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Toxoplasma Gondii Sequesters Centromeres to a Specific Nuclear Toxoplasma gondii sequesters centromeres to a specific nuclear region throughout the cell cycle Carrie F. Brooksa, Maria E. Franciab, Mathieu Gissotc,d,1, Matthew M. Crokenc,d, Kami Kimc,d,2, and Boris Striepena,b,2 aCenter for Tropical and Emerging Global Diseases and bDepartment of Cellular Biology, University of Georgia, Athens, GA 30602; and Departments of cMedicine and dMicrobiology and Immunology, Albert Einstein College of Medicine, Bronx, NY 10461 Edited by Thomas E. Wellems, National Institutes of Health, Bethesda, MD, and approved January 20, 2011 (received for review May 24, 2010) Members of the eukaryotic phylum Apicomplexa are the cause of testine (6). The molecular mechanisms that regulate apicomplexan important human diseases including malaria, toxoplasmosis, and cell division and allow this remarkable flexibility of the cell and cryptosporidiosis. These obligate intracellular parasites produce nuclear division cycle remain poorly understood (7). An important new invasive stages through a complex budding process. The bud- unsolved question is how apicomplexan daughter cells emerge ding cycle is remarkably flexible and can produce varied numbers of with the complete set of chromosomes (∼10 depending on species) progeny to adapt to different host-cell niches. How this complex after passing through multinucleated and polyploid stages. In process is coordinated remains poorly understood. Using Toxo- Sarcocystis neurona the mitotic spindle persists throughout the plasma gondii as a genetic model, we show that a key element to cell cycle, and small monopolar spindles housed in a specialized this coordination is the centrocone, a unique elaboration of the nu- elaboration of the nuclear envelope, the centrocone, are evident clear envelope that houses the mitotic spindle. Exploiting transgenic throughout interphase (8). More recent work in T. gondii identi- parasite lines expressing epitope-tagged centromeric H3 variant fied a molecular marker for the centrocone, the repeat protein CenH3, we identify the centromeres of T. gondii chromosomes by membrane occupation and recognition nexus protein 1 (MORN1) hybridization of chromatin immunoprecipitations to genome-wide (9, 10) that is found in a variety of apicomplexan species repre- microarrays (ChIP-chip). We demonstrate that centromere attach- senting all three cell-division modes (11). ment to the centrocone persists throughout the parasite cell cycle Based on these observations, we speculated that apicomplexan and that centromeres localize to a single apical region within the chromosomes remain permanently attached to the centrocone nucleus. Centromere sequestration provides a mechanism for the throughout the cell cycle and that this physical tethering provides organization of the Toxoplasma nucleus and the maintenance of a critical means to maintain genome integrity (2). We directly genome integrity. tested the tethering hypothesis by developing a marker to visu- alize the centromeres of apicomplexan chromosomes. We used an histone | mitosis epitope-tagged T. gondii centromeric histone 3 variant (CenH3) to identify the centromeres of T. gondii chromosomes and sub- embers of the ancient eukaryotic phylum Apicomplexa are sequently studied the interaction of centromeres and the unique Mresponsible for numerous important human and animal centrocone structure throughout the T. gondii cell cycle. diseases, including malaria and toxoplasmosis. Apicomplexa are obligate intracellular parasites, and the infection is spread from Results and Discussion cell to cell by a motile stage (1). Host-cell invasion results in the Identification of the T. gondii CenH3. The biology of apicomplexan formation of a parasitophorous vacuole in which the parasites chromosomes remains poorly understood. In contrast to most typically reside and develop (some species escape from the initial eukaryotic organisms, chromosomes in Apicomplexa show only vacuole into the host-cell cytoplasm). With few exceptions, par- limited condensation during mitosis, thus complicating chromo- asite replication is confined to the intracellular phase of the some visualization. Chromosome segregation occurs through en- lifecycle. The timing and extent of replication is matched to the domitosis using an intranuclear spindle with the nuclear envelope varied size and biology of the host cell, and the number of progeny remaining intact (12–15). To develop a molecular marker for the can vary from two to thousands. At the core of this flexibility is the centromere of T. gondii chromosomes, we characterized CenH3 budding mechanism by which Apicomplexa replicate. This com- (also referred to as “CenpA”). In most eukaryotes CenH3 replaces plex process encompasses mitosis of the