Use of stable isotope-tagged thymidine and multi-isotope imaging mass spectrometry (MIMS) for quantification of human cardiomyocyte division

Quantification of cellular proliferation in humans is important for understanding biology and responses to injury and disease. However, existing methods require administration of tracers that cannot be ethically administered in humans. We present a protocol for the direct quantification of cellular...

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Published inNature protocols Vol. 16; no. 4; pp. 1995 - 2022
Main Authors Yester, Jessie W., Liu, Honghai, Gyngard, Frank, Ammanamanchi, Niyatie, Little, Kathryn C., Thomas, Dawn, Sullivan, Mara L. G., Lal, Sean, Steinhauser, Matthew L., Kühn, Bernhard
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.04.2021
Nature Publishing Group
Subjects
631/1647/296
631/80/641/151/1431
692/4019/592/2725
Analytical Chemistry
Biological Techniques
Biomedical and Life Sciences
Cardiomyocytes
Cardiovascular diseases
Cardiovascular research
Cell cycle
Cell Division
Cell Nucleus - metabolism
Cell Proliferation
Computational Biology/Bioinformatics
Confocal microscopy
Coronary artery disease
Female
Fetus - cytology
Health aspects
Heart cells
Heart diseases
Human tissues
Humans
Imaging
Imaging, Three-Dimensional
Infant
Infants
Isotope dilution techniques
Isotope Labeling - methods
Leukocytes - cytology
Life Sciences
Mass spectrometry
Mass Spectrometry - methods
Mass spectroscopy
Methods
Microarrays
Myocardium
Myocardium - cytology
Myocytes, Cardiac - cytology
Nitrogen isotopes
Nitrogen Isotopes - urine
Organic Chemistry
Physiological aspects
Ploidies
Polyploidy
Pregnancy
Protocol
Sarcomeres - metabolism
Scientific imaging
Spectroscopy
Stable isotopes
Tetralogy of Fallot
Tetralogy of Fallot - pathology
Thymidine
Thymidine - metabolism
United States
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Abstract Quantification of cellular proliferation in humans is important for understanding biology and responses to injury and disease. However, existing methods require administration of tracers that cannot be ethically administered in humans. We present a protocol for the direct quantification of cellular proliferation in human hearts. The protocol involves administration of non-radioactive, non-toxic stable isotope 15 Nitrogen-enriched thymidine ( 15 N-thymidine), which is incorporated into DNA during S-phase, in infants with tetralogy of Fallot, a common form of congenital heart disease. Infants with tetralogy of Fallot undergo surgical repair, which requires the removal of pieces of myocardium that would otherwise be discarded. This protocol allows for the quantification of cardiomyocyte proliferation in this discarded tissue. We quantitatively analyzed the incorporation of 15 N-thymidine with multi-isotope imaging spectrometry (MIMS) at a sub-nuclear resolution, which we combined with correlative confocal microscopy to quantify formation of binucleated cardiomyocytes and cardiomyocytes with polyploid nuclei. The entire protocol spans 3–8 months, which is dependent on the timing of surgical repair, and 3–4.5 researcher days. This protocol could be adapted to study cellular proliferation in a variety of human tissues. The dynamics of cardiomyocyte cell cycle activity and proliferation in humans are poorly understood. This protocol describes how to measure cell division in infant hearts by multi-isotope imaging spectrometry after incorporation of 15 N-thymidine.
AbstractList Quantification of cellular proliferation in humans is important for understanding biology and responses to injury and disease. However, existing methods require administration of tracers that cannot be ethically administered in humans. We present a protocol for the direct quantification of cellular proliferation in human hearts. The protocol involves administration of non-radioactive, non-toxic stable isotope .sup.15Nitrogen-enriched thymidine (.sup.15N-thymidine), which is incorporated into DNA during S-phase, in infants with tetralogy of Fallot, a common form of congenital heart disease. Infants with tetralogy of Fallot undergo surgical repair, which requires the removal of pieces of myocardium that would otherwise be discarded. This protocol allows for the quantification of cardiomyocyte proliferation in this discarded tissue. We quantitatively analyzed the incorporation of .sup.15N-thymidine with multi-isotope imaging spectrometry (MIMS) at a sub-nuclear resolution, which we combined with correlative confocal microscopy to quantify formation of binucleated cardiomyocytes and cardiomyocytes with polyploid nuclei. The entire protocol spans 3-8 months, which is dependent on the timing of surgical repair, and 3-4.5 researcher days. This protocol could be adapted to study cellular proliferation in a variety of human tissues.
