A mechanical function of myosin II in cell motility

P.Y. Jay; P.A. Pham; S.A. Wong; E.L. Elson

Summary

Myosin II mutant Dictyostelium amoebae crawl more slowly than wild-type cells. Thus, myosin II must contribute to amoeboid locomotion. We propose that contractile forces generated by myosin II help the cell's rear edge to detach from the substratum and retract, allowing the cell to continue forward. To test this hypothesis, we measured the speed of wild-type and myosin II null mutant Dictyostelium cells on surfaces of varying adhesivity. As substratum adhesivity increased, the speed of myosin II null mutant cells decreased substantially compared to wild-type cells, suggesting that the mutant is less able to retract from sticky surfaces. Furthermore, interference reflection microscopy revealed a myosin-II-dependent contraction in wild-type but not null mutant cells that is consistent with a balance of adhesive and contractile forces in retraction. Although myosin II null mutant cells have a defect in retraction, pseudopod extension does not cause the cells to become elongated on sticky surfaces. This suggests a mechanism, based possibly on cytoskeletal tension, for regulating cell shape in locomotion. The tension would result from the transmission of tractional forces through the cytoskeletal network, providing the myosin II null mutant with a limited means of retraction and cell division on a surface.

REFERENCES

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OpenUrl Abstract/FREE Full Text
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(1988). Cortical flow in animal cells. Science 239, 883–888
OpenUrl Abstract/FREE Full Text
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(1979). Induction of spreading during fibroblast movement. J. Cell Biol 81, 684–691
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(1981). Mechanism of retraction of the trailing edge during fibroblast movement. J. Cell Biol 90, 187–200
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3. Lauffenburger D. A.
(1991). Mathematical model for the effects of adhesion and mechanics on cell migration speed. Biophys. J 60, 15–37
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5. Lauffenburger D. A.
(1993). Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J. Cell Biol 122, 729–737
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1. Duband J.-L.,
2. Dufour S.,
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4. Yamada K. M. and
5. Thiery J. P.
(1991). Neural crest cell locomotion induced by antibodies to β1integrins: a tool for studying the roles of substratum molecular avidity and density in migration. J. Cell Sci 98, 517–532
OpenUrl Abstract/FREE Full Text
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2. De Lozanne A. and
3. Spudich J. A.
(1990). Structure and function of the cytoskeleton of a Dictyostelium myosin-defective mutant. J. Cell Biol 110, 367–378
OpenUrl Abstract/FREE Full Text
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2. Todd I. and
3. Owens N.
(1982). Interaction between intracellular vacuoles and the cell surface analysed by finite aperture theory interference reflection microscopy. J. Cell Sci 54, 287–298
OpenUrl Abstract/FREE Full Text
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2. Vince S.
(1982). Substratum wettability and charge influence the spreading of Dictyostelium amoebae and the formation of ultrathin cytoplasmic lamellae. J. Cell Sci 54, 255–285
OpenUrl Abstract
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2. Risse G. and
3. von der Mark K.
(1989). The E8 subfragmentof laminin promotes locomotion of myoblasts over extracellular matrix. J. Cell Biol 109, 799–809
OpenUrl Abstract/FREE Full Text
1. Hendey B.,
2. Klee C. B. and
3. Maxfield F. R.
(1992). Inhibition of neutrophil chemokinesis on vitronectin by inhibitors of calcineurin. Science 258, 296–299
OpenUrl Abstract/FREE Full Text
1. Heuser J.,
2. Zhu Q. and
3. Clarke M.
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OpenUrl Abstract/FREE Full Text
1. Jay P. Y. and
2. Elson E. L.
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OpenUrl CrossRef PubMed Web of Science
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OpenUrl Abstract/FREE Full Text
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2. Kuo S. C.,
3. Elson E. L. and
4. Sheetz M. P.
(1991). Preferential attachment of membrane glycoproteins to the cytoskeleton at the leading edge of lamella. J. Cell Biol 114, 1029–1036
OpenUrl Abstract/FREE Full Text
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2. Lauffenburger D. A.
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2. Titus M. A.,
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OpenUrl Abstract/FREE Full Text
1. Pasternak C.,
2. Spudich J. A. and
3. Elson E. L.
(1989). Capping of surface receptors and concomitant cortical tension are generated by conventional myosin. Nature 341, 549–551
OpenUrl CrossRef PubMed
1. Pasternak C. and
2. Elson E. L.
(1990). Mapping regional mechanical properties of a cell during chemotaxis. J. Cell Biol 111, 7–.
OpenUrl
1. Sepsenwol S. and
2. Taft S. J.
(1990). In vitro induction of crawling in the amoeboid sperm of the nematode parasite, Ascaris suum. Cell Motil. Cytoskel 15, 99–110
OpenUrl CrossRef PubMed
1. Small J. V.
(1989). Microfilament-based motility in non-muscle cells. Curr. Opin. Cell Biol 1, 75–79
OpenUrl CrossRef PubMed
1. Spudich J. A.
(1989). In pursuit of myosin function. Cell Regul 1, 1–11
OpenUrl PubMed Web of Science
1. Todd I.,
2. Mellor J. S. and
3. Gingell D.
(1988). Mapping cell-glass contacts of Dictyostelium amoebae by total internal reflection aqueous fluorescence overcomes a basic ambiguity of interference reflection microscopy. J. Cell Sci 89, 107–114
OpenUrl Abstract/FREE Full Text
1. Tourtellot M. K.,
2. Collins R. D. and
3. Bell W. J.
(1991). The problem of movelength and turn definition in analysis of orientation data. J. Theor. Biol 150, 287–297
OpenUrl CrossRef PubMed Web of Science
1. Wessels D.,
2. Soll D. R.,
3. Knecht D.,
4. Loomis W. F.,
5. De Lozanne A. and
6. Spudich J.
(1988). Cell motility and chemotaxis in Dictyostelium amebae lacking myosin heavy chain. Dev. Biol 128, 164–177
OpenUrl CrossRef PubMed Web of Science
1. Yumura S.,
2. Mori H. and
3. Fukui Y.
(1984). Localization of actin and myosin for the study of ameboid movement in Dictyostelium using improved immunofluorescence. J. Cell Biol 99, 894–899
OpenUrl Abstract/FREE Full Text

