Cited by 71Nuclear Structure and FunctionMicrotubule and mitosis dynamicsMuscle Physiology and Disorders

Amphiphysin 2 Orchestrates Nucleus Positioning and Shape by Linking the Nuclear Envelope to the Actin and Microtubule Cytoskeleton

Open access
D’Alessandro, Manuela, Hnia, Karim, Gache, Vincent, Koch, Catherine, Gavriilidis, Christos, Rodriguez, David, Nicot, Anne-Sophie, Romero, Norma B. +4 more·2015·Developmental Cell

Abstract

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.devcel.2015.09.018

Cites

2 of 2 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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?

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.

Flagged first, then by citations

Research works printed but not linked: 32

  1. [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]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]3. Brenner, S. The genetics of Caenorhabditis elegans Genetics. 1974; 77:71-94 Crossref PubMed Google Scholar
  4. [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
  5. [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
  6. [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
  7. [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
  8. [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
  9. [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
  10. [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
  11. [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
  12. [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
  13. [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
  14. [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
  15. [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
  16. [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
  17. [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
  18. [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
  19. [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
  20. [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
  21. [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
  22. [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
  23. [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
  24. [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
  25. [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
  26. [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
  27. [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
  28. [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
  29. [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
  30. [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
  31. [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
  32. [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

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
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
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