Structures and functions of penta-EF-hand calcium-binding proteins and their interacting partners: enigmatic relationships between ALG-2 and calpain-7

References

• Ross AC, Taylor CL, Yaktine AL, et al., editors. Dietary reference intakes for calcium and vitamin D. Washington (DC): The National Academies Collection: Reports funded by National Institutes of Health; 2011. DOI:10.17226/13050.
   Google Scholar
• Neville MC. Calcium secretion into milk. J Mammary Gland Biol Neoplasia. 2005;10:119–128.
   PubMed Web of Science ®Google Scholar
• Carafoli E, Krebs J. Why calcium? How calcium became the best communicator. J Biol Chem. 2016;291:20849–20857.
   PubMed Web of Science ®Google Scholar
• Yanez M, Gil-Longo J, Campos-Toimil M. Calcium binding proteins. Adv Exp Med Biol. 2012;740:461–482.
   PubMed Web of Science ®Google Scholar
• Kawasaki H, Kretsinger RH. Structural and functional diversity of EF-hand proteins: evolutionary perspectives. Protein Sci. 2017;26:1898–1920.
   PubMed Web of Science ®Google Scholar
• Cheung WY. Calmodulin plays a pivotal role in cellular regulation. Science. 1980;207:19–27.
   PubMed Web of Science ®Google Scholar
• Hoeflich KP, Ikura M. Calmodulin in action: diversity in target recognition and activation mechanisms. Cell. 2002;108:739–742.
   PubMed Web of Science ®Google Scholar
• Sharma RK, Parameswaran S. Calmodulin-binding proteins: a journey of 40 years. Cell Calcium. 2018;75:89–100.
   PubMed Web of Science ®Google Scholar
• Ohno S, Emori Y, Imajoh S, et al. Evolutionary origin of a calcium-dependent protease by fusion of genes for a thiol protease and a calcium-binding protein? Nature. 1984;312:566–570.
   PubMed Web of Science ®Google Scholar
• Sakihama T, Kakidani H, Zenita K, et al. A putative Ca2+-binding protein: structure of the light subunit of porcine calpain elucidated by molecular cloning and protein sequence analysis. Proc Natl Acad Sci USA. 1985;82:6075–6079.
   PubMed Web of Science ®Google Scholar
• Blanchard H, Grochulski P, Li Y, et al. Structure of a calpain Ca2+-binding domain reveals a novel EF-hand and Ca2+-induced conformational changes. Nat Struct Biol. 1997;4:532–538.
   PubMedGoogle Scholar
• Lin GD, Chattopadhyay D, Maki M, et al. Crystal structure of calcium bound domain VI of calpain at 1.9 Å resolution and its role in enzyme assembly, regulation, and inhibitor binding. Nat Struct Biol. 1997;4:539–547.
   PubMedGoogle Scholar
• Maki M, Narayana SV, Hitomi K. A growing family of the Ca2+-binding proteins with five EF-hand motifs. Biochem J. 1997;328:718–720.
   PubMed Web of Science ®Google Scholar
• Vito P, Lacanà E, D’Adamio L. Interfering with apoptosis: ca2+-binding protein ALG-2 and Alzheimer’s disease gene ALG-3. Science. 1996;271:521–525.
   PubMed Web of Science ®Google Scholar
• Maki M, Kitaura Y, Satoh H, et al. Structures, functions and molecular evolution of the penta-EF-hand Ca2+-binding proteins. Biochim Biophys Acta. 2002;1600:51–60.
   PubMed Web of Science ®Google Scholar
• Goll DE, Thompson VF, Li H, et al. The calpain system. Physiol Rev. 2003;83:731–801.
   PubMed Web of Science ®Google Scholar
• Croall DE, Ersfeld K. The calpains: modular designs and functional diversity. Genome Biol. 2007;8:218.
   PubMed Web of Science ®Google Scholar
• Sorimachi H, Hata S, Ono Y. Impact of genetic insights into calpain biology. J Biochem. 2011;150:23–37.
   PubMed Web of Science ®Google Scholar
• Ono Y, Sorimachi H. Calpains: an elaborate proteolytic system. Biochim Biophys Acta. 2012;1824:224–236.
   PubMed Web of Science ®Google Scholar
• Suzuki K, Hata S, Kawabata Y, et al. Structure, activation, and biology of calpain. Diabetes. 2004;53:S12–S18.
