Abstract
This short review traces how our knowledge of the molecular mechanisms of cellular movements originated and developed over the past 50 years. Work on actin-based and microtubule-based movements developed in different ways, but in both fields, the discovery of the key proteins drove progress. Starting from an inventory of zero molecules in 1960, both fields matured spectacularly, so we now know the atomic structures of the important proteins, understand the kinetics and thermodynamics of their interactions, have documented how the molecules behave in cells, and can test theories with molecularly explicit computer simulations of cellular processes.
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References
Adelman MR, Taylor EW (1969a) Further purification and characterization of slime mold myosin and slime mold actin. Biochemistry 8:4976–4988
Adelman MR, Taylor EW (1969b) Isolation of an actomyosin-like protein complex from slime mold plasmodium and the separation of the complex into actin- and myosin-like fractions. Biochemistry 8(12):4964–4975
Adelstein RS, Pollard TD, Kuehl WM (1971) Isolation and characterization of myosin and two myosin fragments from human blood platelets. Proc Natl Acad Sci U S A 68(11):2703–2707
Akhmanova A, Steinmetz MO (2015) Control of microtubule organization and dynamics: two ends in the limelight. Nat Rev Mol Cell Biol 16:711–726
Allen RD, Kamiya N (1964) Primitive motile systems in cell biology. Academic Press, New York, pp 1–642
Allen RD, Weiss DG, Hayden JH, Brown DT, Fujiwake H, Simpson M (1985) Gliding movement of and bidirectional transport along single native microtubules from squid axoplasm: evidence for an active role of microtubules in cytoplasmic transport. J Cell Biol 100(5):1736–1752
Bamburg JR, Harris HE, Weeds AG (1980) Partial purification and characterization of an actin depolymerizing factor from brain. FEBS Lett 121(1):178–182
Barlan K, Gelfand VI (2017) Microtubule-based transport and the distribution, tethering, and organization of organelles. Cold Spring Harb Perspect Biol 9(5). https://doi.org/10.1101/cshperspect.a025817
Basant A, Glotzer M (2018) Spatiotemporal regulation of RhoA during cytokinesis. Curr Biol 28:R570–R580
Bates M, Huang B, Dempsey GT, Zhuang X (2007) Multicolor superresolution imaging with photo-switchable fluorescent probes. Science 317:1749–1753
Belmont LD, Mitchison TJ (1996) Identification of a protein that interacts with tubulin dimers and increases the catastrophe rate of microtubules. Cell 84:623–631
Bettex-Galland M, Luscher EF (1959) Extraction of an actomyosin-like protein from human platelets. Nature 184:276–277
Borisy GG, Taylor EW (1967) The mechanism of action of colchicine: binding of colchicine-3H to cellular protein. J Cell Biol 34:525–534
Bray D, Bourret RB, Simon MI (1993) Computer simulation of the phosphorylation cascade controlling bacterial chemotaxis. Mol Biol Cell 4:469–482
Bretscher A, Weber K (1980) Fimbrin, a new microfilament-associated protein present in microvilli and other cell surface structures. J Cell Biol 86:335–340
Burns RG, Pollard TD (1974) A dynein-like protein from brain. FEBS Lett 40:274–280
Carlsson L, Nyström LE, Sundkvist I, Markey F, Lindberg U (1977) Actin polymerizability is influenced by profilin, a low molecular weight protein in non-muscle cells. J Mol Biol 115:465–483
Castrillon D, Wasserman S (1994) Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120:3367–3377
Cleveland D, Hwo S, Kirschner M (1977) Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J Mol Biol 116:207–225
Cleveland DW, Kirschner MW, Cowan NJ (1978) Isolation of separate mRNAs for alpha- and beta-tubulin and characterization of the corresponding in vitro translation products. Cell 15:1021–1031
CSHSQB (1972) “The mechanism of muscle contraction.” Cold Spring Harbor Symp. Quant. Biol, vol 37. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
DeLozanne A, Spudich JA (1987) Disruption of the Dictyostelium myosin heavy chain gene by homologous recombination. Science 236:1086–1091
Ding DQ, Chikashige Y, Haraguchi T, Hiraoka Y (1998) Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules, as revealed by continuous observation of chromosomes and microtubules in living cells. J Cell Sci 111:701–712
Euteneuer U, McIntosh JR (1981) Structural polarity of kinetochore microtubules in PTK1-cells. J Cell Biol 89:338–345
Finlayson B, Lymn RW, Taylor EW (1969) Studies on the kinetics of formation and dissociation of the actomyosin complex. Biochemistry 8(March 1969):811–819
Fujii T, Iwane AH, Yanagida T, Namba K (2010) Direct visualization of secondary structures of F-actin by electron cryomicroscopy. Nature 467:724–728
