Microtubule-associated Protein 2c Reorganizes Both Microtubules and Microfilaments into Distinct Cytological Structures in an Actin-binding Protein-280–deficient Melanoma Cell Line
Open accessAbstract
The emergence of processes from cells often involves interactions between microtubules and microfilaments. Interactions between these two cytoskeletal systems are particularly apparent in neuronal growth cones. The juvenile isoform of the neuronal microtubule-associated protein 2 (MAP2c) is present in growth cones, where we hypothesize it mediates interactions between microfilaments and microtubules. To approach this problem in vivo, we used the human melanoma cell, M2, which lacks actin-binding protein-280 (ABP-280) and forms membrane blebs, which are not seen in wild-type or ABP-transfected cells. The microinjection of tau or mature MAP2 rescued the blebbing phenotype; MAP2c not only caused cessation of blebbing but also induced the formation of two distinct cellular structures. These were actin-rich lamellae, which often included membrane ruffles, and microtubule-bearing processes. The lamellae collapsed after treatment with cytochalasin D, and the processes retracted after treatment with colchicine. MAP2c was immunocytochemically visualized in zones of the cell that were devoid of tubulin, such as regions within the lamellae and in association with membrane ruffles. In vitro rheometry confirmed that MAP2c is an efficient actin gelation protein capable of organizing actin filaments into an isotropic array at very low concentrations; tau and mature MAP2 do not share this rheologic property. These results suggest that MAP2c engages in functionally specific interactions not only with microtubules but also with microfilaments.
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MAPs bundle actin filaments and cross-link the cellular cytoskeleton formed by microtubules and actin filaments.
“In addition, MAPs bundle actin filaments and cross-link the cellular cytoskeleton formed by microtubules and actin filaments (Fig. 1a)3–10.”
From Multivalent cross-linking of actin filaments and microtubules through the microtubule-associated protein Tau (2017) · cites this paper as [10]
The Results section (‘MAP2c Causes Actin Gelation In Vitro’; page unavailable) reports that MAP2c forms actin bundles at higher concentrations or lower ionic strength. But the Discussion (‘In Vivo Functions of MAP2c’; page unavailable) explicitly says the data cannot determine whether MAP2c cross-links microtubules to actin filaments. The claim presents that cross-linking as established for MAPs generally. (LLM, conf=0.90)
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Ferreira, A., Kincaid, R., & Kosik, K. S. (1993) · Molecular Biology of the Cell · doi:10.1091/mbc.4.12.1225 · Cited by 110 · see citing works
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Research works printed but not linked: 63
- Asai DJ Thompson WC Wilson L Dresden CF Schulman H Purich DL Microtubule-associated proteins (MAPs): a monoclonal antibody to MAP 1 decorates microtubules in vitro but stains stress fibers and not microtubules in vivo. Proc Natl Acad Sci USA 1985 82 1434 1438 3883359 PMC397276
- Baas PW Pienkowski TP Kosik KS Processes induced by tau expression in Sf9 cells have an axon-like microtubule organization J Cell Biol 1991 115 1333 1344 1955477 PMC2289232
- Baorto DM Mellado W Shelanski ML Astrocyte process growth induction by actin breakdown J Cell Biol 1992 117 357 367 1313815 PMC2289411
- Binder LI Frankfurter A Rebhun LI Differential localization of MAP2 and tau in mammalian neurons in situ Proc Natl Acad Sci USA 1986 81 145 166 3089105
- Birgbauer E Dinsmore JH Winckler B Lander AD Solomon F Association of ezrin isoforms with the neuronal cytoskeleton J Neurosci Res 1991 30 232 241 1795406
- Brotschi EA Hartwig JH Stossel TP The gelation of actin by actin-binding protein J Biol Chem 1978 253 8988 8993 721823