   PubMed Web of Science ®Google Scholar
• Suzuki K, Saido TC, Hirai S. Modulation of cellular signals by calpain. Ann NY Acad Sci. 1992;674:218–227.
   PubMed Web of Science ®Google Scholar
• Saido TC, Nagao S, Shiramine M, et al. Distinct kinetics of subunit autolysis in mammalian m-calpain activation. FEBS Lett. 1994;346:263–267.
   PubMed Web of Science ®Google Scholar
• Glading A, Bodnar RJ, Reynolds IJ, et al. Epidermal growth factor activates m-calpain (calpain II), at least in part, by extracellular signal-regulated kinase-mediated phosphorylation. Mol Cell Biol. 2004;24:2499–2512.
   PubMed Web of Science ®Google Scholar
• Ono Y, Ojima K, Shinkai-Ouchi F, et al. An eccentric calpain, CAPN3/p94/calpain-3. Biochimie. 2016;122:169–187.
   PubMed Web of Science ®Google Scholar
• Hoogewijs D, Ebner B, Germani F, et al. Androglobin: a chimeric globin in metazoans that is preferentially expressed in mammalian testes. Mol Biol Evol. 2012;29:1105–1114.
   PubMed Web of Science ®Google Scholar
• Kitaura Y, Watanabe M, Satoh H, et al. Peflin, a novel member of the five-EF-hand-protein family, is similar to the apoptosis-linked gene 2 (ALG-2) protein but possesses nonapeptide repeats in the N-terminal hydrophobic region. Biochem Biophys Res Commun. 1999;263:68–75.
   PubMed Web of Science ®Google Scholar
• Maki M, Maemoto Y, Osako Y, et al. Evolutionary and physical linkage between calpains and penta-EF-hand Ca2+-binding proteins. Febs J. 2012;279:1414–1421.
   PubMed Web of Science ®Google Scholar
• Maki M, Takahara T, Shibata H. Multifaceted roles of ALG-2 in Ca2+-regulated membrane trafficking. Int J Mol Sci. 2016;17:pii: E1401.
   PubMed Web of Science ®Google Scholar
• Ma J, Zhang X, Feng Y, et al. Structural and functional study of apoptosis-linked gene-2·Heme-binding protein 2 interactions in HIV-1 production. J Biol Chem. 2016;291:26670–26685.
   PubMed Web of Science ®Google Scholar
• Kanadome T, Shibata H, Kuwata K, et al. The calcium-binding protein ALG-2 promotes endoplasmic reticulum exit site localization and polymerization of Trk-fused gene (TFG) protein. Febs J. 2017;284:56–76.
   PubMed Web of Science ®Google Scholar
• Takahara T, Inoue K, Arai Y, et al. The calcium-binding protein ALG-2 regulates protein secretion and trafficking via interactions with MISSL and MAP1B proteins. J Biol Chem. 2017;292:17057–17072.
   PubMed Web of Science ®Google Scholar
• Takahara T, Arai Y, Kono Y, et al. A microtubule-associated protein MAP1B binds to and regulates localization of a calcium-binding protein ALG-2. Biochem Biophys Res Commun. 2018;497:492–498.
   PubMed Web of Science ®Google Scholar
• Zhang W, Matsuo R, Takahara T, et al. High sensitive quantitative binding assays using a nanoluciferase-fused probe for analysis of ALG-2-interacting proteins. Methods Mol Biol. 2019;1929:501–516.
   PubMedGoogle Scholar
• Katoh K, Shibata H, Suzuki H, et al. The ALG-2-interacting protein Alix associates with CHMP4b, a human homologue of yeast Snf7 that is involved in multivesicular body sorting. J Biol Chem. 2003;278:39104–39113.
   PubMed Web of Science ®Google Scholar
• Katoh K, Suzuki H, Terasawa Y, et al. The penta-EF-hand protein ALG-2 interacts directly with the ESCRT-I component TSG101, and Ca2+-dependently co-localizes to aberrant endosomes with dominant-negative AAA ATPase SKD1/Vps4B. Biochem J. 2005;391:677–685.
   PubMed Web of Science ®Google Scholar
• Ichioka F, Takaya E, Suzuki H, et al. HD-PTP and Alix share some membrane-traffic related proteins that interact with their Bro1 domains or proline-rich regions. Arch Biochem Biophys. 2007;457:142–149.
