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Published in: Journal of Cardiovascular Magnetic Resonance 1/2015

Open Access 01-12-2015 | Research

Magnetic susceptibility anisotropy of myocardium imaged by cardiovascular magnetic resonance reflects the anisotropy of myocardial filament α-helix polypeptide bonds

Authors: Russell Dibb, Yi Qi, Chunlei Liu

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2015

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Abstract

Background

A key component of evaluating myocardial tissue function is the assessment of myofiber organization and structure. Studies suggest that striated muscle fibers are magnetically anisotropic, which, if measurable in the heart, may provide a tool to assess myocardial microstructure and function.

Methods

To determine whether this weak anisotropy is observable and spatially quantifiable with cardiovascular magnetic resonance (CMR), both gradient-echo and diffusion-weighted data were collected from intact mouse heart specimens at 9.4 Tesla. Susceptibility anisotropy was experimentally calculated using a voxelwise analysis of myocardial tissue susceptibility as a function of myofiber angle. A myocardial tissue simulation was developed to evaluate the role of the known diamagnetic anisotropy of the peptide bond in the observed susceptibility contrast.

Results

The CMR data revealed that myocardial tissue fibers that were parallel and perpendicular to the magnetic field direction appeared relatively paramagnetic and diamagnetic, respectively. A linear relationship was found between the magnetic susceptibility of the myocardial tissue and the squared sine of the myofiber angle with respect to the field direction. The multi-filament model simulation yielded susceptibility anisotropy values that reflected those found in the experimental data, and were consistent that this anisotropy decreased as the echo time increased.

