Amphiphysin 2 Orchestrates Nucleus Positioning and Shape by Linking the Nuclear Envelope to the Actin and Microtubule Cytoskeleton
Open accessAbstract
Nucleus positioning is key for intracellular organization, cell differentiation, and organ development and is affected in many diseases, including myopathies due to alteration in amphiphysin-2 (BIN1). The actin and microtubule cytoskeletons are essential for nucleus positioning, but their crosstalk in this process is sparsely characterized. Here, we report that impairment of amphiphysin/BIN1 in Caenorhabditis elegans, mammalian cells, or muscles from patients with centronuclear myopathy alters nuclear position and shape. We show that AMPH-1/BIN1 binds to nesprin and actin, as well as to the microtubule-binding protein CLIP170 in both species. Expression of the microtubule-anchoring CAP-GLY domain of CLIP170 fused to the nuclear-envelope-anchoring KASH domain of nesprin rescues nuclear positioning defects of amph-1 mutants. Amphiphysins thus play a central role in linking the nuclear envelope with the actin and microtubule cytoskeletons. We propose that BIN1 has a direct and evolutionarily conserved role in nuclear positioning, altered in myopathies.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
BIN1 physically interacts with FAK, binds F-actin and CLIP170 in non-neuronal cells, and directly remodels actin dynamics through its BAR domain.
“BIN1 physically interacts with FA kinase (FAK), which presents strong homology with Pyk2 [90]. In addition, BIN1 binds to F-actin and microtubule-binding protein CLIP170 in non-neuronal cells [21] and directly remodels actin dynamics through its BAR domain [27].”
From The new genetic landscape of Alzheimer’s disease: from amyloid cascade to genetically driven synaptic failure hypothesis? (2019) · cites this paper as [21]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Part of this paper’s reference list could not be split into single entries.
Nicot, A.-S., Toussaint, A., Tosch, V., Kretz, C., Wallgren-Pettersson, C., Iwarsson, E., Kingston, H., Garnier, J.-M., Biancalana, V., Oldfors, A., et al. (2007) · Nature Genetics · doi:10.1038/ng2086 · Cited by 434 · see citing works
Self-citationFalcone, S., Roman, W., Hnia, K., Gache, V., Didier, N., Lainé, J., Auradé, F., Marty, I., Nishino, I., Charlet‐Berguerand, N., et al. (2014) · EMBO Molecular Medicine · doi:10.15252/emmm.201404436 · Cited by 116 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 32
- [1]1. Attali, R. ∙ Warwar, N. ∙ Israel, A. ... Mutation of SYNE-1, encoding an essential component of the nuclear lamina, is responsible for autosomal recessive arthrogryposis Hum. Mol. Genet. 2009; 18:3462-3469 Crossref Scopus (128) PubMed Google Scholar
- [2]2. Bettinger, J.C. ∙ Lee, K. ∙ Rougvie, A.E. Stage-specific accumulation of the terminal differentiation factor LIN-29 during Caenorhabditis elegans development Development. 1996; 122:2517-2527 Crossref PubMed Google Scholar
- [3]3. Brenner, S. The genetics of Caenorhabditis elegans Genetics. 1974; 77:71-94 Crossref PubMed Google Scholar
- [4]4. Chang, W. ∙ Worman, H.J. ∙ Gundersen, G.G. Accessorizing and anchoring the LINC complex for multifunctionality J. Cell Biol. 2015; 208:11-22 Crossref Scopus (213) PubMed Google Scholar
- [6]6. Fernando, P. ∙ Sandoz, J.S. ∙ Ding, W. ... Bin1 SRC homology 3 domain acts as a scaffold for myofiber sarcomere assembly J. Biol. Chem. 2009; 284:27674-27686 Crossref Scopus (29) PubMed Google Scholar
- [7]7. Fridolfsson, H.N. ∙ Ly, N. ∙ Meyerzon, M. ... UNC-83 coordinates kinesin-1 and dynein activities at the nuclear envelope during nuclear migration Dev. Biol. 2010; 338:237-250 Crossref Scopus (110) PubMed Google Scholar