   PubMed Web of Science ®Google Scholar
• Okumura M, Katsuyama AM, Shibata H, et al. VPS37 isoforms differentially modulate the ternary complex formation of ALIX, ALG-2, and ESCRT-I. Biosci Biotechnol Biochem. 2013;77:1715–1721.
   PubMed Web of Science ®Google Scholar
• Okumura M, Takahashi T, Shibata H, et al. Mammalian ESCRT-III-related protein IST1 has a distinctive Met-Pro repeat sequence that is essential for interaction with ALG-2 in the presence of Ca2+. Biosci Biotechnol Biochem. 2013;77:1049–1054.
   PubMed Web of Science ®Google Scholar
• Shibata H, Kanadome T, Sugiura H, et al. A new role for annexin A11 in the early secretory pathway via stabilizing Sec31A protein at the endoplasmic reticulum exit sites (ERES). J Biol Chem. 2015;290:4981–4993.
   PubMed Web of Science ®Google Scholar
• Trioulier Y, Torch S, Blot B, et al. Alix, a protein regulating endosomal trafficking, is involved in neuronal death. J Biol Chem. 2004;279:2046–2052.
   PubMed Web of Science ®Google Scholar
• Shibata H, Yamada K, Mizuno T, et al. The penta-EF-hand protein ALG-2 interacts with a region containing PxY repeats in Alix/AIP1, which is required for the subcellular punctate distribution of the amino-terminal truncation form of Alix/AIP1. J Biochem. 2004;135:117–128.
   PubMed Web of Science ®Google Scholar
• Draeby I, Woods YL, la Cour JM, et al. The calcium binding protein ALG-2 binds and stabilizes Scotin, a p53-inducible gene product localized at the endoplasmic reticulum membrane. Arch Biochem Biophys. 2007;467:87–94.
   PubMed Web of Science ®Google Scholar
• Shibata H, Suzuki H, Kakiuchi T, et al. Identification of Alix-type and Non-Alix-type ALG-2-binding sites in human phospholipid scramblase 3: differential binding to an alternatively spliced isoform and amino acid-substituted mutants. J Biol Chem. 2008;283:9623–9632.
   PubMed Web of Science ®Google Scholar
• Vergarajauregui S, Martina JA, Puertollano R. Identification of the penta-EF-hand protein ALG-2 as a Ca2+-dependent interactor of mucolipin-1. J Biol Chem. 2009;284:36357–36366.
   PubMed Web of Science ®Google Scholar
• Shibata H, Inuzuka T, Yoshida H, et al. The ALG-2 binding site in Sec31A influences the retention kinetics of Sec31A at the endoplasmic reticulum exit sites as revealed by live-cell time-lapse imaging. Biosci Biotechnol Biochem. 2010;74:1819–1826.
   PubMed Web of Science ®Google Scholar
• Osugi K, Suzuki H, Nomura T, et al. Identification of the P-body component PATL1 as a novel ALG-2-interacting protein by in silico and far-Western screening of proline-rich proteins. J Biochem. 2012;151:657–666.
   PubMed Web of Science ®Google Scholar
• Sasaki-Osugi K, Imoto C, Takahara T, et al. Nuclear ALG-2 protein interacts with Ca2+ homeostasis endoplasmic reticulum protein (CHERP) Ca2+-dependently and participates in regulation of alternative splicing of inositol trisphosphate receptor type 1 (IP3R1) pre-mRNA. J Biol Chem. 2013;288:33361–33375.
   PubMed Web of Science ®Google Scholar
• Takahashi T, Kojima K, Zhang W, et al. Structural analysis of the complex between penta-EF-hand ALG-2 protein and Sec31A peptide reveals a novel target recognition mechanism of ALG-2. Int J Mol Sci. 2015;16:3677–3699.
   PubMed Web of Science ®Google Scholar
• Suzuki H, Kawasaki M, Inuzuka T, et al. Structural basis for Ca2+-dependent formation of ALG-2/Alix peptide complex: ca2+/EF3-driven arginine switch mechanism. Structure. 2008;16:1562–1573.
   PubMed Web of Science ®Google Scholar
• Pancsa R, Fuxreiter M. Interactions via intrinsically disordered regions: what kind of motifs? IUBMB Life. 2012;64:513–520.
