Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-19T06:05:00.708Z Has data issue: false hasContentIssue false

Imaging the Cardiovascular System: Seeing Is Believing

Published online by Cambridge University Press:  12 May 2005

Thomas K. Borg
Affiliation:
Department of Cell and Developmental Biology and Anatomy, University of South Carolina, Columbia, SC 29208, USA
James A. Stewart
Affiliation:
Department of Cell and Developmental Biology and Anatomy, University of South Carolina, Columbia, SC 29208, USA
Michael A. Sutton
Affiliation:
Department of Mechanical Engineering, University of South Carolina, Columbia, SC 29208, USA
Get access

Abstract

From the basic light microscope through high-end imaging systems such as multiphoton confocal microscopy and electron microscopes, microscopy has been and will continue to be an essential tool in developing an understanding of cardiovascular development, function, and disease. In this review we briefly touch on a number of studies that illustrate the importance of these forms of microscopy in studying cardiovascular biology. We also briefly review a number of imaging modalities such as computed tomography, (CT) Magnetic resonance imaging (MRI), ultrasound, and positron emission tomography (PET) that, although they do not fall under the realm of microscopy, are imaging modalities that greatly complement microscopy. Finally we examine the role of proper imaging system calibration and the potential importance of calibration in understanding biological tissues, such as the cardiovascular system, that continually undergo deformation in response to strain.

Type
Research Article
Copyright
© 2005 Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abdul-Karim, M.A., Al-Kofahi, K., Brown, E.B., Jain, R.K., & Roysam, B. (2003). Automated tracing and change analysis of angiogenic vasculature from in vivo multiphoton confocal image time series. Microvasc Res 66, 113125.Google Scholar
Ballou, B., Lagerholm, B.C., Ernst, L.A., Bruchez, M.P., & Waggoner, A.S. (2004). Noninvasive imaging of quantum dots in mice. Bioconjugate Chem 15, 7986.Google Scholar
Barker, J., Price, R.L., & Gourdie, R. (2002). Increased association of ZO-1 with connexin43 during remodeling of cardiac gap junctions. Circ Res 90, 317324.Google Scholar
Bay, B.K., Smith, T.S., Fyhrie, D.P., & Saad, M. (1999). Digital volume correlation: Three-dimensional strain mapping using x-ray tomography. Exp Mech 39, 217226.Google Scholar
Bay, B.K., Smith, T.S., & Rashid, M. (2002). Digital volume correlation including rotational degrees of freedom during minimization. Exp Mech 42, 272278.Google Scholar
Biskup, A., Zimmer, T., & Benndorf, K. (2004). FRET between cardiac Na+ channel subunits measured with a confocal microscope and a streak camera. Nat Biotechnol 22, 220224.Google Scholar
Borg, T.K. & Caulfield, J.B. (1981). The collagen matrix of the heart. Fed Proc 40, 20372041.Google Scholar
Brand, P. (1995). Reconstruction tridimension-nelle a partir d'une camera en mouvement: Del'inuence de la precision. Ph.D. thesis, Claude Bernard University, Lyon I, France.
Bruck, H.A. (2002). Biological and biologically inspired materials—Guest editorial. Exp Mech 42, 359361.Google Scholar
Budinger, T.F., Benaron, D.A., & Koretsky, A.P. (1999). Imaging transgenic animals. Ann Rev Biomed Eng 1, 611648.Google Scholar
Bullard, T.A., Borg, T.K., & Price, R.L. (2005). The expression and role of protein kinase C in neonatal cardiac myocyte attachment, cell volume, and myofibril formation is dependent on the composition of the extracellular matrix. Microsc Microanal 11, 224234.Google Scholar
Byeon, M.K., Sugi, Y., Markwald, R.R., & Hoffman, S. (1995). NCAM polypeptides in heart development: Association with Z discs of forms that contain the muscle-specific domain. J Cell Biol 128, 209221.Google Scholar
Carver, W., Price, R.L., Raso, D.S., Terracio, L., & Borg, T.K. (1994). Distribution of β-1 integrin in the developing rat heart. J Histochem Cytochem 42, 167175.Google Scholar
Chu, T.C., Ranson, W.F., Sutton, M.A., & Peters, W.H., III. (1985). Application of digital image correlation techniques to experimental mechanics. Exp Mech 25, 232245.Google Scholar
Croissant, J.D., Carpenter, S., & Bader, D. (2001). Molecular mechanisms of cardiac diversification. In Formation of the Heart and Its Regulation, Tomanek, R.J. & Runyan, R.B. (Eds.), pp. 97108. Boston, MA: Birkhauser.
