Impact of N-Terminal Tags on De Novo Vimentin Intermediate Filament Assembly.

ectopic protein expression fusion proteins immunofluorescence intermediate filaments protein domains

Journal

International journal of molecular sciences
ISSN: 1422-0067
Titre abrégé: Int J Mol Sci
Pays: Switzerland
ID NLM: 101092791

Informations de publication

Date de publication:
06 Jun 2022
Historique:
received: 04 04 2022
revised: 02 06 2022
accepted: 04 06 2022
entrez: 10 6 2022
pubmed: 11 6 2022
medline: 14 6 2022
Statut: epublish

Résumé

Vimentin, a type III intermediate filament protein, is found in most cells along with microfilaments and microtubules. It has been shown that the head domain folds back to associate with the rod domain and this association is essential for filament assembly. The N-terminally tagged vimentin has been widely used to label the cytoskeleton in live cell imaging. Although there is previous evidence that EGFP tagged vimentin fails to form filaments but is able to integrate into a pre-existing network, no study has systematically investigated or established a molecular basis for this observation. To determine whether a tag would affect de novo filament assembly, we used vimentin fused at the N-terminus with two different sized tags, AcGFP (239 residues, 27 kDa) and 3 × FLAG (22 residues; 2.4 kDa) to assemble into filaments in two vimentin-deficient epithelial cells, MCF-7 and A431. We showed that regardless of tag size, N-terminally tagged vimentin aggregated into globules with a significant proportion co-aligning with β-catenin at cell-cell junctions. However, the tagged vimentin aggregates could form filaments upon adding untagged vimentin at a ratio of 1:1 or when introduced into cells containing pre-existing filaments. The resultant filament network containing a mixture of tagged and untagged vimentin was less stable compared to that formed by only untagged vimentin. The data suggest that placing a tag at the N-terminus may create steric hinderance in case of a large tag (AcGFP) or electrostatic repulsion in case of highly charged tag (3 × FLAG) perhaps inducing a conformational change, which deleteriously affects the association between head and rod domains. Taken together our results shows that a free N-terminus is essential for filament assembly as N-terminally tagged vimentin is not only incapable of forming filaments, but it also destabilises when integrated into a pre-existing network.

Identifiants

pubmed: 35683030
pii: ijms23116349
doi: 10.3390/ijms23116349
pmc: PMC9181571
pii:
doi:

