A genetically encoded photoactivatable Rac controls the motility of living cells
A light touch on proteins Many aspects of cellular function depend on when and where in the cell various protein activities are turned 'on' or 'off' at the molecular level. A new technique that uses light to manipulate the activity of a protein at precise times and places within...
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| Vydáno v: | Nature (London) Ročník 461; číslo 7260; s. 104 - 108 |
|---|---|
| Hlavní autoři: | , , , , , , |
| Médium: | Journal Article |
| Jazyk: | angličtina |
| Vydáno: |
London
Nature Publishing Group UK
03.09.2009
Nature Publishing Group |
| Témata: | |
| ISSN: | 0028-0836, 1476-4687, 1476-4687 |
| On-line přístup: | Získat plný text |
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| Abstract | A light touch on proteins
Many aspects of cellular function depend on when and where in the cell various protein activities are turned 'on' or 'off' at the molecular level. A new technique that uses light to manipulate the activity of a protein at precise times and places within the living cell has the potential make the study of this fundamental aspect of protein function a practical proposition. It makes use of a genetically encoded, photoactivatable derivative of Rac1, a GTPase that regulates actin cytoskeletal dynamics, which can be activated by exposure to laser light. This localized activation generates precisely localized cell protrusions and ruffling and can direct cell motility. This approach should be extensible to other proteins.
The precise spatiotemporal dynamics of protein activity remain poorly understood, yet they can be critical in determining cell behaviour. A genetically encoded, photoactivatable version of the protein Rac1, a key GTPase regulating actin cytoskeletal dynamics, has now been produced; this approach enables the manipulation of the activity of Rac1 at precise times and places within a living cell, thus controlling motility.
The precise spatio-temporal dynamics of protein activity are often critical in determining cell behaviour, yet for most proteins they remain poorly understood; it remains difficult to manipulate protein activity at precise times and places within living cells. Protein activity has been controlled by light, through protein derivatization with photocleavable moieties
1
or using photoreactive small-molecule ligands
2
. However, this requires use of toxic ultraviolet wavelengths, activation is irreversible, and/or cell loading is accomplished via disruption of the cell membrane (for example, through microinjection). Here we have developed a new approach to produce genetically encoded photoactivatable derivatives of Rac1, a key GTPase regulating actin cytoskeletal dynamics in metazoan cells
3
,
4
. Rac1 mutants were fused to the photoreactive LOV (light oxygen voltage) domain from phototropin
5
,
6
, sterically blocking Rac1 interactions until irradiation unwound a helix linking LOV to Rac1. Photoactivatable Rac1 (PA-Rac1) could be reversibly and repeatedly activated using 458- or 473-nm light to generate precisely localized cell protrusions and ruffling. Localized Rac activation or inactivation was sufficient to produce cell motility and control the direction of cell movement. Myosin was involved in Rac control of directionality but not in Rac-induced protrusion, whereas PAK was required for Rac-induced protrusion. PA-Rac1 was used to elucidate Rac regulation of RhoA in cell motility. Rac and Rho coordinate cytoskeletal behaviours with seconds and submicrometre precision
7
,
8
. Their mutual regulation remains controversial
9
, with data indicating that Rac inhibits and/or activates Rho
10
,
11
. Rac was shown to inhibit RhoA in mouse embryonic fibroblasts, with inhibition modulated at protrusions and ruffles. A PA-Rac crystal structure and modelling revealed LOV–Rac interactions that will facilitate extension of this photoactivation approach to other proteins. |
|---|---|
| AbstractList | A light touch on proteins
Many aspects of cellular function depend on when and where in the cell various protein activities are turned 'on' or 'off' at the molecular level. A new technique that uses light to manipulate the activity of a protein at precise times and places within the living cell has the potential make the study of this fundamental aspect of protein function a practical proposition. It makes use of a genetically encoded, photoactivatable derivative of Rac1, a GTPase that regulates actin cytoskeletal dynamics, which can be activated by exposure to laser light. This localized activation generates precisely localized cell protrusions and ruffling and can direct cell motility. This approach should be extensible to other proteins.
The precise spatiotemporal dynamics of protein activity remain poorly understood, yet they can be critical in determining cell behaviour. A genetically encoded, photoactivatable version of the protein Rac1, a key GTPase regulating actin cytoskeletal dynamics, has now been produced; this approach enables the manipulation of the activity of Rac1 at precise times and places within a living cell, thus controlling motility.
