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Article ; Online: Cardiac differentiation of chimpanzee induced pluripotent stem cell lines with different subspecies backgrounds.

Takahi, Mika / Hamazaki, Yusuke / Ohnuma, Kiyoshi / Imamura, Masanori

In vitro cellular & developmental biology. Animal

2024

Abstract: The comparative analysis between humans and non-human primates is an instrumental approach for elucidating the evolutional traits and disease propensity of humans. However, in primates, cross-species analyses of their developmental events have ... ...

Abstract	The comparative analysis between humans and non-human primates is an instrumental approach for elucidating the evolutional traits and disease propensity of humans. However, in primates, cross-species analyses of their developmental events have encountered constraints because of the ethical and technical limitations in available sample collection, sequential monitoring, and manipulations. In an endeavor to surmount these challenges, in recent years, induced pluripotent stem cells (iPSCs) have garnered escalating interest as an in vitro tool for cross-species analyses between humans and non-human primates. Meanwhile, compared to humans, there is less information on in vitro differentiation of non-human primate iPSCs, and their genetic diversity including subspecies may cause different eligibility to in vitro differentiation methods. Therefore, antecedent to embarking on a comparative analysis to humans, it is a prerequisite to develop the efficacious methodologies for in vitro differentiation regardless of the intraspecies genetic background in non-human primates. In this study, we executed the in vitro differentiation of cardiomyocytes from four chimpanzee iPSC lines with different subspecies and individual backgrounds. To induce cardiomyocytes from chimpanzee iPSCs, we evaluated our methodology for in vitro cardiac differentiation of human iPSCs. Eventually, with minor alterations, our cardiac differentiation method was applicable to all chimpanzee iPSC lines tested as assessed by the expression of cardiac marker genes and the beating ability. Hence, our in vitro differentiation method will advance iPSC-based research of chimpanzee cardiac development and also hold possible utility to cross-species analyses among primate species.
Language	English
Publishing date	2024-05-16
Publishing country	Germany
Document type	Journal Article
ZDB-ID	1077810-x
ISSN	1543-706X ; 0883-8364 ; 1071-2690
ISSN (online)	1543-706X
ISSN	0883-8364 ; 1071-2690
DOI	10.1007/s11626-024-00914-2
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Article ; Online: Early neurogenic properties of iPSC-derived neurosphere formation in Japanese macaque monkeys.

Nakai, Risako / Hamazaki, Yusuke / Ito, Haruka / Imamura, Masanori

Differentiation; research in biological diversity

2022 Volume 128, Page(s) 33–42

Abstract: Non-human primates are important models for investigations of neural development and evolution, and the use of Japanese macaque monkeys has especially contributed to the advancement of neuroscience studies. However, these studies are restricted by the ... ...

Abstract	Non-human primates are important models for investigations of neural development and evolution, and the use of Japanese macaque monkeys has especially contributed to the advancement of neuroscience studies. However, these studies are restricted by the number of animals able to be evaluated and the invasiveness of the methodologies. Induced pluripotent stem cells (iPSCs) can provide an alternative strategy for investigating neural development in vitro. We have established direct neurosphere (dNS) formation cultures of primate iPSCs as an in vitro model of early neurodevelopment in primate species. Here, we used dNS formation and neuronal differentiation cultures established from Japanese macaque iPSCs (jm-iPSCs) to investigate the usefulness of these cells as an in vitro model of early neural development. Time-course analyses of developmental potency and gene expression kinetics were performed during dNS formation culture of jm-iPSCs. During a 1-week culture, jm-iPSC-derived dNSs became neurogenic by day 3 and underwent stepwise expression changes of key developmental regulators along early neural development in a similar manner to chimpanzee dNS formation previously reported. Meanwhile, a subset of genes, including CYP26A1 and NPTX1, showed differential expression propensity in Japanese macaque, chimpanzee, and human iPSC-derived dNSs. Spontaneous upregulation of NOTCH signaling-associated genes HES5 and DLL1 was also observed in neuronal differentiation cultures of Japanese macaque but not chimpanzee dNSs, possibly reflecting the earlier neurogenic competence in Japanese macaques. The use of jm-iPSCs provides an alternative approach to neurological studies of primate development. Furthermore, jm-iPSCs can be used to investigate species differences in early neural development that are key to primate evolution.
MeSH term(s)	Animals ; Induced Pluripotent Stem Cells ; Macaca fuscata/genetics ; Macaca ; Haplorhini ; Neurogenesis/genetics ; Cell Differentiation/genetics
Language	English
Publishing date	2022-10-14
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	184540-8
ISSN	1432-0436 ; 0301-4681
ISSN (online)	1432-0436
ISSN	0301-4681
DOI	10.1016/j.diff.2022.10.002
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Article ; Online: Generation of chimpanzee induced pluripotent stem cell lines for cross-species comparisons.