   PubMed Web of Science ®Google Scholar
• Berlow RB, Dyson HJ, Wright PE. Functional advantages of dynamic protein disorder. FEBS Lett. 2015;589:2433–2440.
   PubMed Web of Science ®Google Scholar
• Mikasa T, Kugo M, Nishimura S, et al. Thermodynamic characterization of the Ca2+-dependent interaction between SOUL and ALG-2. Int J Mol Sci. 2018;19:pii: E3802.
   PubMed Web of Science ®Google Scholar
• Emori Y, Kawasaki H, Imajoh S, et al. Endogenous inhibitor for calcium-dependent cysteine protease contains four internal repeats that could be responsible for its multiple reactive sites. Proc Natl Acad Sci USA. 1987;84:3590–3594.
   PubMed Web of Science ®Google Scholar
• Maki M, Takano E, Mori H, et al. All four internally repetitive domains of pig calpastatin possess inhibitory activities against calpains I and II. FEBS Lett. 1987;223:174–180.
   PubMed Web of Science ®Google Scholar
• Takano E, Maki M, Mori H, et al. Pig heart calpastatin: identification of repetitive domain structures and anomalous behavior in polyacrylamide gel electrophoresis. Biochemistry. 1988;27:1964–1972.
   PubMed Web of Science ®Google Scholar
• Maki M, Bagci H, Hamaguchi K, et al. Inhibition of calpain by a synthetic oligopeptide corresponding to an exon of the human calpastatin gene. J Biol Chem. 1989 Nov 15;264:18866–18869.
   PubMed Web of Science ®Google Scholar
• Ma H, Yang HQ, Takano E, et al. Requirement of different subdomains of calpastatin for calpain inhibition and for binding to calmodulin-like domains. J Biochem. 1993;113:591–599.
   PubMed Web of Science ®Google Scholar
• Yang HQ, Ma H, Takano E, et al. Analysis of calcium-dependent interaction between amino-terminal conserved region of calpastatin functional domain and calmodulin-like domain of mu-calpain large subunit. J Biol Chem. 1994;269:18977–18984.
   PubMed Web of Science ®Google Scholar
• Ma H, Yang HQ, Takano E, et al. Amino-terminal conserved region in proteinase inhibitor domain of calpastatin potentiates its calpain inhibitory activity by interacting with calmodulin-like domain of the proteinase. J Biol Chem. 1994;269:24430–24436.
   PubMed Web of Science ®Google Scholar
• Takano E, Ma H, Yang HQ, et al. Preference of calcium-dependent interactions between calmodulin-like domains of calpain and calpastatin subdomains. FEBS Lett. 1995;362:93–97.
   PubMed Web of Science ®Google Scholar
• Todd B, Moore D, Deivanayagam CC, et al. A structural model for the inhibition of calpain by calpastatin: crystal structures of the native domain VI of calpain and its complexes with calpastatin peptide and a small molecule inhibitor. J Mol Biol. 2003;328:131–146.
   PubMed Web of Science ®Google Scholar
• Moldoveanu T, Gehring K, Green DR. Concerted multi-pronged attack by calpastatin to occlude the catalytic cleft of heterodimeric calpains. Nature. 2008;456:404–408.
   PubMed Web of Science ®Google Scholar
• Hanna RA, Campbell RL, Davies PL. Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin. Nature. 2008;456:409–412.
   PubMed Web of Science ®Google Scholar
• Kawasaki H, Mizutome H, Kretsinger RH. Interaction sites of PEF proteins for recognition of their targets. Int J Biol Macromol. 2019;133:1035–1041.
   PubMed Web of Science ®Google Scholar
• Hosfield CM, Elce JS, Davies PL, et al. Crystal structure of calpain reveals the structural basis for Ca2+-dependent protease activity and a novel mode of enzyme activation. Embo J. 1999;18:6880–6889.
   PubMed Web of Science ®Google Scholar
• Strobl S, Fernandez-Catalan C, Braun M, et al. The crystal structure of calcium-free human m-calpain suggests an electrostatic switch mechanism for activation by calcium. Proc Natl Acad Sci USA. 2000;97:588–592.
   PubMed Web of Science ®Google Scholar
• Jia J, Han Q, Borregaard N, et al. Crystal structure of human grancalcin, a member of the penta-EF-hand protein family. J Mol Biol. 2000;300:1271–1281.