The precise spatio-temporal dynamics of protein activity are often critical in determining cell behaviour, yet for most proteins they remain poorly understood; it remains difficult to manipulate protein activity at precise times and places within living cells. Protein activity has been controlled by light, through protein derivatization with photocleavable moieties
1
or using photoreactive small-molecule ligands
2
. However, this requires use of toxic ultraviolet wavelengths, activation is irreversible, and/or cell loading is accomplished via disruption of the cell membrane (for example, through microinjection). Here we have developed a new approach to produce genetically encoded photoactivatable derivatives of Rac1, a key GTPase regulating actin cytoskeletal dynamics in metazoan cells
3
,
4
. Rac1 mutants were fused to the photoreactive LOV (light oxygen voltage) domain from phototropin
5
,
6
, sterically blocking Rac1 interactions until irradiation unwound a helix linking LOV to Rac1. Photoactivatable Rac1 (PA-Rac1) could be reversibly and repeatedly activated using 458- or 473-nm light to generate precisely localized cell protrusions and ruffling. Localized Rac activation or inactivation was sufficient to produce cell motility and control the direction of cell movement. Myosin was involved in Rac control of directionality but not in Rac-induced protrusion, whereas PAK was required for Rac-induced protrusion. PA-Rac1 was used to elucidate Rac regulation of RhoA in cell motility. Rac and Rho coordinate cytoskeletal behaviours with seconds and submicrometre precision
7
,
8
. Their mutual regulation remains controversial
9
, with data indicating that Rac inhibits and/or activates Rho
10
,
11
. Rac was shown to inhibit RhoA in mouse embryonic fibroblasts, with inhibition modulated at protrusions and ruffles. A PA-Rac crystal structure and modelling revealed LOV–Rac interactions that will facilitate extension of this photoactivation approach to other proteins. The precise spatio-temporal dynamics of protein activity are often critical in determining cell behaviour, yet for most proteins they remain poorly understood; it remains difficult to manipulate protein activity at precise times and places within living cells. Protein activity has been controlled by light, through protein derivatization with photocleavable moieties or using photoreactive small-molecule ligands. However, this requires use of toxic ultraviolet wavelengths, activation is irreversible, and/or cell loading is accomplished via disruption of the cell membrane (for example, through microinjection). Here we have developed a new approach to produce genetically encoded photoactivatable derivatives of Rac1, a key GTPase regulating actin cytoskeletal dynamics in metazoan cells. Rac1 mutants were fused to the photoreactive LOV (light oxygen voltage) domain from phototropin, sterically blocking Rac1 interactions until irradiation unwound a helix linking LOV to Rac1. Photoactivatable Rac1 (PA-Rac1) could be reversibly and repeatedly activated using 458- or 473-nm light to generate precisely localized cell protrusions and ruffling. Localized Rac activation or inactivation was sufficient to produce cell motility and control the direction of cell movement. Myosin was involved in Rac control of directionality but not in Rac-induced protrusion, whereas PAK was required for Rac-induced protrusion. PA-Rac1 was used to elucidate Rac regulation of RhoA in cell motility. Rac and Rho coordinate cytoskeletal behaviours with seconds and submicrometre precision. Their mutual regulation remains controversial, with data indicating that Rac inhibits and/or activates Rho. Rac was shown to inhibit RhoA in mouse embryonic fibroblasts, with inhibition modulated at protrusions and ruffles. A PA-Rac crystal structure and modelling revealed LOV-Rac interactions that will facilitate extension of this photoactivation approach to other proteins.The precise spatio-temporal dynamics of protein activity are often critical in determining cell behaviour, yet for most proteins they remain poorly understood; it remains difficult to manipulate protein activity at precise times and places within living cells. Protein activity has been controlled by light, through protein derivatization with photocleavable moieties or using photoreactive small-molecule ligands. However, this requires use of toxic ultraviolet wavelengths, activation is irreversible, and/or cell loading is accomplished via disruption of the cell membrane (for example, through microinjection). Here we have developed a new approach to produce genetically encoded photoactivatable derivatives of Rac1, a key GTPase regulating actin cytoskeletal dynamics in metazoan cells. Rac1 mutants were fused to the photoreactive LOV (light oxygen voltage) domain from phototropin, sterically