The established and the predicted roles of dynein light chain in the regulation of mitochondrial apoptosis

References

• Vaux DL, Haecker G, Strasser A. An evolutionary perspective on apoptosis. Cell. 1994;76:777–779.
   PubMed Web of Science ®Google Scholar
• Crawford ED, Wells JA. Caspase substrates and cellular remodeling. Annu Rev Biochem. 2011;80:1055–1087.
   PubMed Web of Science ®Google Scholar
• Strasser A, Harris AW, Huang DC, Krammer PH, Cory S. Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J. 1995;14:6136–6147.
   PubMed Web of Science ®Google Scholar
• Huang Z. The chemical biology of apoptosis Exploring protein-protein interactions and the life and death of cells with small molecules. Chem Biol. 2002;9:1059–1072.
   PubMedGoogle Scholar
• Bender T, Martinou JC. Where killers meet–permeabilization of the outer mitochondrial membrane during apoptosis. Cold Spring Harb Perspect Biol. 2013;5:a011106.
   PubMed Web of Science ®Google Scholar
• Yang J, Liu X, Bhalla K,et al. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science . (New York, NY) 1997;275: 1129–1132.
   PubMed Web of Science ®Google Scholar
• Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science . (New York, NY) 1997;275: 1132–1136.
   PubMed Web of Science ®Google Scholar
• Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 2000;102:33–42.
   PubMed Web of Science ®Google Scholar
• Chipuk JE, Bouchier-Hayes L, Green DR. Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ. 2006;13:1396–1402.
   PubMed Web of Science ®Google Scholar
• Bouillet P, Strasser A. BH3-only proteins - evolutionarily conserved proapoptotic Bcl-2 family members essential for initiating programmed cell death. J Cell Sci. 2002;115:1567–1574.
   PubMed Web of Science ®Google Scholar
• Czabotar PE, Lessene G, Strasser A, Adams JM. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat Rev Mol Cell Bio. 2014;15:49–63.
   PubMed Web of Science ®Google Scholar
• Sattler M, Liang H, Nettesheim D, et al. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science . (New York, NY) 1997;275: 983–986.
   PubMed Web of Science ®Google Scholar
• Huang DC, Tschopp J, Strasser A. Bcl-2 does not inhibit cell death induced by the physiological Fas ligand: implications for the existence of type I and type II cells. Cell Death Differ. 2000;7:754–755.
   PubMed Web of Science ®Google Scholar
• Verhagen AM, Ekert PG, Pakusch M,et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 2000;102:43–53.
   PubMed Web of Science ®Google Scholar
• Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell. 2002;2:183–192.
   PubMed Web of Science ®Google Scholar
• Kuwana T, Bouchier-Hayes L, Chipuk JE, et al. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell. 2005;17:525–535.
   PubMed Web of Science ®Google Scholar
• Willis SN, Chen L, Dewson G, et al. Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev. 2005;19:1294–1305.
   PubMed Web of Science ®Google Scholar
• Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Current Biology: CB. 2000;10:1201–1204.
   PubMed Web of Science ®Google Scholar
• Obexer P, Geiger K, Ambros PF, Meister B, Ausserlechner MJ. FKHRL1-mediated expression of Noxa and Bim induces apoptosis via the mitochondria in neuroblastoma cells. Cell Death Differ. 2007;14:534–547.
   PubMed Web of Science ®Google Scholar
• Cheng EH, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ. VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science . (New York, NY) 2003;301: 513–517.
   PubMed Web of Science ®Google Scholar
• Zaltsman Y, Shachnai L, Yivgi-Ohana N, et al. MTCH2/MIMP is a major facilitator of tBID recruitment to mitochondria. Nat Cell Biol. 2010;12:553–562.
   PubMed Web of Science ®Google Scholar
• Puthalakath H, Huang DC, O’Reilly LA, King SM, Strasser A. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol Cell. 1999;3:287–296.