Conclusions

Though other sources of susceptibility anisotropy in myocardium may exist, the arrangement of peptide bonds in the myofilaments is a significant, and likely the most dominant source of susceptibility anisotropy. This anisotropy can be further exploited to probe the integrity and organization of myofibers in both healthy and diseased heart tissue.
Literature
2.
go back to reference Torbet J, Dickens MJ. Orientation of skeletal muscle actin in strong magnetic fields. FEBS Lett. 1984;173:403–6.PubMedCrossRef Torbet J, Dickens MJ. Orientation of skeletal muscle actin in strong magnetic fields. FEBS Lett. 1984;173:403–6.PubMedCrossRef
3.
go back to reference Bovendeerd PHM, Arts T, Huyghe JM, van Campen DH, Reneman RS. Dependence of local left ventricular wall mechanics on myocardial fiber orientation: A model study. J Biomech. 1992;25:1129–40.PubMedCrossRef Bovendeerd PHM, Arts T, Huyghe JM, van Campen DH, Reneman RS. Dependence of local left ventricular wall mechanics on myocardial fiber orientation: A model study. J Biomech. 1992;25:1129–40.PubMedCrossRef
4.
go back to reference Tezuka F. Muscle fiber orientation in normal and hypertrophied hearts. Tohoku J Exp Med. 1975;117:289–97.PubMedCrossRef Tezuka F. Muscle fiber orientation in normal and hypertrophied hearts. Tohoku J Exp Med. 1975;117:289–97.PubMedCrossRef
5.
go back to reference Wickline SA, Verdonk ED, Wong AK, Shepard RK, Miller JG. Structural remodeling of human myocardial tissue after infarction. Quantification with ultrasonic backscatter. Circulation. 1992;85:259–68.PubMedCrossRef Wickline SA, Verdonk ED, Wong AK, Shepard RK, Miller JG. Structural remodeling of human myocardial tissue after infarction. Quantification with ultrasonic backscatter. Circulation. 1992;85:259–68.PubMedCrossRef
6.
go back to reference Strijkers GJ, Bouts A, Blankesteijn WM, Peeters TH, Vilanova A, van Prooijen MC, et al. Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse. NMR Biomed. 2009;22:182–90.PubMedCrossRef Strijkers GJ, Bouts A, Blankesteijn WM, Peeters TH, Vilanova A, van Prooijen MC, et al. Diffusion tensor imaging of left ventricular remodeling in response to myocardial infarction in the mouse. NMR Biomed. 2009;22:182–90.PubMedCrossRef
7.
go back to reference Fenton F, Karma A. Vortex dynamics in three-dimensional continuous myocardium with fiber rotation: Filament instability and fibrillation. Chaos (Woodbury, NY). 1998;8:20–47.CrossRef Fenton F, Karma A. Vortex dynamics in three-dimensional continuous myocardium with fiber rotation: Filament instability and fibrillation. Chaos (Woodbury, NY). 1998;8:20–47.CrossRef
8.
go back to reference Hsu EW, Muzikant AL, Matulevicius SA, Penland RC, Henriquez CS. Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation. Am J Physiol. 1998;274:H1627–34.PubMed Hsu EW, Muzikant AL, Matulevicius SA, Penland RC, Henriquez CS. Magnetic resonance myocardial fiber-orientation mapping with direct histological correlation. Am J Physiol. 1998;274:H1627–34.PubMed
9.
go back to reference Scollan DF, Holmes A, Winslow R, Forder J. Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging. Am J Physiol. 1998;275:H2308–18.PubMed Scollan DF, Holmes A, Winslow R, Forder J. Histological validation of myocardial microstructure obtained from diffusion tensor magnetic resonance imaging. Am J Physiol. 1998;275:H2308–18.PubMed
10.
go back to reference Sosnovik DE, Mekkaoui C, Huang S, Chen HH, Dai G, Stoeck CT, et al. Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo. Circulation. 2014;129:1731–41.PubMedCentralPubMedCrossRef Sosnovik DE, Mekkaoui C, Huang S, Chen HH, Dai G, Stoeck CT, et al. Microstructural impact of ischemia and bone marrow-derived cell therapy revealed with diffusion tensor magnetic resonance imaging tractography of the heart in vivo. Circulation. 2014;129:1731–41.PubMedCentralPubMedCrossRef
11.
go back to reference Köhler S, Hiller K-H, Waller C, Jakob PM, Bauer WR, Haase A. Visualization of myocardial microstructure using high-resolution T2* imaging at high magnetic field. Magn Reson Med. 2003;49:371–5.PubMedCrossRef Köhler S, Hiller K-H, Waller C, Jakob PM, Bauer WR, Haase A. Visualization of myocardial microstructure using high-resolution T2* imaging at high magnetic field. Magn Reson Med. 2003;49:371–5.PubMedCrossRef