Fujiwara K, Pollard TD (1976) Fluorescent antibody localization of myosin in the cytoplasm, cleavage furrow, and mitotic spindle of human cells. J Cell Biol 71(3):848–875
Gibbons IR, Rowe AJ (1965) Dynein: a protein with adenosine triphosphatase activity from cilia. Science 149:424–426
Goldman R, Pollard TD, Rosenbaum J (1976) Cell motility. Cold Spring Harb Press, Cold Spring Harbor
Goodson HV, Spudich JA (1993) Molecular evolution of the myosin family: relationships derived from comparisons of amino acid sequences. Proc Natl Acad Sci U S A 90:659–663
Guertin DA, Trautmann S, McCollum D (2002) Cytokinesis in eukaryotes. Microbiol Mol Biol Rev 66(2):155–178
Hartwig JH, Stossel TP (1975) Isolation and properties of actin, myosin and a new actin-binding protein in rabbit alveolar macrophages. J Biol Chem 250:5695–5705
Hatano S, Oosawa F (1966) Isolation and characterization of plasmodium actin. Biochim Biophys Acta 127:488–498
Hatano S, Tazawa M (1968) Isolation, purification and characterization of myosin B from myxomycete plasmodium. Biochim Biophys Acta 154:507–519
Hayashi I, Ikura M (2003) Crystal structure of the amino-terminal microtubule-binding domain of end-binding protein 1 (EB1). J Biol Chem 278:36430–36434
Howard J, Hyman AA (2007) Microtubule polymerases and depolymerases. Curr Opin Cell Biol 19:31–35
Hoyt MA, He L, Loo KK, Saunders WS (1992) Two Saccharomyces cerevisiae kinesin-related gene products required for mitotic spindle assembly. J Cell Biol 118:109–120
Huxley HE (1969) Mechanism of muscular contraction. Science 164:1356–1366
Huxley AF, Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233:533–538
Inoué S (1981) Video image processing greatly enhances contrast, quality, and speed in polarization-based microscopy. J Cell Biol 89:346–356
Inoué S, Sato H (1967) Cell motility by labile association of molecules. The nature of mitotic spindle fibers and their role in chromosome movement. J Gen Physiol 50(Suppl):259–292
Isenberg GH, Aebi U, Pollard TD (1980) An actin binding protein from Acanthamoeba regulates actin filament polymerization and interactions. Nature 288(5790):455–459
Ishikawa H, Bischoff R, Holtzer H (1969) Formation of arrowhead complexes with heavy meromyosin in a variety of cell types. J Cell Biol 43:312–328
Koenig M, Kunkel LM (1990) Detailed analysis of the repeat domain of dystrophin reveals four potential hinge segments that may confer flexibility. J Biol Chem 265(8):4560–4566
Kouyama T, Mihashi K (1981) Fluorimetry study of N-(1-pyrenyl)iodoacetamide-labelled F-actin. Local structural change of actin protomer both on polymerization and on binding of heavy meromyosin. Eur J Biochem 114(1):33–38
Kull FJ, Sablin EP, Lau R, Fletterick RJ, Vale RD (1996) Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature 380:550–555
Lazarides E, Burridge K (1975) Alpha-actinin: immunofluorescent localization of a muscle structural protein in nonmuscle cells. Cell 6:289–298
Lazarides E, Weber K (1974) Actin antibody: the specific visualization of actin filaments in non-muscle cells. Proc Natl Acad Sci U S A 71:2268–2272
Lowey AG (1952) An actomyosin-like substance from the plasmodium of a myxomycete. J Cell Comp Physiol 40:127–156
Lymm RW, Taylor EW (1971) Mechanism of adenosine triphosphate hydrolysis by acto-myosin. Biochemist 10:4617–4624
Mabuchi I, Okuno M (1977) The effect of myosin antibody on the division of starfish blastomeres. J Cell Biol 74(1):251–263
Machesky LM, Atkinson SJ, Ampe C, Vandekerckhove J, Pollard TD (1994) Purification of a cortical complex containing two unconventional actins from Acanthamoeba by affinity chromatography on profilin agarose. J Cell Biol 127(1):107–115
Marchesi VT, Steers E Jr (1968) Selective solubilization of a protein component of the red cell membrane. Science 159(811):203–204
McIntosh JR (2016) Mitosis. Cold Spring Harb Perspect Biol 8(9). https://doi.org/10.1101/cshperspect.a023218
McNally FJ, Vale RD (1993) Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75:419–429
Mitchison T, Kirschner M (1984) Dynamic instability of microtubule growth. Nature 312:237–242
Moore PB, Huxley HE, DeRosier DJ (1970) Three-dimensional reconstruction of F-actin, thin filaments and decorated thin filaments. J Mol Biol 50:279–295
Mullins RD, Heuser JA, Pollard TD (1998) The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc Natl Acad Sci U S A 95(11):6181–6186
Nishida E, Maekawa S, Muneyuki E, Sakai H (1984) Action of a 19K protein from porcine brain on actin polymerization - a new functional class of actin-binding proteins. J Biochem 95:387–398
Ochs S (1972) Fast axoplasmic transport of materials in mammalian nerve and its integrative role. Ann N Y Acad Sci 193:43–58