   PubMed Web of Science ®Google Scholar
• Puthalakath H, Villunger A, O’Reilly LA, et al. Bmf: a proapoptotic BH3-only protein regulated by interaction with the myosin V actin motor complex, activated by anoikis. Science . (New York, NY) 2001;293: 1829–1832.
   PubMed Web of Science ®Google Scholar
• Zhu Y, Swanson BJ, Wang M, et al. Constitutive association of the proapoptotic protein Bim with Bcl-2-related proteins on mitochondria in T cells. Proc Natl Acad Sci U S A. 2004;101:7681–7686.
   PubMed Web of Science ®Google Scholar
• Wilfling F, Weber A, Potthoff S, et al. BH3-only proteins are tail-anchored in the outer mitochondrial membrane and can initiate the activation of Bax. Cell Death Differ. 2012;19:1328–1336.
   PubMed Web of Science ®Google Scholar
• Grespi F, Soratroi C, Krumschnabel G, et al. BH3-only protein Bmf mediates apoptosis upon inhibition of CAP-dependent protein synthesis. Cell Death Differ. 2010;17:1672–1683.
   PubMed Web of Science ®Google Scholar
• King A, Li L, Wong DM, et al. Dynein light chain regulates adaptive and innate B cell development by distinctive genetic mechanisms. PLoS Genet. 2017;13:e1007010.
   PubMed Web of Science ®Google Scholar
• Singh PK, Roukounakis A, Frank DO, et al. Dynein light chain 1 induces assembly of large Bim complexes on mitochondria that stabilize Mcl-1 and regulate apoptosis. Genes Dev. 2017;31:1754–1769.
   PubMed Web of Science ®Google Scholar
• Herzig RP, Andersson U, Scarpulla RC. Dynein light chain interacts with NRF-1 and EWG, structurally and functionally related transcription factors from humans and drosophila. J Cell Sci. 2000;113(Pt 23):4263–4273.
   PubMed Web of Science ®Google Scholar
• Pfister KK, Shah PR, Hummerich H, et al. Genetic analysis of the cytoplasmic dynein subunit families. PLoS Genet. 2006;2:e1.
   PubMed Web of Science ®Google Scholar
• Pfister KK, Fay RB, Witman GB. Purification and polypeptide composition of dynein ATPases from Chlamydomonas flagella. Cell Motil. 1982;2:525–547.
   PubMedGoogle Scholar
• Piperno G, Luck DJ. Outer and inner arm dyneins from flagella of Chlamydomonas reinhardtii. Prog Clin Biol Res. 1982;80:95–99.
   PubMedGoogle Scholar
• Dick T, Ray K, Salz HK, Chia W. Cytoplasmic dynein (ddlc1) mutations cause morphogenetic defects and apoptotic cell death in Drosophila melanogaster. Mol Cell Biol. 1996;16:1966–1977.
   PubMed Web of Science ®Google Scholar
• Lightcap CM, Kari G, Arias-Romero LE, Chernoff J, Rodeck U, Williams JC. Interaction with LC8 is required for Pak1 nuclear import and is indispensable for zebrafish development. PloS One. 2009;4:e6025.
   PubMed Web of Science ®Google Scholar
• Goggolidou P, Stevens JL, Agueci F, et al. ATMIN is a transcriptional regulator of both lung morphogenesis and ciliogenesis. Development . (Cambridge, England) 2014;141: 3966–3977.
   PubMed Web of Science ®Google Scholar
• Li W, Yi P, Ou G. Somatic CRISPR-Cas9-induced mutations reveal roles of embryonically essential dynein chains in Caenorhabditis elegans cilia. J Cell Biol. 2015;208:683–692.
   PubMed Web of Science ®Google Scholar
• Jurado S, Gleeson K, O’Donnell K, et al. The Zinc-finger protein ASCIZ regulates B cell development via DYNLL1 and Bim. J Exp Med. 2012;209:1629–1639.