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[1] Bell G. I.
(1978). Models for the specific adhesion of cells to cells. Science 200, 618–627
OpenUrl Abstract/FREE Full Text

[2] Bell G. I.

[3] Bray D. and
White J. G.
(1988). Cortical flow in animal cells. Science 239, 883–888
OpenUrl Abstract/FREE Full Text

[4] Bray D. and

[5] White J. G.

[6] Chen W.-T.
(1979). Induction of spreading during fibroblast movement. J. Cell Biol 81, 684–691
OpenUrl Abstract/FREE Full Text

[7] Chen W.-T.

[8] Chen W.-T.
(1981). Mechanism of retraction of the trailing edge during fibroblast movement. J. Cell Biol 90, 187–200
OpenUrl Abstract/FREE Full Text

[9] Chen W.-T.

[10] DiMilla P. A.,
Barbee K. and
Lauffenburger D. A.
(1991). Mathematical model for the effects of adhesion and mechanics on cell migration speed. Biophys. J 60, 15–37
OpenUrl PubMed Web of Science

[11] DiMilla P. A.,

[12] Barbee K. and

[13] Lauffenburger D. A.

[14] DiMilla P. A.,
Stone J. A.,
Quinn J. A.,
Albelda S. M. and
Lauffenburger D. A.
(1993). Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J. Cell Biol 122, 729–737
OpenUrl Abstract/FREE Full Text

[15] DiMilla P. A.,

[16] Stone J. A.,

[17] Quinn J. A.,

[18] Albelda S. M. and

[19] Lauffenburger D. A.