- Caceres A Kosik KS Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons Nature (Lond) 1990 343 461 463 2105469
- Caceres A Potrebic S Kosik KS The effect of tau antisense oligonucleotides on neurite formation of cultured cerebellar macroneurons J Neurosci 1991 11 1515 1523 1904479 PMC6575418
- Caceres A Mautino J Kosik KS Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation Neuron 1992 9 607 618 1389180
- Chen J Kanai Y Cowan NJ Hirokawa N Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons Nature (Lond) 1992 360 674 677 1465130
- Cooper JA Bryan J Schwab BD Frieden C Loftus DJ Elson EL Microinjection of gelsolin into living cells J Cell Biol 1987 104 491 501 3029140 PMC2114549
- Correas I Padilla R Avila J The tubulin-binding sequence of brain microtubule-associated proteins, tau and MAP-2, is also involved in actin binding Biochem J 1990 269 61 64 2115775 PMC1131531
- Cross D Vial C Maccioni RB A tau-like protein interacts with stress fibers and microtubules in human and rodent cultured cell lines J Cell Sci 1993 105 51 60 7689576
- Cunningham C Actin polymerization and intracellular solvent flow in cell surface blebbing J Cell Biol 1995 129 1589 1599 7790356 PMC2291187
- Cunningham CC Gorlin JB Kwiatkowski DJ Hartwig JH Janmey PJ Byers HR Stossel TP Actin-binding protein requirement for cortical stability and efficient locomotion Science (Wash DC) 1992 255 325 327 1549777
- Dentler WL Adams C Flagellar microtubule dynamics in Chlamydomonas: cytochalasin D induces periods of microtubule shortening and elongation; and colchicine induces disassembly of the distal, but not proximal, half of the flagellum J Cell Biol 1992 117 1289 1298 1607390 PMC2289510
- Drechsel DN Hyman AA Cobb MH Kirschner MW Modulation of the dynamic instability of tubulin assembly by the microtubule-associated tau Mol Biol Cell 1992 3 1141 1154 1421571 PMC275678
- Edson K Weisshaar B Matus A Actin depolymerisation induces process formation on MAP2-transfected non-neuronal cells Development (Camb) 1993 117 689 700 8392463
- Flory, P.J. 1953. Principles of Polymer Chemistry. Cornell University Press, Ithaca, NY. 672. pp.
- Forscher P Smith SJ Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone J Cell Biol 1988 107 1505 1516 3170637 PMC2115246
- Fung MC Chiu KY Weber T Chang TW Chang NT Detection and purification of a recombinant human B lymphotropic virus (HHV-6) in the baculovirus expression system by limiting dilution and DNA dot-blot hybridization J Virol Methods 1988 19 33 42 3280584
- Garner CC Matus A Different forms of microtubule-associated protein 2 are encoded by separate mRNA transcripts J Cell Biol 1988 106 779 783 3346325 PMC2115073
- Griffith LM Pollard TD Evidence for actin filament-microtubule interaction mediated by microtubule-associated proteins J Cell Biol 1978 78 958 965 568144 PMC2110189
- Griffith LM Pollard TD The interaction of actin filaments with microtubules and microtubule-associated proteins J Biol Chem 1982 257 9143 9151 6124545
- Hartwig JH Shevlin P The architecture of actin filaments and the ultrastructural location of actin-binding protein in the periphery of lung macrophages J Cell Biol 1986 103 1007 1020 3745263 PMC2114287
- Hartwig J Thelen M Rosen A Janmey P Nairn A Aderem A The MARCKS protein is an actin filament crosslinking protein regulated by protein kinase C-mediated phosphorylation and by calcium/calmodulin Nature (Lond) 1992 356 618 622 1560845
- Janmey PA A torsion pendulum for measurement of the viscoelasticity of biopolymers and its application to actin networks J Biochem Biophys Methods 1991 22 41 53 2005359
- Janmey PA Hvidt S Peetermans J Lamb J Ferry JD Stossel TP Viscoelasticity of F-actin and F-actin/gelsolin complexes Biochemistry 1988 27 8218 8227 2852957