   PubMed Web of Science ®Google Scholar
• Zaytseva O, Tenis N, Mitchell N, et al. The novel zinc finger protein dASCIZ regulates mitosis in Drosophila via an essential role in dynein light-chain expression. Genetics. 2014;196:443–453.
   PubMed Web of Science ®Google Scholar
• Espindola FS, Suter DM, Partata LB, et al. The light chain composition of chicken brain myosin-Va: calmodulin, myosin-II essential light chains, and 8-kDa dynein light chain/PIN. Cell Motil Cytoskeleton. 2000;47:269–281.
   PubMed Web of Science ®Google Scholar
• Wilson MJ, Salata MW, Susalka SJ, Pfister KK. Light chains of mammalian cytoplasmic dynein: identification and characterization of a family of LC8 light chains. Cell Motil Cytoskeleton. 2001;49:229–240.
   PubMed Web of Science ®Google Scholar
• Day Cl, Puthalakath H, Skea G, et al. Localization of dynein light chains 1 and 2 and their pro-apoptotic ligands. Biochem J. 2004;377:597–605.
   PubMed Web of Science ®Google Scholar
• Radnai L, Rapali P, Hodi Z, et al. Affinity, avidity, and kinetics of target sequence binding to LC8 dynein light chain isoforms. J Biol Chem. 2010;285:38649–38657.
   PubMed Web of Science ®Google Scholar
• King SM. Dynein-independent functions of DYNLL1/LC8: redox state sensing and transcriptional control. Sci Signal. 2008;1:pe51.
   PubMed Web of Science ®Google Scholar
• King Sm, Barbarese E, Dillman Jf, 3rd, et al. Brain cytoplasmic and flagellar outer arm dyneins share a highly conserved Mr 8,000 light chain. J Biol Chem. 1996;271:19358–19366.
   PubMed Web of Science ®Google Scholar
• Barbar E. Dynein light chain LC8 is a dimerization hub essential in diverse protein networks. Biochemistry. 2008;47:503–508.
   PubMed Web of Science ®Google Scholar
• Rapali P, Szenes A, Radnai L, Bakos A, Pal G, Nyitray L. DYNLL/LC8: a light chain subunit of the dynein motor complex and beyond. FEBS J. 2011;278:2980–2996.
   PubMed Web of Science ®Google Scholar
• Williams JC, Roulhac PL, Roy AG, Vallee RB, Fitzgerald MC, Hendrickson WA. Structural and thermodynamic characterization of a cytoplasmic dynein light chain-intermediate chain complex. Proc Natl Acad Sci U S A. 2007;104:10028–10033.
   PubMed Web of Science ®Google Scholar
• Hornbeck PV, Zhang B, Murray B, Kornhauser JM, Latham V, PhosphoSitePlus SE. mutations PTMs and Recalibrations. Nucl Acids Res. 2014;2015(43):D512–20.
   Google Scholar
• Song C, Wen W, Rayala SK, et al. Serine 88 phosphorylation of the 8-kDa dynein light chain 1 is a molecular switch for its dimerization status and functions. J Biol Chem. 2008;283:4004–4013.
   PubMed Web of Science ®Google Scholar
• Erdos G, Szaniszlo T, Pajkos M, et al. Novel linear motif filtering protocol reveals the role of the LC8 dynein light chain in the Hippo pathway. PLoS Comput Biol. 2017;13:e1005885.
   PubMed Web of Science ®Google Scholar
• Clark SA, Jespersen N, Woodward C, Barbar E. Multivalent IDP assemblies: unique properties of LC8-associated, IDP duplex scaffolds. FEBS Lett. 2015;589:2543–2551.
   PubMed Web of Science ®Google Scholar
• Rapali P, Garcia-Mayoral MF, Martinez-Moreno M, et al. LC8 dynein light chain (DYNLL1) binds to the C-terminal domain of ATM-interacting protein (ATMIN/ASCIZ) and regulates its subcellular localization. Biochem Biophys Res Commun. 2011;414:493–498.