Imamura, Masanori / Nakai, Risako / Ohnuki, Mari / Hamazaki, Yusuke / Tanabe, Hideyuki / Sato, Momoka / Harishima, Yu / Horikawa, Musashi / Watanabe, Mao / Oota, Hiroki / Nakagawa, Masato / Suzuki, Shunsuke / Enard, Wolfgang

In vitro cellular & developmental biology. Animal

2024

Abstract: As humans' closest living relatives, chimpanzees offer valuable insights into human evolution. However, technical and ethical limitations hinder investigations into the molecular and cellular foundations that distinguish chimpanzee and human traits. ... ...

Abstract	As humans' closest living relatives, chimpanzees offer valuable insights into human evolution. However, technical and ethical limitations hinder investigations into the molecular and cellular foundations that distinguish chimpanzee and human traits. Recently, induced pluripotent stem cells (iPSCs) have emerged as a novel model for functional comparative studies and provided a non-invasive alternative for studying embryonic phenomena. In this study, we generated five new chimpanzee iPSC lines from peripheral blood cells and skin fibroblasts with SeV vectors carrying four reprogramming factors (human OCT3/4, SOX2, KLF4, and L-MYC) and characterized their pluripotency and differentiation potential. We also examined the expression of a human-specific non-coding RNA, HSTR1, which is predicted to be involved in human brain development. Our results show that the chimpanzee iPSCs possess pluripotent characteristics and can differentiate into various cell lineages. Moreover, we found that HSTR1 is expressed in human iPSCs and their neural derivatives but not in chimpanzee counterparts, supporting its possible role in human-specific brain development. As iPSCs are inherently variable due to genetic and epigenetic differences in donor cells or reprogramming procedures, it is essential to expand the number of chimpanzee iPSC lines to comprehensively capture the molecular and cellular properties representative of chimpanzees. Hence, our cells provide a valuable resource for investigating the function and regulation of human-specific transcripts such as HSTR1 and for understanding human evolution more generally.
Language	English
Publishing date	2024-02-22
Publishing country	Germany
Document type	Journal Article
ZDB-ID	1077810-x
ISSN	1543-706X ; 0883-8364 ; 1071-2690
ISSN (online)	1543-706X
ISSN	0883-8364 ; 1071-2690
DOI	10.1007/s11626-024-00853-y
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Article ; Online: Sequence divergence and retrotransposon insertion underlie interspecific epigenetic differences in primates.

Hirata, Mayu / Ichiyanagi, Tomoko / Katoh, Hirokazu / Hashimoto, Takuma / Suzuki, Hikaru / Nitta, Hirohisa / Kawase, Masaki / Nakai, Risako / Imamura, Masanori / Ichiyanagi, Kenji

Molecular biology and evolution

2022

Abstract: Changes in the epigenome can affect the phenotype without the presence of changes in the genomic sequence. Given the high identity of the human and chimpanzee genome sequences, a substantial portion of their phenotypic divergence likely arises from ... ...

Abstract	Changes in the epigenome can affect the phenotype without the presence of changes in the genomic sequence. Given the high identity of the human and chimpanzee genome sequences, a substantial portion of their phenotypic divergence likely arises from epigenomic differences between the two species. In this study, the transcriptome and epigenome were determined for induced pluripotent stem cells (iPSCs) generated from human and chimpanzee individuals. The transcriptome and epigenomes for trimethylated histone H3 at lysine-4 (H3K4me3) and lysine-27 (H3K27me3) showed high levels of similarity between the two species. However, there were some differences in histone modifications. Although such regions, in general, did not show significant enrichment of interspecies nucleotide variations, gains in binding motifs for pluripotency-related transcription factors, especially POU5F1 and SOX2, were frequently found in species-specific H3K4me3 regions. We also revealed that species-specific insertions of retrotransposons, including the LTR5_Hs subfamily in human and a newly identified LTR5_Pt subfamily in chimpanzee, created species-specific H3K4me3 regions associated with increased expression of nearby genes. Human iPSCs have more species-specific H3K27me3 regions, resulting in more abundant bivalent domains. Only a limited number of these species-specific H3K4me3 and H3K27me3 regions overlap with species-biased enhancers in cranial neural crest cells, suggesting that differences in the epigenetic state of developmental enhancers appear late in development. Therefore, iPSCs serve as a suitable starting material for studying evolutionary changes in epigenome dynamics during development.
Language	English
Publishing date	2022-10-11
Publishing country	United States
Document type	Journal Article
ZDB-ID	998579-7
ISSN	1537-1719 ; 0737-4038
ISSN (online)	1537-1719
ISSN	0737-4038
DOI	10.1093/molbev/msac208
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Article ; Online: Predicted structural differences of four fertility-related Y-chromosome proteins in Macaca mulatta, M. fascicularis, and their Indochinese hybrids.