Quantification of cellular proliferation in humans is important for understanding biology and responses to injury and disease. However, existing methods require administration of tracers that cannot be ethically administered in humans. We present a protocol for the direct quantification of cellular proliferation in human hearts. The protocol involves administration of non-radioactive, non-toxic stable isotope 15Nitrogen-enriched thymidine (15N-thymidine), which is incorporated into DNA during S-phase, in infants with tetralogy of Fallot, a common form of congenital heart disease. Infants with tetralogy of Fallot undergo surgical repair, which requires the removal of pieces of myocardium that would otherwise be discarded. This protocol allows for the quantification of cardiomyocyte proliferation in this discarded tissue. We quantitatively analyzed the incorporation of 15N-thymidine with multi-isotope imaging spectrometry (MIMS) at a sub-nuclear resolution, which we combined with correlative confocal microscopy to quantify formation of binucleated cardiomyocytes and cardiomyocytes with polyploid nuclei. The entire protocol spans 3–8 months, which is dependent on the timing of surgical repair, and 3–4.5 researcher days. This protocol could be adapted to study cellular proliferation in a variety of human tissues.The dynamics of cardiomyocyte cell cycle activity and proliferation in humans are poorly understood. This protocol describes how to measure cell division in infant hearts by multi-isotope imaging spectrometry after incorporation of 15N-thymidine.
Quantification of cellular proliferation in humans is important for understanding biology and responses to injury and disease. However, existing methods require administration of tracers that cannot be ethically administered in humans. We present a protocol for the direct quantification of cellular proliferation in human hearts. The protocol involves administration of non-radioactive, non-toxic stable isotope 15 Nitrogen-enriched thymidine ( 15 N-thymidine), which is incorporated into DNA during S-phase, in infants with tetralogy of Fallot, a common form of congenital heart disease. Infants with tetralogy of Fallot undergo surgical repair, which requires the removal of pieces of myocardium that would otherwise be discarded. This protocol allows for the quantification of cardiomyocyte proliferation in this discarded tissue. We quantitatively analyzed the incorporation of 15 N-thymidine with multi-isotope imaging spectrometry (MIMS) at a sub-nuclear resolution, which we combined with correlative confocal microscopy to quantify formation of binucleated cardiomyocytes and cardiomyocytes with polyploid nuclei. The entire protocol spans 3–8 months, which is dependent on the timing of surgical repair, and 3–4.5 researcher days. This protocol could be adapted to study cellular proliferation in a variety of human tissues. The dynamics of cardiomyocyte cell cycle activity and proliferation in humans are poorly understood. This protocol describes how to measure cell division in infant hearts by multi-isotope imaging spectrometry after incorporation of 15 N-thymidine.
Quantification of cellular proliferation in humans is important for understanding biology and responses to injury and disease. However, existing methods require administration of tracers that cannot be ethically administered in humans. We present a protocol for the direct quantification of cellular proliferation in human hearts. The protocol involves administration of non-radioactive, non-toxic stable isotope 15 Nitrogen-enriched thymidine ( 15 N-thymidine), which is incorporated into DNA during S-phase, in infants with tetralogy of Fallot, a common form of congenital heart disease. Infants with tetralogy of Fallot undergo surgical repair, which requires the removal of pieces of myocardium that would otherwise be discarded. This protocol allows for the quantification of cardiomyocyte proliferation in this discarded tissue. We quantitatively analyzed the incorporation of 15 N-thymidine with multi-isotope imaging spectrometry (MIMS) at a sub-nuclear resolution, which we combined with correlative confocal microscopy to quantify formation of binucleated cardiomyocytes and cardiomyocytes with polyploid nuclei. The entire protocol spans 3–8 months, which is dependent on the timing of surgical repair, and 3–4.5 researcher days. This protocol could be adapted to study cellular proliferation in a variety of human tissues.
