LINC complex protein nesprin-2 has pro-apoptotic activity via Bcl-2 family proteins.


Journal

Cell death discovery
ISSN: 2058-7716
Titre abrégé: Cell Death Discov
Pays: United States
ID NLM: 101665035

Informations de publication

Date de publication:
15 Jan 2024
Historique:
received: 21 09 2023
accepted: 06 12 2023
revised: 13 11 2023
medline: 16 1 2024
pubmed: 16 1 2024
entrez: 15 1 2024
Statut: epublish

Résumé

The apoptotic intrinsic pathway is initiated by perforation of the mitochondrial outer membrane by the effector pro-apoptotic proteins of the Bcl-2 family, Bax and Bak. Bax and Bak need to be activated, a process facilitated by the action of BH3-only pro-apoptotic members of the Bcl-2 family. The latter either directly activates the effector proteins or antagonizes the action of pro-survival Bcl-2 family members such as Bcl-x

Identifiants

pubmed: 38225256
doi: 10.1038/s41420-023-01763-w
pii: 10.1038/s41420-023-01763-w
doi:

Types de publication

Journal Article

Langues

eng

Pagination

29

Subventions

Organisme : NIGMS NIH HHS
ID : R35 GM136403
Pays : United States

Informations de copyright

© 2024. The Author(s).

