Uncovering the BIN1-SH3 interactome underpinning centronuclear myopathy.

Publisher: eLife Sciences Publications, Ltd Country of Publication: England NLM ID: 101579614 Publication Model: Electronic Cited Medium: Internet ISSN: 2050-084X (Electronic) Linking ISSN: 2050084X NLM ISO Abbreviation: Elife Subsets: MEDLINE

Original Publication: Cambridge, UK : eLife Sciences Publications, Ltd., 2012-

Myopathies, Structural, Congenital*/metabolism ; Myopathies, Structural, Congenital*/genetics ; Adaptor Proteins, Signal Transducing*/metabolism ; Adaptor Proteins, Signal Transducing*/genetics ; Tumor Suppressor Proteins*/metabolism ; Tumor Suppressor Proteins*/genetics ; Nuclear Proteins*/metabolism ; Nuclear Proteins*/genetics ; src Homology Domains*; Humans ; Protein Binding ; Dynamin II/metabolism ; Dynamin II/genetics ; Mutation

Truncation of the protein-protein interaction SH3 domain of the membrane remodeling Bridging Integrator 1 (BIN1, Amphiphysin 2) protein leads to centronuclear myopathy. Here, we assessed the impact of a set of naturally observed, previously uncharacterized BIN1 SH3 domain variants using conventional in vitro and cell-based assays monitoring the BIN1 interaction with dynamin 2 (DNM2) and identified potentially harmful ones that can be also tentatively connected to neuromuscular disorders. However, SH3 domains are typically promiscuous and it is expected that other, so far unknown partners of BIN1 exist besides DNM2, that also participate in the development of centronuclear myopathy. In order to shed light on these other relevant interaction partners and to get a holistic picture of the pathomechanism behind BIN1 SH3 domain variants, we used affinity interactomics. We identified hundreds of new BIN1 interaction partners proteome-wide, among which many appear to participate in cell division, suggesting a critical role of BIN1 in the regulation of mitosis. Finally, we show that the identified BIN1 mutations indeed cause proteome-wide affinity perturbation, signifying the importance of employing unbiased affinity interactomic approaches.
Competing Interests: BZ, EE, BM, LN, MP, ZD, SO, GT, JL, GG No competing interests declared
(© 2024, Zambo et al.)