[20] Duband J.-L.,
Dufour S.,
Yamada S. S.,
Yamada K. M. and
Thiery J. P.
(1991). Neural crest cell locomotion induced by antibodies to β1integrins: a tool for studying the roles of substratum molecular avidity and density in migration. J. Cell Sci 98, 517–532
OpenUrl Abstract/FREE Full Text

[21] Duband J.-L.,

[22] Dufour S.,

[23] Yamada S. S.,

[24] Yamada K. M. and

[25] Thiery J. P.

[26] Fukui Y.,
De Lozanne A. and
Spudich J. A.
(1990). Structure and function of the cytoskeleton of a Dictyostelium myosin-defective mutant. J. Cell Biol 110, 367–378
OpenUrl Abstract/FREE Full Text

[27] Fukui Y.,

[28] De Lozanne A. and

[29] Spudich J. A.

[30] Gingell D.,
Todd I. and
Owens N.
(1982). Interaction between intracellular vacuoles and the cell surface analysed by finite aperture theory interference reflection microscopy. J. Cell Sci 54, 287–298
OpenUrl Abstract/FREE Full Text

[31] Gingell D.,

[32] Todd I. and

[33] Owens N.

[34] Gingell D. and
Vince S.
(1982). Substratum wettability and charge influence the spreading of Dictyostelium amoebae and the formation of ultrathin cytoplasmic lamellae. J. Cell Sci 54, 255–285
OpenUrl Abstract

[35] Gingell D. and

[36] Vince S.

[37] Goodman S. L.,
Risse G. and
von der Mark K.
(1989). The E8 subfragmentof laminin promotes locomotion of myoblasts over extracellular matrix. J. Cell Biol 109, 799–809
OpenUrl Abstract/FREE Full Text

[38] Goodman S. L.,

[39] Risse G. and

[40] von der Mark K.

[41] Hendey B.,
Klee C. B. and
Maxfield F. R.
(1992). Inhibition of neutrophil chemokinesis on vitronectin by inhibitors of calcineurin. Science 258, 296–299
OpenUrl Abstract/FREE Full Text

[42] Hendey B.,

[43] Klee C. B. and

[44] Maxfield F. R.

[45] Heuser J.,
Zhu Q. and
Clarke M.
(1993). Proton pumps populate the contractile vacuoles of Dictyostelium amoebae. J. Cell Biol 121, 1311–1327
OpenUrl Abstract/FREE Full Text

[46] Heuser J.,

[47] Zhu Q. and

[48] Clarke M.

[49] Jay P. Y. and
Elson E. L.
(1992). Surface particle transport mechanism independent of myosin II in Dictyostelium. Nature 356, 438–440
OpenUrl CrossRef PubMed Web of Science

[50] Jay P. Y. and

[51] Elson E. L.

[52] Kolega J.
(1986). Effects of mechanical tension on protrusive activity and microfilament and intermediate filament organization in an epidermal epithelium moving in culture. J. Cell Biol 102, 1400–1411
OpenUrl Abstract/FREE Full Text

[53] Kolega J.

[54] Kucik D. F.,
Kuo S. C.,
Elson E. L. and
Sheetz M. P.
(1991). Preferential attachment of membrane glycoproteins to the cytoskeleton at the leading edge of lamella. J. Cell Biol 114, 1029–1036
OpenUrl Abstract/FREE Full Text

[55] Kucik D. F.,

[56] Kuo S. C.,

[57] Elson E. L. and

[58] Sheetz M. P.

[59] Kuo S. C. and
Lauffenburger D. A.
(1993). Relationship between receptor/ligand binding affinity and adhesion strength. Biophys. J 65, 2191–2200
OpenUrl PubMed

[60] Kuo S. C. and

[61] Lauffenburger D. A.

