A transient helix in the disordered region of dynein light intermediate chain links the motor to structurally diverse adaptors for cargo transport
All animal cells use the motor cytoplasmic dynein 1 (dynein) to transport diverse cargo toward microtubule minus ends and to organize and position microtubule arrays such as the mitotic spindle. Cargo-specific adaptors engage with dynein to recruit and activate the motor, but the molecular mechanism...
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| Published in: | PLoS biology Vol. 17; no. 1; p. e3000100 |
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| Main Authors: | , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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United States
Public Library of Science
07.01.2019
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| ISSN: | 1545-7885, 1544-9173, 1545-7885 |
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| Abstract | All animal cells use the motor cytoplasmic dynein 1 (dynein) to transport diverse cargo toward microtubule minus ends and to organize and position microtubule arrays such as the mitotic spindle. Cargo-specific adaptors engage with dynein to recruit and activate the motor, but the molecular mechanisms remain incompletely understood. Here, we use structural and dynamic nuclear magnetic resonance (NMR) analysis to demonstrate that the C-terminal region of human dynein light intermediate chain 1 (LIC1) is intrinsically disordered and contains two short conserved segments with helical propensity. NMR titration experiments reveal that the first helical segment (helix 1) constitutes the main interaction site for the adaptors Spindly (SPDL1), bicaudal D homolog 2 (BICD2), and Hook homolog 3 (HOOK3). In vitro binding assays show that helix 1, but not helix 2, is essential in both LIC1 and LIC2 for binding to SPDL1, BICD2, HOOK3, RAB-interacting lysosomal protein (RILP), RAB11 family-interacting protein 3 (RAB11FIP3), ninein (NIN), and trafficking kinesin-binding protein 1 (TRAK1). Helix 1 is sufficient to bind RILP, whereas other adaptors require additional segments preceding helix 1 for efficient binding. Point mutations in the C-terminal helix 1 of Caenorhabditis elegans LIC, introduced by genome editing, severely affect development, locomotion, and life span of the animal and disrupt the distribution and transport kinetics of membrane cargo in axons of mechanosensory neurons, identical to what is observed when the entire LIC C-terminal region is deleted. Deletion of the C-terminal helix 2 delays dynein-dependent spindle positioning in the one-cell embryo but overall does not significantly perturb dynein function. We conclude that helix 1 in the intrinsically disordered region of LIC provides a conserved link between dynein and structurally diverse cargo adaptor families that is critical for dynein function in vivo. |
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| AbstractList | All animal cells use the motor cytoplasmic dynein 1 (dynein) to transport diverse cargo toward microtubule minus ends and to organize and position microtubule arrays such as the mitotic spindle. Cargo-specific adaptors engage with dynein to recruit and activate the motor, but the molecular mechanisms remain incompletely understood. Here, we use structural and dynamic nuclear magnetic resonance (NMR) analysis to demonstrate that the C-terminal region of human dynein light intermediate chain 1 (LIC1) is intrinsically disordered and contains two short conserved segments with helical propensity. NMR titration experiments reveal that the first helical segment (helix 1) constitutes the main interaction site for the adaptors Spindly (SPDL1), bicaudal D homolog 2 (BICD2), and Hook homolog 3 (HOOK3). In vitro binding assays show that helix 1, but not helix 2, is essential in both LIC1 and LIC2 for binding to SPDL1, BICD2, HOOK3, RAB-interacting lysosomal protein (RILP), RAB11 family-interacting protein 3 (RAB11FIP3), ninein (NIN), and trafficking kinesin-binding protein 1 (TRAK1). Helix 1 is sufficient to bind RILP, whereas other adaptors require additional segments preceding helix 1 for efficient binding. Point mutations in the C-terminal helix 1 of Caenorhabditis elegans LIC, introduced by genome editing, severely affect development, locomotion, and life span of the animal and disrupt the distribution and transport kinetics of membrane cargo in axons of mechanosensory neurons, identical to what is observed when the entire LIC C-terminal region is deleted. Deletion of the C-terminal helix 2 delays dynein-dependent spindle positioning in the one-cell embryo but overall does not significantly perturb dynein function. We conclude that helix 1 in the intrinsically disordered region of LIC provides a conserved link between dynein and structurally diverse cargo adaptor families that is critical for dynein function in vivo. All animal cells use the motor cytoplasmic dynein 1 (dynein) to transport diverse cargo toward microtubule minus ends and to organize and position microtubule arrays such as the mitotic spindle. Cargo-specific adaptors engage with dynein to recruit and activate the motor, but the molecular mechanisms remain incompletely understood. Here, we use structural and dynamic nuclear magnetic resonance (NMR) analysis to demonstrate that the C-terminal region of human