   PubMed Web of Science ®Google Scholar
• Jurado S, Conlan LA, Baker EK, et al. ATM substrate Chk2-interacting Zn2+ finger (ASCIZ) Is a bi-functional transcriptional activator and feedback sensor in the regulation of dynein light chain (DYNLL1) expression. J Biol Chem. 2012;287:3156–3164.
   PubMed Web of Science ®Google Scholar
• Midoux P, Pigeon L, Goncalves C, Pichon C. Peptides mediating DNA transport on microtubules and their impact on non-viral gene transfer efficiency. Biosci Rep. 2017;37:BSR20170995.
   Web of Science ®Google Scholar
• Rapali P, Radnai L, Suveges D, et al. Directed evolution reveals the binding motif preference of the LC8/DYNLL hub protein and predicts large numbers of novel binders in the human proteome. PloS One. 2011;6:e18818.
   PubMed Web of Science ®Google Scholar
• Lightcap CM, Sun S, Lear JD, Rodeck U, Polenova T, Williams JC. Biochemical and structural characterization of the Pak1-LC8 interaction. J Biol Chem. 2008;283:27314–27324.
   PubMed Web of Science ®Google Scholar
• O’Connor L, Strasser A, O’Reilly LA, et al. Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 1998;17:384–395.
   PubMed Web of Science ®Google Scholar
• Kang Y, Fielden LF, Stojanovski D. Mitochondrial protein transport in health and disease. Semin Cell Dev Biol. 2018;76:142–153.
   PubMed Web of Science ®Google Scholar
• Perciavalle RM, Stewart DP, Koss B, et al. Anti-apoptotic MCL-1 localizes to the mitochondrial matrix and couples mitochondrial fusion to respiration. Nat Cell Biol. 2012;14:575–583.
   PubMed Web of Science ®Google Scholar
• Nguyen M, Millar DG, Yong VW, Korsmeyer SJ, Shore GC. Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence. J Biol Chem. 1993;268:25265–25268.
   PubMed Web of Science ®Google Scholar
• Lindsay J, Esposti MD, Gilmore AP. Bcl-2 proteins and mitochondria–specificity in membrane targeting for death. Biochim Biophys Acta. 2011;1813:532–539.
   PubMed Web of Science ®Google Scholar
• Vadlamudi RK, Bagheri-Yarmand R, Yang Z, et al. Dynein light chain 1, a p21-activated kinase 1-interacting substrate, promotes cancerous phenotypes. Cancer Cell. 2004;5:575–585.
   PubMed Web of Science ®Google Scholar
• Wong DM, Li L, Jurado S, et al. The transcription factor ASCIZ and its target DYNLL1 are essential for the development and expansion of MYC-driven B cell lymphoma. Cell Rep. 2016;14:1488–1499.
   PubMed Web of Science ®Google Scholar
• Hinds MG, Smits C, Fredericks-Short R, et al. Bim, Bad and Bmf: intrinsically unstructured BH3-only proteins that undergo a localized conformational change upon binding to prosurvival Bcl-2 targets. Cell Death Differ. 2007;14:128–136.
   PubMed Web of Science ®Google Scholar
• Fan J, Zhang Q, Tochio H, Li M, Zhang M. Structural basis of diverse sequence-dependent target recognition by the 8 kDa dynein light chain. J Mol Biol. 2001;306:97–108.
   PubMed Web of Science ®Google Scholar
• Wang L, Hare M, Hays TS, Barbar E. Dynein light chain LC8 promotes assembly of the coiled-coil domain of swallow protein. Biochemistry. 2004;43:4611–4620.
   PubMed Web of Science ®Google Scholar
• Nyarko A, Hare M, Hays TS, Barbar E. The intermediate chain of cytoplasmic dynein is partially disordered and gains structure upon binding to light-chain LC8. Biochemistry. 2004;43:15595–15603.