Ruiz, Cody A / Chaney, Morgan E / Imamura, Masanori / Imai, Hiroo / Tosi, Anthony J

Proteins

2020 Volume 89, Issue 3, Page(s) 361–370

Abstract: Species in the genus Macaca typically live in multimale-multifemale social groups with male macaques exhibiting some of the largest testis: body weight ratios among primates. Males are believed to experience intense levels of sperm competition. Several ... ...

Abstract	Species in the genus Macaca typically live in multimale-multifemale social groups with male macaques exhibiting some of the largest testis: body weight ratios among primates. Males are believed to experience intense levels of sperm competition. Several spermatogenesis genes are located on the Y-chromosome and, interestingly, occasional hybridization between two species has led to the introgression of the rhesus macaque (Macaca mulatta) Y-chromosome deep into the range of the long-tailed macaque (M. fascicularis). These observations have led to the prediction that the successful introgression of the rhesus Y-haplotype is due to functional differences in spermatogenesis genes compared to those of the native long-tailed Y-haplotype. We examine here four Y-chromosomal loci-RBMY, XKRY, and two nearly identical copies of CDY-and their corresponding protein sequences. The genes were surveyed in representative animals from north of, south of, and within the rhesus x long-tailed introgression zone. Our results show a series of non-synonymous amino acid substitutions present between the two Y-haplotypes. Protein structure modeling via I-TASSER revealed different folding patterns between the two species' Y-proteins, and functional predictions via TreeSAAP further reveal physicochemical differences as a result of non-synonymous substitutions. These differences inform our understanding of the evolution of primate Y-proteins involved in spermatogenesis and, in turn, have biomedical implications for human male fertility.
MeSH term(s)	Amino Acid Substitution/genetics ; Animals ; Computational Biology ; Genetic Introgression/genetics ; Haplotypes/genetics ; Macaca fascicularis/genetics ; Macaca mulatta/genetics ; Male ; Models, Molecular ; Nuclear Proteins/chemistry ; Nuclear Proteins/genetics ; RNA-Binding Proteins/chemistry ; RNA-Binding Proteins/genetics ; Sequence Alignment ; Sequence Analysis, Protein ; Y Chromosome/genetics
Chemical Substances	Nuclear Proteins ; RNA-Binding Proteins
Language	English
Publishing date	2020-11-15
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	806683-8
ISSN	1097-0134 ; 0887-3585
ISSN (online)	1097-0134
ISSN	0887-3585
DOI	10.1002/prot.26021
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Article ; Online: Molecular histology of spermatogenesis in the Japanese macaque monkey (Macaca fuscata).

Okada, Sawako / Kuroki, Kota / Ruiz, Cody A / Tosi, Anthony J / Imamura, Masanori

Primates; journal of primatology

2020 Volume 62, Issue 1, Page(s) 113–121

Abstract: Non-human primates are our closest relatives and therefore offer valuable comparative models for human evolutionary studies and biomedical research. As such, Japanese macaques (Macaca fuscata) have contributed to the advancement of primatology in both ... ...