Dennie, J., Mandeville, J.B., Boxerman, J.L., Packard, S.D., Rosen, B.R., & Weeisskoff, R.M. (1998). NMR imaging of changes in vascular morphology due to tumor angiogenesis. Magn Reson Med 40, 793799.Google Scholar
Ding, B.O., Price, R.L., Goldsmith, E.C., Borg, T.K., Yan, X., Douglas, P.S., Ma, L., Weinberg, E.O., Thielen, T., Bartunek, J., & Lorell, B.H. (2000). Left ventricular hypertrophy in ascending aortic stenosis mice: Anoikis and the progression to early failure. Circulation 101, 28542862.Google Scholar
Efimov, I.R., Nikolski, V.P., & Salama, G. (2004). Optical imaging of the heart. Circ Res 94, 2133.Google Scholar
Ehler, E., Horowits, R., Zuppinger, C., Price, R.L., Perriard, E., Leu, M., Caroni, P., Sussman, M., Eppenberger, H.M., & Perriard, J.C. (2001). Alterations at the intercalated disk associated with dilated cardiomyopathy in two mouse models. J Cell Biol 153, 763772.Google Scholar
Ellis, E.F., McKinney, J.S., Willoughby, K.A., Liang, S., & Povlishock, T.J. (1995). A new model for rapid stretch-induced injury of cells in culture: Characterization of the model using astrocytes. J Neurotrauma 12, 325339.Google Scholar
Evans, H.J., Sweet, J.K., Price, R.L., Yost, M., & Goodwin, R.L. (2003). A novel 3-D culture system for the study of cardiac myocyte development. Am J Physiol (Heart Circ Physiol) 285, H570578.Google Scholar
Funderburg, F.M. & Markwald, R.R. (1986). Conditioning of native substrates by chondroitin sulfate proteoglycans during cardiac mesenchymal cell migration. J Cell Biol 103, 24752487.Google Scholar
Gillies, R., Bhujwalla, Z.M., Evelhoch, J., Garwood, M., Neeman, M., Robinson, S.P., Stoak, C.H., & Van Der Sanden, B. (2000). Applications of magnetic resonance in model systems: Tumor biology and physiology. Neoplasia 2, 139151.Google Scholar
Goldsmith, E.C., Carver, W., McFadden, A., Goldsmith, J.G., Price, R.L., Sussman, M., Lorell, B.H., Cooper, G., & Borg, T.K. (2003). Integrin shedding as a mechanism of cellular adaptation during cardiac growth. Am J Physiol (Heart Circ Physiol) 284, H22272234.Google Scholar
Goldsmith, E.C., Hoffman, A., Morales, M.O., Potts, J.D., Price, R.L., McFadden, A., Rice, M., & Borg, T.K. (2004). Organization of fibroblasts in the heart. Dev Dyn 230, 787794.Google Scholar
Helm, J.D., McNeill, S.R., & Sutton, M.A. (1996). Improved 3-D image correlation for surface displacement measurement. Opt Eng 35, 19111920.Google Scholar
Herschman, H.R. (2003). Micro-PET imaging and small animal models of disease. Curr Opin Immunol 15, 378384.Google Scholar
Hunter, P.J. & Borg, T.K. (2003). Innovation: Integration from proteins to organs: The Physiome Project. Nat Rev Mol Cell Biol 4, 237243.Google Scholar
Jaffer, F.A. & Weissleder, R. (2004). Seeing within. Molecular imaging of the cardiovascular system. Circ Res 94, 433445.Google Scholar
Jares-Erijman, E.A. & Jovin, T.M. (2003). FRET imaging. Nat Biotechnol 21, 13871395.Google Scholar
Jerome, W.G., Handt, S., & Hantgan, R.R. (2005). Endothelial cells organize fibrin clots into structures that are more resistant to lysis. Microsc Microanal 11, 268277.Google Scholar
Josephson, L., Perez, M., & Weissleder, R. (2001). Magnetic nanosensors of detection of oligonucleotide sequences. Angew Chem (Int Ed Eng) 40, 32043206.Google Scholar
Kirby, M.L. (2001). Getting to the heart of cardiac morphogenesis. Circ Res 88, 370372.Google Scholar
Lakatta, E.G., Maltsev, V.A., Bogdanov, K.Y., Stern, M.D., & Vinogradova, T.M. (2003). Cyclic variation of intracellular calcium: A critical factor for cardiac pacemaker cell dominance. Circ Res 21, e4550.Google Scholar
Lin, J.J-C., Wang, D., Reiter, R.S., Wang, Q., Lin, J.L-C., & Williams, H.S. (2001). Differentially expressed genes and cardiac morphogenesis. In Formation of the Heart and Its Regulation, Tomanek, R.J. & Runyan, R.B. (Eds.), pp. 7596. Boston, MA: Birkhauser.
