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ZYG-12/Hook's dual role as a dynein adaptor for early endosomes and nuclei is regulated by alternative splicing of its cargo binding domain

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Title: ZYG-12/Hook's dual role as a dynein adaptor for early endosomes and nuclei is regulated by alternative splicing of its cargo binding domain
Authors: Carvalho, Cátia, Moreira, Matilde, Barbosa, Daniel J., Chan, Fung-Yi, Koehnen, Carlota Boal, Teixeira, Vanessa, Rocha, Helder, Green, Mattie, Carvalho, Ana Xavier, Cheerambathur, Dhanya K., Gassmann, Reto
Source: Molecular Biology of the Cell; 20240101, Issue: Preprints
Abstract: The microtubule motor cytoplasmic dynein-1 transports and positions various organelles, but the molecular basis of this functional diversity is not fully understood. Cargo adaptors of the Hook protein family recruit dynein to early endosomes (EE) in fungi and human cells by forming the FTS–Hook–FHIP (FHF) complex. By contrast, the C. elegansHook homolog ZYG-12 recruits dynein to the nuclear envelope (NE) in the meiotic gonad and mitotic early embryo by forming a Linker of Nucleoskeleton and Cytoskeleton (LINC) complex. Here, we demonstrate that ZYG-12 recruits dynein to EE in epithelia. We identify and functionally characterize the homologs of FTS (UBC-19) and FHIP (FHIP-1) that constitute the C. elegansFHF complex, validate the predicted FHIP-1–RAB-5 binding interface in vivo, and show that ZYG-12 forms FHF via a conserved segment that precedes, and is distinct from, its C-terminal NE targeting domain. Finally, we show that C-terminal ZYG-12 splice isoforms differ in their ability to target to the NE and EE. We conclude that the C. elegansHook adaptor evolved to recruit dynein to two distinct organelles, and that cargo specificity of ZYG-12 is regulated by alternative splicing.
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  Data: ZYG-12/Hook's dual role as a dynein adaptor for early endosomes and nuclei is regulated by alternative splicing of its cargo binding domain
– Name: Author
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  Group: Au
  Data: <searchLink fieldCode="AR" term="%22Carvalho%2C+Cátia%22">Carvalho, Cátia</searchLink><br /><searchLink fieldCode="AR" term="%22Moreira%2C+Matilde%22">Moreira, Matilde</searchLink><br /><searchLink fieldCode="AR" term="%22Barbosa%2C+Daniel+J%2E%22">Barbosa, Daniel J.</searchLink><br /><searchLink fieldCode="AR" term="%22Chan%2C+Fung-Yi%22">Chan, Fung-Yi</searchLink><br /><searchLink fieldCode="AR" term="%22Koehnen%2C+Carlota+Boal%22">Koehnen, Carlota Boal</searchLink><br /><searchLink fieldCode="AR" term="%22Teixeira%2C+Vanessa%22">Teixeira, Vanessa</searchLink><br /><searchLink fieldCode="AR" term="%22Rocha%2C+Helder%22">Rocha, Helder</searchLink><br /><searchLink fieldCode="AR" term="%22Green%2C+Mattie%22">Green, Mattie</searchLink><br /><searchLink fieldCode="AR" term="%22Carvalho%2C+Ana+Xavier%22">Carvalho, Ana Xavier</searchLink><br /><searchLink fieldCode="AR" term="%22Cheerambathur%2C+Dhanya+K%2E%22">Cheerambathur, Dhanya K.</searchLink><br /><searchLink fieldCode="AR" term="%22Gassmann%2C+Reto%22">Gassmann, Reto</searchLink>
– Name: TitleSource
  Label: Source
  Group: Src
  Data: Molecular Biology of the Cell; 20240101, Issue: Preprints
– Name: Abstract
  Label: Abstract
  Group: Ab
  Data: The microtubule motor cytoplasmic dynein-1 transports and positions various organelles, but the molecular basis of this functional diversity is not fully understood. Cargo adaptors of the Hook protein family recruit dynein to early endosomes (EE) in fungi and human cells by forming the FTS–Hook–FHIP (FHF) complex. By contrast, the C. elegansHook homolog ZYG-12 recruits dynein to the nuclear envelope (NE) in the meiotic gonad and mitotic early embryo by forming a Linker of Nucleoskeleton and Cytoskeleton (LINC) complex. Here, we demonstrate that ZYG-12 recruits dynein to EE in epithelia. We identify and functionally characterize the homologs of FTS (UBC-19) and FHIP (FHIP-1) that constitute the C. elegansFHF complex, validate the predicted FHIP-1–RAB-5 binding interface in vivo, and show that ZYG-12 forms FHF via a conserved segment that precedes, and is distinct from, its C-terminal NE targeting domain. Finally, we show that C-terminal ZYG-12 splice isoforms differ in their ability to target to the NE and EE. We conclude that the C. elegansHook adaptor evolved to recruit dynein to two distinct organelles, and that cargo specificity of ZYG-12 is regulated by alternative splicing.
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      – Type: doi
        Value: 10.1091/mbc.E24-08-0364
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      – Code: eng
        Text: English
    Titles:
      – TitleFull: ZYG-12/Hook's dual role as a dynein adaptor for early endosomes and nuclei is regulated by alternative splicing of its cargo binding domain
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            NameFull: Carvalho, Cátia
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            – D: 01
              M: 01
              Text: 20240101
              Type: published
              Y: 2024
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              Value: Preprints
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            – TitleFull: Molecular Biology of the Cell
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