Atomic Force Microscopy: an innovative technology to explore cardiomyocyte cell surface in cardiac physio/pathophysiology

Atomic Force Microscopy (AFM) has emerged these recent years as a multifunctional toolbox for studying biological samples in physiological conditions. Although its use has spread among biologists community, cardiology remains a scientific field where not been extensively used yet. Heart diseases are nowadays a major human threat, and cause the death of millions of people each year. A convergent point to all heart diseases seems to be related to the defect of the cardiomyocyte, the contractile unit of the he reason, many scientists got interested in this cell type. However, very few studies use a technology such as AFM and its derivatives (force spectroscopy, multiparametric imaging) to explore this cell. The aim of this review is thus to give a comprehensive an interest of the biophysical approach made possible by AFM studies. We will show how AFM has been and can be used to study fix living cardiomyocytes, and, how combined with other types of microscopy, it can help getting a better understanding o pathologies or drugs. This review is the first dedicated to the use of AFM technics in cardiology, and gives new insights in fundamental questions surrounding cardiomyocytes, that can be answered using such a technology.

[1]  F. Despas,et al.  Ephrin-B1 Is a Novel Specific Component of the Lateral Membrane of the Cardiomyocyte and Is Essential for the Stability of Cardiac Tissue Architecture Cohesion , 2012, Circulation research.

[2]  D. Müller,et al.  Multiparametric imaging of biological systems by force-distance curve–based AFM , 2013, Nature Methods.

[3]  D. Murphy,et al.  Isolation of single atrial and ventricular cells from the human heart. , 1982, Canadian Medical Association journal.

[4]  R. Mitchell,et al.  Quantification of Cardiomyocyte Hypertrophy by Cardiac Magnetic Resonance: Implications for Early Cardiac Remodeling , 2013, Circulation.

[5]  K. Broadley,et al.  The Langendorff heart preparation—Reappraisal of its role as a research and teaching model for coronary vasoactive drugs , 1979 .

[6]  J. Mauzeroll,et al.  Scanning Electrochemical Microscopy of Living Cells , 2012 .

[7]  Julia Gorelik,et al.  A novel Z-groove index characterizing myocardial surface structure. , 2006, Cardiovascular research.

[8]  Christophe Vieu,et al.  Nanomechanical properties of dead or alive single-patterned bacteria. , 2009, Langmuir : the ACS journal of surfaces and colloids.

[9]  J. Rouleau,et al.  Characterization of myocardium, isolated cardiomyocytes, and blood pressure in WKHA and WKY rats. , 2002, American journal of physiology. Heart and circulatory physiology.

[10]  Martin J. Lohse,et al.  β2-Adrenergic Receptor Redistribution in Heart Failure Changes cAMP Compartmentation , 2010, Science.

[11]  Quan-mei Sun,et al.  In situ mechanical analysis of cardiomyocytes at nano scales. , 2012, Nanoscale.

[12]  Patrice Soumillion,et al.  Multiparametric atomic force microscopy imaging of single bacteriophages extruding from living bacteria , 2013, Nature Communications.

[13]  Sandor Kasas,et al.  OpenFovea: open-source AFM data processing software , 2012, Nature Methods.

[14]  Nadine Aubry,et al.  Aging increases stiffness of cardiac myocytes measured by atomic force microscopy nanoindentation. , 2003, American journal of physiology. Heart and circulatory physiology.

[15]  Julia Gorelik,et al.  Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart , 2009, Proceedings of the National Academy of Sciences.

[16]  P. Hansma,et al.  The scanning ion-conductance microscope. , 1989, Science.

[17]  M. Radmacher,et al.  Mapping interaction forces with the atomic force microscope. , 1994, Biophysical Journal.

[18]  G. Fonarow,et al.  Epidemiology and risk profile of heart failure , 2011, Nature Reviews Cardiology.

[19]  G. Thollet,et al.  A history of scanning electron microscopy developments: towards "wet-STEM" imaging. , 2007, Micron.

[20]  M. Rols,et al.  Destabilization induced by electropermeabilization analyzed by atomic force microscopy. , 2013, Biochimica et biophysica acta.

[21]  J. François,et al.  Nanoscale Effects of Caspofungin against Two Yeast Species, Saccharomyces cerevisiae and Candida albicans , 2013, Antimicrobial Agents and Chemotherapy.