- Janmey PA Hvidt S Lamb J Stossel TP Resemblance of actinbinding protein/actin gels to covalently crosslinked networks Nature (Lond) 1990 345 89 92 2158633
- Kindler S Schulz B Goedert M Garner CC Molecular structure of microtubule-associated protein 2b and 2c from rat brain J Biol Chem 1990 265 19679 19684 2174050
- Kitts PA Ayres MD Possee RD Linearization of baculovirus DNA enhances the recovery of recombinant virus expression vectors Nucl Acids Res 1990 18 5667 5672 2216760 PMC332298
- Knops J Kosik KS Lee G Pardee JD Cohen GL McConlogue L Overexpression of tau in a nonneuronal cell induces long cellular processes J Cell Biol 1991 114 725 733 1678391 PMC2289897
- Knowles R Leclerc N Kosik KS Organization of actin and microtubules during process formation in tau-expressing Sf9 cells Cell Motil Cytoskel 1994 28 256 264 7954853
- Kosik KS Orecchio LD Binder L Trojanowski JQ Lee VM-Y Lee G Epitopes that span the tau molecule are shared with paired helical filaments Neuron 1988 1 817 825 2483104
- Kotani S Nishida E Kumagai H Sakai H Calmodulin inhibits interaction of actin with MAP2 and tau, two major microtubule-associated proteins J Biol Chem 1985 260 10779 10783 4030771
- Leclerc N Baas PW Garner CC Kosik KS Juvenile and mature MAP2 isoforms induce distinct patterns of process outgrowth Mol Biol Cell 1996 7 443 455 8868472 PMC275896
- Lin C-H Forscher P Cytoskeletal remodeling during growth conetarget interactions J Cell Biol 1993 121 1369 1383 8509456 PMC2119712
- Lo SH Janmey PA Hartwig JH Chen LB Interactions of tensin with actin and identification of its three distinct actin-binding domains J Cell Biol 1994 125 1067 1075 8195290 PMC2120063
- McLaughlin PJ Weeds AG Actin-binding protein complexes at atomic resolution Annu Rev Biophys Biomol Struct 1995 24 643 675 7663130
- Moraga DM Nunez P Garrido J Maccioni RB A tau fragment containing a repetitive sequence induces bundling of actin filaments J Neurochem 1993 61 979 986 8360695
- Morishima M Kosik KS The pool of MAP kinase associated with microtubules is small but constitutively active Mol Biol Cell 1996 7 893 905 8816996 PMC275941
- Nathke IS Adams CL Polakis P Selin JH Nelson WJ The adenomatous polyposis coli tumor suppressor protein localizes to plasma membrane sites involved in active cell migration J Cell Biol 1996 134 165 179 8698812 PMC2120913
- Nishida E Kuwaki T Sakai H Phosphorylation of microtubule- associated proteins (MAPs) and pH of the medium control interaction between MAPs and actin filaments J Biochem (Tokyo) 1981 90 575 578 7298606
- Panda D Daijo JE Jordan MA Wilson L Kinetic stabilization of microtubule dynamics at steady state in vitroby substoichiometric concentrations of tubulin-colchicine complex Biochemistry 1995 34 9921 9929 7632691
- Papandrikopoulou A Doll T Tucker RP Garner CC Matus A Embryonic MAP2 lacks the cross-linking sidearm sequences and dendritic targeting signal of adult MAP2 Nature (Lond) 1989 340 650 652 2770869
- Pollard TD A falling ball apparatus to measure filament cross-linking Methods Cell Biol 1982 24 301 311 7048020
- Pollard TD Selden SC Maupin P Interaction of actin filaments with microtubules J Cell Biol 1984 99 33s 37s 6430911 PMC2275605
- Rochlin MW Wickline KM Bridgman PC Microtubule stability decreases axon elongation but not axoplasm production J Neurosci 1996 16 3236 3246 8627361 PMC6579152
- Sanchez I Cohen WD Assembly and bundling of marginal band microtubule protein: role of tau Cell Motil Cytoskel 1994 29 57 71 7820858
- Satillaro RF Interaction of microtubule-associated protein 2 with actin filaments Biochemistry 1986 25 2003 2009 3707926
- Satillaro RF Dentler WL LeCluyse EL Microtubule-associated proteins (MAPs) and the organization of actin filaments in vitro J Cell Biol 1981 90 467 473 6270155 PMC2111865
- Selden SC Pollard TD Interaction of actin filaments with microtubules is mediated by microtubule-associated proteins and regulated by phosphorylation Ann NY Acad Sci 1986 466 803 812 3460455
