Nuclear myosin I regulates cell membrane tension
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
27480647
PubMed Central
PMC4969604
DOI
10.1038/srep30864
PII: srep30864
Knihovny.cz E-zdroje
- MeSH
- buněčná membrána metabolismus MeSH
- buněčné jádro metabolismus MeSH
- exocytóza fyziologie MeSH
- fibroblasty cytologie metabolismus MeSH
- HeLa buňky MeSH
- kultivované buňky MeSH
- kůže cytologie metabolismus MeSH
- lidé MeSH
- mikrofilamenta metabolismus MeSH
- myosin typu I metabolismus MeSH
- myši knockoutované MeSH
- myši MeSH
- pohyb buněk MeSH
- tvar buňky MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- myosin typu I MeSH
Plasma membrane tension is an important feature that determines the cell shape and influences processes such as cell motility, spreading, endocytosis and exocytosis. Unconventional class 1 myosins are potent regulators of plasma membrane tension because they physically link the plasma membrane with adjacent cytoskeleton. We identified nuclear myosin 1 (NM1) - a putative nuclear isoform of myosin 1c (Myo1c) - as a new player in the field. Although having specific nuclear functions, NM1 localizes predominantly to the plasma membrane. Deletion of NM1 causes more than a 50% increase in the elasticity of the plasma membrane around the actin cytoskeleton as measured by atomic force microscopy. This higher elasticity of NM1 knock-out cells leads to 25% higher resistance to short-term hypotonic environment and rapid cell swelling. In contrast, overexpression of NM1 in wild type cells leads to an additional 30% reduction of their survival. We have shown that NM1 has a direct functional role in the cytoplasm as a dynamic linker between the cell membrane and the underlying cytoskeleton, regulating the degree of effective plasma membrane tension.
Zobrazit více v PubMed
Pestic-Dragovich L. et al.. A myosin I isoform in the nucleus. Science 290, 337–341 (2000). PubMed
Ihnatovych I., Migocka-Patrzalek M., Dukh M. & Hofmann W. A. Identification and characterization of a novel myosin Ic isoform that localizes to the nucleus. Cytoskeleton 69, 555–565, doi: 10.1002/cm.21040 (2012). PubMed DOI
Adams R. J. & Pollard T. D. Binding of myosin I to membrane lipids. Nature 340, 565–568, doi: 10.1038/340565a0 (1989). PubMed DOI
Nambiar R., McConnell R. E. & Tyska M. J. Control of cell membrane tension by myosin-I. Proceedings of the National Academy of Sciences of the United States of America 106, 11972–11977, doi: 10.1073/pnas.0901641106 (2009). PubMed DOI PMC
Olety B., Walte M., Honnert U., Schillers H. & Bahler M. Myosin 1G (Myo1G) is a haematopoietic specific myosin that localizes to the plasma membrane and regulates cell elasticity. FEBS letters 584, 493–499, doi: 10.1016/j.febslet.2009.11.096 (2010). PubMed DOI
Hokanson D. E. & Ostap E. M. Myo1c binds tightly and specifically to phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate. Proceedings of the National Academy of Sciences of the United States of America 103, 3118–3123, doi: 10.1073/pnas.0505685103 (2006). PubMed DOI PMC
Bose A. et al.. Unconventional myosin Myo1c promotes membrane fusion in a regulated exocytic pathway. Molecular and cellular biology 24, 5447–5458, doi: 10.1128/MCB.24.12.5447-5458.2004 (2004). PubMed DOI PMC
Fan Y., Eswarappa S. M., Hitomi M. & Fox P. L. Myo1c facilitates G-actin transport to the leading edge of migrating endothelial cells. The Journal of cell biology 198, 47–55, doi: 10.1083/jcb.201111088 (2012). PubMed DOI PMC
Hagan G. N., Lin Y., Magnuson M. A., Avruch J. & Czech M. P. A Rictor-Myo1c complex participates in dynamic cortical actin events in 3T3-L1 adipocytes. Molecular and cellular biology 28, 4215–4226, doi: 10.1128/MCB.00867-07 (2008). PubMed DOI PMC
Maravillas-Montero J. L., Gillespie P. G., Patino-Lopez G., Shaw S. & Santos-Argumedo L. Myosin 1c participates in B cell cytoskeleton rearrangements, is recruited to the immunologic synapse, and contributes to antigen presentation. Journal of immunology 187, 3053–3063, doi: 10.4049/jimmunol.1004018 (2011). PubMed DOI