Abstract	Non-human primates are our closest relatives and therefore offer valuable comparative models for human evolutionary studies and biomedical research. As such, Japanese macaques (Macaca fuscata) have contributed to the advancement of primatology in both field and laboratory settings. Specifically, Japanese macaques serve as an excellent model for investigating postnatal development and seasonal breeding in primates because of their relatively prolonged juvenile period and distinct seasonal breeding activity in adulthood. Pioneering histological studies have examined the developmental associations between their reproductive states and spermatogenesis by morphological observation. However, a molecular histological atlas of Japanese macaque spermatogenesis is only in its infancy, limiting our understanding of spermatogenesis ontogeny related to their reproductive changes. Here, we performed immunofluorescence analyses of spermatogenesis in Japanese macaque testes to determine the expression of a subset of marker proteins. The present molecular histological analyses readily specified major spermatogonial subtypes as SALL4
MeSH term(s)	Animals ; Chromosomes, Mammalian/physiology ; Immunohistochemistry ; Macaca fuscata/genetics ; Macaca fuscata/growth & development ; Macaca fuscata/metabolism ; Male ; Spermatogenesis/physiology ; Spermatogonia/cytology ; Spermatogonia/metabolism ; Testis/cytology ; Testis/metabolism
Keywords	covid19
Language	English
Publishing date	2020-08-17
Publishing country	Japan
Document type	Comparative Study ; Journal Article
ZDB-ID	2100453-5
ISSN	1610-7365 ; 0032-8332
ISSN (online)	1610-7365
ISSN	0032-8332
DOI	10.1007/s10329-020-00857-8
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Article ; Online: Modeling of early neural development in vitro by direct neurosphere formation culture of chimpanzee induced pluripotent stem cells.

Kitajima, Ryunosuke / Nakai, Risako / Imamura, Takuya / Kameda, Tomonori / Kozuka, Daiki / Hirai, Hirohisa / Ito, Haruka / Imai, Hiroo / Imamura, Masanori

Stem cell research

2020 Volume 44, Page(s) 101749

Abstract: Evolutionary developmental biology of our closest living relative, the chimpanzee (Pan troglodytes), is essential for understanding the origin of human traits. However, it is difficult to access developmental events in the chimpanzee in vivo because of ... ...

Abstract	Evolutionary developmental biology of our closest living relative, the chimpanzee (Pan troglodytes), is essential for understanding the origin of human traits. However, it is difficult to access developmental events in the chimpanzee in vivo because of technical and ethical restrictions. Induced pluripotent stem cells (iPSCs) offer an alternative in vitro model system to investigate developmental events by overcoming the limitations of in vivo study. Here, we generated chimpanzee iPSCs from adult skin fibroblasts and reconstructed early neural development using in vitro differentiation culture conditions. Chimpanzee iPSCs were established using straightforward methods, namely, lipofection of plasmid vectors carrying human reprogramming factors, combined with maintenance in a comprehensive feeder-free culture. Ultimately, direct neurosphere formation culture induced rapid and efficient differentiation of neural stem cells from chimpanzee iPSCs. Time course analysis of neurosphere formation demonstrated ontogenetic changes in gene expression profiles and developmental potency along an early neural development path from epiblasts to radial glia. Our iPSC culture system is a potent tool for investigating the molecular and cellular foundation underlying chimpanzee early neural development and better understanding of human brain evolution.
MeSH term(s)	Animals ; Cell Differentiation ; Cellular Reprogramming ; Fibroblasts ; Humans ; Induced Pluripotent Stem Cells ; Neurogenesis ; Pan troglodytes
Language	English
Publishing date	2020-02-28
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1876-7753
ISSN (online)	1876-7753
DOI	10.1016/j.scr.2020.101749
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Article: Molecular histology of spermatogenesis in the Japanese macaque monkey (Macaca fuscata)

Okada, Sawako / Kuroki, Kota / Ruiz, Cody A / Tosi, Anthony J / Imamura, Masanori

Primates

Abstract	Non-human primates are our closest relatives and therefore offer valuable comparative models for human evolutionary studies and biomedical research. As such, Japanese macaques (Macaca fuscata) have contributed to the advancement of primatology in both field and laboratory settings. Specifically, Japanese macaques serve as an excellent model for investigating postnatal development and seasonal breeding in primates because of their relatively prolonged juvenile period and distinct seasonal breeding activity in adulthood. Pioneering histological studies have examined the developmental associations between their reproductive states and spermatogenesis by morphological observation. However, a molecular histological atlas of Japanese macaque spermatogenesis is only in its infancy, limiting our understanding of spermatogenesis ontogeny related to their reproductive changes. Here, we performed immunofluorescence analyses of spermatogenesis in Japanese macaque testes to determine the expression of a subset of marker proteins. The present molecular histological analyses readily specified major spermatogonial subtypes as SALL4+ A spermatogonia and Ki67+/C-KIT+ B spermatogonia. The expression of DAZL, SCP1, Î³H2AX, VASA, and calmegin further showed sequential changes regarding the protein expression profile and chromosomal structures during spermatogenesis in a differentiation stage-specific manner. Accordingly, comparative analyses between subadults and adults identified spermatogenic deficits in differentiation and synchronization in subadult testes. Our findings provide a new diagnostic platform for dissecting spermatogenic status and reproduction in the Japanese macaques.
Keywords	covid19
Publisher	WHO
Document type	Article
Note	WHO #Covidence: #32803510
Database	COVID19

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Article: Cell-intrinsic reprogramming capability: gain or loss of pluripotency in germ cells.