Quantification of cellular proliferation in humans is important for understanding biology and responses to injury and disease. However, existing methods require administration of tracers that cannot be ethically administered in humans. We present a protocol for the direct quantification of cellular proliferation in human hearts. The protocol involves administration of non-radioactive, non-toxic stable isotope .sup.15Nitrogen-enriched thymidine (.sup.15N-thymidine), which is incorporated into DNA during S-phase, in infants with tetralogy of Fallot, a common form of congenital heart disease. Infants with tetralogy of Fallot undergo surgical repair, which requires the removal of pieces of myocardium that would otherwise be discarded. This protocol allows for the quantification of cardiomyocyte proliferation in this discarded tissue. We quantitatively analyzed the incorporation of .sup.15N-thymidine with multi-isotope imaging spectrometry (MIMS) at a sub-nuclear resolution, which we combined with correlative confocal microscopy to quantify formation of binucleated cardiomyocytes and cardiomyocytes with polyploid nuclei. The entire protocol spans 3-8 months, which is dependent on the timing of surgical repair, and 3-4.5 researcher days. This protocol could be adapted to study cellular proliferation in a variety of human tissues. The dynamics of cardiomyocyte cell cycle activity and proliferation in humans are poorly understood. This protocol describes how to measure cell division in infant hearts by multi-isotope imaging spectrometry after incorporation of .sup.15N-thymidine.
Quantification of cellular proliferation in humans is important for understanding biology and responses to injury and disease. However, existing methods require administration of tracers that cannot be ethically administered in humans. We present a protocol for the direct quantification of cellular proliferation in human hearts. The protocol involves administration of non-radioactive, non-toxic stable isotope Nitrogen-enriched thymidine ( N-thymidine), which is incorporated into DNA during S-phase, in infants with tetralogy of Fallot, a common form of congenital heart disease. Infants with tetralogy of Fallot undergo surgical repair, which requires the removal of pieces of myocardium that would otherwise be discarded. This protocol allows for the quantification of cardiomyocyte proliferation in this discarded tissue. We quantitatively analyzed the incorporation of N-thymidine with multi-isotope imaging spectrometry (MIMS) at a sub-nuclear resolution, which we combined with correlative confocal microscopy to quantify formation of binucleated cardiomyocytes and cardiomyocytes with polyploid nuclei. The entire protocol spans 3-8 months, which is dependent on the timing of surgical repair, and 3-4.5 researcher days. This protocol could be adapted to study cellular proliferation in a variety of human tissues.
Audience Academic
Author Yester, Jessie W.
Steinhauser, Matthew L.
Sullivan, Mara L. G.
Liu, Honghai
Thomas, Dawn
Lal, Sean
Kühn, Bernhard
Gyngard, Frank
Ammanamanchi, Niyatie
Little, Kathryn C.