Linder, E. (1960). Myofibrils in the early development of the chick embryo hearts as observed with the electron microscope. Anat Rec 180, 234235.Google Scholar
Luo, P.F., Chao, Y.J., & Sutton, M.A. (1993). Accurate measurement of three-dimensional deformations in deformable and rigid bodies using computer vision. Exp Mech 33, 123133.Google Scholar
Manasek, F.J. (1968). Embryonic development of the heart. I. A light and electron microscopic study of myocardial development in the early chick embryo. J Morphol 125, 329365.Google Scholar
Markwald, R.R. (1973). Distribution and relationship of precursor Z material to organizing myofibrillar bundles in embryonic rat and hamster ventricular myocytes. J Mol Cell Cardiol 5, 341350.Google Scholar
Miller, C.E., Thompson, R.P., Bigelow, M.R., Gittinger, G., Trusk, T.C., & Sedmera, D. (2005). Confocal imaging of the embryonic heart: How deep? Microsc Microanal 11, 216223.Google Scholar
Miller, C.E., Vanni, M.A., Taber, L.A., & Keller, B.B. (1997). Passive stress-strain measurements in the stage-16 and stage-18 embryonic chick heart. J Biomech Eng 119, 445451.Google Scholar
Mitchell, H.L., Kniest, H.T., & Won-Jin, O. (1999). Digital photogrammetry and microscope photographs. Photogrammetric Rec 16, 695704.Google Scholar
Morales, M.O., Price, R.L., & Goldsmith, E.C. (2005). Expression of discoidin domain receptor 2 (DDR2) in the developing heart. Microsc Microanal 11, 260267.Google Scholar
Nakayama, M., Yan, X., Price, R.L., Borg, T.K., Ito, K., Sanbe, A., Robbins, J., & Lorell, B.H. (2005). Chronic ventricular myocyte specific overexpression of angiotensin II type 2 receptor results in intrinsic myocyte contractile dysfunction. Am J Physiol 288, H317H327.Google Scholar
Pautler, R.G. & Fraser, S.E. (2003). The year(s) of the contrast agent—micro-MRI in the new millennium. Curr Opin Immunol 15, 385392.Google Scholar
Pexieder, T. (1988). SEM in studies on abnormal cardiac development. Teratology 37, 289292.Google Scholar
Pfister, B.J., Weihs, T.P., Betenbaugh, M., & Bao, G. (2003). An in vitro uniaxial stretch model for axonal injury. Ann Biomed Eng 31, 589598.Google Scholar
Plank, D.M. & Sussman, M.A. (2005). Impaired intracellular Ca2+ dynamics in live cardiomyocytes revealed by rapid line scan confocal microscopy. Microsc Microanal 11, 235243.Google Scholar
Price, R.L., Carver, W., Simpson, D.G., Fu, L., Zhao, J., Borg, T.K., & Terracio, L. (1997). The effects of angiotensin II and specific angiotensin receptor blockers on embryonic cardiac development and looping patterns. Dev Biol 192, 572584.Google Scholar
Price, R.L., Nakagawa, M., Terracio, L., & Borg, T.K. (1992). Ultrastructural localization of laminin on in vivo embryonic, neonatal, and adult rat cardiac myocytes and in early rat embryos raised in whole embryo culture. J Histochem Cytochem 40, 13731381.Google Scholar
Price, R.L., Thielen, T.R., Borg, T.K., & Terracio, L. (2001). Cardiac defects associated with the absence of the platelet-derived growth factor alpha receptor in the Patch mouse. Microsc Microanal 7, 5665.Google Scholar
Ravn, O., Andersen, N.A., & Sorensen, A.T. (1993). Auto-calibration in automation systems using vision. In Proceedings of the 3rd International Symposium on Experimental Robotics—ISER'93, Koyoto, Japan, October 1993. pp. 206218.