blocking Rac1 interactions until irradiation unwound a helix linking LOV to Rac1. Photoactivatable Rac1 (PA-Rac1) could be reversibly and repeatedly activated using 458- or 473-nm light to generate precisely localized cell protrusions and ruffling. Localized Rac activation or inactivation was sufficient to produce cell motility and control the direction of cell movement. Myosin was involved in Rac control of directionality but not in Rac-induced protrusion, whereas PAK was required for Rac-induced protrusion. PA-Rac1 was used to elucidate Rac regulation of RhoA in cell motility. Rac and Rho coordinate cytoskeletal behaviours with seconds and submicrometre precision. Their mutual regulation remains controversial, with data indicating that Rac inhibits and/or activates Rho. Rac was shown to inhibit RhoA in mouse embryonic fibroblasts, with inhibition modulated at protrusions and ruffles. A PA-Rac crystal structure and modelling revealed LOV-Rac interactions that will facilitate extension of this photoactivation approach to other proteins. To ensure that the photoactivatable Rac1 would induce no dominant-negative effects and that its activity would not be subject to upstream regulation, mutations were introduced to abolish GTP hydrolysis and diminish interactions with nucleotide exchange factors, guanine nucleotide dissociation inhibitors (Q61L) and GTPase activating proteins (E91H and N92H) (Supplementary Fig. 2 and Supplementary text 'Characterization of Rac1 constructs'). Using this advantage, we examined the role of myosin, a key mediator of actin-based contractility, in Rac-induced motility.\n Consistent with pull-down assays (Fig. 1b and Supplementary Fig. 1a), adding or removing even one residue from the connection between LOV and Rac resulted in conformational ensembles with exposed effector binding sites. The precise spatio-temporal dynamics of protein activity are often critical in determining cell behaviour, yet for most proteins they remain poorly understood; it remains difficult to manipulate protein activity at precise times and places within living cells. Protein activity has been controlled by light, through protein derivatization with photocleavable moieties or using photoreactive small-molecule ligands. However, this requires use of toxic ultraviolet wavelengths, activation is irreversible, and/or cell loading is accomplished via disruption of the cell membrane (for example, through microinjection). Here we have developed a new approach to produce genetically encoded photoactivatable derivatives of Rac1, a key GTPase regulating actin cytoskeletal dynamics in metazoan cells. Rac1 mutants were fused to the photoreactive LOV (light oxygen voltage) domain from phototropin, sterically blocking Rac1 interactions until irradiation unwound a helix linking LOV to Rac1. Photoactivatable Rac1 (PA-Rac1) could be reversibly and repeatedly activated using 458- or 473-nm light to generate precisely localized cell protrusions and ruffling. Localized Rac activation or inactivation was sufficient to produce cell motility and control the direction of cell movement. Myosin was involved in Rac control of directionality but not in Rac-induced protrusion, whereas PAK was required for Rac-induced protrusion. PA-Rac1 was used to elucidate Rac regulation of RhoA in cell motility. Rac and Rho coordinate cytoskeletal behaviours with seconds and submicrometre precision. Their mutual regulation remains controversial, with data indicating that Rac inhibits and/or activates Rho. Rac was shown to inhibit RhoA in mouse embryonic fibroblasts, with inhibition modulated at protrusions and ruffles. A PA-Rac crystal structure and modelling revealed LOV-Rac interactions that will facilitate extension of this photoactivation approach to other proteins. The precise spatio-temporal dynamics of protein activity are often critical in determining cell behaviour, yet for most proteins they remain poorly understood; it remains difficult to manipulate protein activity at precise times and places within living cells. Protein activity has been controlled by light, through protein derivatization with photocleavable moieties1 or using photoreactive small molecule ligands2. However, this requires use of toxic UV wavelengths, activation is irreversible, and/or cell loading is accomplished via disruption of the cell membrane (i.e. through microinjection). We have developed a new approach to produce genetically-encoded photo-activatable derivatives of Rac1, a key GTPase regulating actin cytoskeletal dynamics3,4. Rac1 mutants were fused to the photoreactive LOV (light oxygen voltage) domain from phototropin5,6, sterically blocking Rac1 interactions until irradiation unwound a helix linking LOV to Rac1. Photoactivatable Rac1 (PA-Rac1) could be reversibly and repeatedly activated using 