Substances chimiques

Vimentin 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Références

J Biol Chem. 2012 Aug 17;287(34):28349-61
pubmed: 22740688
Cells. 2016 Jul 05;5(3):
pubmed: 27399781
J Mol Biol. 2009 Feb 20;386(2):544-53
pubmed: 19136013
Exp Cell Res. 1994 Jul;213(1):128-42
pubmed: 8020583
BMC Cancer. 2018 May 3;18(1):519
pubmed: 29724197
J Cell Biol. 1993 Jul;122(2):395-407
pubmed: 8320262
J Biol Chem. 2009 Mar 13;284(11):7330-8
pubmed: 19117942
Cancers (Basel). 2021 Oct 05;13(19):
pubmed: 34638469
Cold Spring Harb Perspect Biol. 2016 Nov 1;8(11):
pubmed: 27803112
FASEB J. 2010 Jun;24(6):1838-51
pubmed: 20097873
J Cell Biol. 1988 Mar;106(3):761-71
pubmed: 2450098
Biophys J. 2018 May 22;114(10):2408-2418
pubmed: 29754715
Redox Biol. 2019 May;23:101098
pubmed: 30658903
J Cell Biol. 1998 Oct 5;143(1):147-57
pubmed: 9763427
J Biol Chem. 2006 Oct 13;281(41):30393-9
pubmed: 16901892
J Struct Biol. 1996 Jul-Aug;117(1):55-69
pubmed: 8776888
Mol Biol Cell. 2017 Apr 1;28(7):848-857
pubmed: 28360214
J Cell Biol. 1990 Nov;111(5 Pt 1):1971-85
pubmed: 1699950
J Cell Biol. 2002 May 27;157(5):795-806
pubmed: 12034772
Nat Commun. 2019 Sep 13;10(1):4200
pubmed: 31519880
J Struct Biol. 2000 Nov;132(2):83-94
pubmed: 11162730
Cell Growth Differ. 1995 Oct;6(10):1245-50
pubmed: 8845301
Cell Biol Int Rep. 1990 Jul;14(7):583-94
pubmed: 2203542
Cancer Res. 2003 May 15;63(10):2658-64
pubmed: 12750294
Dev Cell. 2020 Jan 27;52(2):210-222.e7
pubmed: 31928973
Curr Protoc Protein Sci. 2013 Sep 24;73:9.9.1-9.9.23
pubmed: 24510596
J Biol Chem. 1993 Nov 25;268(33):24916-25
pubmed: 7693709
Mol Biol Cell. 2011 Jul 1;22(13):2282-9
pubmed: 21562225
J Virol. 1996 Aug;70(8):5564-71
pubmed: 8764070
Exp Cell Res. 2002 Oct 1;279(2):344-53
pubmed: 12243759
Cell Mol Life Sci. 2011 Sep;68(18):3033-46
pubmed: 21637948
J Mol Biol. 1996 Dec 20;264(5):933-53
pubmed: 9000622
J Cell Sci. 1994 Jun;107 ( Pt 6):1593-607
pubmed: 7962200
EMBO J. 2002 Mar 15;21(6):1255-66
pubmed: 11889032
Mol Cell Biol. 2011 Sep;31(18):3773-89
pubmed: 21746880
J Cell Sci. 1994 Jun;107 ( Pt 6):1609-22
pubmed: 7962201
Mol Biol Cell. 1999 May;10(5):1289-95
pubmed: 10233144
Int J Dev Biol. 2008;52(4):353-63
pubmed: 18415935
Cell. 1991 Sep 20;66(6):1301-11
pubmed: 1717157
J Cell Sci. 1983 Sep;63:43-67
pubmed: 6313713
Am J Pathol. 1997 Feb;150(2):483-95
pubmed: 9033265
Cold Spring Harb Perspect Biol. 2018 Jul 2;10(7):
pubmed: 29967009
Oncotarget. 2015 Jun 30;6(18):15966-83
pubmed: 25965826
Mol Vis. 2008 Jul 10;14:1282-7
pubmed: 18618007
Nature. 1987 Aug 13-19;328(6131):649-52
pubmed: 3039376
Biochim Biophys Acta. 2013 Jun;1833(6):1283-93
pubmed: 23458836
Cells. 2020 Dec 05;9(12):
pubmed: 33291479
Exp Cell Res. 2007 Jun 10;313(10):2050-62
pubmed: 17512929
Cell. 1991 Jan 25;64(2):365-80
pubmed: 1703046
Oncogene. 2019 May;38(21):4075-4094
pubmed: 30696956
J Neurosci Res. 1993 Oct 1;36(2):163-72
pubmed: 8263969
J Cell Sci. 1995 Nov;108 ( Pt 11):3463-71
pubmed: 8586658
Int J Clin Exp Pathol. 2018 Jan 01;11(1):199-207
pubmed: 31938101
Sci Rep. 2020 Nov 11;10(1):19525
pubmed: 33177544
Proc Natl Acad Sci U S A. 2012 Aug 21;109(34):13620-5
pubmed: 22869704
J Natl Cancer Inst. 1973 Nov;51(5):1417-23
pubmed: 4357758
Methods Enzymol. 2016;568:389-426
pubmed: 26795478
J Natl Cancer Inst. 1973 Nov;51(5):1409-16
pubmed: 4357757
J Natl Cancer Inst. 1974 Sep;53(3):661-74