   PubMed Web of Science ®Google Scholar
• Jia J, Tarabykina S, Hansen C, et al. Structure of apoptosis-linked protein ALG-2: insights into Ca2+-induced changes in penta-EF-hand proteins. Structure. 2001;9:267–275.
   PubMed Web of Science ®Google Scholar
• Xie X, Dwyer MD, Swenson L, et al. Crystal structure of calcium-free human sorcin: a member of the penta-EF-hand protein family. Protein Sci. 2001;10:2419–2425.
   PubMed Web of Science ®Google Scholar
• Okumura M, Ichioka F, Kobayashi R, et al. Penta-EF-hand protein ALG-2 functions as a Ca2+-dependent adaptor that bridges Alix and TSG101. Biochem Biophys Res Commun. 2009;386:237–241.
   PubMed Web of Science ®Google Scholar
• von Schwedler UK, Stuchell M, Müller B, et al. The protein network of HIV budding. Cell. 2003;114:701–713.
   PubMed Web of Science ®Google Scholar
• Maki M, Suzuki H, Shibata H. Structure and function of ALG-2, a penta-EF-hand calcium-dependent adaptor protein. Sci China Life Sci. 2011;54:770–779.
   PubMed Web of Science ®Google Scholar
• McCullough J, Frost A, Sundquist WI. Structures, functions, and dynamics of ESCRT-III/Vps4 membrane remodeling and fission complexes. Annu Rev Cell Dev Biol. 2018;34:85–109.
   PubMed Web of Science ®Google Scholar
• Christ L, Raiborg C, Wenzel EM, et al. Cellular functions and molecular mechanisms of the ESCRT membrane-scission machinery. Trends Biochem Sci. 2017;42:42–56.
   PubMed Web of Science ®Google Scholar
• Woodman P. ESCRT-III on endosomes: new functions, new activation pathway. Biochem J. 2016;473:e5–8.
   PubMed Web of Science ®Google Scholar
• Weiss ER, Göttlinger H. The role of cellular factors in promoting HIV budding. J Mol Biol. 2011;410:525–533.
   PubMed Web of Science ®Google Scholar
• Agromayor M, Martin-Serrano J. Knowing when to cut and run: mechanisms that control cytokinetic abscission. Trends Cell Biol. 2013;23:433–441.
   PubMed Web of Science ®Google Scholar
• Nabhan JF, Hu R, Oh RS, et al. Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc Natl Acad Sci USA. 2012;109:4146–4151.
   PubMed Web of Science ®Google Scholar
• Scheffer LL, Sreetama SC, Sharma N, et al. Mechanism of Ca2+-triggered ESCRT assembly and regulation of cell membrane repair. Nat Commun. 2014;5:5646.
   PubMed Web of Science ®Google Scholar
• Satoh H, Shibata H, Nakano Y, et al. ALG-2 interacts with the amino-terminal domain of annexin XI in a Ca2+-dependent manner. Biochem Biophys Res Commun. 2002;291:1166–1172.
   PubMed Web of Science ®Google Scholar
• Satoh H, Nakano Y, Shibata H, et al. The penta-EF-hand domain of ALG-2 interacts with amino-terminal domains of both annexin VII and annexin XI in a Ca2+-dependent manner. Biochim Biophys Acta. 2002;1600:61–67.
   PubMed Web of Science ®Google Scholar
• Sønder SL, Boye TL, Tölle R, et al. Annexin A7 is required for ESCRT III-mediated plasma membrane repair. Sci Rep. 2019;9:6726.
   PubMed Web of Science ®Google Scholar
• Skowyra ML, Schlesinger PH, Naismith TV, et al. Triggered recruitment of ESCRT machinery promotes endolysosomal repair. Science. 2018;360:eaar5078.
   PubMed Web of Science ®Google Scholar
• Radulovic M, Schink KO, Wenzel EM, et al. ESCRT-mediated lysosome repair precedes lysophagy and promotes cell survival. Embo J. 2018;37:pii: e99753.
   PubMed Web of Science ®Google Scholar
• Shibata H. Adaptor functions of the Ca2+-binding protein ALG-2 in protein transport from the endoplasmic reticulum. Biosci Biotechnol Biochem. 2019;83:20–32.