458 or 473 nm light to generate precisely localized cell protrusions and ruffling. Localized Rac activation or inactivation was sufficient to produce cell motility and control the direction of cell movement. Myosin was involved in Rac control of directionality but not in Rac-induced protrusion, while PAK was required for Rac-induced protrusion. PA-Rac1 was used to elucidate Rac regulation of RhoA in cell motility. Rac and Rho coordinate cytoskeletal behaviours with seconds and submicron precision7,8. Their mutual regulation remains controversial9, with data indicating that Rac inhibits and/or activates Rho10,11. Rac was shown to inhibit RhoA in living cells, with inhibition modulated at protrusions and ruffles. A PA-Rac crystal structure and modelling revealed LOV-Rac interactions that will facilitate extension of this photoactivation approach to other proteins. |
| Audience | Academic |
| Author | Lungu, Oana I. Schlichting, Ilme Jaehrig, Angelika Wu, Yi I. Kuhlman, Brian Hahn, Klaus M. Frey, Daniel |
| Author_xml | – sequence: 1 givenname: Yi I. surname: Wu fullname: Wu, Yi I. email: yiwu@med.unc.edu organization: Department of Pharmacology,, Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina 27599, USA – sequence: 2 givenname: Daniel surname: Frey fullname: Frey, Daniel organization: Department of Biomolecular Mechanisms, Max Planck Institute for Medical Research, Jahn-Strasse 29, 69120 Heidelberg, Germany – sequence: 3 givenname: Oana I. surname: Lungu fullname: Lungu, Oana I. organization: Department of Pharmacology,, Department of Biochemistry and Biophysics, and, Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina 27599, USA – sequence: 4 givenname: Angelika surname: Jaehrig fullname: Jaehrig, Angelika organization: Department of Pharmacology,, Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina 27599, USA – sequence: 5 givenname: Ilme surname: Schlichting fullname: Schlichting, Ilme organization: Department of Biomolecular Mechanisms, Max Planck Institute for Medical Research, Jahn-Strasse 29, 69120 Heidelberg, Germany – sequence: 6 givenname: Brian surname: Kuhlman fullname: Kuhlman, Brian organization: Department of Biochemistry and Biophysics, and, Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina 27599, USA – sequence: 7 givenname: Klaus M. surname: Hahn fullname: Hahn, Klaus M. email: khahn@med.unc.edu organization: Department of Pharmacology,, Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina 27599, USA |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=21860112$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/19693014$$D View this record in MEDLINE/PubMed |
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| Keywords | Motility Enzyme Triphosphoric monoester hydrolases Photoactivation Rodentia dGTPase Esterases Recombinant cell Metazoa Cellular motility Vertebrata Regulation(control) Mammalia Mouse Embryonic cell Dynamics Hydrolases Cytoskeleton Mutation Fibroblast |
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| Snippet | A light touch on proteins
Many aspects of cellular function depend on when and where in the cell various protein activities are turned 'on' or 'off' at the... The precise spatio-temporal dynamics of protein activity are often critical in determining cell behaviour, yet for most proteins they remain poorly understood;... To ensure that the photoactivatable Rac1 would induce no dominant-negative effects and that its activity would not be subject to upstream regulation, mutations... |
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| SubjectTerms | Animals Avena - genetics Binding sites Biological and medical sciences Cell Line Cell Movement - radiation effects Cell physiology Cell Surface Extensions Cell Survival Cells Cryptochromes Crystal structure Crystallization Crystallography, X-Ray Embryo, Mammalian - cytology Enzyme Activation - radiation effects Fibroblasts Flavoproteins - chemistry Flavoproteins - genetics Flavoproteins - metabolism Fluorescence Recovery After Photobleaching Fundamental and applied biological sciences. Psychology Genetic Engineering - methods HeLa Cells Humanities and Social Sciences Humans Hydrogen bonds letter Measurement Mice Models, Molecular Molecular and cellular biology Motility Motility and taxis Motion pictures multidisciplinary Mutation Myosins - metabolism Physiological aspects Protein Conformation Proteins rac1 GTP-Binding Protein - chemistry rac1 GTP-Binding Protein - genetics rac1 GTP-Binding Protein - metabolism rac1 GTP-Binding Protein - radiation effects rho GTP-Binding Proteins - antagonists & inhibitors rho GTP-Binding Proteins - metabolism rhoA GTP-Binding Protein Science Studies |
| Title | A genetically encoded photoactivatable Rac controls the motility of living cells |
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