Otto JJ, Kane RE, Bryan J (1979) Formation of filopodia in coelomocytes: localization of fascin, a 58,000 Dalton actin cross-linking protein. Cell 17:285–293
Paschal BM, Vallee RB (1987) Retrograde transport by the microtubule-associated protein MAP 1C. Nature 330(6144):181–183
Paul A, Pollard TD (2009) Review of the mechanism of processive actin filament elongation by formins. Cell Motil Cytoskel 66:606–617
Pollard TD (2003) Functional genomics of cell morphology using RNA interference: pick your style, broad or deep. J Biol 2(4):25
Pollard TD (2013) No question about exciting questions in cell biology. PLoS Biol 11:e1001734
Pollard TD (2017) Nine unanswered questions about cytokinesis. J Cell Biol 216:3007–3016
Pollard TD, Ito S (1970) Cytoplasmic filaments of Amoeba proteus. I. The role of filaments in consistency changes and movement. J Cell Biol 46(2):267–289
Pollard TD, Korn ED (1973) Acanthamoeba myosin. I. Isolation from Acanthamoeba castellanii of an enzyme similar to muscle myosin. J Biol Chem 248(13):4682–4690
Pollard TD, Wu J-Q (2010) Understanding cytokinesis: lessons from fission yeast. Nat Rev Mol Cell Biol 11:149–155
Pomerat CM, Rounds DE, Raiborn CW, Pollard TD (1964) Observations on newborn rat dorsal root ganglia in vitro following gamma irradiation. In: Haley, Snider (eds) Response of the Nervous System to Ionizing Radiation. Little, Brown and Company, Boston, p 175
Pruyne D, Evangelista M, Yang C, Bi E, Zigmond S, Bretscher A, Boone C (2002) Role of formins in actin assembly: nucleation and barbed-end association. Science 297(5581):612–615
Safer D, Elzinga M, Nachmias VT (1991) Thymosin beta 4 and Fx, an actin-sequestering peptide, are indistinguishable. J Biol Chem 266(7):4029–4032
Sagot I, Rodal AA, Moseley J, Goode BL, Pellman D (2002) An actin nucleation mechanism mediated by Bni1 and profilin. Nat Cell Biol 4(8):626–631
Saunders WS, Hoyt MA (1992) Kinesin-related proteins required for structural integrity of the mitotic spindle. Cell 70:451–458
Schroeder TE (1973) Actin in dividing cells: contractile ring filaments bind heavy meromyosin. Proc Natl Acad Sci U S A 70(6):1688–1692
Stachowiak MR, Laplante C, Chin HF, Guirao B, Karatekin E, Pollard TD, O’Shaughnessy B (2014) Mechanism of cytokinetic contractile ring constriction in fission yeast. Dev Cell 29:547–561
Szent-Gyorgyi A (1945) Studies on muscle. Acta Physiol Scand 9(Suppl. 25):1–115
Thompson CM, Wolpert L (1963) The isolation of motile cytoplasm from Amoeba proteus. Exp Cell Res 32:156–160
Vale RD, Reese TS, Sheetz MP (1985) Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42(1):39–50
Vavylonis D, Wu J-Q, Hao S, O’Shaughnessy B, Pollard TD (2008) Assembly mechanism of the contractile ring for cytokinesis by fission yeast. Science 319:97–100
Walker RA, O’Brien ET, Pryer NK, Soboeiro MF, Voter WA, Erickson HP, Salmon ED (1988) Dynamic instability of individual microtubules analyzed by video light microscopy: rate constants and transition frequencies. J Cell Biol 107(4):1437–1448
Wang YL, Lanni F, McNeil PL, Ware BR, Taylor DL (1982) Mobility of cytoplasmic and membrane-associated actin in living cells. Proc Natl Acad Sci U S A 79:4660–4664
Weisenberg R, Borisy GG, Taylor EW (1968) The colchicine-binding protein of mammalian brain and its relation to microtubules. Biochemistry 7:4466–4479
Weiss P (1967) Neuronal dynamics and axonal flow. 3. Cellulifugal transport of labeled neuroplasm in isolated nerve preparations. Proc Natl Acad Sci U S A 57:1239–1245
White JG, Amos WB, Fordham M (1987) An evaluation of confocal versus conventional imaging of biological structures by fluorescence light microscopy. J Cell Biol 105:41–48
Wu JQ, Pollard TD (2005) Counting cytokinesis proteins globally and locally in fission yeast. Science 310(5746):310–314
Yin HL, Stossel TP (1979) Control of cytoplasmic actin gel-sol transformation by gelsolin, a calcium-dependent regulatory protein. Nature 281(5732):583–586
Zheng Y, Wong ML, Alberts B, Mitchison T (1995) Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature 378:578–583
Acknowledgements
The author thanks Laurent Blanchoin, Enrique De La Cruz, and Mike Ostap for organizing this volume.
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Research in the author’s laboratory has been supported by the National Institute of General Medical Sciences of the National Institutes of Health under award numbers R01GM026132 and R01GM026338. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
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Thomas D. Pollard declares that he has no conflict of interest.
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This article does not contain any studies with human participants or animals performed by the author.