- Stossel TP On the crawling of animal cells Science (Wash DC) 1993 260 1086 1094 8493552
- Tanaka E Sabry J Making the connection: cytoskeletal rearrangements during growth cone guidance Cell 1995 83 171 176 7585934
- Tanaka E Ho T Kirschner MW The role of microtubule dynamics in growth cone mobility and axonal growth J Cell Biol 1995 128 139 155 7822411 PMC2120332
- Toso RJ Jordan MA Farrell KW Matsumoto B Wilson L Kinetic stabilization of microtubule dynamic instability in vitroby vinblastine Biochemistry 1993 32 1285 1293 8448138
- Umeyama T Okabe S Kanai Y Hirokawa N Dynamics of microtubules bundled by microtubule-associated protein 2C (MAP2C) J Cell Biol 1993 120 451 465 8421058 PMC2119507
- Waterman-Storer CM Karki S Holzbaur EL The p150Glued component of the dynactin complex binds to both microtubules and the actin-related protein centractin (Arp-1) Proc Natl Acad Sci USA 1995 92 1634 1638 7878030 PMC42574
- Watts RG Howard TH Role of tropomyosin, α-actinin, and actin binding protein 280 in stabilizing Triton insoluble F-actin in basal and chemotactic factor activated neutrophils Cell Motil Cytoskel 1994 28 155 164 8087874
- Way M Pope B Weeds AG Evidence for functional homology in the F-actin binding domains of gelsolin and α-actinin: implications for the requirements of severing and capping J Cell Biol 1992 119 835 842 1331120 PMC2289707
- Wille H Mandelkow E-M Dingus J Vallee RB Binder LI Mandelkow E Domain structure and antiparallel dimers of microtubule- associated protein 2 (MAP2) J Struct Biol 1992a 108 49 61 1373291
- Wille H Mandelkow E-M Mandelkow E The juvenile microtubule-associated protein MAP2c is a rod-like molecule that forms antiparallel dimers J Biol Chem 1992b 267 10737 10742 1375231
- Winkler B Solomon F A role for microtubule bundles in the morphogenesis of chicken erythrocytes Proc Natl Acad Sci USA 1991 88 6033 6037 1676841 PMC52016
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Tracy, T. E., Sohn, P. D., Minami, S. S., Wang, C., Min, S.-W., Li, Y., Zhou, Y., Le, D., Lo, I., Ponnusamy, R., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.005 · Cited by 277 · see citing works
Cabrales Fontela, Y., Kadavath, H., Biernat, J., Riedel, D., Mandelkow, E., & Zweckstetter, M. (2017) · Nature Communications · doi:10.1038/s41467-017-02230-8 · Cited by 148 · see citing works
- Authors
- Cunningham, C. C., Leclerc, N., Flanagan, L. A., Lu, M., Janmey, P. A., & Kosik, K. S.
- Affiliations
- Brigham and Women's Hospital (US)
- *Department of Medicine, Division of Experimental Medicine, ‡Department of Neurology, Center for Neurologic Diseases, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts 02115
- Corresponding author
- Leclerc, Nicole
- Venue
- The Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 1997-02-24
- Volume
- 136
- Issue
- 4
- Pages
- 845-857
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC2132495
- OpenAlex
- W2023263503
- Cited by
- 88
- References
- 1
- Citations by year
- 2024: 1 · 2023: 1 · 2022: 3 · 2021: 1 · 2020: 2 · 2019: 3 · 2018: 2 · 2017: 4 · 2016: 3 · 2015: 1 · 2014: 2 · 2012: 4
- FWCI
- 2.92
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (1r55ca057479-01)
- National Heart, Lung, and Blood Institute (HL-48743, P01HL048743)
- National Cancer Institute (CA57479)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-38452, P01DK038452)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR038910)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Keywords
- MAP2c, membrane blebs, ruffles, tau protein, cytoskeletal rearrangement, cellular processes, rheology
- MeSH terms
- Actins, Carrier Proteins, Humans, Melanoma, Microfilament Proteins, Actin Cytoskeleton, Microinjections, Microtubule-Associated Proteins, Microtubules, Tumor Cells, Cultured, tau Proteins, Cell Size
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