12.
go back to reference Yamada N, Imakita S, Sakuma T, Takamiya M. Intracranial calcification on gradient-echo phase image: depiction of diamagnetic susceptibility. Radiology. 1996;198:171–8.PubMedCrossRef Yamada N, Imakita S, Sakuma T, Takamiya M. Intracranial calcification on gradient-echo phase image: depiction of diamagnetic susceptibility. Radiology. 1996;198:171–8.PubMedCrossRef
15.
go back to reference Lee J, Shmueli K, Fukunaga M, van Gelderen P, Merkle H, Silva AC, et al. Sensitivity of MRI resonance frequency to the orientation of brain tissue microstructure. Proc Natl Acad Sci USA. 2010;107(11):5130–5.PubMedCentralPubMedCrossRef Lee J, Shmueli K, Fukunaga M, van Gelderen P, Merkle H, Silva AC, et al. Sensitivity of MRI resonance frequency to the orientation of brain tissue microstructure. Proc Natl Acad Sci USA. 2010;107(11):5130–5.PubMedCentralPubMedCrossRef
16.
go back to reference Xie L, Dibb R, Cofer GP, Li W, Nicholls PJ, Johnson GA, et al. Susceptibility tensor imaging of the kidney and its microstructural underpinnings. Magn Reson Med. 2014;73:1270–81.PubMedCrossRef Xie L, Dibb R, Cofer GP, Li W, Nicholls PJ, Johnson GA, et al. Susceptibility tensor imaging of the kidney and its microstructural underpinnings. Magn Reson Med. 2014;73:1270–81.PubMedCrossRef
17.
go back to reference Pauling L, Corey RB, Branson HR. The structure of proteins; two hydrogen-bonded helical configurations of the polypeptide chain. Proc Natl Acad Sci USA. 1951;37:205–11.PubMedCentralPubMedCrossRef Pauling L, Corey RB, Branson HR. The structure of proteins; two hydrogen-bonded helical configurations of the polypeptide chain. Proc Natl Acad Sci USA. 1951;37:205–11.PubMedCentralPubMedCrossRef
20.
go back to reference Angeli S, Befera N, Peyrat J-M, Calabrese E, Johnson GA, Constantinides C. A high-resolution cardiovascular magnetic resonance diffusion tensor map from ex-vivo C57BL/6 murine hearts. J Cardiovasc Magn Reson. 2014;16:77.PubMedCentralPubMedCrossRef Angeli S, Befera N, Peyrat J-M, Calabrese E, Johnson GA, Constantinides C. A high-resolution cardiovascular magnetic resonance diffusion tensor map from ex-vivo C57BL/6 murine hearts. J Cardiovasc Magn Reson. 2014;16:77.PubMedCentralPubMedCrossRef
21.
go back to reference Li W, Avram AV, Wu B, Xiao X, Liu C. Integrated Laplacian-based phase unwrapping and background phase removal for quantitative susceptibility mapping. NMR Biomed. 2014;27:219–27.PubMedCentralPubMedCrossRef Li W, Avram AV, Wu B, Xiao X, Liu C. Integrated Laplacian-based phase unwrapping and background phase removal for quantitative susceptibility mapping. NMR Biomed. 2014;27:219–27.PubMedCentralPubMedCrossRef
22.
go back to reference Salomir R, de Senneville BD, Moonen CTW. A fast calculation method for magnetic field inhomogeneity due to an arbitrary distribution of bulk susceptibility. Concepts Magn Reson B. 2003;19B:26–34.CrossRef Salomir R, de Senneville BD, Moonen CTW. A fast calculation method for magnetic field inhomogeneity due to an arbitrary distribution of bulk susceptibility. Concepts Magn Reson B. 2003;19B:26–34.CrossRef
23.
go back to reference Shmueli K, de Zwart JA, van Gelderen P, Li T-Q, Dodd SJ, Duyn JH. Magnetic susceptibility mapping of brain tissue in vivo using MRI phase data. Magn Reson Med. 2009;62:1510–22.PubMedCentralPubMedCrossRef Shmueli K, de Zwart JA, van Gelderen P, Li T-Q, Dodd SJ, Duyn JH. Magnetic susceptibility mapping of brain tissue in vivo using MRI phase data. Magn Reson Med. 2009;62:1510–22.PubMedCentralPubMedCrossRef
24.
go back to reference Liu T, Spincemaille P, de Rochefort L, Kressler B, Wang Y. Calculation of susceptibility through multiple orientation sampling (COSMOS): A method for conditioning the inverse problem from measured magnetic field map to susceptibility source image in MRI. Magn Reson Med. 2009;61:196–204.PubMedCrossRef Liu T, Spincemaille P, de Rochefort L, Kressler B, Wang Y. Calculation of susceptibility through multiple orientation sampling (COSMOS): A method for conditioning the inverse problem from measured magnetic field map to susceptibility source image in MRI. Magn Reson Med. 2009;61:196–204.PubMedCrossRef
