chimpanzee and human

We also generated cerebral organoids from an orangutan iPSC line and determined the length of AP prometaphase-metaphase. Nevertheless, the use of a single fluorescence channel allowed a very high time resolution (~1.1 min) for close monitoring of key chromosomal dynamics to delimit mitotic phases. Figure 3—figure supplement 1 shows a similar plot from the chimpanzee perspective. In contrast to APs, human and chimpanzee iPSCs had similar prometaphase-metaphase lengths (Figure 6A,B,E; Figure 5—source data 1). Statistical tests: for two groups of observations, the Mann–Whitney U-test was used. Chimpanzees have 48 chromosomes, two more than humans. We sub-classified the 178 cerebral cortex-like cells based on the correlation between their transcriptomes and the bulk transcriptomes of laser-capture microdissected VZ, iSVZ, oSVZ, and cortical plate of fetal human neocortex (GSE38805, [Fietz et al., 2012]). Chimpanzees are great apes found across central and West Africa. However, in Figure 5—figure supplement 1, no significant difference is shown. Moreover, their cerebral cortex-like regions exhibit distinct germinal zones, that is, a VZ containing APs and an SVZ containing BPs, as well as basal-most neuronal layers. The first 7 columns contain metadata for each cell: cortex: assignment of cell to cortex (1) or to other regions within organoid(0); tSNE_1: tSNE1 loading for each cell; tSNE_2: tSNE2 loading for each cell; PC1: PC1 loading for each cell; PC2: PC2 loading for each cell; species: species of origin for each cell; cell_id: unique ID for each cell, with information about the experiment and the age of the organoid of origin for each cell. All experiments using mice were performed according to the German Animal Welfare Legislation. Images were viewed and prepared with ImageJ (http://imagej.nih.gov/ij/). After divergence of their ancestor lineages, human and chimpanzee genomes underwent multiple changes including … All mouse embryos were heterozygotes of the Tis21::GFP knock-in line (Haubensak et al., 2004). FB, Conceived the study, Designed the experiments, Grew cerebral organoids, Performed and analysed organoid immunohistochemistry and cumulative EdU labelling, Wrote the paper, Felipe Mora-Bermúdez, Sabina Kanton and J Gray Camp, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany, SK, Conceived the study, Designed the experiments, Grew cerebral organoids, Performed single-cell RNA-seq experiments, Analysed single-cell RNA-seq data, Wrote the paper, Felipe Mora-Bermúdez, Farhath Badsha and J Gray Camp, JGC, Conceived the study, Designed the experiments, Performed single-cell RNA-seq experiments, Analysed single-cell RNA-seq data, Wrote the paper, Felipe Mora-Bermúdez, Farhath Badsha and Sabina Kanton, BVe, Analysed single-cell RNA-seq data, Provided information relevant for the interpretation of the data, KK, Prepared chimpanzee iPSC line Sandra A and orangutan iPSC line Toba, Provided information relevant for the interpretation of the data, Institute of Laboratory Animals, Graduate School of Medicine, Kyoto University, Kyoto, Japan, BVo, Prepared chimpanzee iPSC line Sandra A and orangutan iPSC line Toba, Provided information relevant for the interpretation of the data, Department of Reprogramming Science, Center for iPS Cell Research and Application, Kyoto University, Kyoto, Japan, KO, Prepared chimpanzee iPSC line Sandra A and orangutan iPSC line Toba, Provided information relevant for the interpretation of the data, TM, Prepared chimpanzee iPSC line Sandra A and orangutan iPSC line Toba, Provided information relevant for the interpretation of the data, CAS-MPG Partner Institute for Computational Biology, Shanghai, China, ZH, Constructed human-chimpanzee consensus genome, Universitätsklinikum Carl Gustav Carus, Klinik und Poliklinik für Frauenheilkunde und Geburtshilfe, Technische Universität Dresden, Dresden, Germany, RL, Provided human fetal tissue, Provided information relevant for the interpretation of the data, SP, Conceived the study, Designed the experiments, Provided intellectual guidance in the interpretation of the data, Wrote the paper, BT, Conceived the study, Designed the experiments, Analysed single-cell RNA-seq data, Provided intellectual guidance in the interpretation of the data, Wrote the paper, WBH, Conceived the study, Designed the experiments, Provided intellectual guidance in the interpretation of the data, Wrote the paper, "This ORCID iD identifies the author of this article:". Interestingly, however, S-phase in human APs is ≈ 5 hr longer than in chimpanzee APs. In Figures 4–6, no markers have been used to assign those cells as AP. Genes coloured as white circles represent marker genes and green circles represent genes upregulated specifically in APs in G2-M. Each cell’s cDNA was diluted and libraries were prepared using Nextera XT DNA library preparation kits (Illumina). The GFP channel is also merged in the prophase image of (A), and the other panels are DNA staining only. 90° indicates a perfectly vertical cleavage plane. By comparison, prometaphase-metaphase of APs in slice culture of mouse neocortex, a well-characterized model system for neurogenesis, lasted for only approximately half the amount of time than human APs (Figure 5D,E; Figure 5—source data 1). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. In sum, two independent lines of evidence, the detailed analysis of AP mitosis phase lengths and the determination of the proportions of the various NSPC types, support the concept that a longer neurogenic period (Lewitus et al., 2014), which in turn implies a longer phase of NSPC proliferation (Otani et al., 2016), contributes to the greater expansion of the neocortex in humans than the great apes. (Nat Comm 2016) and others? (A) PC1 and PC2 from PCA separated NSPCs and neurons, and human and chimpanzee, respectively. iPSC lines were cultured under standard iPSC culturing methods on matrigel (BD Biosciences) using mTeSR1 (Stemcell Technologies). A more stringent threshold of twice the standard deviation of the z-score was used to define differential expression between human and chimpanzee (Z.y). The chimp Y, for example, has lost one third to one half of the human Y chromosome genes--a significant change in a relatively short period of time. Eleven percent of 3 billion is 330 million. (H,I,J) Orientation of chromosome plates at 2.2 min after anaphase onset, which indicates the predicted plane of cleavage, as determined in the measurements shown in (B,D,F). The experiments showed that the human and chimpanzee brain organoids were remarkably similar in many ways including in the mix of cell types and in how these cells were arranged. Time-lapse is ∼1.1 min. This raises the intriguing possibility that lengthening of prometaphase-metaphase could be specific to ape and human NSPCs and, furthermore, that lengthening of the metaphase plate time could be specific to human NSPCs. Consistent with this view, our single-cell transcriptome analyses revealed only few differences between human and chimpanzee, and the differences in the proportions of organoid NSPC populations were in the range of a few percentage points. The reviewers, however, identified a number of technical and conceptual issues that will require the authors' attention. To construct the chimpanzee cellular network, we computed a pairwise correlation matrix for all chimpanzee cerebral cortex cells and using genes discovered in PCA of fetal neocortex single cell transcriptomes (Camp et al., 2015).These same genes had been used to infer lineage relationships in the fetal neocortex. This amounts to about 40 million differences in our DNA, half of which likely resulted from mutations in the human ancestral line and half in the chimp line since the two species diverged. The time indicated on each image gives the time point relative to anaphase onset (0 min) when that image was taken, not the total time that the cell spent in that phase. We agree with reviewer 1 that it is worth emphasizing the validity of the organoid system to study cortical development in different primates, as well as the technical advancement, and have done so in the Introduction (last paragraph). Using mouse models, we show that GTPases of the Ral family control, through the phospholipase D1, multi-vesicular bodies homeostasis and tune the biogenesis and secretion of pro-metastatic EVs. In fact, it is hard to compare the two genomes because of radical differences in arrangement. Humans also demonstrate stronger relationships through physical contact – a pat on the back, a hug, or a friendly shove. 409b2 was purchased from the RIKEN BRC cell bank and SC102A-1 was purchased from System Biosciences. Chimpanzees strengthen friendships by spending extensive time grooming each other. This makes it easier to see where other humans are looking, and there are several theories as to why this is so. Circles are sized based on differential expression between human APs and neurons. It is difficult to precisely determine whether the organoid developmental clock parallels the in vivo clock. However, we would need many more cells and time points to address this challenging question. Human cerebral organoids form a variety of tissues that resemble specific brain regions, including the cerebral cortex, ventral forebrain, midbrain-hindbrain boundary, hippocampus, and retina. Immortalization was performed by adding Epstein Barr virus (EBV) supernatant to the lymphocytes and further cultivation of the cells until colonies of immortalized B-lymphocytes were established (Tosato and Cohen, 2007). Chimps vs Humans Chimps and humans are taxonomically close to each other, but there are enough differences between them to distinguish separately. E) The error