dynein light intermediate chain 1 (LIC1) is intrinsically disordered and contains two short conserved segments with helical propensity. NMR titration experiments reveal that the first helical segment (helix 1) constitutes the main interaction site for the adaptors Spindly (SPDL1), bicaudal D homolog 2 (BICD2), and Hook homolog 3 (HOOK3). In vitro binding assays show that helix 1, but not helix 2, is essential in both LIC1 and LIC2 for binding to SPDL1, BICD2, HOOK3, RAB-interacting lysosomal protein (RILP), RAB11 family-interacting protein 3 (RAB11FIP3), ninein (NIN), and trafficking kinesin-binding protein 1 (TRAK1). Helix 1 is sufficient to bind RILP, whereas other adaptors require additional segments preceding helix 1 for efficient binding. Point mutations in the C-terminal helix 1 of Caenorhabditis elegans LIC, introduced by genome editing, severely affect development, locomotion, and life span of the animal and disrupt the distribution and transport kinetics of membrane cargo in axons of mechanosensory neurons, identical to what is observed when the entire LIC C-terminal region is deleted. Deletion of the C-terminal helix 2 delays dynein-dependent spindle positioning in the one-cell embryo but overall does not significantly perturb dynein function. We conclude that helix 1 in the intrinsically disordered region of LIC provides a conserved link between dynein and structurally diverse cargo adaptor families that is critical for dynein function in vivo. A highly conserved mechanism links the microtubule minus end–directed motor dynein to structurally diverse cargo adaptors through its light intermediate chain; this interaction is crucial for dynein function in vivo. The large size and complex organization of animal cells make the correct and efficient distribution of intracellular content a challenge. The solution is to use motor proteins, which harness energy from ATP hydrolysis to walk along actin filaments or microtubules, for directional transport of cargo. The multi-subunit motor cytoplasmic dynein 1 (dynein) is responsible for transport directed toward the minus ends of microtubules. An important question is how dynein is recruited to its diverse cargo, which includes organelles such as endosomes and mitochondria, proteins, and mRNA. In this study, we use nuclear magnetic resonance spectroscopy to show that the light intermediate chain (LIC) subunit of human dynein uses a short helix in its disordered C-terminal region to bind structurally distinct adaptor proteins that connect the motor to specific cargo. We then use genome editing in the animal model C. elegans to demonstrate the functional relevance of the C-terminal LIC helix for dynein-dependent cargo transport in neurons. Thus, dynein recruitment to cargo involves a highly conserved interaction between LIC and adaptor proteins. All animal cells use the motor cytoplasmic dynein 1 (dynein) to transport diverse cargo toward microtubule minus ends and to organize and position microtubule arrays such as the mitotic spindle. Cargo-specific adaptors engage with dynein to recruit and activate the motor, but the molecular mechanisms remain incompletely understood. Here, we use structural and dynamic nuclear magnetic resonance (NMR) analysis to demonstrate that the C-terminal region of human dynein light intermediate chain 1 (LIC1) is intrinsically disordered and contains two short conserved segments with helical propensity. NMR titration experiments reveal that the first helical segment (helix 1) constitutes the main interaction site for the adaptors Spindly (SPDL1), bicaudal D homolog 2 (BICD2), and Hook homolog 3 (HOOK3). In vitro binding assays show that helix 1, but not helix 2, is essential in both LIC1 and LIC2 for binding to SPDL1, BICD2, HOOK3, RAB-interacting lysosomal protein (RILP), RAB11 family-interacting protein 3 (RAB11FIP3), ninein (NIN), and trafficking kinesin-binding protein 1 (TRAK1). Helix 1 is sufficient to bind RILP, whereas other adaptors require additional segments preceding helix 1 for efficient binding. Point mutations in the C-terminal helix 1 of Caenorhabditis elegans LIC, introduced by genome editing, severely affect development, locomotion, and life span of the animal and disrupt the distribution and transport kinetics of membrane cargo in axons of mechanosensory neurons, identical to what is observed when the entire LIC C-terminal region is deleted. Deletion of the C-terminal helix 2 delays dynein-dependent spindle positioning in the one-cell embryo but overall does not significantly perturb dynein function. We conclude that helix 1 in the intrinsically disordered region of LIC provides a conserved link between dynein and structurally diverse cargo adaptor families that is critical for dynein function in vivo.All animal cells use the motor cytoplasmic dynein 1 (dynein) to transport diverse cargo toward microtubule minus ends and to organize and position microtubule arrays such as the mitotic spindle. Cargo-specific adaptors engage with dynein to recruit and activate the motor, but the molecular mechanisms remain incompletely understood. Here, we use structural and dynamic nuclear magnetic resonance (NMR) analysis to demonstrate that the C-terminal region of human dynein light intermediate chain 1 (LIC1) is intrinsically disordered and contains two short conserved segments with helical