region retains the ability to increase IP 3 production but fails to mediate IP 3 and ITPR1 binding. In association with this ability of ORP4L, it enhances Ca 2+ release from the ER and subsequent cytosolic and mitochondrial parallel Ca 2+ spike oscillations that stimulate mitochondrial energetics and thus maintains cell survival. These data support a novel model in which ORP4L is a cofactor of ITPR1, which increases ITPR1 sensitivity to IP 3 and enables ER Ca 2+ release.-Cao, X., Chen, J., Li, D., Xie, P., Xu, M., Lin, W., Li, S., Pan, G., Tang, Y., Xu, J., Olkkonen, V. M., Yan, D., Zhong, W. ORP4L couples IP 3 to ITPR1 in control of endoplasmic reticulum calcium release.

Informacja

ORP4L couples IP 3 to ITPR1 in control of endoplasmic reticulum calcium release.