[22]  D. Michele,et al.  Blebbistatin extends culture life of adult mouse cardiac myocytes and allows efficient and stable transgene expression. , 2008, American journal of physiology. Heart and circulatory physiology.

[23]  T. Smart,et al.  Method for estimating the tip geometry of scanning ion conductance microscope pipets. , 2012, Analytical chemistry.

[24]  Flavien Pillet,et al.  Atomic Force Microscopy and pharmacology: from microbiology to cancerology. , 2014, Biochimica et biophysica acta.

[25]  J. Kugler,et al.  Subjective Light Pattern Spectroscopy in the Encephalographic Frequency Range , 1959, Nature.

[26]  F. Kajiya,et al.  Increased passive stiffness of cardiomyocytes in the transverse direction and residual actin and myosin cross-bridge formation in hypertrophied rat hearts induced by chronic β-adrenergic stimulation. , 2013, Circulation journal : official journal of the Japanese Circulation Society.

[27]  Giovanni Dietler,et al.  Stiffness tomography by atomic force microscopy. , 2009, Biophysical journal.

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

[29]  Yves F Dufrêne,et al.  Atomic force microscopy – looking at mechanosensors on the cell surface , 2012, Journal of Cell Science.

[30]  J. Dubochet,et al.  Cryo-electron microscopy of viruses , 1984, Nature.

[31]  D. Klenerman,et al.  Scanning ion conductance microscopy: a convergent high-resolution technology for multi-parametric analysis of living cardiovascular cells , 2011, Journal of the Royal Society Interface.

[32]  Daniel J Müller,et al.  Atomic force microscopy: a nanoscopic window on the cell surface. , 2011, Trends in cell biology.

[33]  W. Kraus,et al.  Endothelial, cardiac muscle and skeletal muscle exhibit different viscous and elastic properties as determined by atomic force microscopy. , 2001, Journal of biomechanics.

[34]  T. Okano,et al.  Ultrastructural Features of Ischemic Tissue following Application of a Bio-Membrane Based Progenitor Cardiomyocyte Patch for Myocardial Infarction Repair , 2014, PloS one.

[35]  I R At,et al.  Sample preparation procedures for biological atomic force microscopy , 2005 .

[36]  Jangwook P. Jung,et al.  Imaging cardiac extracellular matrices: a blueprint for regeneration. , 2012, Trends in biotechnology.

[37]  L. Chopinet,et al.  Atomic force and electron microscopic-based study of sarcolemmal surface of living cardiomyocytes unveils unexpected mitochondrial shift in heart failure. , 2014, Journal of molecular and cellular cardiology.

[38]  R. Duval,et al.  Nanoscale effects of antibiotics on P. aeruginosa. , 2011, Nanomedicine : nanotechnology, biology, and medicine.

[39]  D. Mozaffarian,et al.  Heart disease and stroke statistics--2010 update: a report from the American Heart Association. , 2010, Circulation.

[40]  Y. Dufrêne,et al.  Detection and localization of single molecular recognition events using atomic force microscopy , 2006, Nature Methods.

[41]  F. Conlon,et al.  Myocardial lineage development. , 2010, Circulation research.

[42]  Yves F Dufrêne,et al.  Direct measurement of hydrophobic forces on cell surfaces using AFM. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[43]  J. Latgé,et al.  High-resolution imaging of chemical and biological sites on living cells using peak force tapping atomic force microscopy. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[44]  Yves F Dufrêne,et al.  Force nanoscopy of cell mechanics and cell adhesion. , 2013, Nanoscale.

[45]  N. Dhalla,et al.  Defective calcium handling in cardiomyocytes isolated from hearts subjected to ischemia-reperfusion. , 2005, American journal of physiology. Heart and circulatory physiology.

[46]  E. Dague,et al.  Nanoscale analysis of the effects of antibiotics and CX1 on a Pseudomonas aeruginosa multidrug-resistant strain , 2012, Scientific Reports.

[47]  M. Denyer,et al.  Preliminary study on the suitability of a pharmacological bio-assay based on cardiac myocytes cultured over microfabricated microelectrode arrays , 1998, Medical and Biological Engineering and Computing.

[48]  Pulkki,et al.  Cardiomyocyte apoptosis and progression of heart failure to transplantation , 1999, European journal of clinical investigation.

