Marshalin, a microtubule minus-end binding protein, regulates cytoskeletal structure in the organ of Corti

Jing Zheng*, David Furness, Chongwen Duan, Katharine K. Miller, Roxanne M. Edge, Jessie Chen, Kazuaki Homma, Carole M. Hackney, Peter Dallos, Mary Ann Cheatham

*Corresponding author for this work

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

Dramatic structural changes in microtubules (MT) and the assembly of complicated intercellular connections are seen during the development of the cellular matrix of the sense organ for hearing, the organ of Corti. This report examines the expression of marshalin, a minus-end binding protein, during this process of cochlear development. We discovered that marshalin is abundantly expressed in both sensory hair cells and supporting cells. In the adult, prominent marshalin expression is observed in the cuticular plates of hair cells and in the noncentrosomal MT organization centers (MTOC) of Deiters' and pillar cells. Based upon differences in marshalin expression patterns seen in the organ of Corti, we identified eight isoforms ranging from 863 to 1280 amino acids. mRNAs/proteins associated with marshalin's isoforms are detected at different times during development. These isoforms carry various protein-protein interacting domains, including coiled-coil (CC), calponin homology (CH), proline-rich (PR), and MT-binding domains, referred to as CKK. We, therefore, examined membranous organelles and structural changes in the cytoskeleton induced by expressing two of these marshalin isoforms in vitro. Long forms containing CC and PR domains induce thick, spindle-shaped bundles, whereas short isoforms lacking CC and PR induce more slender variants that develop into densely woven networks. Together, these data suggest that marshalin is closely associated with noncentrosomal MTOCs, and may be involved in MT bundle formation in supporting cells. As a scaffolding protein with multiple isoforms, marshalin is capable of modifying cytoskeletal networks, and consequently organelle positioning, through interactions with various protein partners present in different cells.

Original languageEnglish (US)
Pages (from-to)1192-1202
Number of pages11
JournalBiology Open
Volume2
Issue number11
DOIs
StatePublished - Nov 15 2013

Fingerprint

Organ of Corti
Microtubules
microtubules
binding proteins
Carrier Proteins
Protein Isoforms
Proline
proline
cells
Proteins
Organelles
hairs
organelles
proteins
Cells
Microtubule-Organizing Center
Sense Organs
scaffolding proteins
sense organs
Cochlea

Keywords

  • CAMSAP3
  • Cochlea
  • Microtubule minus-end binding protein
  • Nezha
  • Noncentrosomal MTOC
  • Patronin

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Zheng, J., Furness, D., Duan, C., Miller, K. K., Edge, R. M., Chen, J., ... Cheatham, M. A. (2013). Marshalin, a microtubule minus-end binding protein, regulates cytoskeletal structure in the organ of Corti. Biology Open, 2(11), 1192-1202. https://doi.org/10.1242/bio.20135603
Zheng, Jing ; Furness, David ; Duan, Chongwen ; Miller, Katharine K. ; Edge, Roxanne M. ; Chen, Jessie ; Homma, Kazuaki ; Hackney, Carole M. ; Dallos, Peter ; Cheatham, Mary Ann. / Marshalin, a microtubule minus-end binding protein, regulates cytoskeletal structure in the organ of Corti. In: Biology Open. 2013 ; Vol. 2, No. 11. pp. 1192-1202.
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Zheng, J, Furness, D, Duan, C, Miller, KK, Edge, RM, Chen, J, Homma, K, Hackney, CM, Dallos, P & Cheatham, MA 2013, 'Marshalin, a microtubule minus-end binding protein, regulates cytoskeletal structure in the organ of Corti', Biology Open, vol. 2, no. 11, pp. 1192-1202. https://doi.org/10.1242/bio.20135603

Marshalin, a microtubule minus-end binding protein, regulates cytoskeletal structure in the organ of Corti. / Zheng, Jing; Furness, David; Duan, Chongwen; Miller, Katharine K.; Edge, Roxanne M.; Chen, Jessie; Homma, Kazuaki; Hackney, Carole M.; Dallos, Peter; Cheatham, Mary Ann.

In: Biology Open, Vol. 2, No. 11, 15.11.2013, p. 1192-1202.

Research output: Contribution to journalArticle

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T1 - Marshalin, a microtubule minus-end binding protein, regulates cytoskeletal structure in the organ of Corti

AU - Zheng, Jing

AU - Furness, David

AU - Duan, Chongwen

AU - Miller, Katharine K.

AU - Edge, Roxanne M.

AU - Chen, Jessie

AU - Homma, Kazuaki

AU - Hackney, Carole M.

AU - Dallos, Peter

AU - Cheatham, Mary Ann

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N2 - Dramatic structural changes in microtubules (MT) and the assembly of complicated intercellular connections are seen during the development of the cellular matrix of the sense organ for hearing, the organ of Corti. This report examines the expression of marshalin, a minus-end binding protein, during this process of cochlear development. We discovered that marshalin is abundantly expressed in both sensory hair cells and supporting cells. In the adult, prominent marshalin expression is observed in the cuticular plates of hair cells and in the noncentrosomal MT organization centers (MTOC) of Deiters' and pillar cells. Based upon differences in marshalin expression patterns seen in the organ of Corti, we identified eight isoforms ranging from 863 to 1280 amino acids. mRNAs/proteins associated with marshalin's isoforms are detected at different times during development. These isoforms carry various protein-protein interacting domains, including coiled-coil (CC), calponin homology (CH), proline-rich (PR), and MT-binding domains, referred to as CKK. We, therefore, examined membranous organelles and structural changes in the cytoskeleton induced by expressing two of these marshalin isoforms in vitro. Long forms containing CC and PR domains induce thick, spindle-shaped bundles, whereas short isoforms lacking CC and PR induce more slender variants that develop into densely woven networks. Together, these data suggest that marshalin is closely associated with noncentrosomal MTOCs, and may be involved in MT bundle formation in supporting cells. As a scaffolding protein with multiple isoforms, marshalin is capable of modifying cytoskeletal networks, and consequently organelle positioning, through interactions with various protein partners present in different cells.

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