Rosenquist, T.H. & Monaghan, D.T. (2001). Homocysteine and the N-methyl-d-aspartate (NMDA) receptor: Are they keys to conotruncal abnormalities? In Formation of the Heart and Its Regulation, Tomanek, R.J. & Runyan, R.B. (Eds.), pp. 251272. Boston, MA: Birkhauser.
Rubart, M., Wang, E., Dunn, K.W., & Field, L.J. (2003). Two photon molecular excitation imaging of Ca2+ transients in Langendorff-perfused mouse hearts. Am J Physiol Cell Physiol 284, C16541668.Google Scholar
Rudim, M. & Weissleder, R. (2003). Molecular imaging in drug discovery and development. Nat Rev Drug Discov 2, 123131.Google Scholar
Schreier, H.W., Braasch, J., & Sutton, M.A. (2000). On systematic errors in digital image correlation. Opt Eng 39, 29152921.Google Scholar
Schreier, H.W., Garcia, D., & Sutton, M.A. (2004). Advances in stereo light microscopy. Exp Mech 44, 278289.Google Scholar
Schreier, H.W. & Sutton, M.A. (2002). Effect of higher order displacement fields on digital image correlation displacement component estimates. Exp Mech 42, 303311.Google Scholar
Sedmera, D., Reckova, M., Rosengarten, C., Torres, M.I., Gourdie, R.G., & Thompson, R.P. (2005). Optical mapping of electrical activation in the developing heart. Microsc Microanal 11, 209215.Google Scholar
Seki, S., Magashima, M., Yamada, Y., Tsutsuura, M., Kobayashi, T., Namiki, A., & Tohse, N. (2003). Fetal and postnatal development of Ca++ transients and Ca++ sparks in rat cardiomyocytes. Cardiovasc Res 58, 535548.Google Scholar
Shields, A.F., Grierson, J.R., Dohmen, B.M., Machulla, H.J., Stayanoff, J.C., Lawhorn-Crews, J.M., Obradovich, J.E., Muzik, O., & Mangner, T.J. (1998). Imaging proliferation in vivo with [18F]FLT and positron tomography. Nat Med 4, 13341336.Google Scholar
Shiraishi, I., Takamatsu, T., Price, R.L., & Fujita, S. (1997). Temporal and spatial patterns of phosphotyrosine immunolocalization during cardiac myofibrillogenesis of the chicken embryo. Anat Embryol 196, 8188.Google Scholar
Sipkins, D.A., Cheresgm, D.A., Kazemi, M.R., Nevin, L.M., Bednarski, M.D., & Li, K.C. (1998). Detection of tumor angiogenesis in vivo by αvβ3-targeted magnetic resonance imaging. Nat Med 4, 623626.Google Scholar
Soufan, A.T, Ruijter, J.M., van den Hoff, M.J., de Boer, P.A., Hagoort, J., & Moorman, A.F. (2003). Three dimensional reconstruction of gene expression patterns during cardiac development. Physiol Genom 13, 187195.Google Scholar
Stato, M., Johnson, M., Zhang, B., Le, K., Gambhir, S.S., Carey, M., & Wu, L. (2003). Optimization of adenoviral vectors to directly amplified prostrate-specific expression for imaging and gene therapy. Mol Ther 8, 726737.Google Scholar
Streeter, D.D., Jr. (1979). Gross morphology and fiber geometry of the heart. In Handbook of Physiology, The Cardiovascular System 1, Verne, R.M. (Ed.), pp. 61112. Washington, DC: American Physiology Society.