Références

Chang W, Worman HJ, Gundersen GG. Accessorizing and anchoring the LINC complex for multifunctionality. J Cell Biol. 2015;208:11–22.
pubmed: 25559183 pmcid: 4284225 doi: 10.1083/jcb.201409047
Burke B. Chain reaction: LINC complexes and nuclear positioning. F1000Res. 2019;8.
Starr DA. KASH and SUN proteins. Curr Biol. 2011;21:R414–415.
pubmed: 21640895 pmcid: 5518751 doi: 10.1016/j.cub.2011.04.022
Hao H, Starr DA. SUN/KASH interactions facilitate force transmission across the nuclear envelope. Nucleus. 2019;10:73–80.
pubmed: 30888237 pmcid: 6527376 doi: 10.1080/19491034.2019.1595313
Jahed Z, Domkam N, Ornowski J, Yerima G, Mofrad MRK. Molecular models of LINC complex assembly at the nuclear envelope. J Cell Sci. 2021;134.
Zhang Q, Ragnauth CD, Skepper JN, Worth NF, Warren DT, Roberts RG, et al. Nesprin-2 is a multi-isomeric protein that binds lamin and emerin at the nuclear envelope and forms a subcellular network in skeletal muscle. J Cell Sci. 2005;118:673–87.
pubmed: 15671068 doi: 10.1242/jcs.01642
Zhang Q, Skepper JN, Yang F, Davies JD, Hegyi L, Roberts RG, et al. Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J Cell Sci. 2001;114:4485–98.
pubmed: 11792814 doi: 10.1242/jcs.114.24.4485
Kutscheidt S, Zhu R, Antoku S, Luxton GW, Stagljar I, Fackler OT, et al. FHOD1 interaction with nesprin-2G mediates TAN line formation and nuclear movement. Nat Cell Biol. 2014;16:708–15.
pubmed: 24880667 pmcid: 4113092 doi: 10.1038/ncb2981
Antoku S, Wu W, Joseph LC, Morrow JP, Worman HJ, Gundersen GG. ERK1/2 phosphorylation of FHOD connects signaling and nuclear positioning alternations in cardiac laminopathy. Dev Cell. 2019;51:602–616.e12.
pubmed: 31794718 pmcid: 7561008 doi: 10.1016/j.devcel.2019.10.023
Jayo A, Malboubi M, Antoku S, Chang W, Ortiz-Zapater E, Groen C, et al. Fascin regulates nuclear movement and deformation in migrating cells. Dev Cell. 2016;38:371–83.
pubmed: 27554857 pmcid: 4997957 doi: 10.1016/j.devcel.2016.07.021
Goncalves JC, Quintremil S, Yi J, Vallee RB. Nesprin-2 recruitment of BicD2 to the nuclear envelope controls dynein/kinesin-mediated neuronal migration in vivo. Curr Biol. 2020;30:3116–3129.e4.
pubmed: 32619477 pmcid: 9670326 doi: 10.1016/j.cub.2020.05.091
Lindenboim L, Zohar H, Worman HJ, Stein R. The nuclear envelope: target and mediator of the apoptotic process. Cell Death Discov. 2020;6:29.
pubmed: 32351716 pmcid: 7184752 doi: 10.1038/s41420-020-0256-5
Pogmore JP, Uehling D, Andrews DW. Pharmacological targeting of executioner proteins: controlling life and death. J Med Chem. 2021;64:5276–90.
pubmed: 33939407 doi: 10.1021/acs.jmedchem.0c02200
Kalkavan H, Green DR. MOMP, cell suicide as a BCL-2 family business. Cell Death Differ. 2018;25:46–55.
pubmed: 29053143 doi: 10.1038/cdd.2017.179
Moldoveanu T, Czabotar PE. BAX, BAK, and BOK: A coming of age for the BCL-2 family effector proteins. Cold Spring Harbor Perspect Biol. 2020;12.
Dadsena S, King LE, Garcia-Saez AJ. Apoptosis regulation at the mitochondria membrane level. Biochim Biophys Acta Biomembr. 2021;1863:183716.
pubmed: 34343535 doi: 10.1016/j.bbamem.2021.183716
Adams JM, Cory S. The BCL-2 arbiters of apoptosis and their growing role as cancer targets. Cell Death Differ. 2018;25:27–36.
pubmed: 29099483 doi: 10.1038/cdd.2017.161
Kaloni D, Diepstraten ST, Strasser A, Kelly GL. BCL-2 protein family: attractive targets for cancer therapy. Apoptosis. 2022;28:20–38.
Martinou JC, Youle RJ. Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell. 2011;21:92–101.
pubmed: 21763611 pmcid: 3156409 doi: 10.1016/j.devcel.2011.06.017
Gross A, Katz SG. Non-apoptotic functions of BCL-2 family proteins. Cell Death Differ. 2017;24:1348–58.
pubmed: 28234359 pmcid: 5520452 doi: 10.1038/cdd.2017.22