25.
go back to reference de Rochefort L, Liu T, Kressler B, Liu J, Spincemaille P, Lebon V, et al. Quantitative susceptibility map reconstruction from MR phase data using bayesian regularization: validation and application to brain imaging. Magn Reson Med. 2010;63:194–206.PubMed de Rochefort L, Liu T, Kressler B, Liu J, Spincemaille P, Lebon V, et al. Quantitative susceptibility map reconstruction from MR phase data using bayesian regularization: validation and application to brain imaging. Magn Reson Med. 2010;63:194–206.PubMed
27.
28.
go back to reference Wang R, Benner T, Sorensen AG, Weeden VJ. Diffusion Toolkit: A Software Package for Diffusion Imaging Data Processing and Tractography. In: Proceedings of the 15th Annual ISMRM, Berlin, Germany. 2007. p. 3720. Wang R, Benner T, Sorensen AG, Weeden VJ. Diffusion Toolkit: A Software Package for Diffusion Imaging Data Processing and Tractography. In: Proceedings of the 15th Annual ISMRM, Berlin, Germany. 2007. p. 3720.
29.
go back to reference Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage. 2006;31:1116–28.PubMedCrossRef Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage. 2006;31:1116–28.PubMedCrossRef
30.
go back to reference Kabsch W, Mannherz HG, Suck D. Three-dimensional structure of the complex of actin and DNase I at 4.5 A resolution. EMBO J. 1985;4:2113–8.PubMedCentralPubMed Kabsch W, Mannherz HG, Suck D. Three-dimensional structure of the complex of actin and DNase I at 4.5 A resolution. EMBO J. 1985;4:2113–8.PubMedCentralPubMed
32.
go back to reference Pepe FA, Ashton FT, Street C, Weisel J. The myosin filament. X. Observation of nine subfilaments in transverse sections. Tissue Cell. 1986;18:499–508.PubMedCrossRef Pepe FA, Ashton FT, Street C, Weisel J. The myosin filament. X. Observation of nine subfilaments in transverse sections. Tissue Cell. 1986;18:499–508.PubMedCrossRef
33.
34.
go back to reference Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC. Atomic structure of the actin: DNase I complex. Nature. 1990;347:37–44.PubMedCrossRef Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC. Atomic structure of the actin: DNase I complex. Nature. 1990;347:37–44.PubMedCrossRef
35.
go back to reference Luna A, Amekraz B, Tortajada J, Morizur JP, Alcamí M, Mó O, et al. Modeling the Interactions between Peptide Functions and Cu(I): Formamide − Cu + Reactions in the Gas Phase. J Am Chem Soc. 1998;120:5411–26.CrossRef Luna A, Amekraz B, Tortajada J, Morizur JP, Alcamí M, Mó O, et al. Modeling the Interactions between Peptide Functions and Cu(I): Formamide − Cu + Reactions in the Gas Phase. J Am Chem Soc. 1998;120:5411–26.CrossRef
36.
go back to reference Tigelaar HL, Flygare WH. Molecular zeeman effect in formamide and the alpha-proton chemical shift in poly(L-alanine). J Am Chem Soc. 1972;94:343–6.PubMedCrossRef Tigelaar HL, Flygare WH. Molecular zeeman effect in formamide and the alpha-proton chemical shift in poly(L-alanine). J Am Chem Soc. 1972;94:343–6.PubMedCrossRef
37.
go back to reference Nordhoy W, Anthonsen HW, Bruvold M, Brurok H, Skarra S, Krane J, et al. Intracellular manganese ions provide strong T1 relaxation in rat myocardium. Magn Reson Med. 2004;52:506–14.PubMedCrossRef Nordhoy W, Anthonsen HW, Bruvold M, Brurok H, Skarra S, Krane J, et al. Intracellular manganese ions provide strong T1 relaxation in rat myocardium. Magn Reson Med. 2004;52:506–14.PubMedCrossRef
38.
go back to reference Aliev MK, Dos Santos P, Hoerter JA, Soboll S, Tikhonov AN, Saks VA. Water content and its intracellular distribution in intact and saline perfused rat hearts revisited. Cardiovasc Res. 2002;53:48–58.PubMedCrossRef Aliev MK, Dos Santos P, Hoerter JA, Soboll S, Tikhonov AN, Saks VA. Water content and its intracellular distribution in intact and saline perfused rat hearts revisited. Cardiovasc Res. 2002;53:48–58.PubMedCrossRef