   PubMed Web of Science ®Google Scholar
• Rayl M, Truitt M, Held A, et al. Penta-EF-hand protein peflin is a negative regulator of ER-To-Golgi transport. PLoS One. 2016 Jun 8;11:e0157227.
   PubMed Web of Science ®Google Scholar
• McGourty CA, Akopian D, Walsh C, et al. Regulation of the CUL3 ubiquitin ligase by a calcium-dependent co-adaptor. Cell. 2016;167:525–538.
   PubMed Web of Science ®Google Scholar
• Villalobo A, Ishida H, Vogel HJ, et al. Calmodulin as a protein linker and a regulator of adaptor/scaffold proteins. Biochim Biophys Acta Mol Cell Res. 2018;1865:507–521.
   PubMed Web of Science ®Google Scholar
• Monroe N, Hill CP. Meiotic Clade AAA ATPases: protein polymer disassembly machines. J Mol Biol. 2016;428:1897–1911.
   PubMed Web of Science ®Google Scholar
• Yorikawa C, Takaya E, Osako Y, et al. Human calpain 7/PalBH associates with a subset of ESCRT-III-related proteins in its N-terminal region and partly localizes to endocytic membrane compartments. J Biochem. 2008;143:731–745.
   PubMed Web of Science ®Google Scholar
• Osako Y, Maemoto Y, Tanaka R, et al. Autolytic activity of human calpain 7 is enhanced by ESCRT-III-related protein IST1 through MIT-MIM interaction. Febs J. 2010;277:4412–4426.
   PubMed Web of Science ®Google Scholar
• Maeda T. The signaling mechanism of ambient pH sensing and adaptation in yeast and fungi. Febs J. 2012;279:1407–1413.
   PubMed Web of Science ®Google Scholar
• Rodríguez-Galán O, Galindo A, Hervás-Aguilar A, et al. Physiological involvement in pH signaling of Vps24-mediated recruitment of Aspergillus PalB cysteine protease to ESCRT-III. J Biol Chem. 2009;284:4404–4412.
   PubMed Web of Science ®Google Scholar
• Subramanian S, Woolford CA, Desai JV, et al. cis- and trans-acting localization determinants of pH response regulator Rim13 in Saccharomyces cerevisiae. Eukaryot Cell. 2012;11:1201–1209.
   PubMedGoogle Scholar
• Maemoto Y, Kiso S, Shibata H, et al. Analysis of limited proteolytic activity of calpain-7 using non-physiological substrates in mammalian cells. Febs J. 2013;280:2594–2607.
   PubMed Web of Science ®Google Scholar
• Maemoto Y, Osako Y, Goto E, et al. Calpain-7 binds to CHMP1B at its second alpha-helical region and forms a ternary complex with IST1. J Biochem. 2011;150:411–421.
   PubMed Web of Science ®Google Scholar
• Maemoto Y, Ono Y, Kiso S, et al. Involvement of calpain-7 in epidermal growth factor receptor degradation via the endosomal sorting pathway. Febs J. 2014;281:3642–3655.
   PubMed Web of Science ®Google Scholar
• Sadoul R, Laporte MH, Chassefeyre R, et al. The role of ESCRT during development and functioning of the nervous system. Semin Cell Dev Biol. 2018;74:40–49.
   PubMed Web of Science ®Google Scholar
• Vincent O, Rainbow L, Tilburn J, et al. YPXL/I is a protein interaction motif recognized by Aspergillus PalA and its human homologue, AIP1/Alix. Mol Cell Biol. 2003;23:1647–1655.
   PubMed Web of Science ®Google Scholar
• Sun S, Zhou X, Corvera J, et al. ALG-2 activates the MVB sorting function of ALIX through relieving its intramolecular interaction. Cell Discov. 2015;1:15018.
   PubMed Web of Science ®Google Scholar
• Schöneberg J, Lee IH, Iwasa JH, et al. Reverse-topology membrane scission by the ESCRT proteins. Nat Rev Mol Cell Biol. 2017;18:5–17.
   PubMed Web of Science ®Google Scholar
• Schöneberg J, Pavlin MR, Yan S, et al. ATP-dependent force generation and membrane scission by ESCRT-III and Vps4. Science. 2018;362:1423–1428.
   PubMed Web of Science ®Google Scholar