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Ordered kinetochore assembly in the human-pathogenic basidiomycetous yeast Cryptococcus neoformans.

Publication ,  Journal Article
Kozubowski, L; Yadav, V; Chatterjee, G; Sridhar, S; Yamaguchi, M; Kawamoto, S; Bose, I; Heitman, J; Sanyal, K
Published in: mBio
October 1, 2013

UNLABELLED: 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.

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Published In

mBio

DOI

EISSN

2150-7511

Publication Date

October 1, 2013

Volume

4

Issue

5

Start / End Page

e00614 / e00613

Location

United States

Related Subject Headings

  • Mitosis
  • Kinetochores
  • Humans
  • Fungal Proteins
  • Cryptococcus neoformans
  • Cryptococcosis
  • Chromosomes, Fungal
  • 3207 Medical microbiology
  • 3107 Microbiology
  • 3101 Biochemistry and cell biology
 

Citation

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ICMJE
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Kozubowski, L., Yadav, V., Chatterjee, G., Sridhar, S., Yamaguchi, M., Kawamoto, S., … Sanyal, K. (2013). Ordered kinetochore assembly in the human-pathogenic basidiomycetous yeast Cryptococcus neoformans. MBio, 4(5), e00614–e00613. https://doi.org/10.1128/mBio.00614-13
Kozubowski, Lukasz, Vikas Yadav, Gautam Chatterjee, Shreyas Sridhar, Masashi Yamaguchi, Susumu Kawamoto, Indrani Bose, Joseph Heitman, and Kaustuv Sanyal. “Ordered kinetochore assembly in the human-pathogenic basidiomycetous yeast Cryptococcus neoformans.MBio 4, no. 5 (October 1, 2013): e00614–e00613. https://doi.org/10.1128/mBio.00614-13.
Kozubowski L, Yadav V, Chatterjee G, Sridhar S, Yamaguchi M, Kawamoto S, et al. Ordered kinetochore assembly in the human-pathogenic basidiomycetous yeast Cryptococcus neoformans. mBio. 2013 Oct 1;4(5):e00614–e00613.
Kozubowski, Lukasz, et al. “Ordered kinetochore assembly in the human-pathogenic basidiomycetous yeast Cryptococcus neoformans.MBio, vol. 4, no. 5, Oct. 2013, pp. e00614–e00613. Pubmed, doi:10.1128/mBio.00614-13.
Kozubowski L, Yadav V, Chatterjee G, Sridhar S, Yamaguchi M, Kawamoto S, Bose I, Heitman J, Sanyal K. Ordered kinetochore assembly in the human-pathogenic basidiomycetous yeast Cryptococcus neoformans. mBio. 2013 Oct 1;4(5):e00614–e00613.

Published In

mBio

DOI

EISSN

2150-7511

Publication Date

October 1, 2013

Volume

4

Issue

5

Start / End Page

e00614 / e00613

Location

United States

Related Subject Headings

  • Mitosis
  • Kinetochores
  • Humans
  • Fungal Proteins
  • Cryptococcus neoformans
  • Cryptococcosis
  • Chromosomes, Fungal
  • 3207 Medical microbiology
  • 3107 Microbiology
  • 3101 Biochemistry and cell biology