Ichim G, Tait SW. A fate worse than death: apoptosis as an oncogenic process. Nat Rev Cancer. 2016;16:539–48.
pubmed: 27364482 doi: 10.1038/nrc.2016.58
Delbridge AR, Grabow S, Strasser A, Vaux DL. Thirty years of BCL-2: translating cell death discoveries into novel cancer therapies. Nat Rev Cancer. 2016;16:99–109.
pubmed: 26822577 doi: 10.1038/nrc.2015.17
Lindenboim L, Blacher E, Borner C, Stein R. Regulation of stress-induced nuclear protein redistribution: a new function of Bax and Bak uncoupled from Bcl-x(L). Cell Death Differ. 2010;17:346–59.
pubmed: 19816507 doi: 10.1038/cdd.2009.145
Lindenboim L, Ferrando-May E, Borner C, Stein R. Non-canonical function of Bax in stress-induced nuclear protein redistribution. Cell Mol Life Sci. 2013;70:3013–27.
pubmed: 23475110 doi: 10.1007/s00018-013-1306-4
Lindenboim L, Sasson T, Worman HJ, Borner C, Stein R. Cellular stress induces Bax-regulated nuclear bubble budding and rupture followed by nuclear protein release. Nucleus. 2014;5:527–41.
pubmed: 25482068 pmcid: 4615202 doi: 10.4161/19491034.2014.970105
Lindenboim L, Grozki D, Amsalem-Zafran AR, Pena-Blanco A, Gundersen GG, Borner C, et al. Apoptotic stress induces Bax-dependent, caspase-independent redistribution of LINC complex nesprins. Cell Death Discov. 2020;6:90.
pubmed: 33024575 pmcid: 7501853 doi: 10.1038/s41420-020-00327-6
Chang W, Antoku S, Ostlund C, Worman HJ, Gundersen GG. Linker of nucleoskeleton and cytoskeleton (LINC) complex-mediated actin-dependent nuclear positioning orients centrosomes in migrating myoblasts. Nucleus. 2015;6:77–88.
pubmed: 25587885 pmcid: 4615731 doi: 10.1080/19491034.2015.1004947
Hsu YT, Youle RJ. Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J Biol Chem. 1998;273:10777–83.
pubmed: 9553144 doi: 10.1074/jbc.273.17.10777
Luxton GW, Gomes ER, Folker ES, Vintinner E, Gundersen GG. Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement. Science. 2010;329:956–9.
pubmed: 20724637 pmcid: 3938394 doi: 10.1126/science.1189072
Arsenovic PT, Ramachandran I, Bathula K, Zhu R, Narang JD, Noll NA, et al. Nesprin-2G, a component of the nuclear LINC complex, is subject to myosin-dependent tension. Biophys J. 2016;110:34–43.
pubmed: 26745407 pmcid: 4805861 doi: 10.1016/j.bpj.2015.11.014
Zhu R, Antoku S, Gundersen GG. Centrifugal displacement of nuclei reveals multiple LINC complex mechanisms for homeostatic nuclear positioning. Curr Biol. 2017;27:3097–3110.e5.
pubmed: 28988861 pmcid: 5688853 doi: 10.1016/j.cub.2017.08.073
Lindenboim L, Borner C, Stein R. Nuclear proteins acting on mitochondria. Biochim Biophys Acta. 2011;1813:584–96.
pubmed: 21130123 doi: 10.1016/j.bbamcr.2010.11.016
Dewson G, Kluck RM. Mechanisms by which Bak and Bax permeabilise mitochondria during apoptosis. J Cell Sci. 2009;122:2801–8.
pubmed: 19795525 pmcid: 2736138 doi: 10.1242/jcs.038166
Todt F, Cakir Z, Reichenbach F, Emschermann F, Lauterwasser J, Kaiser A, et al. Differential retrotranslocation of mitochondrial Bax and Bak. EMBO J. 2015;34:67–80.
pubmed: 25378477 doi: 10.15252/embj.201488806
Llambi F, Moldoveanu T, Tait SW, Bouchier-Hayes L, Temirov J, McCormick LL, et al. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell. 2011;44:517–31.
pubmed: 22036586 pmcid: 3221787 doi: 10.1016/j.molcel.2011.10.001
Duong NT, Morris GE, Lam le T, Zhang Q, Sewry CA, Shanahan CM, et al. Nesprins: tissue-specific expression of epsilon and other short isoforms. PLoS ONE. 2014;9:e94380.
pubmed: 24718612 pmcid: 3981789 doi: 10.1371/journal.pone.0094380
Tse C, Shoemaker AR, Adickes J, Anderson MG, Chen J, Jin S, et al. ABT-263: a potent and orally bioavailable Bcl-2 family inhibitor. Cancer Res. 2008;68:3421–8.
pubmed: 18451170 doi: 10.1158/0008-5472.CAN-07-5836
