Ordered Kinetochore Assembly in the Human-Pathogenic Basidiomycetous Yeast <named-content content-type="genus-species">Cryptococcus neoformans</named-content>

ABSTRACT Kinetochores facilitate interaction between chromosomes and the spindle apparatus. The formation of a metazoan trilayered kinetochore is an ordered event in which inner, middle, and outer layers assemble during disassembly of the nuclear envelope during mitosis. The existence of a similar s...

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Autores principales:	Lukasz Kozubowski, Vikas Yadav, Gautam Chatterjee, Shreyas Sridhar, Masashi Yamaguchi, Susumu Kawamoto, Indrani Bose, Joseph Heitman, Kaustuv Sanyal
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/cd4feb7755014a05a1b56c61ae135b7d
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spelling	oai:doaj.org-article:cd4feb7755014a05a1b56c61ae135b7d2021-11-15T15:42:47ZOrdered Kinetochore Assembly in the Human-Pathogenic Basidiomycetous Yeast <named-content content-type="genus-species">Cryptococcus neoformans</named-content>10.1128/mBio.00614-132150-7511https://doaj.org/article/cd4feb7755014a05a1b56c61ae135b7d2013-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00614-13https://doaj.org/toc/2150-7511ABSTRACT Kinetochores facilitate interaction between chromosomes and the spindle apparatus. The formation of a metazoan trilayered kinetochore is an ordered event in which inner, middle, and outer layers assemble during disassembly of the nuclear envelope during mitosis. The existence of a similar strong correlation between kinetochore assembly and nuclear envelope breakdown in unicellular eukaryotes is unclear. Studies in the hemiascomycetous budding yeasts Saccharomyces cerevisiae and Candida albicans suggest that an ordered kinetochore assembly may not be evolutionarily conserved. Here, we utilized high-resolution time-lapse microscopy to analyze the localization patterns of a series of putative kinetochore proteins in the basidiomycetous budding yeast Cryptococcus neoformans, a human pathogen. Strikingly, similar to most metazoa but atypical of yeasts, the centromeres are not clustered but positioned adjacent to the nuclear envelope in premitotic C. neoformans cells. The centromeres gradually coalesce to a single cluster as cells progress toward mitosis. The mitotic clustering of centromeres seems to be dependent on the integrity of the mitotic spindle. To study the dynamics of the nuclear envelope, we followed the localization of two marker proteins, Ndc1 and Nup107. Fluorescence microscopy of the nuclear envelope and components of the kinetochore, along with ultrastructure analysis by transmission electron microscopy, reveal that in C. neoformans, the kinetochore assembles in an ordered manner prior to mitosis in concert with a partial opening of the nuclear envelope. Taken together, the results of this study demonstrate that kinetochore dynamics in C. neoformans is reminiscent of that of metazoans and shed new light on the evolution of mitosis in eukaryotes. IMPORTANCE Successful propagation of genetic material in progeny is essential for the survival of any organism. A proper kinetochore-microtubule interaction is crucial for high-fidelity chromosome segregation. An error in this process can lead to loss or gain of chromosomes, a common feature of most solid cancers. Several proteins assemble on centromere DNA to form a kinetochore. However, significant differences in the process of kinetochore assembly exist between unicellular yeasts and multicellular metaozoa. Here, we examined the key events that lead to formation of a proper kinetochore in a basidiomycetous budding yeast, Cryptococcus neoformans. We found that, during the progression of the cell cycle, nonclustered centromeres gradually clustered and kinetochores assembled in an ordered manner concomitant with partial opening of the nuclear envelope in this organism. These events have higher similarity to mitotic events of metazoans than to those previously described in other yeasts.Lukasz KozubowskiVikas YadavGautam ChatterjeeShreyas SridharMasashi YamaguchiSusumu KawamotoIndrani BoseJoseph HeitmanKaustuv SanyalAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 5 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Lukasz Kozubowski Vikas Yadav Gautam Chatterjee Shreyas Sridhar Masashi Yamaguchi Susumu Kawamoto Indrani Bose Joseph Heitman Kaustuv Sanyal Ordered Kinetochore Assembly in the Human-Pathogenic Basidiomycetous Yeast <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