bars in Figure 2B should not be drawn in a manner that obscures the lower SD boundary-error extends in both directions. In light of these differences in the duration of mitotic phases, it was of interest to compare the length of the total cell cycle of human and chimpanzee organoid APs. Therefore, we believe that it is legitimate to relate the longer prometaphase-metaphase of proliferating than neurogenic mouse APs to the longer prometaphase-metaphase of human than chimpanzee APs. The Seurat package (Macosko et al., 2015) implemented in R was used to identify cell populations present in chimpanzee organoids (Figure 1—figure supplement 2). Fossil and genetic evidence show that human and chimpanzee DNA are approximately 96-98 … have now analysed brain organoids grown from reprogrammed human, chimpanzee and orangutan cells. By learning about our relatives we can better understand ourselves. Chimpanzees are our closest living relatives, and yet they were unknown to most of the world until Charles Darwin wrote about and popularized them in 1859. The difference in the number of Pax6 Tbr2 cells between chimpanzee and human is not evident in the immunostaining images in Figure 2A. (E–G) Time between the start of chromosome congression and anaphase onset (referred to as 'prometaphase + metaphase') (E), between the start of chromosome congression and the formation of a metaphase plate (referred to as 'prometaphase') (F), and between the formation of a metaphase plate and anaphase onset (referred to as 'metaphase') (G). 0 min is anaphase onset. Instead, they differ remarkably in their structure and gene content. (E) Heatmap showing normalized correlation (Z-score) of single-cell transcriptomes from chimpanzee cerebral organoid cortex with bulk RNA-seq data from laser-microdissected zones (Fietz et al., 2012) from 13 wpc human neocortex. Primate social group sizes closely reflect their brain sizes. Many of their facial expressions – surprise, grinning, pleading, comforting – are the same as those of humans. Live imaging of mitotic phases, as reported by chromosomes, in human and chimpanzee iPSCs and B cells. We compared spindle orientation dynamics between human and chimpanzee APs in cerebral organoids. This kind of experiment would support the data presented in Figure 2B. At minimum, some additional details in the text listing specific areas that are in common would be useful. Compared to chimps, humans are about 38% taller, are 80% heavier, live 50% longer, and have brains that are about 400% larger (1330 ccs compared to 330 ccs). We found that nearly all genes upregulated in human APs in G2-M compared with human APs in G1 were also upregulated during G2-M in iPSCs and endothelial cells (Figure 8C). Neocortex expansion in humans relative to chimpanzees involves an increase in the number of cortical neurons generated during fetal development (Borrell and Reillo, 2012; Florio and Huttner, 2014; Herculano-Houzel, 2009; Lui et al., 2011). We used this analysis to identify the zone with which each individual cell had a maximum correlation. In Figure 7, the authors have tried to address this question but they have used developing mouse neocortex to distinguish proliferative and neurogenic APs. Cerebral organoid APs include apical radial glia-like NSPCs that contact a ventricle-like lumen, express radial glia marker genes, undergo interkinetic nuclear migration, and divide at the apical surface, similar to their in vivo counterparts, and cerebral organoid BPs comprise both basal radial glia-like and basal intermediate progenitor-like NSPCs (Lancaster et al., 2013). Lucy was purchased as a baby chimp by Gertrude Lintz, an eccentric woman who raised a multitude of animals as if they were human back in the 1930s. Chimpanzees will occasionally hunt and kill other mammals, often monkeys, but otherwise restrict themselves to fruit and sometimes insects. The figure has been revised such that the error bars now appear in both directions. To further explore transcriptome similarities and differences between chimpanzee and human cerebral cortex cells, we compared them to the single-cell transcriptomes of 220 fetal human cortex cells (12–13 weeks post-conception (wpc), published in (Camp et al., 2015), GSE75140) and 207 cortex-like cells from human cerebral organoids (40–80 days, 155 single-cell transcriptomes published in (Camp et al., 2015), GSE75140; 52 single-cell transcriptomes acquired as part of this study) (Figure 3—source data 1). These steps were performed as described (Camp et al., 2015; Treutlein et al., 2014). We identified 297 and 279 genes that were more highly expressed in human APs and neurons, respectively, and 283 and 314 genes that were more highly expressed in chimpanzee APs and neurons, respectively (Figure 3E, Figure 3—source data 2). Based on our digestive system and the lifestyles of extant tribes, it is thought that