Automated image analysis identifies signaling pathways regulating distinct signatures of cardiac myocyte hypertrophy.

Cardiac hypertrophy is controlled by a complex signal transduction and gene regulatory network, containing multiple layers of crosstalk and feedback. While numerous individual components of this network have been identified, understanding how these elements are coordinated to regulate heart growth remains a challenge. Past approaches to measure cardiac myocyte hypertrophy have been manual and often qualitative, hindering the ability to systematically characterize the network's higher-order control structure and identify therapeutic targets. Here, we develop and validate an automated image analysis approach for objectively quantifying multiple hypertrophic phenotypes from immunofluorescence images. This approach incorporates cardiac myocyte-specific optimizations and provides quantitative measures of myocyte size, elongation, circularity, sarcomeric organization, and cell-cell contact. As a proof-of-concept, we examined the hypertrophic response to α-adrenergic, β-adrenergic, tumor necrosis factor (TNFα), insulin-like growth factor-1 (IGF-1), and fetal bovine serum pathways. While all five hypertrophic pathways increased myocyte size, other hypertrophic metrics were differentially regulated, forming a distinct phenotype signature for each pathway. Sarcomeric organization was uniquely enhanced by α-adrenergic signaling. TNFα and α-adrenergic pathways markedly decreased cell circularity due to increased myocyte protrusion. Surprisingly, adrenergic and IGF-1 pathways differentially regulated myocyte-myocyte contact, potentially forming a feed-forward loop that regulates hypertrophy. Automated image analysis unlocks a range of new quantitative phenotypic data, aiding dissection of the complex hypertrophic signaling network and enabling myocyte-based high-content drug screening.

[1]  J. Sadoshima,et al.  Myosin light chain kinase mediates sarcomere organization during cardiac hypertrophy in vitro , 2000, Nature Medicine.

[2]  Alan Garfinkel,et al.  Computational Models Reduce Complexity and Accelerate Insight Into Cardiac Signaling Networks , 2010 .

[3]  A. Thorburn,et al.  Cell density and contraction regulate p 38 MAP kinase-dependent responses in neonatal rat cardiac myocytes , 1999 .

[4]  R. Schwartz,et al.  Conditional Deletion of Focal Adhesion Kinase Leads to Defects in Ventricular Septation and Outflow Tract Alignment , 2007, Molecular and Cellular Biology.

[5]  Polina Golland,et al.  Voronoi-Based Segmentation of Cells on Image Manifolds , 2005, CVBIA.

[6]  Sumeet Dua,et al.  Segmentation of Fluorescence Microscopy Cell Images Using Unsupervised Mining , 2010, The open medical informatics journal.

[7]  W J McKenna,et al.  Relation between myocyte disarray and outcome in hypertrophic cardiomyopathy. , 2001, The American journal of cardiology.

[8]  M.,et al.  Statistical and Structural Approaches to Texture , 2022 .

[9]  E. Olson,et al.  Cardiac plasticity. , 2008, The New England journal of medicine.

[10]  N. Otsu A threshold selection method from gray level histograms , 1979 .

[11]  M. Shichiri,et al.  Insulinlike Growth Factor‐I Induces Hypertrophy With Enhanced Expression of Muscle Specific Genes in Cultured Rat Cardiomyocytes , 1993, Circulation.

[12]  P. Simpson Norepinephrine-stimulated hypertrophy of cultured rat myocardial cells is an alpha 1 adrenergic response. , 1983, The Journal of clinical investigation.

[13]  Paul Matsudaira,et al.  Linking microscopy and high content screening in large-scale biomedical research. , 2007, Methods in molecular biology.

[14]  T. Thum,et al.  A phenotypic screen to identify hypertrophy-modulating microRNAs in primary cardiomyocytes. , 2012, Journal of molecular and cellular cardiology.

[15]  A. Thorburn,et al.  Cell density and contraction regulate p38 MAP kinasedependent responses in neonatal rat cardiac myocytes. , 1999, American journal of physiology. Heart and circulatory physiology.

[16]  Anne E Carpenter,et al.  A Lentiviral RNAi Library for Human and Mouse Genes Applied to an Arrayed Viral High-Content Screen , 2006, Cell.

[17]  T. Hewett,et al.  A truncated cardiac troponin T molecule in transgenic mice suggests multiple cellular mechanisms for familial hypertrophic cardiomyopathy. , 1998, The Journal of clinical investigation.

[18]  S. Cook,et al.  Are transgenic mice the 'alkahest' to understanding myocardial hypertrophy and failure? , 2009, Journal of molecular and cellular cardiology.

[19]  Pekka Ruusuvuori,et al.  Open Access Research Article Evaluation of Methods for Detection of Fluorescence Labeled Subcellular Objects in Microscope Images , 2022 .

[20]  L. Kedes,et al.  Adrenergic regulation of the skeletal alpha-actin gene promoter during myocardial cell hypertrophy. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Thomas Eschenhagen,et al.  Engineering Myocardial Tissue , 2005, Circulation research.

[22]  J. Molkentin,et al.  Regulation of cardiac hypertrophy by intracellular signalling pathways , 2006, Nature Reviews Molecular Cell Biology.

[23]  Anne E Carpenter,et al.  CellProfiler: image analysis software for identifying and quantifying cell phenotypes , 2006, Genome Biology.

[24]  Andrew D McCulloch,et al.  Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. , 2008, Biophysical journal.

[25]  Anne E Carpenter,et al.  RNAi living-cell microarrays for loss-of-function screens in Drosophila melanogaster cells , 2004, Nature Methods.

[26]  Karl-Ludwig Laugwitz,et al.  Patient-specific induced pluripotent stem-cell models for long-QT syndrome. , 2010, New England Journal of Medicine.

[27]  C. Long,et al.  A growth factor for cardiac myocytes is produced by cardiac nonmyocytes. , 1991, Cell regulation.

[28]  A. Lusis,et al.  Cardiovascular networks: systems-based approaches to cardiovascular disease. , 2010, Circulation.

[29]  David A. Kass,et al.  Tackling heart failure in the twenty-first century , 2008, Nature.

[30]  Marc Bickle,et al.  The beautiful cell: high-content screening in drug discovery , 2010, Analytical and bioanalytical chemistry.

[31]  D. Zechner,et al.  A Role for the p38 Mitogen-activated Protein Kinase Pathway in Myocardial Cell Growth, Sarcomeric Organization, and Cardiac-specific Gene Expression , 1997, The Journal of cell biology.

[32]  Bing Li,et al.  Active Contour External Force Using Vector Field Convolution for Image Segmentation , 2007, IEEE Transactions on Image Processing.

[33]  Jeffrey Robbins,et al.  With great power comes great responsibility: using mouse genetics to study cardiac hypertrophy and failure. , 2009, Journal of molecular and cellular cardiology.