description	ABSTRACT Kinetochores facilitate interaction between chromosomes and the spindle apparatus. The formation of a metazoan trilayered kinetochore is an ordered event in which inner, middle, and outer layers assemble during disassembly of the nuclear envelope during mitosis. The existence of a similar strong correlation between kinetochore assembly and nuclear envelope breakdown in unicellular eukaryotes is unclear. Studies in the hemiascomycetous budding yeasts Saccharomyces cerevisiae and Candida albicans suggest that an ordered kinetochore assembly may not be evolutionarily conserved. Here, we utilized high-resolution time-lapse microscopy to analyze the localization patterns of a series of putative kinetochore proteins in the basidiomycetous budding yeast Cryptococcus neoformans, a human pathogen. Strikingly, similar to most metazoa but atypical of yeasts, the centromeres are not clustered but positioned adjacent to the nuclear envelope in premitotic C. neoformans cells. The centromeres gradually coalesce to a single cluster as cells progress toward mitosis. The mitotic clustering of centromeres seems to be dependent on the integrity of the mitotic spindle. To study the dynamics of the nuclear envelope, we followed the localization of two marker proteins, Ndc1 and Nup107. Fluorescence microscopy of the nuclear envelope and components of the kinetochore, along with ultrastructure analysis by transmission electron microscopy, reveal that in C. neoformans, the kinetochore assembles in an ordered manner prior to mitosis in concert with a partial opening of the nuclear envelope. Taken together, the results of this study demonstrate that kinetochore dynamics in C. neoformans is reminiscent of that of metazoans and shed new light on the evolution of mitosis in eukaryotes. IMPORTANCE Successful propagation of genetic material in progeny is essential for the survival of any organism. A proper kinetochore-microtubule interaction is crucial for high-fidelity chromosome segregation. An error in this process can lead to loss or gain of chromosomes, a common feature of most solid cancers. Several proteins assemble on centromere DNA to form a kinetochore. However, significant differences in the process of kinetochore assembly exist between unicellular yeasts and multicellular metaozoa. Here, we examined the key events that lead to formation of a proper kinetochore in a basidiomycetous budding yeast, Cryptococcus neoformans. We found that, during the progression of the cell cycle, nonclustered centromeres gradually clustered and kinetochores assembled in an ordered manner concomitant with partial opening of the nuclear envelope in this organism. These events have higher similarity to mitotic events of metazoans than to those previously described in other yeasts.
format	article
author	Lukasz Kozubowski Vikas Yadav Gautam Chatterjee Shreyas Sridhar Masashi Yamaguchi Susumu Kawamoto Indrani Bose Joseph Heitman Kaustuv Sanyal
author_facet	Lukasz Kozubowski Vikas Yadav Gautam Chatterjee Shreyas Sridhar Masashi Yamaguchi Susumu Kawamoto Indrani Bose Joseph Heitman Kaustuv Sanyal
author_sort	Lukasz Kozubowski
title	Ordered Kinetochore Assembly in the Human-Pathogenic Basidiomycetous Yeast <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
title_short	Ordered Kinetochore Assembly in the Human-Pathogenic Basidiomycetous Yeast <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
title_full	Ordered Kinetochore Assembly in the Human-Pathogenic Basidiomycetous Yeast <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
title_fullStr	Ordered Kinetochore Assembly in the Human-Pathogenic Basidiomycetous Yeast <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
title_full_unstemmed	Ordered Kinetochore Assembly in the Human-Pathogenic Basidiomycetous Yeast <named-content content-type="genus-species">Cryptococcus neoformans</named-content>
title_sort	ordered kinetochore assembly in the human-pathogenic basidiomycetous yeast <named-content content-type="genus-species">cryptococcus neoformans</named-content>
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/cd4feb7755014a05a1b56c61ae135b7d
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Ordered Kinetochore Assembly in the Human-Pathogenic Basidiomycetous Yeast <named-content content-type="genus-species">Cryptococcus neoformans</named-content>

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