   PubMed Web of Science ®Google Scholar
• Regue L, Sdelci S, Bertran MT, Caelles C, Reverter D, Roig J. DYNLL/LC8 protein controls signal transduction through the Nek9/Nek6 signaling module by regulating Nek6 binding to Nek9. J Biol Chem. 2011;286:18118–18129.
   PubMed Web of Science ®Google Scholar
• Gallego P, Velazquez-Campoy A, Regue L, Roig J, Reverter D. Structural analysis of the regulation of the DYNLL/LC8 binding to Nek9 by phosphorylation. J Biol Chem. 2013;288:12283–12294.
   PubMed Web of Science ®Google Scholar
• Haq T, Richards MW, Burgess SG, et al. Mechanistic basis of Nek7 activation through Nek9 binding and induced dimerization. Nat Commun. 2015;6:8771.
   PubMed Web of Science ®Google Scholar
• Akiyama T, Bouillet P, Miyazaki T, et al. Regulation of osteoclast apoptosis by ubiquitylation of proapoptotic BH3-only Bcl-2 family member Bim. EMBO J. 2003;22:6653–6664.
   PubMed Web of Science ®Google Scholar
• Ewings KE, Hadfield-Moorhouse K, Wiggins CM, et al. ERK1/2-dependent phosphorylation of BimEL promotes its rapid dissociation from Mcl-1 and Bcl-xL. EMBO J. 2007;26:2856–2867.
   PubMed Web of Science ®Google Scholar
• Wuilleme-Toumi S, Trichet V, Gomez-Bougie P, Gratas C, Bataille R, Amiot M. Reciprocal protection of Mcl-1 and Bim from ubiquitin-proteasome degradation. Biochem Biophys Res Commun. 2007;361:865–869.
   PubMed Web of Science ®Google Scholar
• Czabotar PE, Lee EF, van Delft MF, et al. Structural insights into the degradation of Mcl-1 induced by BH3 domains. Proc Natl Acad Sci U S A. 2007;104:6217–6222.
   PubMed Web of Science ®Google Scholar
• Wiggins CM, Tsvetkov P, Johnson M, et al. BIM(EL), an intrinsically disordered protein, is degraded by 20S proteasomes in the absence of poly-ubiquitylation. J Cell Sci. 2011;124:969–977.
   PubMed Web of Science ®Google Scholar
• Stewart DP, Koss B, Bathina M, Perciavalle RM, Bisanz K, Opferman JT. Ubiquitin-independent degradation of antiapoptotic MCL-1. Mol Cell Biol. 2010;30:3099–3110.
   PubMed Web of Science ®Google Scholar
• Weber A, Heinlein M, Dengjel J, Alber C, Singh PK, Hacker G. The deubiquitinase Usp27x stabilizes the BH3-only protein Bim and enhances apoptosis. EMBO Rep. 2016;17:724–738.
   PubMed Web of Science ®Google Scholar
• Tsvetkov P, Reuven N, Shaul Y. The nanny model for IDPs. Nat Chem Biol. 2009;5:778–781.
   PubMed Web of Science ®Google Scholar
• Krappmann D, Wulczyn FG, Scheidereit C. Different mechanisms control signal-induced degradation and basal turnover of the NF-kappaB inhibitor IkappaB alpha in vivo. EMBO J. 1996;15:6716–6726.
   PubMed Web of Science ®Google Scholar
• Lei K, Davis RJ. JNK phosphorylation of Bim-related members of the Bcl2 family induces Bax-dependent apoptosis. Proc Natl Acad Sci U S A. 2003;100:2432–2437.
   PubMed Web of Science ®Google Scholar
• Hubner A, Barrett T, Flavell RA, Davis RJ. Multisite phosphorylation regulates Bim stability and apoptotic activity. Mol Cell. 2008;30:415–425.