Cosentino K, Hertlein V, Jenner A, Dellmann T, Gojkovic M, Pena-Blanco A, et al. The interplay between BAX and BAK tunes apoptotic pore growth to control mitochondrial-DNA-mediated inflammation. Mol Cell. 2022;82:933–949.e939.
pubmed: 35120587 pmcid: 8901441 doi: 10.1016/j.molcel.2022.01.008
Popgeorgiev N, Jabbour L, Gillet G. Subcellular localization and dynamics of the Bcl-2 family of proteins. Front Cell Dev Biol. 2018;6:13.
pubmed: 29497611 pmcid: 5819560 doi: 10.3389/fcell.2018.00013
Hao H, Kalra S, Jameson LE, Guerrero LA, Cain NE, Bolivar J, et al. The nesprin-1/-2 ortholog ANC-1 regulates organelle positioning in C. elegans independently from its KASH or actin-binding domains. eLife. 2021;10.
Farmer T, O’Neill KL, Naslavsky N, Luo X, Caplan S. Retromer facilitates the localization of Bcl-xL to the mitochondrial outer membrane. Mol Biol Cell. 2019;30:1138–46.
pubmed: 30840537 pmcid: 6724524 doi: 10.1091/mbc.E19-01-0044
Zhang Q, Bethmann C, Worth NF, Davies JD, Wasner C, Feuer A, et al. Nesprin-1 and -2 are involved in the pathogenesis of Emery Dreifuss muscular dystrophy and are critical for nuclear envelope integrity. Hum Mol Genet. 2007;16:2816–33.
pubmed: 17761684 doi: 10.1093/hmg/ddm238
Li Mow Chee F, Beernaert B, Griffith BGC, Loftus AEP, Kumar Y, Wills JC, et al. Mena regulates nesprin-2 to control actin-nuclear lamina associations, trans-nuclear membrane signalling and gene expression. Nat Commun. 2023;14:1602.
pubmed: 36959177 pmcid: 10036544 doi: 10.1038/s41467-023-37021-x
Östlund C, Folker ES, Choi JC, Gomes ER, Gundersen GG, Worman HJ. Dynamics and molecular interactions of linker of nucleoskeleton and cytoskeleton (LINC) complex proteins. J Cell Sci. 2009;122:4099–108.
pubmed: 19843581 pmcid: 2776502 doi: 10.1242/jcs.057075
Razafsky D, Hodzic D. A variant of nesprin1 giant devoid of KASH domain underlies the molecular etiology of autosomal recessive cerebellar ataxia type I. Neurobiol Dis. 2015;78:57–67.
pubmed: 25843669 pmcid: 4426048 doi: 10.1016/j.nbd.2015.03.027
Khatau SB, Bloom RJ, Bajpai S, Razafsky D, Zang S, Giri A, et al. The distinct roles of the nucleus and nucleus-cytoskeleton connections in three-dimensional cell migration. Sci Rep. 2012;2:488.
pubmed: 22761994 pmcid: 3388469 doi: 10.1038/srep00488
Luke Y, Zaim H, Karakesisoglou I, Jaeger VM, Sellin L, Lu W, et al. Nesprin-2 Giant (NUANCE) maintains nuclear envelope architecture and composition in skin. J Cell Sci. 2008;121:1887–98.
pubmed: 18477613 doi: 10.1242/jcs.019075
Lindenboim L, Kringel S, Braun T, Borner C, Stein R. Bak but not Bax is essential for Bcl-xS-induced apoptosis. Cell Death Differ. 2005;12:713–23.
pubmed: 15861188 doi: 10.1038/sj.cdd.4401638
Benjamini Y, Krieger AM, Yekutieli D. Adaptive linear step-up procedures that control the false discovery rate. Biometrika. 2006;93:491–507.
doi: 10.1093/biomet/93.3.491

Auteurs

Liora Lindenboim (L)

Department of Neurobiology, School of Neurobiology, Biochemistry and Biophysics, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, 69978, Israel.

Hila Zohar (H)

Department of Neurobiology, School of Neurobiology, Biochemistry and Biophysics, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, 69978, Israel.

Gregg G Gundersen (GG)

Department of Pathology and Cell Biology, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY, 10032, USA.

Howard J Worman (HJ)

Department of Pathology and Cell Biology, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY, 10032, USA.
Department of Medicine, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY, 10032, USA.

Reuven Stein (R)

Department of Neurobiology, School of Neurobiology, Biochemistry and Biophysics, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, 69978, Israel. reuvens@tauex.tau.ac.il.

Classifications MeSH