An Unbiased Proteomics Method to Assess the Maturation of Human Pluripotent Stem Cell–Derived Cardiomyocytes
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Rationale: Human pluripotent stem cell (hPSC)–derived cardiomyocytes exhibit the properties of fetal cardiomyocytes, which limits their applications. Various methods have been used to promote maturation of hPSC-cardiomyocytes; however, there is a lack of an unbiased and comprehensive method for accurate assessment of the maturity of hPSC-cardiomyocytes. Objective: We aim to develop an unbiased proteomics strategy integrating high-throughput top-down targeted proteomics and bottom-up global proteomics for the accurate and comprehensive assessment of hPSC-cardiomyocyte maturation. Methods and Results: Utilizing hPSC-cardiomyocytes from early- and late-stage 2-dimensional monolayer culture and 3-dimensional engineered cardiac tissue, we demonstrated the high reproducibility and reliability of a top-down proteomics method, which enabled simultaneous quantification of contractile protein isoform expression and associated post-translational modifications. This method allowed for the detection of known maturation-associated contractile protein alterations and, for the first time, identified contractile protein post-translational modifications as promising new markers of hPSC-cardiomyocytes maturation. Most notably, decreased phosphorylation of α-tropomyosin was found to be associated with hPSC-cardiomyocyte maturation. By employing a bottom-up global proteomics strategy, we identified candidate maturation-associated markers important for sarcomere organization, cardiac excitability, and Ca 2+ homeostasis. In particular, upregulation of myomesin 1 and transmembrane 65 was associated with hPSC-cardiomyocyte maturation and validated in cardiac development, making these promising markers for assessing maturity of hPSC-cardiomyocytes. We have further validated α-actinin isoforms, phospholamban, dystrophin, αB-crystallin, and calsequestrin 2 as novel maturation-associated markers, in the developing mouse cardiac ventricles. Conclusions: We established an unbiased proteomics method that can provide accurate and specific assessment of the maturity of hPSC-cardiomyocytes and identified new markers of maturation. Furthermore, this integrated proteomics strategy laid a strong foundation for uncovering the molecular pathways involved in cardiac development and disease using hPSC-cardiomyocytes.
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The heart is uniquely sensitive to alternative splicing (frequently altered in congenital heart diseases), explaining the B/D-HPP's interest in developing assays for splice isoform-specific changes in cardiomyocyte development and maturation.
“In parallel, the heart is uniquely sensitive to alternative splicing (frequently altered in congenital heart diseases), explaining the B/D-HPP’s interest in developing assays for splice isoform-specific changes in cardiomyocyte development and maturation122,123.”
From A high-stringency blueprint of the human proteome (2020) · cites this paper as [123]
Distinct changes in protein isoform expression, such as a switch from atrial to ventricular isoform of myosin light chain 1, were observed between the two maturation states.
“Distinct changes in protein isoform expression, such as a switch in expression from the atrial to the ventricular isoform of myosin light chain 1, were observed between the two maturation states.”
From Top-down proteomics: challenges, innovations, and applications in basic and clinical research (2020) · cites this paper as [151]
Top-down proteomics was employed to quantify contractile protein isoform and PTM changes between early and late-stage 2D hiPSC-CM monolayers and 3D hiPSC-ECTs.
“The top-down proteomics was employed to quantify contractile protein isoform and PTM changes between early and late-stage 2D hiPSC-CM monolayers and 3D hiPSC-ECTs (Figure 5) [151].”
From Top-down proteomics: challenges, innovations, and applications in basic and clinical research (2020) · cites this paper as [151]
A decrease in alpha tropomyosin phosphorylation was discovered as a promising new marker of hPSC-CM maturation.
“For the first time, contractile PTMs such as a decrease in alpha tropomyosin phosphorylation were discovered as promising new markers of hPSC-CMs maturation.”
From Top-down proteomics: challenges, innovations, and applications in basic and clinical research (2020) · cites this paper as [151]
Cai et al. developed an unbiased method for assessing hiPSC-CM maturation by combining functional assessments and proteomics in 2D monolayer systems and 3D engineered cardiac tissues.
“To address this challenge, Cai et al. developed an unbiased method for the assessment of hiPSC-CMs maturation by combining functional assessments and proteomics to assess CM maturation in 2-dimensional (2D) monolayer systems and 3-dimensional (3D) engineered cardiac tissues (ECTs) [151].”
From Top-down proteomics: challenges, innovations, and applications in basic and clinical research (2020) · cites this paper as [151]
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- Authors
- Cai, W., Zhang, J., de Lange, W. J., Gregorich, Z. R., Karp, H., Farrell, E. T., Mitchell, S. D., Tucholski, T., Lin, Z., Biermann, M., McIlwain, S. J., Ralphe, J. C., Kamp, T. J., & Ge, Y.
- Affiliations
- University of Wisconsin System (US)
- University of Wisconsin–Madison (US)
- Department of Pediatrics (W.J.d.L., E.T.F., J.C.R.), University of Wisconsin-Madison.
- Corresponding author
- Kamp, Timothy J.
- Ge, Ying
- ORCID
- Venue
- Circulation Research
- Published
- 2019-11-08
- Volume
- 125
- Issue
- 11
- Pages
- 936-953
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- PMC
- PMC6852699
- OpenAlex
- W2978210721
- Cited by
- 78
- References
- 72
- Citations by year
- 2026: 7 · 2025: 6 · 2024: 11 · 2023: 16 · 2022: 6 · 2021: 15 · 2020: 14 · 2019: 2
- FWCI
- 3.06
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Circulation Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- American Heart Association
- Strong
- National Institutes of Health (1s10od018475-01)
- National Heart, Lung, and Blood Institute (U01HL148690, F30HL126452, U01HL134764, R01HL109810, R01HL129798, R01HL096971, T32HL007936)
- National Institute of General Medical Sciences (R01GM125085, R01GM117058, T32GM008688, T32GM008692, T32GM008505)
- National Center for Research Resources (P41RR002301)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- human pluripotent stem cell-derived cardiomyocytes, cardiomyocyte maturation, post-translational modification, phospholamban, dystrophin, alphaB-crystallin, CASQ2, sarcomere organization, cardiac excitability, calcium homeostasis, engineered heart tissue, heart development
- MeSH terms
- Cell Differentiation, Cell Line, Chromatography, Liquid, Humans, Phenotype, Proteins, Time Factors, Reproducibility of Results, Bias, Cell Culture Techniques, Spectrometry, Mass, Electrospray Ionization, Myocytes, Cardiac, Proteomics, Tandem Mass Spectrometry, Induced Pluripotent Stem Cells, High-Throughput Screening Assays
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