Diefenbach T. J. et al.. Myosin 1c and myosin IIB serve opposing roles in lamellipodial dynamics of the neuronal growth cone. The Journal of cell biology 158, 1207–1217 (2002). PubMed PMC
Wang F. S., Liu C. W., Diefenbach T. J. & Jay D. G. Modeling the role of myosin 1c in neuronal growth cone turning. Biophysical journal 85, 3319–3328, doi: 10.1016/S0006-3495(03)74751-1 (2003). PubMed DOI PMC
Bose A. et al.. Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature 420, 821–824, doi: 10.1038/nature01246 (2002). PubMed DOI
Tiwari A., Jung J. J., Inamdar S. M., Nihalani D. & Choudhury A. The myosin motor Myo1c is required for VEGFR2 delivery to the cell surface and for angiogenic signaling. American journal of physiology. Heart and circulatory physiology 304, H687–696, doi: 10.1152/ajpheart.00744.2012 (2013). PubMed DOI PMC
Dumont R. A., Zhao Y. D., Holt J. R., Bahler M. & Gillespie P. G. Myosin-I isozymes in neonatal rodent auditory and vestibular epithelia. Journal of the Association for Research in Otolaryngology: JARO 3, 375–389, doi: 10.1007/s101620020049 (2002). PubMed DOI PMC
Gillespie P. G. & Cyr J. L. Myosin-1c, the hair cell’s adaptation motor. Annual review of physiology 66, 521–545, doi: 10.1146/annurev.physiol.66.032102.112842 (2004). PubMed DOI
Gillespie P. G. & Muller U. Mechanotransduction by hair cells: models, molecules, and mechanisms. Cell 139, 33–44, doi: 10.1016/j.cell.2009.09.010 (2009). PubMed DOI PMC
Hofmann W. A. et al.. Nuclear myosin I is necessary for the formation of the first phosphodiester bond during transcription initiation by RNA polymerase II. Journal of cellular biochemistry 99, 1001–1009, doi: 10.1002/jcb.21035 (2006). PubMed DOI
Philimonenko V. V. et al.. Nuclear actin and myosin I are required for RNA polymerase I transcription. Nature cell biology 6, 1165–1172, doi: 10.1038/ncb1190 (2004). PubMed DOI
Venit T. et al.. Mouse nuclear myosin I knock-out shows interchangeability and redundancy of myosin isoforms in the cell nucleus. PloS one 8, e61406, doi: 10.1371/journal.pone.0061406 (2013). PubMed DOI PMC
de Lanerolle P. & Serebryannyy L. Nuclear actin and myosins: life without filaments. Nature cell biology 13, 1282–1288, doi: 10.1038/ncb2364 (2011). PubMed DOI
Obrdlik A. et al.. Nuclear myosin 1 is in complex with mature rRNA transcripts and associates with the nuclear pore basket. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 24, 146–157, doi: 10.1096/fj.09-135863 (2010). PubMed DOI
Percipalle P. et al.. The chromatin remodelling complex WSTF-SNF2h interacts with nuclear myosin 1 and has a role in RNA polymerase I transcription. EMBO reports 7, 525–530, doi: 10.1038/sj.embor.7400657 (2006). PubMed DOI PMC
Dundr M. et al.. Actin-dependent intranuclear repositioning of an active gene locus in vivo. The Journal of cell biology 179, 1095–1103, doi: 10.1083/jcb.200710058 (2007). PubMed DOI PMC
Chuang C. H. et al.. Long-range directional movement of an interphase chromosome site. Current biology: CB 16, 825–831, doi: 10.1016/j.cub.2006.03.059 (2006). PubMed DOI
Mehta I. S., Amira M., Harvey A. J. & Bridger J. M. Rapid chromosome territory relocation by nuclear motor activity in response to serum removal in primary human fibroblasts. Genome biology 11, R5, doi: 10.1186/gb-2010-11-1-r5 (2010). PubMed DOI PMC
Dzijak R. et al.. Specific nuclear localizing sequence directs two myosin isoforms to the cell nucleus in calmodulin-sensitive manner. PloS one 7, e30529, doi: 10.1371/journal.pone.0030529 (2012). PubMed DOI PMC
Hokanson D. E., Laakso J. M., Lin T., Sept D. & Ostap E. M. Myo1c binds phosphoinositides through a putative pleckstrin homology domain. Molecular biology of the cell 17, 4856–4865, doi: 10.1091/mbc.E06-05-0449 (2006). PubMed DOI PMC
Kahle M., Pridalova J., Spacek M., Dzijak R. & Hozak P. Nuclear myosin is ubiquitously expressed and evolutionary conserved in vertebrates. Histochemistry and cell biology 127, 139–148, doi: 10.1007/s00418-006-0231-0 (2007). PubMed DOI
