In Vivo Lineage Tracing of Polyploid Hepatocytes Reveals Extensive Proliferation during Liver Regeneration

The identity of cellular populations that drive liver regeneration after injury is the subject of intense study, and the contributions of polyploid hepatocytes to organ regeneration and homeostasis have not been systematically assessed. Here, we developed a multicolor reporter allele system to genet...

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Published in	Cell stem cell Vol. 26; no. 1; pp. 34 - 47.e3
Main Authors	Matsumoto, Tomonori, Wakefield, Leslie, Tarlow, Branden David, Grompe, Markus
Format	Journal Article
Language	English
Published	United States Elsevier Inc 02.01.2020
Subjects	Cell Proliferation hepatocyte Hepatocytes Humans lineage tracing Liver Liver Regeneration ploidy conveyor ploidy reduction Polyploidy ploidy conveyor ploidy reduction hepatocyte lineage tracing polyploidy
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Abstract	The identity of cellular populations that drive liver regeneration after injury is the subject of intense study, and the contributions of polyploid hepatocytes to organ regeneration and homeostasis have not been systematically assessed. Here, we developed a multicolor reporter allele system to genetically label and trace polyploid cells in situ. Multicolored polyploid hepatocytes undergo ploidy reduction and subsequent re-polyploidization after transplantation, providing direct evidence of the hepatocyte ploidy conveyor model. Marker segregation revealed that ploidy reduction rarely involves chromosome missegregation in vivo. We also traced polyploid hepatocytes in several different liver injury models and found robust proliferation in all settings. Importantly, ploidy reduction was seen in all injury models studied. We therefore conclude that polyploid hepatocytes have extensive regenerative capacity in situ and routinely undergo reductive mitoses during regenerative responses. [Display omitted] •A genetic system to trace polyploid cells in any organ in vivo was developed•Polyploid hepatocytes regenerate injured livers and frequently reduce their ploidy•Ploidy-reduced progeny proliferates and re-polyploidizes in subsequent mitoses•Chromosome segregation during ploidy reduction is not random but faithful Polyploid cells are common in several mammalian tissues. Using a genetic system to label and trace polyploid cells in vivo, Matsumoto et al. showed that polyploid hepatocytes are major contributors to regeneration of chronically injured livers. Polyploid hepatocytes proliferate continuously and dynamically decrease and increase their ploidy while remaining proliferative.
AbstractList	The identity of cellular populations that drive liver regeneration after injury is the subject of intense study, and the contributions of polyploid hepatocytes to organ regeneration and homeostasis have not been systematically assessed. Here, we developed a multicolor reporter allele system to genetically label and trace polyploid cells in situ. Multicolored polyploid hepatocytes undergo ploidy reduction and subsequent re-polyploidization after transplantation, providing direct evidence of the hepatocyte ploidy conveyor model. Marker segregation revealed that ploidy reduction rarely involves chromosome missegregation in vivo. We also traced polyploid hepatocytes in several different liver injury models and found robust proliferation in all settings. Importantly, ploidy reduction was seen in all injury models studied. We therefore conclude that polyploid hepatocytes have extensive regenerative capacity in situ and routinely undergo reductive mitoses during regenerative responses. [Display omitted] •A genetic system to trace polyploid cells in any organ in vivo was developed•Polyploid hepatocytes regenerate injured livers and frequently reduce their ploidy•Ploidy-reduced progeny proliferates and re-polyploidizes in subsequent mitoses•Chromosome segregation during ploidy reduction is not random but faithful Polyploid cells are common in several mammalian tissues. Using a genetic system to label and trace polyploid cells in vivo, Matsumoto et al. showed that polyploid hepatocytes are major contributors to regeneration of chronically injured livers. Polyploid hepatocytes proliferate continuously and dynamically decrease and increase their ploidy while remaining proliferative. The identity of cellular populations that drive liver regeneration after injury is the subject of intense study, and the contributions of polyploid hepatocytes to organ regeneration and homeostasis have not been systematically assessed. Here we developed a multicolor reporter allele system to genetically label and trace polyploid cells in situ. Multicolored polyploid hepatocytes undergo ploidy reduction and subsequent re-polyploidization after transplantation, providing direct evidence for the hepatocyte ploidy conveyor model. Marker segregation revealed that ploidy reduction rarely involves chromosome missegregation in vivo. We also traced polyploid hepatocytes