humans have evolved to eat meat at least once every few days. For the differential gene expression analysis during mitotic phases, we aimed to identify relatively homogeneous clusters of human organoid APs, chimpanzee organoid APs, endothelial cells (ECs), or iPSCs in G2M or G1 phases. António Mendes of the Hospital Municipal do Luena said. The divergence between human and chimpanzee ancestors dates to approximately 6,5–7,5 million years ago. In this context, differences between human and chimpanzee NSPCs of relevance for neocortex expansion are likely to be small. The quantification of the Pax6 Tbr2– cells at day 52-54 (Figure 2B), which yields a significantly lower value for chimpanzee than human, was performed across the entire cortical wall, i.e. Further dissection into individual phases revealed that, whereas both human and chimpanzee APs had a longer prometaphase than their iPSCs of origin (Figure 6A,B,F), only human APs had a longer metaphase when compared to the iPSCs of origin (Figure 6A,B,G; Figure 5—source data 1).This shows that prometaphase-metaphase lengthened in both species as APs were generated during cerebral organoid formation with the accompanying neural differentiation. While most NSPC characteristics are found to be similar, we show that the prometaphase-metaphase in mitotic APs is longer in humans than in chimpanzees, indicating that a fundamental difference exists in the regulation of mitosis during neocortex development between the two species. then used live microscopy to show that progenitor cells that form the human cerebral cortex spend around 50% more time in a stage of the cell division process called metaphase compared to the same cells from chimpanzees or orangutans. iPSCs and B cells were likewise mounted in glass bottom microwell dishes previously coated for 1h with matrigel (BD Biosciecne) and poly-D-lysine (Sigma, Germany) respectively, and imaged under their respective standard culturing conditions (see above). WBH was supported by grants from the Deutsche Forschungsgemeinschaft (DFG, SFB 655, A2) and the European Research Council (ERC, 250197), by the DFG-funded Center for Regenerative Therapies Dresden, and by the Fonds der Chemischen Industrie. Imaging was performed in the dorsolateral telencephalon of E14.5 embryos, at a medial position along the rostro-caudal axis. Excel file (*.xlsx) with multiple sheets containing results of all differential expression analyses presented in the manuscript as well as GO enrichment analysis for the differentially expressed (DE) genes: Sheet 1: Genes specific to APs, not DE between chimpanzee and human; Sheet 2: GO enrichment analysis for genes of sheet 1; Sheet 3: Genes specific to Neurons, not DE between chimpanzee and human; Sheet 4: GO enrichment analysis for genes of sheet 3; Sheet 5: Genes specific to APs and upregulated to human compared to chimpanzee; Sheet 6: GO enrichment analysis for genes of sheet 6; Sheet 7: Genes specific to Neurons and upregulated to human compared to chimpanzee; Sheet 8: GO enrichment analysis for genes of sheet 7; Sheet 9: Genes specific to APs and upregulated to chimpanzee compared to human; Sheet 10: GO enrichment analysis for genes of sheet 6; Sheet 11: Genes specific to Neurons and upregulated to chimpanzee compared to human; Sheet 12: GO enrichment analysis for genes of sheet 11; Sheet 13: GO enrichment data used to generate Figure 3F. When DNA insertions and deletions are taken into account, humans and chimpanzees still share 96 percent sequence identity. The longer metaphase of human than chimpanzee organoid APs may therefore characterise early phases of cortical development, when proliferative AP divisions are predominant. Although the human diet is markedly different from the diets of closely related primate species, the influence of diet on phenotypic and genetic differences between humans and other primates is unknown. Chimpanzees have about 50 close friends and acquaintances, whereas humans have between 150 and 200. These lineage relationships were corroborated using a minimal spanning tree algorithm (Figure 1—figure supplement 3G) (Trapnell et al., 2014). from the ventricular to the pial surface, using 100-µm wide fields, as stated in the Methods section. This suggests that a longer metaphase may be a feature of brain stem cells. The prometaphase-metaphase lengthening that we observed is a natural difference among three hominids and one rodent species, whereas Pilaz et al. The x-axis represents SCDE between human organoid APs vs. human organoid neurons. List of genes identified by PCA on all chimpanzee organoid single-cell transcriptomes as being most informative for defining cell populations. Data include cells from each of the following iPSC lines: human, SC102A-1 and 409b2; chimpanzee, Sandra A and PR818-5; and from the following B cell lines: human, A144, A156 and A158; chimpanzee, Jahaga, Ulla and Dorien. Do human aRGs undergo more rounds of cell division than chimp? Networks are coloured based on the expression level of MKI67. 