An in Situ Atlas of Mitochondrial DNA in Mammalian Tissues Reveals High Content in Stem and Proliferative Compartments
Mitochondria regulate ATP production, metabolism, and cell death. Alterations in mitochondrial DNA (mtDNA) sequence and copy number are implicated in aging and organ dysfunction in diverse inherited and sporadic diseases. Because most measurements of mtDNA use homogenates of complex tissues, little...
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| Published in | The American journal of pathology Vol. 190; no. 7; pp. 1565 - 1579 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Elsevier Inc
01.07.2020
American Society for Investigative Pathology |
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| Online Access | Get full text |
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| Abstract | Mitochondria regulate ATP production, metabolism, and cell death. Alterations in mitochondrial DNA (mtDNA) sequence and copy number are implicated in aging and organ dysfunction in diverse inherited and sporadic diseases. Because most measurements of mtDNA use homogenates of complex tissues, little is known about cell-type–specific mtDNA copy number heterogeneity in normal physiology, aging, and disease. Thus, the precise cell types whose loss of mitochondrial activity and altered mtDNA copy number that result in organ dysfunction in aging and disease have often not been clarified. Here, an in situ hybridization approach to generate a single-cell–resolution atlas of mtDNA content in mammalian tissues was validated. In hierarchically organized self-renewing tissues, higher levels of mtDNA were observed in stem/proliferative compartments compared with differentiated compartments. Striking zonal patterns of mtDNA levels in the liver reflected the known oxygen tension gradient. In the kidney, proximal and distal tubules had markedly higher mtDNA levels compared with cells within glomeruli and collecting duct epithelial cells. In mice, decreased mtDNA levels were visualized in renal tubules as a function of aging, which was prevented by calorie restriction. This study provides a novel approach for quantifying species- and cell-type–specific mtDNA copy number and dynamics in any normal or diseased tissue that can be used for monitoring the effects of interventions in animal and human studies. |
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| AbstractList | Mitochondria regulate ATP production, metabolism, and cell death. Alterations in mitochondrial DNA (mtDNA) sequence and copy number are implicated in aging and organ dysfunction in diverse inherited and sporadic diseases. Because most measurements of mtDNA use homogenates of complex tissues, little is known about cell-type–specific mtDNA copy number heterogeneity in normal physiology, aging, and disease. Thus, the precise cell types whose loss of mitochondrial activity and altered mtDNA copy number that result in organ dysfunction in aging and disease have often not been clarified. Here, an in situ hybridization approach to generate a single-cell–resolution atlas of mtDNA content in mammalian tissues was validated. In hierarchically organized self-renewing tissues, higher levels of mtDNA were observed in stem/proliferative compartments compared with differentiated compartments. Striking zonal patterns of mtDNA levels in the liver reflected the known oxygen tension gradient. In the kidney, proximal and distal tubules had markedly higher mtDNA levels compared with cells within glomeruli and collecting duct epithelial cells. In mice, decreased mtDNA levels were visualized in renal tubules as a function of aging, which was prevented by calorie restriction. This study provides a novel approach for quantifying species- and cell-type–specific mtDNA copy number and dynamics in any normal or diseased tissue that can be used for monitoring the effects of interventions in animal and human studies. Mitochondria regulate ATP production, metabolism, and cell death. Alterations in mitochondrial DNA (mtDNA) sequence and copy number are implicated in aging and organ dysfunction in diverse inherited and sporadic diseases. Because most measurements of mtDNA use homogenates of complex tissues, little is known about cell-type-specific mtDNA copy number heterogeneity in normal physiology, aging, and disease. Thus, the precise cell types whose loss of mitochondrial activity and altered mtDNA copy number that result in organ dysfunction in aging and disease have often not been clarified. Here, an in situ hybridization approach to generate a single-cell-resolution atlas of mtDNA content in mammalian tissues was validated. In hierarchically organized self-renewing tissues, higher levels of mtDNA were observed in stem/proliferative compartments compared with differentiated compartments. Striking zonal patterns of mtDNA levels in the liver reflected the known oxygen tension gradient. In the kidney, proximal and distal tubules had markedly higher mtDNA levels compared with cells within glomeruli and collecting duct epithelial cells. In mice, decreased mtDNA levels were visualized in renal tubules as a function of aging, which was prevented by calorie restriction. This study provides a novel approach for quantifying species- and cell-type-specific mtDNA copy number and dynamics in any normal or diseased tissue that can be used for monitoring the effects of interventions in animal and human studies.Mitochondria regulate ATP production, metabolism, and cell death. Alterations in mitochondrial DNA (mtDNA) sequence and copy number are implicated