AuthorAffiliation 2 Center for NanoImaging, Division of Genetics, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Cambridge, MA, USA
5 School of Medical Sciences, Faculty of Medicine and Health, University of Sydney, Sydney, New South Wales, Australia
8 Aging Institute, University of Pittsburgh, Bridgeside Point 1, Pittsburgh, PA, USA
4 Center for Biologic Imaging, University of Pittsburgh School of Medicine, Department of Cell Biology, Pittsburgh, PA, USA
6 Division of Cardiology, Royal Prince Alfred Hospital, Sydney, New South Wales, Australia
10 Present address: UPMC Shadyside Hospital, Pittsburgh, PA, USA
1 Division of Cardiology, Pediatric Institute for Heart Regeneration and Therapeutics (I-HRT), UPMC Children’s Hospital of Pittsburgh and Department of Pediatrics, Pittsburgh, PA, USA
3 Clinical Research Support Services (CRSS), UPMC Children’s Hospital of Pittsburgh and Department of Pediatrics, Pittsburgh, PA, USA
7 UPMC Heart and Vascular Institute, UPMC Presbyterian, Pitts
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  organization: Division of Cardiology, Pediatric Institute for Heart Regeneration and Therapeutics (I-HRT), UPMC Children’s Hospital of Pittsburgh and Department of Pediatrics, McGowan Institute of Regenerative Medicine, University of Pittsburgh School of Medicine
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33627842$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright The Author(s), under exclusive licence to Springer Nature Limited 2021
COPYRIGHT 2021 Nature Publishing Group
The Author(s), under exclusive licence to Springer Nature Limited 2021.
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IngestDate Tue Sep 17 21:16:35 EDT 2024
Wed Nov 06 08:30:13 EST 2024
Thu Feb 22 23:38:03 EST 2024
Tue Nov 12 23:27:31 EST 2024
Thu Aug 01 19:18:36 EDT 2024
Thu Sep 12 17:37:18 EDT 2024
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Notes J.W.Y. developed the outline and wrote the first draft of the manuscript. N.A., K.C.L., D.T., and J.W.Y. developed the approach for ascertainment of myocardial samples. N.A. developed the protocol for curation of samples and sections. K.C.L. developed the approach for recruitment of eligible families and guiding them through the clinical research protocol. M.L.G.S. developed the protocol for sample processing. N.A. and S.L. completed the in vitro experiments. F.G. and M.L.S developed and wrote the NanoSIMS protocol. H.L. developed and wrote the protocol for analysis of ploidy. M.L.S. and B.K. conceived the research approach and protocol and wrote the manuscript. All authors edited the manuscript.
Author contributions
ORCID 0000-0001-5287-9246
0000-0002-1855-7072
0000-0003-3772-1998
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8221415
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SSID ssj0047367
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SecondaryResourceType review_article
Snippet Quantification of cellular proliferation in humans is important for understanding biology and responses to injury and disease. However, existing methods...
SourceID pubmedcentral
proquest
gale
crossref
pubmed
springer
SourceType Open Access Repository
Aggregation Database
Index Database
Publisher
StartPage 1995
SubjectTerms 631/1647/296
631/80/641/151/1431
692/4019/592/2725
Analytical Chemistry
Biological Techniques
Biomedical and Life Sciences
Cardiomyocytes
Cardiovascular diseases
Cardiovascular research
Cell cycle
Cell Division
Cell Nucleus - metabolism
Cell Proliferation
Computational Biology/Bioinformatics
Confocal microscopy
Coronary artery disease
Female
Fetus - cytology
Health aspects
Heart cells
Heart diseases
Human tissues
Humans
Imaging
Imaging, Three-Dimensional
Infant
Infants
Isotope dilution techniques
Isotope Labeling - methods
Leukocytes - cytology
Life Sciences
Mass spectrometry
Mass Spectrometry - methods
Mass spectroscopy
Methods
Microarrays
Myocardium
Myocardium - cytology
Myocytes, Cardiac - cytology
Nitrogen isotopes
Nitrogen Isotopes - urine
Organic Chemistry
Physiological aspects
Ploidies
Polyploidy
Pregnancy
Protocol
Sarcomeres - metabolism
Scientific imaging
Spectroscopy
Stable isotopes
Tetralogy of Fallot
Tetralogy of Fallot - pathology
Thymidine
Thymidine - metabolism
Title Use of stable isotope-tagged thymidine and multi-isotope imaging mass spectrometry (MIMS) for quantification of human cardiomyocyte division
URI https://link.springer.com/article/10.1038/s41596-020-00477-y
https://www.ncbi.nlm.nih.gov/pubmed/33627842
https://www.proquest.com/docview/2512577774
https://pubmed.ncbi.nlm.nih.gov/PMC8221415
Volume 16
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