- [8]8. Fugier, C. ∙ Klein, A.F. ∙ Hammer, C. ... Misregulated alternative splicing of BIN1 is associated with T tubule alterations and muscle weakness in myotonic dystrophy Nat. Med. 2011; 17:720-725 Crossref Scopus (258) PubMed Google Scholar
- [9]9. Gomes, E.R. ∙ Jani, S. ∙ Gundersen, G.G. Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells Cell. 2005; 121:451-463 Full Text Full Text (PDF) Scopus (492) PubMed Google Scholar
- [10]10. Gupta, K.K. ∙ Joyce, M.V. ∙ Slabbekoorn, A.R. ... Probing interactions between CLIP-170, EB1, and microtubules J. Mol. Biol. 2010; 395:1049-1062 Crossref Scopus (23) PubMed Google Scholar
- [11]11. Hnia, K. ∙ Tronchère, H. ∙ Tomczak, K.K. ... Myotubularin controls desmin intermediate filament architecture and mitochondrial dynamics in human and mouse skeletal muscle J. Clin. Invest. 2011; 121:70-85 Crossref Scopus (109) PubMed Google Scholar
- [12]12. Kamath, R.S. ∙ Fraser, A.G. ∙ Dong, Y. ... Systematic functional analysis of the Caenorhabditis elegans genome using RNAi Nature. 2003; 421:231-237 Crossref Scopus (2878) PubMed Google Scholar
- [13]13. Kolotuev, I. ∙ Schwab, Y. ∙ Labouesse, M. A precise and rapid mapping protocol for correlative light and electron microscopy of small invertebrate organisms Biol. Cell. 2010; 102:121-132 Crossref Scopus (65) Google Scholar
- [14]14. Labouesse, M. Deficiency screen based on the monoclonal antibody MH27 to identify genetic loci required for morphogenesis of the Caenorhabditis elegans embryo Dev. Dyn. 1997; 210:19-32 Crossref Scopus (28) PubMed Google Scholar
- [15]15. Lee, E. ∙ Marcucci, M. ∙ Daniell, L. ... Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle Science. 2002; 297:1193-1196 Crossref Scopus (351) PubMed Google Scholar
- [16]16. Lombardi, M.L. ∙ Jaalouk, D.E. ∙ Shanahan, C.M. ... The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton J. Biol. Chem. 2011; 286:26743-26753 Crossref Scopus (398) PubMed Google Scholar
- [17]17. Luxton, G.W. ∙ Gomes, E.R. ∙ Folker, E.S. ... Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement Science. 2010; 329:956-959 Crossref Scopus (351) PubMed Google Scholar
- [18]18. Maciver, S.K. ∙ Zot, H.G. ∙ Pollard, T.D. Characterization of actin filament severing by actophorin from Acanthamoeba castellanii J. Cell Biol. 1991; 115:1611-1620 Crossref Scopus (202) PubMed Google Scholar
- [19]19. McMahon, H.T. ∙ Gallop, J.L. Membrane curvature and mechanisms of dynamic cell membrane remodelling Nature. 2005; 438:590-596 Crossref Scopus (1742) PubMed Google Scholar
- [20]20. Metzger, T. ∙ Gache, V. ∙ Xu, M. ... MAP and kinesin-dependent nuclear positioning is required for skeletal muscle function Nature. 2012; 484:120-124 Crossref Scopus (205) PubMed Google Scholar
- [21]21. Meunier, B. ∙ Quaranta, M. ∙ Daviet, L. ... The membrane-tubulating potential of amphiphysin 2/BIN1 is dependent on the microtubule-binding cytoplasmic linker protein 170 (CLIP-170) Eur. J. Cell Biol. 2009; 88:91-102 Crossref Scopus (41) PubMed Google Scholar
- [23]23. Pant, S. ∙ Sharma, M. ∙ Patel, K. ... AMPH-1/Amphiphysin/Bin1 functions with RME-1/Ehd1 in endocytic recycling Nat. Cell Biol. 2009; 11:1399-1410 Crossref Scopus (159) PubMed Google Scholar
- [24]24. Plewniak, F. ∙ Bianchetti, L. ∙ Brelivet, Y. ... PipeAlign: A new toolkit for protein family analysis Nucleic Acids Res. 2003; 31:3829-3832 Crossref Scopus (106) PubMed Google Scholar
- [25]25. Prokic, I. ∙ Cowling, B.S. ∙ Laporte, J. Amphiphysin 2 (BIN1) in physiology and diseases J. Mol. Med. (Berl.). 2014; 92:453-463 Crossref Scopus (107) PubMed Google Scholar