[49]  H. Butt,et al.  Force measurements with the atomic force microscope: Technique, interpretation and applications , 2005 .

[50]  Yves F Dufrêne,et al.  Chemical force microscopy of single live cells. , 2007, Nano letters.

[51]  Yves F Dufrêne,et al.  High-resolution cell surface dynamics of germinating Aspergillus fumigatus conidia. , 2008, Biophysical journal.

[52]  D. Klenerman,et al.  Nanoscale live-cell imaging using hopping probe ion conductance microscopy , 2009, Nature Methods.

[53]  M. Rols,et al.  Imaging living cells surface and quantifying its properties at high resolution using AFM in QI™ mode. , 2013, Micron.

[54]  P. Hansma,et al.  Scanning tunneling microscopy and atomic force microscopy: application to biology and technology. , 1988, Science.

[55]  F. Matysik,et al.  Recent advances in high resolution scanning electrochemical microscopy of living cells--a review. , 2013, Analytica chimica acta.

[56]  B. Maisch,et al.  The use of endomyocardial biopsy in heart failure. , 1988, European heart journal.

[57]  M. Zheng,et al.  Acidosis-induced p38 MAPK activation and its implication in regulation of cardiac contractility. , 2004, Acta pharmacologica Sinica.

[58]  A. Bizzini,et al.  Force volume and stiffness tomography investigation on the dynamics of stiff material under bacterial membranes , 2012, Journal of molecular recognition : JMR.

[59]  E. Lakatta,et al.  Culture and adenoviral infection of adult mouse cardiac myocytes: methods for cellular genetic physiology. , 2000, American journal of physiology. Heart and circulatory physiology.

[60]  E. Ehler,et al.  Characterisation of postnatal growth of the murine heart , 2001, Anatomy and Embryology.

[61]  A. Leite-Moreira,et al.  Pathophysiology of chronic heart failure. , 2009, Revista portuguesa de cardiologia : orgao oficial da Sociedade Portuguesa de Cardiologia = Portuguese journal of cardiology : an official journal of the Portuguese Society of Cardiology.

[62]  J. Lead,et al.  Assessment of cross-flow filtration for the size fractionation of freshwater colloids and particles. , 2005, Talanta.

[63]  T. Pereira,et al.  Mesenchymal Stem Cells from Extra-Embryonic Tissues for Tissue Engineering – Regeneration of the Peripheral Nerve , 2013 .

[64]  W F Heinz,et al.  Spatially resolved force spectroscopy of biological surfaces using the atomic force microscope. , 1999, Trends in biotechnology.

[65]  Y. Dufrêne Application of atomic force microscopy to microbial surfaces: from reconstituted cell surface layers to living cells. , 2001, Micron.

[66]  Etienne Dague,et al.  Multiparametric imaging of adhesive nanodomains at the surface of Candida albicans by atomic force microscopy. , 2015, Nanomedicine : nanotechnology, biology, and medicine.

[67]  A. Terzic,et al.  Increased number of cardiomyocytes in cross-sections from tachycardia-induced cardiomyopathic hearts. , 1999, International journal of molecular medicine.

[68]  Wolfgang J. Parak,et al.  Mapping the mechanical pulse of single cardiomyocytes with the atomic force microscope , 1999, European Biophysics Journal.

[69]  J. François,et al.  Uncovering by Atomic Force Microscopy of an original circular structure at the yeast cell surface in response to heat shock , 2014, BMC Biology.

[70]  M. Masse,et al.  Primary cultures of embryonic rat heart cells , 1981, In Vitro.

[71]  A. Caminade,et al.  Probing single molecule interactions by AFM using bio-functionalized dendritips , 2012 .

[72]  H. Sawada,et al.  Performance of R005 Microscope and Aberration Correction System , 2008 .

[73]  L. Kirshenbaum,et al.  The interplay between cell death signaling pathways in the heart. , 2014, Trends in cardiovascular medicine.

[74]  N. Benech,et al.  Diabetes increases stiffness of live cardiomyocytes measured by atomic force microscopy nanoindentation. , 2014, American journal of physiology. Cell physiology.

[75]  William E Louch,et al.  Methods in cardiomyocyte isolation, culture, and gene transfer. , 2011, Journal of molecular and cellular cardiology.

[76]  G. Binnig,et al.  Tunneling through a controllable vacuum gap , 1982 .