Sutton, M.A., Cheng, M.Q., Peters, W.H., III, Chao, Y.J., & McNeill, S.R. (1986). Application of an optimized digital correlation method to planar deformation analysis. Image Vis Comput 4, 143150.Google Scholar
Sutton, M.A., McNeill, S.R., Helm, J.D., & Schreier, H.W. (2000). Computer vision applied to shape and deformation measurement. In Trends in Optical Non-Destructive Testing and Inspection, Rastogi, P.K. & Inaudi, D. (Eds.) pp. 571591. New York: Elsevier.
Taber, L.A., Lin, I.E., & Clark, E.B. (1995). Mechanics of cardiac looping. Dev Dyn 203, 4250.Google Scholar
Tauer, U. (2002). Advantages and risks of multiphoton microscopy in physiology. Exp Physiol 87, 709714.Google Scholar
Triggs, B., McLauchlan, P., Hartley, R., & Fitzgibbon, A. (1999). Bundle adjustment-A modern synthesis. Proceedings of the ICCV Workshop on Vision Algorithms, 1999, Corfu, Greece. pp. 298372.
Wang, J.J., Clermont, P., & Yin, F.C. (2000). Contractility affects stress fiber remodeling and reorientation of endothelial cells subjected to cyclic mechanical stretching. Ann Biomed Eng 28, 11651171.Google Scholar
Weissleder, R. (2002). Scaling down imaging: Molecular mapping of cancer in mice. Nat Rev Cancer 2, 1118.Google Scholar
Weissleder, R., Elizondo, G., Wittenberg, J., Rabito, C.A, Bengele, H.H., & Josephson, L. (1990). Ultrasmall superparamagnetic iron oxide: Characterization of a new class of contrast agents for MR imaging. Radiology 175, 489493.Google Scholar
Yan, X., Price, R.L., Nakayama, M., Ito, K., Schuldt, A., Manning, W.J., Sanbe, A., Borg, T.K., Robbins, J., & Lorell, B.H. (2003). Ventricular specific expression of angiotensin II Type 2 receptor causes dilated cardiomyopathy and heart failure in transgenic mice. Am J Physiol (Heart Circ Physiol) 285, H21792187.Google Scholar
Yelbuz, T.M., Waldo, K.L., Zhang, X., Zdanoicz, M., Parker, J., Creazzo, T.L., Johnson, G.A., & Kirby, M.L. (2003). Myocardial volume and organization are changed by failure of addition of secondary heart field myocardium to the cardiac outflow tract. Dev Dyn 228, 152160.Google Scholar
Yost, M.J, Baicu, C.F., Stonerock, C.E., Goodwin, R.L., Price, R.L., Davis, J.M., Evans, H., Watson, P.D., Gore, C.M., Sweet, J., Creech, L., Zile, M.R., & Terracio, L. (2004). A novel tubular scaffold for cardiovascular tissue engineering. Tissue Eng 10, 273284.Google Scholar
Zaccolo, M. (2004). Use of chimeric fluorescent proteins and fluorescence resonance energy to monitor cellular responses. Circ Res 94, 866873.Google Scholar
Zagar, B., Fornaris, R., & Ferrara, K. (1998). Evaluation of tumor angiogenesis with US: Imaging, Doppler and contrast agents. Acad Radiol 7, 809824.Google Scholar
Zhang, Z. (1999). A flexible new technique for camera calibration. Microsoft Technical Report MSR-TR-98-71. Available at research.microsoft.com/research/pubs/view.aspx?pubid=843.
Zima, A.V., Kockskamper, J., Mejia-alvarez, R., & Blatter, L.A. (2003). Pyruvate modulates cardiac sarcoplasmic reticulum Ca++ release in rats via mitochondria-dependent and -independent mechanisms. J Physiol 550(Pt3), 765783.Google Scholar