in aging and organ dysfunction in diverse inherited and sporadic diseases. Because most measurements of mtDNA use homogenates of complex tissues, little is known about cell-type-specific mtDNA copy number heterogeneity in normal physiology, aging, and disease. Thus, the precise cell types whose loss of mitochondrial activity and altered mtDNA copy number that result in organ dysfunction in aging and disease have often not been clarified. Here, an in situ hybridization approach to generate a single-cell-resolution atlas of mtDNA content in mammalian tissues was validated. In hierarchically organized self-renewing tissues, higher levels of mtDNA were observed in stem/proliferative compartments compared with differentiated compartments. Striking zonal patterns of mtDNA levels in the liver reflected the known oxygen tension gradient. In the kidney, proximal and distal tubules had markedly higher mtDNA levels compared with cells within glomeruli and collecting duct epithelial cells. In mice, decreased mtDNA levels were visualized in renal tubules as a function of aging, which was prevented by calorie restriction. This study provides a novel approach for quantifying species- and cell-type-specific mtDNA copy number and dynamics in any normal or diseased tissue that can be used for monitoring the effects of interventions in animal and human studies. Mitochondria regulate ATP production, metabolism, and cell death. Alterations in mitochondrial DNA (mtDNA) sequence and copy number are implicated in aging and organ dysfunction in diverse inherited and sporadic diseases. Because most measurements of mtDNA use homogenates of complex tissues, little is known about cell-type–specific mtDNA copy number heterogeneity in normal physiology, aging, and disease. Thus, the precise cell types whose loss of mitochondrial activity and altered mtDNA copy number that result in organ dysfunction in aging and disease have often not been clarified. Here, an in situ hybridization approach to generate a single-cell–resolution atlas of mtDNA content in mammalian tissues was validated. In hierarchically organized self-renewing tissues, higher levels of mtDNA were observed in stem/proliferative compartments compared with differentiated compartments. Striking zonal patterns of mtDNA levels in the liver reflected the known oxygen tension gradient. In the kidney, proximal and distal tubules had markedly higher mtDNA levels compared with cells within glomeruli and collecting duct epithelial cells. In mice, decreased mtDNA levels were visualized in renal tubules as a function of aging, which was prevented by calorie restriction. This study provides a novel approach for quantifying species- and cell-type–specific mtDNA copy number and dynamics in any normal or diseased tissue that can be used for monitoring the effects of interventions in animal and human studies. |
| Author | Haffner, Michael C. Baena-Del Valle, Javier Wang, Xiaoxin X. De Marzo, Angelo M. Zheng, Qizhi Peiffer, Lauren B. Hicks, Jessica L. Yegnasubramanian, Srinivasan Levi, Moshe Ozbek, Busra Chen, Jiayu Rosenberg, Avi Z. |
| Author_xml | – sequence: 1 givenname: Jiayu orcidid: 0000-0002-0566-0396 surname: Chen fullname: Chen, Jiayu organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland – sequence: 2 givenname: Qizhi surname: Zheng fullname: Zheng, Qizhi organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland – sequence: 3 givenname: Lauren B. orcidid: 0000-0003-1592-1980 surname: Peiffer fullname: Peiffer, Lauren B. organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland – sequence: 4 givenname: Jessica L. surname: Hicks fullname: Hicks, Jessica L. organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland – sequence: 5 givenname: Michael C. surname: Haffner fullname: Haffner, Michael C. organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland – sequence: 6 givenname: Avi Z. surname: Rosenberg fullname: Rosenberg, Avi Z. organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland – sequence: 7 givenname: Moshe orcidid: 0000-0001-6403-2261 surname: Levi fullname: Levi, Moshe organization: Department of Biochemistry and Molecular and Cellular Biology, Georgetown University, Washington, DC – sequence: 8 givenname: Xiaoxin X. surname: Wang fullname: Wang, Xiaoxin X. organization: Department of Biochemistry and Molecular and Cellular Biology, Georgetown University, Washington, DC – sequence: 9 givenname: Busra surname: Ozbek fullname: Ozbek, Busra organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland – sequence: 10 givenname: Javier orcidid: 0000-0001-8417-8946 surname: Baena-Del Valle fullname: Baena-Del Valle, Javier organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland – sequence: 11 givenname: Srinivasan surname: Yegnasubramanian fullname: Yegnasubramanian, Srinivasan organization: Department of Urology and Oncology, Johns Hopkins University School of Medicine, Baltimore, Maryland – sequence: 12 givenname: Angelo M. surname: De Marzo fullname: De Marzo, Angelo M. email: ademarz@jhmi.edu organization: Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32304697$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Aging - physiology Animals Atlases as Topic Cell Proliferation DNA Copy Number Variations DNA, Mitochondrial - analysis Female Humans In Situ Hybridization - methods Male Mice Mice, Inbred C57BL Stem Cells |
| Title | An in Situ Atlas of Mitochondrial DNA in Mammalian Tissues Reveals High Content in Stem and Proliferative Compartments |
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