   PubMed Web of Science ®Google Scholar
• Geissler A, Haun F, Frank DO, et al. Apoptosis induced by the fungal pathogen gliotoxin requires a triple phosphorylation of Bim by JNK. Cell Death Differ. 2013;20:1317–1329.
   PubMed Web of Science ®Google Scholar
• Hubner A, Cavanagh-Kyros J, Rincon M, Flavell RA, Davis RJ. Functional cooperation of the proapoptotic Bcl2 family proteins Bmf and Bim in vivo. Mol Cell Biol. 2010;30:98–105.
   PubMed Web of Science ®Google Scholar
• Morales AA, Olsson A, Celsing F, Osterborg A, Jondal M, Osorio LM. Expression and transcriptional regulation of functionally distinct Bmf isoforms in B-chronic lymphocytic leukemia cells. Leukemia. 2004;18:41–47.
   PubMed Web of Science ®Google Scholar
• Kutuk O, Letai A. Displacement of Bim by Bmf and Puma rather than increase in Bim level mediates paclitaxel-induced apoptosis in breast cancer cells. Cell Death Differ. 2010;17:1624–1635.
   PubMed Web of Science ®Google Scholar
• Lane DP. Cancer. p53 Guardian of the Genome. Nature. 1992;358:15–16.
   PubMed Web of Science ®Google Scholar
• Lo KW, Kan HM, Chan LN, et al. The 8-kDa dynein light chain binds to p53-binding protein 1 and mediates DNA damage-induced p53 nuclear accumulation. J Biol Chem. 2005;280:8172–8179.
   PubMedGoogle Scholar
• Stelter P, Kunze R, Flemming D, et al. Molecular basis for the functional interaction of dynein light chain with the nuclear-pore complex. Nat Cell Biol. 2007;9:788–796.
   PubMed Web of Science ®Google Scholar
• Martinez-Moreno M, Navarro-Lerida I, Roncal F, et al. Recognition of novel viral sequences that associate with the dynein light chain LC8 identified through a pepscan technique. FEBS Lett. 2003;544:262–267.
   PubMed Web of Science ®Google Scholar
• Theerawatanasirikul S, Phecharat N, Prawettongsopon C, Chaicumpa W, Lekcharoensuk P. Dynein light chain DYNLL1 subunit facilitates porcine circovirus type 2 intracellular transports along microtubules. Arch Virol. 2017;162:677–686.
   PubMed Web of Science ®Google Scholar
• Osseman Q, Gallucci L, Au S, et al. The chaperone dynein LL1 mediates cytoplasmic transport of empty and mature hepatitis B virus capsids. J Hepatol. 2017;68:441–448.
   PubMed Web of Science ®Google Scholar
• Hernaez B, Tarrago T, Giralt E, Escribano JM, Alonso C. Small peptide inhibitors disrupt a high-affinity interaction between cytoplasmic dynein and a viral cargo protein. J Virol. 2010;84:10792–10801.
   PubMed Web of Science ®Google Scholar
• Bauer A, Nolden T, Nemitz S, Perlson E, Finke S. A dynein light chain 1 binding motif in rabies virus polymerase L protein plays a role in microtubule reorganization and viral primary transcription. J Virol. 2015;89:9591–9600.
   PubMed Web of Science ®Google Scholar
• Hernaez B, Diaz-Gil G, Garcia-Gallo M, et al. The African swine fever virus dynein-binding protein p54 induces infected cell apoptosis. FEBS Lett. 2004;569:224–228.
   PubMed Web of Science ®Google Scholar
• Dosztanyi Z, Csizmok V, Tompa P, Simon I. IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics . (Oxford, England) 2005;21: 3433–3434.
   PubMed Web of Science ®Google Scholar
• Prilusky J, Felder CE, Zeev-Ben-Mordehai T, et al. FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded. Bioinformatics . (Oxford, England) 2005;21: 3435–3438.
   PubMed Web of Science ®Google Scholar