Mi H., Muruganujan A. & Thomas P. D. PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic acids research 41, D377–386, doi: 10.1093/nar/gks1118 (2013). PubMed DOI PMC
Thomas P. D. et al.. Applications for protein sequence-function evolution data: mRNA/protein expression analysis and coding SNP scoring tools. Nucleic acids research 34, W645–650 (2006). PubMed PMC
McConnell R. E. & Tyska M. J. Leveraging the membrane - cytoskeleton interface with myosin-1. Trends in cell biology 20, 418–426, doi: 10.1016/j.tcb.2010.04.004 (2010). PubMed DOI PMC
Baraldi E. et al.. Structure of the PH domain from Bruton’s tyrosine kinase in complex with inositol 1,3,4,5-tetrakisphosphate. Structure 7, 449–460 (1999). PubMed
Tall E. G., Spector I., Pentyala S. N., Bitter I. & Rebecchi M. J. Dynamics of phosphatidylinositol 4,5-bisphosphate in actin-rich structures. Current biology: CB 10, 743–746 (2000). PubMed
Hoffmann E. K., Lambert I. H. & Pedersen S. F. Physiology of cell volume regulation in vertebrates. Physiological reviews 89, 193–277, doi: 10.1152/physrev.00037.2007 (2009). PubMed DOI
Iitaka D. et al.. Blockade of chloride ion transport enhances the cytocidal effect of hypotonic solution in gastric cancer cells. J Surg Res 176, 524–534, doi: 10.1016/j.jss.2011.10.039 (2012). PubMed DOI
Brandstaetter H., Kendrick-Jones J. & Buss F. Myo1c regulates lipid raft recycling to control cell spreading, migration and Salmonella invasion. Journal of cell science 125, 1991–2003, doi: 10.1242/jcs.097212 (2012). PubMed DOI PMC
Almuzzaini B., Sarshad A. A., Farrants A. K. & Percipalle P. Nuclear myosin 1 contributes to a chromatin landscape compatible with RNA polymerase II transcription activation. BMC biology 13, 35, doi: 10.1186/s12915-015-0147-z (2015). PubMed DOI PMC
Cross S. E., Jin Y. S., Rao J. & Gimzewski J. K. Nanomechanical analysis of cells from cancer patients. Nature nanotechnology 2, 780–783, doi: 10.1038/nnano.2007.388 (2007). PubMed DOI
Cross S. E. et al.. AFM-based analysis of human metastatic cancer cells. Nanotechnology 19, 384003, doi: 10.1088/0957-4484/19/38/384003 (2008). PubMed DOI
Faria E. C. et al.. Measurement of elastic properties of prostate cancer cells using AFM. The Analyst 133, 1498–1500, doi: 10.1039/b803355b (2008). PubMed DOI
Guck J. et al.. Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophysical journal 88, 3689–3698, doi: 10.1529/biophysj.104.045476 (2005). PubMed DOI PMC
Lekka M. et al.. Cancer cell detection in tissue sections using AFM. Archives of biochemistry and biophysics 518, 151–156, doi: 10.1016/j.abb.2011.12.013 (2012). PubMed DOI
Li Q. S., Lee G. Y., Ong C. N. & Lim C. T. AFM indentation study of breast cancer cells. Biochemical and biophysical research communications 374, 609–613, doi: 10.1016/j.bbrc.2008.07.078 (2008). PubMed DOI
Remmerbach T. W. et al.. Oral cancer diagnosis by mechanical phenotyping. Cancer research 69, 1728–1732, doi: 10.1158/0008-5472.CAN-08-4073 (2009). PubMed DOI
Lekka M. et al.. Cancer cell recognition–mechanical phenotype. Micron 43, 1259–1266, doi: 10.1016/j.micron.2012.01.019 (2012). PubMed DOI
Darling E. M., Zauscher S., Block J. A. & Guilak F. A thin-layer model for viscoelastic, stress-relaxation testing of cells using atomic force microscopy: do cell properties reflect metastatic potential? Biophysical journal 92, 1784–1791, doi: 10.1529/biophysj.106.083097 (2007). PubMed DOI PMC
Park S., Koch D., Cardenas R., Kas J. & Shih C. K. Cell motility and local viscoelasticity of fibroblasts. Biophysical journal 89, 4330–4342, doi: 10.1529/biophysj.104.053462 (2005). PubMed DOI PMC
Trinkle-Mulcahy L. et al.. Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. The Journal of cell biology 183, 223–239, doi: 10.1083/jcb.200805092 (2008). PubMed DOI PMC
Sasseville A. M. & Raymond Y. Lamin A precursor is localized to intranuclear foci. Journal of cell science 108(Pt 1), 273–285 (1995). PubMed
Bolte S. & Cordelieres F. P. A guided tour into subcellular colocalization analysis in light microscopy. Journal of microscopy 224, 213–232, doi: 10.1111/j.1365-2818.2006.01706.x (2006). PubMed DOI