- [26]26. Puckelwartz, M.J. ∙ Kessler, E. ∙ Zhang, Y. ... Disruption of nesprin-1 produces an Emery Dreifuss muscular dystrophy-like phenotype in mice Hum. Mol. Genet. 2009; 18:607-620 Crossref Scopus (163) PubMed Google Scholar
- [27]27. Rajgor, D. ∙ Shanahan, C.M. Nesprins: from the nuclear envelope and beyond Expert Rev. Mol. Med. 2013; 15:e5 Crossref Scopus (150) PubMed Google Scholar
- [28]28. Romero, N.B. Centronuclear myopathies: a widening concept Neuromuscul. Disord. 2010; 20:223-228 Full Text Full Text (PDF) Scopus (196) PubMed Google Scholar
- [29]29. Sharp, D.J. ∙ Ross, J.L. Microtubule-severing enzymes at the cutting edge J. Cell Sci. 2012; 125:2561-2569 Crossref Scopus (170) PubMed Google Scholar
- [30]30. Starr, D.A. ∙ Han, M. Role of ANC-1 in tethering nuclei to the actin cytoskeleton Science. 2002; 298:406-409 Crossref Scopus (334) PubMed Google Scholar
- [31]31. Vallee, R.B. A taxol-dependent procedure for the isolation of microtubules and microtubule-associated proteins (MAPs) J. Cell Biol. 1982; 92:435-442 Crossref Scopus (429) PubMed Google Scholar
- [32]32. Williams-Masson, E.M. ∙ Heid, P.J. ∙ Lavin, C.A. ... The cellular mechanism of epithelial rearrangement during morphogenesis of the Caenorhabditis elegans dorsal hypodermis Dev. Biol. 1998; 204:263-276 Crossref Scopus (106) PubMed Google Scholar
- [33]33. Zhang, Q. ∙ Bethmann, C. ∙ Worth, N.F. ... 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; 16:2816-2833 Crossref Scopus (424) PubMed Google Scholar
- [34]34. Zhang, X. ∙ Lei, K. ∙ Yuan, X. ... SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice Neuron. 2009; 64:173-187 Full Text Full Text (PDF) Scopus (378) PubMed Google Scholar
Cited by
Sorted by citations
Dourlen, P., Kilinc, D., Malmanche, N., Chapuis, J., & Lambert, J.-C. (2019) · Acta Neuropathologica · doi:10.1007/s00401-019-02004-0 · Cited by 168 · see citing works
Nuclear Mechanotransduction in Skeletal Muscle
Jabre, S., Hleihel, W., & Coirault, C. (2021) · Cells · doi:10.3390/cells10020318 · Cited by 31 · see citing works
- Authors
- D’Alessandro, M., Hnia, K., Gache, V., Koch, C., Gavriilidis, C., Rodriguez, D., Nicot, A.-S., Romero, N. B., Schwab, Y., Gomes, E., Labouesse, M., & Laporte, J.
- Affiliations
- Lyon 1 Université (FR)
- Centre National de la Recherche Scientifique (FR)
- École Normale Supérieure de Lyon (FR)
- Institut de Myologie (FR)
- University of Lisbon (PT)
- Corresponding author
- D’Alessandro, Manuela
- Laporte, Jocelyn
- ORCID
- Venue
- Developmental Cell
- Publisher
- Elsevier BV
- Published
- 2015-10
- Volume
- 35
- Issue
- 2
- Pages
- 186-198
- ISSN
- 1534-5807 (ISSN-L)
- OpenAlex
- W1870115160
- Cited by
- 71
- References
- 2
- Citations by year
- 2026: 2 · 2025: 9 · 2024: 3 · 2023: 3 · 2022: 5 · 2021: 10 · 2020: 6 · 2019: 8 · 2018: 10 · 2017: 10 · 2016: 5
- FWCI
- 3.29
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Cell (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-10-LABX-0030)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Keywords
- BIN1, nuclear positioning, nuclear shape, nuclear envelope, actin cytoskeleton, microtubule cytoskeleton, nesprins, centronuclear myopathy, myopathy, KASH domain, CAP-Gly domain, Caenorhabditis elegans
- MeSH terms
- Actins, Animals, Cell Nucleus, Chlorocebus aethiops, Cytoplasm, Cytoskeleton, Humans, Microfilament Proteins, Microtubule-Associated Proteins, Microtubules, Neoplasm Proteins, Nerve Tissue Proteins, Nuclear Envelope, Nuclear Proteins, Caenorhabditis elegans, Muscle, Skeletal, COS Cells, Myopathies, Structural, Congenital, Multiprotein Complexes, Cell Shape, HEK293 Cells
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review