pubmed: 4412247
Oncogene. 2001 May 24;20(23):2868-76
pubmed: 11420699
PLoS One. 2009;4(3):e4849
pubmed: 19287496
Mol Biol Cell. 2004 Mar;15(3):990-1002
pubmed: 14668478
J Cell Biol. 1998 Oct 5;143(1):159-70
pubmed: 9763428
PLoS One. 2016 Aug 08;11(8):e0160901
pubmed: 27501229
Cells. 2021 Sep 17;10(9):
pubmed: 34572105
Cell. 1990 Sep 21;62(6):1063-71
pubmed: 2169348
J Cell Biochem. 1994 Jan;54(1):100-9
pubmed: 8126080
Int J Mol Sci. 2020 Apr 09;21(7):
pubmed: 32283594
Nat Commun. 2015 Jun 02;6:7287
pubmed: 26031447
J Biol Chem. 1989 Oct 25;264(30):18119-27
pubmed: 2808368
Cells. 2018 Sep 21;7(10):
pubmed: 30248895
Proc Natl Acad Sci U S A. 2022 Feb 8;119(6):
pubmed: 35078919
Nat Commun. 2018 Mar 2;9(1):930
pubmed: 29500346
J Biol Chem. 2004 Oct 22;279(43):44841-6
pubmed: 15231822
J Cell Biol. 1990 Aug;111(2):553-65
pubmed: 1696263
Exp Mol Med. 2005 Oct 31;37(5):427-35
pubmed: 16264267
J Cell Sci. 2008 Nov 15;121(Pt 22):3737-46
pubmed: 18940912
J Cell Sci. 1992 Feb;101 ( Pt 2):363-81
pubmed: 1629250
Proc Natl Acad Sci U S A. 2007 Mar 27;104(13):5378-82
pubmed: 17369356
J Cell Biol. 2007 Jun 4;177(5):795-807
pubmed: 17535969
J Cell Sci. 1992 Mar;101 ( Pt 3):687-700
pubmed: 1522151
Carcinogenesis. 1995 Oct;16(10):2515-21
pubmed: 7586160
Cell. 1980 Nov;22(2 Pt 2):629-32
pubmed: 6160916
Sci Adv. 2022 Feb 25;8(8):eabm2696
pubmed: 35213220
Am J Physiol Cell Physiol. 2008 Apr;294(4):C869-78
pubmed: 18256275
Curr Opin Cell Biol. 2015 Feb;32:65-72
pubmed: 25596497
Cell Commun Signal. 2021 Mar 15;19(1):33
pubmed: 33722250
J Biol Chem. 2000 Sep 22;275(38):29772-8
pubmed: 10887173
J Biol Chem. 2003 Mar 7;278(10):8526-30
pubmed: 12458200
Biomaterials. 2014 Feb;35(5):1359-66
pubmed: 24268665
J Mol Biol. 2004 Jun 25;340(1):97-114
pubmed: 15184025
J Biol Chem. 2010 May 14;285(20):15278-15285
pubmed: 20231271
Cell Stress Chaperones. 2009 Jul;14(4):381-9
pubmed: 19137416
J Cell Sci. 1998 Jul;111 ( Pt 13):1767-78
pubmed: 9625740
Eur J Pharm Sci. 2002 Aug;16(3):151-7
pubmed: 12128169
Nature. 1992 Mar 19;356(6366):244-6
pubmed: 1372711
J Biol Chem. 2002 Apr 26;277(17):14933-41
pubmed: 11827972
Proc Natl Acad Sci U S A. 1993 Sep 15;90(18):8392-6
pubmed: 7690960

Auteurs

Saima Usman (S)

Centre for Oral Immunobiology and Regenerative Medicine, Institute of Dentistry, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, Newark Street, London E1 2AT, UK.

Hebah Aldehlawi (H)

Department of Oral Diagnostic Sciences, Division of Oral Pathology and Medicine, Faculty of Dentistry, King Abdul Aziz University, Jeddah 21589, Saudi Arabia.

Thuan Khanh Ngoc Nguyen (TKN)

Centre for Oral Immunobiology and Regenerative Medicine, Institute of Dentistry, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, Newark Street, London E1 2AT, UK.

Muy-Teck Teh (MT)

Centre for Oral Immunobiology and Regenerative Medicine, Institute of Dentistry, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, Newark Street, London E1 2AT, UK.

Ahmad Waseem (A)

Centre for Oral Immunobiology and Regenerative Medicine, Institute of Dentistry, Barts and The London School of Medicine and Dentistry, Queen Mary University of London, Newark Street, London E1 2AT, UK.
Centre for Immunobiology and Regenerative Medicine, Blizard Institute, 4 Newark Street, London E1 2AT, UK.

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