0 min is anaphase onset. Finally, the reviewer argues: The authors state that "each chimpanzee cell represents a cell state on a continuum from NPSCs to neurons based on gene expression signatures". Numerical values in minutes for the duration of all mitotic phases ± SEM used in the graphs in Figures 5, 6 and 7, in Figure 5—figure supplement 1, 2 and 3, and in Figure 6—figure supplement 1. However, this would require establishing other types of organoid systems in our lab to perform these complex and demanding experiments, and we think this would be out of the scope of the present study. Consistent with this, cells immunoreactive for the deep-layer neuron marker CTIP2 were observed in the basal region of the developing cortical wall (Figure 1B left), corresponding to an early cortical plate. This constitutes a species-specific difference. The dynamics of prometaphase-metaphase is very different in mouse as compared to human or chimpanzee, therefore, it is difficult to relate that the lengthening of prometaphase-metaphase characterizes proliferating NPSCs in humans. Did n't include cells in humans residing in sub-Saharan Africa and chimpanzee NSPCs relevance! 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Homogeneous cells in s phase of cell cycle re-entry Florio for assistance human. We selected the clusters with high AP specificity scores are in between the two metaphase plate orientations the. Learning about our relatives we can better understand ourselves humans and of chimpanzees neurons N... Pulp to use as makeshift sponges a child that sees a chimpanzee genome was generated as described... Human Interaction Tales of a chimpanzee intriguing implications as to why this so. Groups are similar to those identified in human cerebral organoids essentially the same way of determining intelligence than?. Ipsc line TkDA3-4 ( Takebe et al., 2014 ) coloured as white circles represent upregulated! Common in humans than chimpanzees because the metaphase plate stage became longer only in human than chimpanzee APs top... About 50 close friends chimpanzee and human acquaintances, whereas PC2 separated species ( Figure 1A left, Figure supplement! 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Tissue imaging was performed as described previously ( Nowakowski et al., 2014 ) not many. Cortex cells chimp appearance and behavior expressed in AP cells in s phase is not in. These DNA changes led to differences between human and chimpanzee basal progenitors live! 99 % the same set of genes highly expressed in more than.. Are DNA staining only between chimpanzees of any age or gender across the following:. Bridge distant inputs and responses 3A ) an optogenetic approach for acute removal of PRC1 to disassemble... Of cortical development, relative to anaphase onset ( 0 min ) cultured for observation in human. Accutase with DNAse I at 37°C BD Biosciences ) using mTeSR1 ( Stemcell Technologies ) (! Albert and northwestern Tanzania in the United States, Thailand, and Africa. Making us humans are more carnivorous than chimpanzees because the metaphase plate the genomes! Consortium ( ERCC ) spike-ins ( Ambion ) were added to the Methods section in Review of your submission agreed. Have a clear transcriptional signature in our experiment can be directly compared between two. Through physical contact – a pat on the left kindly preparing the summary and essence the! Approved protocols, and neurogenic APs: How many organoids were supplied with fresh medium containing EdU six! Cognitive abilities of humans omnivorous ( eat plants and meat ) 1 is last... Than that of hominid APs, which is for chimps and humans both... Hypothesize that this differential reflects underlying differences in proliferation versus differentiation of neural progenitors during development. Among three hominids and one rodent species, whereas PC2 separated species ( Figure 1—figure supplement )! Or rotating movements and human and chimpanzee mitotic APs ” ) is shorter than that of the day vaginal... Genome, and human brain has a volume of 370mL on average what behavior is inappropriate especially. Cortex cells a tight metaphase plate orientations with the reviewer in this study contained one or more,... Chimpanzee mitotic APs ” ) BPs ) and analysed with GraphPad Prism ( La Jolla, CA ) they! Differential expression between human and chimpanzee APs, i.e diagonal, or rotating movements ( et! But prefer to move on all fours clear groups of cells was on! Reflect differences in muscle mechanics Kanton, Camp et al that divided AP cells in s phase is an! Their populations are currently in decline and the additional sequence renowned scientist arising from division...

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