nucleus, assembly of the the canonical histone 3 in the nucleosomes of centromeric DNA cytoskeletal and membrane elements that form the pellicle, and can be used to visualize the centromeres (16). Computational loading of the growing bud with organelles, and finally emergence analysis of the T. gondii genome reveals three putative histone H3 of fully formed new invasive daughters from the mother cell (2). genes. Genes TGME49_061240 and TGME49_018260 (toxodb.org Based on this underlying scheme, Apicomplexa have evolved version 6.2) appear to encode the canonical H3 and H3.3 variants three distinct cell-division types (Fig. S1A). Toxoplasma tachy- (17, 18). TGME49_025410 encodes an H3 protein with a unique zoites, featuring the simplest form, endodyogeny, bud into two 99-amino acid insertion at the N terminus (see multiple sequence daughters after each round of DNA replication (3). Plasmodium, the causative agent of malaria, divides by schizogony, whereby the cell proceeds through several rounds of DNA replication and Author contributions: C.F.B., M.E.F., M.G., K.K., and B.S. designed research; C.F.B., M.E.F., and M.G. performed research; C.F.B., M.E.F., M.G., M.M.C., K.K., and B.S. analyzed data; mitosis before the now multinucleate schizont gives rise to mul- and M.G., K.K., and B.S. wrote the paper. tiple zoites at once (4). Sarcocystis, a widespread tissue parasite of The authors declare no conflict of interest. MICROBIOLOGY mammals, uses endopolygeny (5). In this division mode, multiple rounds of DNA replication occur without nuclear division, and This article is a PNAS Direct Submission. upon budding the large polyploid nucleus is parceled out in Data deposition: The microarray data reported in this paper have been deposited in the Toxoplasma Genomics Resource database, http://www.toxodb.org. multiple daughters. 1Present address: Center for Infection and Immunity of Lille, Unité Mixte de Recherche Interestingly, these parasite species can switch from one division 8204, Centre National de la Recherche Scientifique, 59019 Lille, France. fi mode to another depending on the developmental stage, thus ne- 2To whom correspondence may be addressed. E-mail: [email protected] or tuning replication to different tissue and host-cell environments. [email protected]. For example, Toxoplasma gondii replicates by endodyogeny in in- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. termediate hosts but replicates by schizogony within the cat in- 1073/pnas.1006741108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1006741108 PNAS | March 1, 2011 | vol. 108 | no. 9 | 3767–3772 Downloaded by guest on September 29, 2021 alignment in Fig. S1B). N-terminal extensions are a hallmark of nome. As a control, we immunoprecipitated and hybridized CenH3 (19). chromatin associated with the canonical H3 variant (23). To validate these assignments, the coding sequence of each H3 As shown in Fig. 2A, we detected significant hybridization of gene was amplified from T. gondii mRNA, cloned into a plasmid the CenH3-HA ChIP to the genomic chip for 12 of the 14 chro- construct fused to a C-terminal YFP tag, and expressed in tachy- mosomes (see Materials and Methods for details on peak calling zoites. As expected, histones H3 and H3.3 label the entire nucleus (Fig. 1 A and B). TGME49_025410 showed faint labeling through- out the nucleus in addition to a more intense spot (Fig. 1C). We were unable to establish stable transformants for this gene using the plasmid constructs driving expression of the CenH3-YFP cassette or a CenH3-HA cassette. Expression of the transgene from these plasmids was driven by the strong α-tubulin promoter, and it seemed likely that inappropriate strength or timing of ex- pression was detrimental to the parasite, as described for CenH3 overexpression in other organisms (20). To provide appropriate expression, we introduced an epitope- tagging cassette into a genomic TgCenH3 locus cosmid clone by recombineering (21) and established stable clonal T. gondii TgCenH3-HA lines. When these parasites were subjected to im- munofluorescence assays using an HA-specific antibody, a single nuclear spot was evident (Fig. 1D). PCR and Southern analysis of genomic DNA from these clones revealed a single nonhomologous insertion of the modified cosmid into the parasite genome, and Western blot of protein extracts indicated the presence of a tagged protein of appropriate size (Fig. 1 E and F). Identification of Toxoplasma Centromeres by ChIP and Microarray Analysis. The T. gondii genome is distributed into 14 chromosomes (22). CenH3 staining typically shows multiple foci reflecting the number of chromosomes (16). It therefore was surprising to ob- serve a single TgCenH3-positive spot. To confirm the localization of TgCenH3 to the centromeres, we determined
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