Structural basis for disassembly of katanin heterododecamers

The reorganization of microtubules in mitosis, meiosis, and development requires the microtubule-severing activity of katanin. Katanin is a heterodimer composed of an TPase ssociated with diverse cellular ctivities (AAA) subunit and a regulatory subunit. Microtubule severing requires ATP hydrolysis...

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Published in:The Journal of biological chemistry Vol. 293; no. 27; p. 10590
Main Authors: Nithianantham, Stanley, McNally, Francis J, Al-Bassam, Jawdat
Format: Journal Article
Language:English
Published: United States 06.07.2018
Subjects:
Adenosine Triphosphatases - chemistry
Adenosine Triphosphatases - metabolism
Animals
Caenorhabditis elegans - enzymology
Caenorhabditis elegans Proteins - chemistry
Caenorhabditis elegans Proteins - metabolism
Crystallography, X-Ray
Humans
Katanin - chemistry
Katanin - metabolism
Meiosis
Microtubules
Protein Conformation
Protein Multimerization
Spindle Apparatus
X-ray crystallography
microtubule
microtubule-associated protein (MAP)
tubulin
meiosis
mitosis
ISSN:1083-351X, 1083-351X
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Abstract The reorganization of microtubules in mitosis, meiosis, and development requires the microtubule-severing activity of katanin. Katanin is a heterodimer composed of an TPase ssociated with diverse cellular ctivities (AAA) subunit and a regulatory subunit. Microtubule severing requires ATP hydrolysis by katanin's conserved AAA ATPase domains. Whereas other AAA ATPases form stable hexamers, we show that katanin forms only a monomer or dimers of heterodimers in solution. Katanin oligomers consistent with hexamers of heterodimers or heterododecamers were only observed for an ATP hydrolysis-deficient mutant in the presence of ATP. X-ray structures of katanin's AAA ATPase in monomeric nucleotide-free and pseudo-oligomeric ADP-bound states revealed conformational changes in the AAA subdomains that explained the structural basis for the instability of the katanin heterododecamer. We propose that the rapid dissociation of katanin AAA oligomers may lead to an autoinhibited state that prevents inappropriate microtubule severing or that cyclical disassembly into heterodimers may critically contribute to the microtubule-severing mechanism.
AbstractList The reorganization of microtubules in mitosis, meiosis, and development requires the microtubule-severing activity of katanin. Katanin is a heterodimer composed of an TPase ssociated with diverse cellular ctivities (AAA) subunit and a regulatory subunit. Microtubule severing requires ATP hydrolysis by katanin's conserved AAA ATPase domains. Whereas other AAA ATPases form stable hexamers, we show that katanin forms only a monomer or dimers of heterodimers in solution. Katanin oligomers consistent with hexamers of heterodimers or heterododecamers were only observed for an ATP hydrolysis-deficient mutant in the presence of ATP. X-ray structures of katanin's AAA ATPase in monomeric nucleotide-free and pseudo-oligomeric ADP-bound states revealed conformational changes in the AAA subdomains that explained the structural basis for the instability of the katanin heterododecamer. We propose that the rapid dissociation of katanin AAA oligomers may lead to an autoinhibited state that prevents inappropriate microtubule severing or that cyclical disassembly into heterodimers may critically contribute to the microtubule-severing mechanism.
The reorganization of microtubules in mitosis, meiosis, and development requires the microtubule-severing activity of katanin. Katanin is a heterodimer composed of an ATPase associated with diverse cellular activities (AAA) subunit and a regulatory subunit. Microtubule severing requires ATP hydrolysis by katanin's conserved AAA ATPase domains. Whereas other AAA ATPases form stable hexamers, we show that katanin forms only a monomer or dimers of heterodimers in solution. Katanin oligomers consistent with hexamers of heterodimers or heterododecamers were only observed for an ATP hydrolysis-deficient mutant in the presence of ATP. X-ray structures of katanin's AAA ATPase in monomeric nucleotide-free and pseudo-oligomeric ADP-bound states revealed conformational changes in the AAA subdomains that explained the structural basis for the instability of the katanin heterododecamer. We propose that the rapid dissociation of katanin AAA oligomers may lead to an autoinhibited state that prevents inappropriate microtubule severing or that cyclical disassembly into heterodimers may critically contribute to the microtubule-severing mechanism.The reorganization of microtubules in mitosis, meiosis, and development requires the microtubule-severing activity of katanin. Katanin is a heterodimer composed of an ATPase associated with diverse cellular activities (AAA) subunit and a regulatory subunit. Microtubule severing requires ATP hydrolysis by katanin's conserved AAA ATPase domains. Whereas other AAA ATPases form stable hexamers, we show that katanin forms only a monomer or dimers of heterodimers in solution. Katanin oligomers consistent with hexamers of heterodimers or heterododecamers were only observed for an ATP hydrolysis-deficient mutant in the presence of ATP. X-ray structures of katanin's AAA ATPase in monomeric nucleotide-free and pseudo-oligomeric ADP-bound states revealed conformational changes in the AAA subdomains that explained the structural basis for the instability of the katanin heterododecamer. We propose that the rapid dissociation of katanin AAA oligomers may lead to an autoinhibited state that prevents inappropriate microtubule severing or that cyclical disassembly into heterodimers may critically contribute to the microtubule-severing mechanism.
Author Nithianantham, Stanley
Al-Bassam, Jawdat
McNally, Francis J
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  organization: From the Department of Molecular Cellular Biology University of California, Davis, California 95616
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  givenname: Francis J
  surname: McNally
  fullname: McNally, Francis J
  organization: From the Department of Molecular Cellular Biology University of California, Davis, California 95616
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  givenname: Jawdat
  surname: Al-Bassam
  fullname: Al-Bassam, Jawdat
  email: jawdat@ucdavis.edu
  organization: From the Department of Molecular Cellular Biology University of California, Davis, California 95616 jawdat@ucdavis.edu
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Issue 27
Keywords X-ray crystallography
microtubule
microtubule-associated protein (MAP)
tubulin
meiosis
mitosis
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License 2018 by The American Society for Biochemistry and Molecular Biology, Inc.
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Snippet The reorganization of microtubules in mitosis, meiosis, and development requires the microtubule-severing activity of katanin. Katanin is a heterodimer...
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SubjectTerms Adenosine Triphosphatases - chemistry
Adenosine Triphosphatases - metabolism
Animals
Caenorhabditis elegans - enzymology
Caenorhabditis elegans Proteins - chemistry
Caenorhabditis elegans Proteins - metabolism
Crystallography, X-Ray
Humans
Katanin - chemistry
Katanin - metabolism
Meiosis
Microtubules
Protein Conformation
Protein Multimerization
Spindle Apparatus
Title Structural basis for disassembly of katanin heterododecamers
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