propensity. NMR titration experiments reveal that the first helical segment (helix 1) constitutes the main interaction site for the adaptors Spindly (SPDL1), bicaudal D homolog 2 (BICD2), and Hook homolog 3 (HOOK3). In vitro binding assays show that helix 1, but not helix 2, is essential in both LIC1 and LIC2 for binding to SPDL1, BICD2, HOOK3, RAB-interacting lysosomal protein (RILP), RAB11 family-interacting protein 3 (RAB11FIP3), ninein (NIN), and trafficking kinesin-binding protein 1 (TRAK1). Helix 1 is sufficient to bind RILP, whereas other adaptors require additional segments preceding helix 1 for efficient binding. Point mutations in the C-terminal helix 1 of Caenorhabditis elegans LIC, introduced by genome editing, severely affect development, locomotion, and life span of the animal and disrupt the distribution and transport kinetics of membrane cargo in axons of mechanosensory neurons, identical to what is observed when the entire LIC C-terminal region is deleted. Deletion of the C-terminal helix 2 delays dynein-dependent spindle positioning in the one-cell embryo but overall does not significantly perturb dynein function. We conclude that helix 1 in the intrinsically disordered region of LIC provides a conserved link between dynein and structurally diverse cargo adaptor families that is critical for dynein function in vivo. |
| Audience | Academic |
| Author | Born, Alexandra McCabe, Maxwell Gassmann, Reto Gama, José B. Vögeli, Beat Nichols, Parker J. Barbosa, Daniel J. Celestino, Ricardo Henen, Morkos A. Carvalho, Ana X. Carvalho, Cátia |
| AuthorAffiliation | 2 Instituto de Investigação e Inovação em Saúde (i3S), Universidade do Porto, Porto, Portugal 4 Faculty of Pharmacy, Mansoura University, Mansoura, Egypt 1 Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto, Porto, Portugal 3 Department of Biochemistry and Molecular Genetics, University of Colorado Denver, Anschutz Medical Campus, Aurora, Colorado, United States of America Johns Hopkins University, UNITED STATES |
| AuthorAffiliation_xml | – name: 4 Faculty of Pharmacy, Mansoura University, Mansoura, Egypt – name: 3 Department of Biochemistry and Molecular Genetics, University of Colorado Denver, Anschutz Medical Campus, Aurora, Colorado, United States of America – name: Johns Hopkins University, UNITED STATES – name: 2 Instituto de Investigação e Inovação em Saúde (i3S), Universidade do Porto, Porto, Portugal – name: 1 Instituto de Biologia Molecular e Celular (IBMC), Universidade do Porto, Porto, Portugal |
| Author_xml | – sequence: 1 givenname: Ricardo orcidid: 0000-0002-9605-6433 surname: Celestino fullname: Celestino, Ricardo – sequence: 2 givenname: Morkos A. orcidid: 0000-0003-4835-5583 surname: Henen fullname: Henen, Morkos A. – sequence: 3 givenname: José B. orcidid: 0000-0002-7011-1502 surname: Gama fullname: Gama, José B. – sequence: 4 givenname: Cátia orcidid: 0000-0002-4312-7445 surname: Carvalho fullname: Carvalho, Cátia – sequence: 5 givenname: Maxwell orcidid: 0000-0002-3599-694X surname: McCabe fullname: McCabe, Maxwell – sequence: 6 givenname: Daniel J. surname: Barbosa fullname: Barbosa, Daniel J. – sequence: 7 givenname: Alexandra orcidid: 0000-0001-8258-0982 surname: Born fullname: Born, Alexandra – sequence: 8 givenname: Parker J. orcidid: 0000-0003-1930-6408 surname: Nichols fullname: Nichols, Parker J. – sequence: 9 givenname: Ana X. surname: Carvalho fullname: Carvalho, Ana X. – sequence: 10 givenname: Reto orcidid: 0000-0002-0360-2977 surname: Gassmann fullname: Gassmann, Reto – sequence: 11 givenname: Beat orcidid: 0000-0003-1176-3137 surname: Vögeli fullname: Vögeli, Beat |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30615611$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2019 Public Library of Science 2019 Celestino et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2019 Celestino et al 2019 Celestino et al |
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| DOI | 10.1371/journal.pbio.3000100 |
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| SubjectTerms | Adapters Adaptor Proteins, Signal Transducing - metabolism Animals Axons Biochemistry Biological transport, Active Biology and Life Sciences Caenorhabditis elegans - genetics Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Cargo transportation Carrier Proteins - metabolism Chains Clonal deletion Conserved Sequence Cytoplasmic Dyneins - genetics Cytoplasmic Dyneins - metabolism Dynactin Complex Dynein Dyneins - genetics Dyneins - metabolism Embryos Genetics Genome editing Genomes HeLa Cells Homology Humans Kinesin Kinetics Life span Light Locomotion Lysosomal protein Lysosomes - metabolism Microtubule-Associated Proteins - metabolism Microtubules - metabolism Molecular modelling Motility Mutation Nematodes NMR Nuclear magnetic resonance Nuclear Magnetic Resonance, Biomolecular - methods Observations Physiological aspects Protein Binding - physiology Protein transport Protein Transport - genetics Protein Transport - physiology Proteins Research and Analysis Methods Segments Software Spectrum analysis Spindle Apparatus Supervision Titration |
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| Title | A transient helix in the disordered region of dynein light intermediate chain links the motor to structurally diverse adaptors for cargo transport |
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