in several different liver injury models and found robust proliferation in all settings. Importantly, ploidy reduction was seen in all injury models studied. We therefore conclude that polyploid hepatocytes have extensive regenerative capacity in situ and routinely undergo reductive mitoses during regenerative responses. Polyploid cells are common in several mammalian tissues. Using a genetic system to label and trace polyploid cells in vivo, Matsumoto et al. showed that polyploid hepatocytes are major contributors to regeneration of chronically injured livers. Polyploid hepatocytes continuously proliferate, and dynamically decrease and increase their ploidy while remaining proliferative. The identity of cellular populations that drive liver regeneration after injury is the subject of intense study, and the contributions of polyploid hepatocytes to organ regeneration and homeostasis have not been systematically assessed. Here, we developed a multicolor reporter allele system to genetically label and trace polyploid cells in situ. Multicolored polyploid hepatocytes undergo ploidy reduction and subsequent re-polyploidization after transplantation, providing direct evidence of the hepatocyte ploidy conveyor model. Marker segregation revealed that ploidy reduction rarely involves chromosome missegregation in vivo. We also traced polyploid hepatocytes in several different liver injury models and found robust proliferation in all settings. Importantly, ploidy reduction was seen in all injury models studied. We therefore conclude that polyploid hepatocytes have extensive regenerative capacity in situ and routinely undergo reductive mitoses during regenerative responses. The identity of cellular populations that drive liver regeneration after injury is the subject of intense study, and the contributions of polyploid hepatocytes to organ regeneration and homeostasis have not been systematically assessed. Here, we developed a multicolor reporter allele system to genetically label and trace polyploid cells in situ. Multicolored polyploid hepatocytes undergo ploidy reduction and subsequent re-polyploidization after transplantation, providing direct evidence of the hepatocyte ploidy conveyor model. Marker segregation revealed that ploidy reduction rarely involves chromosome missegregation in vivo. We also traced polyploid hepatocytes in several different liver injury models and found robust proliferation in all settings. Importantly, ploidy reduction was seen in all injury models studied. We therefore conclude that polyploid hepatocytes have extensive regenerative capacity in situ and routinely undergo reductive mitoses during regenerative responses.The identity of cellular populations that drive liver regeneration after injury is the subject of intense study, and the contributions of polyploid hepatocytes to organ regeneration and homeostasis have not been systematically assessed. Here, we developed a multicolor reporter allele system to genetically label and trace polyploid cells in situ. Multicolored polyploid hepatocytes undergo ploidy reduction and subsequent re-polyploidization after transplantation, providing direct evidence of the hepatocyte ploidy conveyor model. Marker segregation revealed that ploidy reduction rarely involves chromosome missegregation in vivo. We also traced polyploid hepatocytes in several different liver injury models and found robust proliferation in all settings. Importantly, ploidy reduction was seen in all injury models studied. We therefore conclude that polyploid hepatocytes have extensive regenerative capacity in situ and routinely undergo reductive mitoses during regenerative responses.
Author	Wakefield, Leslie Tarlow, Branden David Grompe, Markus Matsumoto, Tomonori
AuthorAffiliation	3. Gastroenterology and Hepatology, Stanford University, Stanford, California, 94305, USA 4. Lead Contact 1. Department of Pediatrics, Oregon Health and Science University, Portland, Oregon, 97239, USA 2. JSPS Overseas Research Fellow, Japan Society for the Promotion of Science, Chiyoda-ku, Tokyo, 102-0083, Japan
AuthorAffiliation_xml	– name: 4. Lead Contact – name: 2. JSPS Overseas Research Fellow, Japan Society for the Promotion of Science, Chiyoda-ku, Tokyo, 102-0083, Japan – name: 3. Gastroenterology and Hepatology, Stanford University, Stanford, California, 94305, USA – name: 1. Department of Pediatrics, Oregon Health and Science University, Portland, Oregon, 97239, USA
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Snippet	The identity of cellular populations that drive liver regeneration after injury is the subject of intense study, and the contributions of polyploid hepatocytes...
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SubjectTerms	Cell Proliferation hepatocyte Hepatocytes Humans lineage tracing Liver Liver Regeneration ploidy conveyor ploidy reduction Polyploidy
Title	In Vivo Lineage Tracing of Polyploid Hepatocytes Reveals Extensive Proliferation during Liver Regeneration
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