J Biol Chem. 2021 Jan-Jun;296:100077. (PMID: 33187981)
J Biol Chem. 1998 Apr 3;273(14):8169-76. (PMID: 9525921)
Biochim Biophys Acta. 2015 Oct;1853(10 Pt A):2560-9. (PMID: 26079855)
EMBO J. 2004 Nov 10;23(22):4413-22. (PMID: 15483625)
J Mol Biol. 2019 Mar 15;431(6):1234-1249. (PMID: 30726710)
Nucleic Acids Res. 2020 Jan 8;48(D1):D296-D306. (PMID: 31680160)
Bioessays. 2023 Jun;45(6):e2300007. (PMID: 36998104)
EMBO J. 1998 Sep 15;17(18):5273-85. (PMID: 9736607)
Science. 2002 Aug 16;297(5584):1193-6. (PMID: 12183633)
FEBS J. 2017 Oct;284(19):3218-3229. (PMID: 28755476)
Mol Cell. 1998 Dec;2(6):877-85. (PMID: 9885575)
Cell. 2021 May 27;184(11):3022-3040.e28. (PMID: 33961781)
Nucleic Acids Res. 2015 Jan;43(Database issue):D1140-4. (PMID: 25378319)
Nature. 2021 Aug;596(7873):590-596. (PMID: 34293799)
J Biol Chem. 1997 May 16;272(20):13419-25. (PMID: 9148966)
Sci Adv. 2022 Dec 21;8(51):eade3828. (PMID: 36542723)
Nucleic Acids Res. 2002 Jul 15;30(14):3059-66. (PMID: 12136088)
Nucleic Acids Res. 2023 Jan 6;51(D1):D523-D531. (PMID: 36408920)
Nucleic Acids Res. 2001 Jan 1;29(1):308-11. (PMID: 11125122)
Am J Med Genet A. 2005 Apr 30;134(3):338-40. (PMID: 15690409)
Nature. 1994 Nov 24;372(6504):375-9. (PMID: 7802869)
J Clin Invest. 2017 Dec 1;127(12):4477-4487. (PMID: 29130937)
Nat Methods. 2022 Jun;19(6):679-682. (PMID: 35637307)
Mol Cell. 2012 Jun 29;46(6):884-92. (PMID: 22749401)
Nat Genet. 1996 Jun;13(2):175-82. (PMID: 8640223)
Nature. 2020 May;581(7809):434-443. (PMID: 32461654)
Neuromuscul Disord. 2021 Dec;31(12):1313-1357. (PMID: 34930546)
J Cell Biol. 2023 Feb 6;222(2):. (PMID: 36445308)
J Biol Chem. 2016 Jul 29;291(31):16307-17. (PMID: 27268056)
Nucleic Acids Res. 2020 Jan 8;48(D1):D835-D844. (PMID: 31777943)
J Neurochem. 1998 Jun;70(6):2369-76. (PMID: 9603201)
Nucleic Acids Res. 2019 Jul 2;47(W1):W191-W198. (PMID: 31066453)
Nat Commun. 2022 Sep 17;13(1):5472. (PMID: 36115835)
Nat Genet. 2005 Nov;37(11):1207-9. (PMID: 16227997)
Nat Methods. 2015 Aug;12(8):787-93. (PMID: 26053890)
Science. 2004 Jan 23;303(5657):495-9. (PMID: 14645856)
Curr Biol. 2002 Dec 23;12(24):2111-7. (PMID: 12498685)
J Mol Biol. 2005 Aug 5;351(1):182-94. (PMID: 15992821)
Nucleic Acids Res. 2007 Jul;35(Web Server issue):W455-9. (PMID: 17576682)
Nucleic Acids Res. 2009 Feb;37(3):939-44. (PMID: 19106141)
J Mol Med (Berl). 2014 May;92(5):453-63. (PMID: 24590001)
Nat Commun. 2022 Nov 11;13(1):6849. (PMID: 36369230)
Nat Genet. 2007 Sep;39(9):1134-9. (PMID: 17676042)
J Cell Biol. 2021 Dec 6;220(12):. (PMID: 34633413)
Proteomics. 2007 Jun;7(11):1775-85. (PMID: 17474147)
J Cell Biol. 2002 Jun 24;157(7):1175-86. (PMID: 12082078)
Nucleic Acids Res. 2017 Jul 3;45(W1):W464-W469. (PMID: 28387819)
Front Mol Neurosci. 2018 Nov 14;11:421. (PMID: 30487734)
Anal Biochem. 2023 Feb 15;663:115017. (PMID: 36526023)
Nature. 2020 Apr;580(7803):402-408. (PMID: 32296183)
Gastroenterology. 2006 Mar;130(3):794-809. (PMID: 16530520)
J Gen Physiol. 2022 Sep 5;154(9):. (PMID: 35980353)
Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):331-5. (PMID: 8552632)
Int J Mol Sci. 2022 Jun 03;23(11):. (PMID: 35682949)
Biochemistry. 2014 Nov 25;53(46):7297-309. (PMID: 25350771)
Brain. 2014 Dec;137(Pt 12):3160-70. (PMID: 25260562)
Protein Expr Purif. 2006 Nov;50(1):89-101. (PMID: 16884919)
Sci Transl Med. 2019 Mar 20;11(484):. (PMID: 30894500)
J Cell Sci. 2003 Oct 15;116(Pt 20):4159-68. (PMID: 12972505)
Nucleic Acids Res. 2012 Jul;40(13):6353-66. (PMID: 22457068)
Genes Dev. 2001 Nov 15;15(22):2967-79. (PMID: 11711432)
Proc Natl Acad Sci U S A. 2022 Mar 1;119(9):. (PMID: 35217605)
Hum Mol Genet. 2015 Oct 1;24(19):5542-54. (PMID: 26199319)
Structure. 2020 Jul 7;28(7):747-759.e3. (PMID: 32294469)
Science. 2022 Mar 11;375(6585):eabi6983. (PMID: 35271311)

post doc grant Institut de génétique et de biologie moléculaire et cellulaire; CRCN starting package Inserm; 2015 Ligue Contre le Cancer; ANR-18-CE92-0017 Agence Nationale de la Recherche; ANR-22-CE44-0018 Agence Nationale de la Recherche; ANR-22-CE11-0026 Agence Nationale de la Recherche; 23933 AFM-Téléthon; K139284 OTKA

Keywords: BIN1; SH3 domain; biochemistry; biophysics; chemical biology; human; interactomics; myopathy

0 (BIN1 protein, human)
0 (Adaptor Proteins, Signal Transducing)
0 (Tumor Suppressor Proteins)
0 (Nuclear Proteins)
EC 3.6.5.5 (Dynamin II)

Date Created: 20240712 Date Completed: 20240712 Latest Revision: 20240715

20240715

PMC11245310

10.7554/eLife.95397

38995680