[62] Manstein D. J.,
Titus M. A.,
De Lozanne A. and
Spudich J. A.
(1989). Gene replacement in Dictyostelium: generation of myosin null mutants. EMBO J 8, 923–932
OpenUrl PubMed Web of Science

[63] Manstein D. J.,

[64] Titus M. A.,

[65] De Lozanne A. and

[66] Spudich J. A.

[67] Nelson G. A.,
Roberts T. M. and
Ward S.
(1982). Caenorhabditis elegans spermatazoan locomotion: amoeboid movement with almost no actin. J. Cell Biol 92, 121–131
OpenUrl Abstract/FREE Full Text

[68] Nelson G. A.,

[69] Roberts T. M. and

[70] Ward S.

[71] Pasternak C.,
Spudich J. A. and
Elson E. L.
(1989). Capping of surface receptors and concomitant cortical tension are generated by conventional myosin. Nature 341, 549–551
OpenUrl CrossRef PubMed

[72] Pasternak C.,

[73] Spudich J. A. and

[74] Elson E. L.

[75] Pasternak C. and
Elson E. L.
(1990). Mapping regional mechanical properties of a cell during chemotaxis. J. Cell Biol 111, 7–.
OpenUrl

[76] Pasternak C. and

[77] Elson E. L.

[78] Sepsenwol S. and
Taft S. J.
(1990). In vitro induction of crawling in the amoeboid sperm of the nematode parasite, Ascaris suum. Cell Motil. Cytoskel 15, 99–110
OpenUrl CrossRef PubMed

[79] Sepsenwol S. and

[80] Taft S. J.

[81] Small J. V.
(1989). Microfilament-based motility in non-muscle cells. Curr. Opin. Cell Biol 1, 75–79
OpenUrl CrossRef PubMed

[82] Small J. V.

[83] Spudich J. A.
(1989). In pursuit of myosin function. Cell Regul 1, 1–11
OpenUrl PubMed Web of Science

[84] Spudich J. A.

[85] Todd I.,
Mellor J. S. and
Gingell D.
(1988). Mapping cell-glass contacts of Dictyostelium amoebae by total internal reflection aqueous fluorescence overcomes a basic ambiguity of interference reflection microscopy. J. Cell Sci 89, 107–114
OpenUrl Abstract/FREE Full Text

[86] Todd I.,

[87] Mellor J. S. and

[88] Gingell D.

[89] Tourtellot M. K.,
Collins R. D. and
Bell W. J.
(1991). The problem of movelength and turn definition in analysis of orientation data. J. Theor. Biol 150, 287–297
OpenUrl CrossRef PubMed Web of Science

[90] Tourtellot M. K.,

[91] Collins R. D. and

[92] Bell W. J.

[93] Wessels D.,
Soll D. R.,
Knecht D.,
Loomis W. F.,
De Lozanne A. and
Spudich J.
(1988). Cell motility and chemotaxis in Dictyostelium amebae lacking myosin heavy chain. Dev. Biol 128, 164–177
OpenUrl CrossRef PubMed Web of Science

[94] Wessels D.,

[95] Soll D. R.,

[96] Knecht D.,

[97] Loomis W. F.,

[98] De Lozanne A. and

[99] Spudich J.

[100] Yumura S.,
Mori H. and
Fukui Y.
(1984). Localization of actin and myosin for the study of ameboid movement in Dictyostelium using improved immunofluorescence. J. Cell Biol 99, 894–899
OpenUrl Abstract/FREE Full Text

[101] Yumura S.,

[102] Mori H. and

[103] Fukui Y.

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New funding scheme supports sustainable events

Mole – The Corona files

JCS and COVID-19

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Summary

REFERENCES

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Related articles

Cited by...

More in this TOC section

Similar articles

Other journals from The Company of Biologists

Cell scientist to watch: Janet Iwasa

New funding scheme supports sustainable events

Mole – The Corona files

JCS and COVID-19