Imamura, Masanori / Lin, Zachary Yu-Ching / Okano, Hideyuki

Reproductive medicine and biology

2012 Volume 12, Issue 1, Page(s) 1–14

Abstract: In multicellular organisms, germ cells are an extremely specialized cell type with the vital function of transmitting genetic information across generations. In this respect, they are responsible for the perpetuity of species, and are separated from ... ...

Abstract	In multicellular organisms, germ cells are an extremely specialized cell type with the vital function of transmitting genetic information across generations. In this respect, they are responsible for the perpetuity of species, and are separated from somatic lineages at each generation. Interestingly, in the past two decades research has shown that germ cells have the potential to proceed along two distinct pathways: gametogenesis or pluripotency. Unequivocally, the primary role of germ cells is to produce gametes, the sperm or oocyte, to produce offspring. However, under specific conditions germ cells can become pluripotent, as shown by teratoma formation in vivo or cell culture-induced reprogramming in vitro. This phenomenon seems to be a general propensity of germ cells, irrespective of developmental phase. Recent attempts at cellular reprogramming have resulted in the generation of induced pluripotent stem cells (iPSCs). In iPSCs, the intracellular molecular networks instructing pluripotency have been activated and override the exclusively somatic cell programs that existed. Because the generation of iPSCs is highly artificial and depends on gene transduction, whether the resulting machinery reflects any physiological cell-intrinsic programs is open to question. In contrast, germ cells can spontaneously shift their fate to pluripotency during in-vitro culture. Here, we review the two fates of germ cells, i.e., differentiation and reprogramming. Understanding the molecular mechanisms regulating differentiation versus reprogramming would provide invaluable insight into understanding the mechanisms of cellular reprogramming that generate iPSCs.
Language	English
Publishing date	2012-06-19
Publishing country	Japan
Document type	Journal Article ; Review
ZDB-ID	2185775-1
ISSN	1447-0578 ; 1445-5781
ISSN (online)	1447-0578
ISSN	1445-5781
DOI	10.1007/s12522-012-0131-z
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Article ; Online: Generation of germ cells in vitro in the era of induced pluripotent stem cells.

Imamura, Masanori / Hikabe, Orie / Lin, Zachary Yu-Ching / Okano, Hideyuki

Molecular reproduction and development

2014 Volume 81, Issue 1, Page(s) 2–19

Abstract: Induced pluripotent stem cells (iPSCs) are stem cells that can be artificially generated via "cellular reprogramming" using gene transduction in somatic cells. iPSCs have enormous potential in stem-cell biology as they can give rise to numerous cell ... ...

Abstract	Induced pluripotent stem cells (iPSCs) are stem cells that can be artificially generated via "cellular reprogramming" using gene transduction in somatic cells. iPSCs have enormous potential in stem-cell biology as they can give rise to numerous cell lineages, including the three germ layers. An evaluation of germ-line competency by blastocyst injection or tetraploid complementation, however, is critical for determining the developmental potential of mouse iPSCs towards germ cells. Recent studies have demonstrated that primordial germ cells obtained by the in vitro differentiation of iPSCs produce functional gametes as well as healthy offspring. These findings illustrate not only that iPSCs are developmentally similar to embryonic stem cells (ESCs), but also that somatic cells from adult tissues can produce gametes in vitro, that is, if they are reprogrammed into iPSCs. In this review, we discuss past and recent advances in the in vitro differentiation of germ cells using pluripotent stem cells, with an emphasis on ESCs and iPSCs. While this field of research is still at a stage of infancy, it holds great promises for investigating the mechanisms of germ-cell development, especially in humans, and for advancing reproductive and developmental engineering technologies in the future.
MeSH term(s)	Animals ; Bioengineering/methods ; Bioengineering/trends ; Cell Differentiation/physiology ; Embryonic Stem Cells/cytology ; Germ Cells/cytology ; Germ Cells/growth & development ; Humans ; Induced Pluripotent Stem Cells/cytology ; Mice
Language	English
Publishing date	2014-01
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	20321-x
ISSN	1098-2795 ; 1040-452X
ISSN (online)	1098-2795
ISSN	1040-452X
DOI	10.1002/mrd.22259
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