39.
go back to reference Chu SC, Xu Y, Balschi JA, Springer CS. Bulk magnetic susceptibility shifts in NMR studies of compartmentalized samples: use of paramagnetic reagents. Magn Reson Med. 1990;13:239–62.PubMedCrossRef Chu SC, Xu Y, Balschi JA, Springer CS. Bulk magnetic susceptibility shifts in NMR studies of compartmentalized samples: use of paramagnetic reagents. Magn Reson Med. 1990;13:239–62.PubMedCrossRef
40.
go back to reference Barth E, Stämmler G, Speiser B, Schaper J. Ultrastructural quantitation of mitochondria and myofilaments in cardiac muscle from 10 different animal species including man. J Mol Cell Cardiol. 1992;24:669–81.PubMedCrossRef Barth E, Stämmler G, Speiser B, Schaper J. Ultrastructural quantitation of mitochondria and myofilaments in cardiac muscle from 10 different animal species including man. J Mol Cell Cardiol. 1992;24:669–81.PubMedCrossRef
42.
go back to reference Dibb R, Li W, Cofer G, Liu C. Microstructural origins of gadolinium-enhanced susceptibility contrast and anisotropy. Magn Reson Med. 2014;72:1702–11.PubMedCrossRef Dibb R, Li W, Cofer G, Liu C. Microstructural origins of gadolinium-enhanced susceptibility contrast and anisotropy. Magn Reson Med. 2014;72:1702–11.PubMedCrossRef
43.
go back to reference Adzamli IK, Jolesz FA, Bleier AR, Mulkern RV, Sandor T. The effect of gadolinium DTPA on tissue water compartments in slow- and fast-twitch rabbit muscles. Magn Reson Med. 1989;11:172–81.PubMedCrossRef Adzamli IK, Jolesz FA, Bleier AR, Mulkern RV, Sandor T. The effect of gadolinium DTPA on tissue water compartments in slow- and fast-twitch rabbit muscles. Magn Reson Med. 1989;11:172–81.PubMedCrossRef
44.
go back to reference Damon BM, Gregory CD, Hall KL, Stark HJ, Gulani V, Dawson MJ. Intracellular acidification and volume increases explain R2 decreases in exercising muscle. Magn Reson Med. 2002;47:14–23.PubMedCrossRef Damon BM, Gregory CD, Hall KL, Stark HJ, Gulani V, Dawson MJ. Intracellular acidification and volume increases explain R2 decreases in exercising muscle. Magn Reson Med. 2002;47:14–23.PubMedCrossRef
45.
go back to reference Carpenter JP, He T, Kirk P, Roughton M, Anderson LJ, de Noronha SV, et al. Calibration of myocardial T2 and T1 against iron concentration. J Cardiovasc Magn Reson. 2014;16:62.PubMedCentralPubMedCrossRef Carpenter JP, He T, Kirk P, Roughton M, Anderson LJ, de Noronha SV, et al. Calibration of myocardial T2 and T1 against iron concentration. J Cardiovasc Magn Reson. 2014;16:62.PubMedCentralPubMedCrossRef
46.
go back to reference Shepherd TM, Thelwall PE, Stanisz GJ, Blackband SJ. Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue. Magn Reson Med. 2009;62:26–34.PubMedCentralPubMedCrossRef Shepherd TM, Thelwall PE, Stanisz GJ, Blackband SJ. Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue. Magn Reson Med. 2009;62:26–34.PubMedCentralPubMedCrossRef
47.
go back to reference Wu B, Li W, Avram AV, Gho SM, Liu C. Fast and tissue-optimized mapping of magnetic susceptibility and T2* with multi-echo and multi-shot spirals. Neuroimage. 2012;59:297–305.PubMedCentralPubMedCrossRef Wu B, Li W, Avram AV, Gho SM, Liu C. Fast and tissue-optimized mapping of magnetic susceptibility and T2* with multi-echo and multi-shot spirals. Neuroimage. 2012;59:297–305.PubMedCentralPubMedCrossRef
48.
go back to reference Kucharczyk W, Henkelman RM. Visibility of calcium on MR and CT: can MR show calcium that CT cannot? Am J Neuroradiol. 1994;15:1145–8.PubMed Kucharczyk W, Henkelman RM. Visibility of calcium on MR and CT: can MR show calcium that CT cannot? Am J Neuroradiol. 1994;15:1145–8.PubMed
49.
go back to reference Moulder PV, Eichelberger L, Rams JJ, Greenburg AG. Water, nitrogen, and electrolyte content of right and left ventricular walls and interventricular septum of normal canine hearts. Circ Res. 1966;19:662–7.PubMedCrossRef Moulder PV, Eichelberger L, Rams JJ, Greenburg AG. Water, nitrogen, and electrolyte content of right and left ventricular walls and interventricular septum of normal canine hearts. Circ Res. 1966;19:662–7.PubMedCrossRef
51.
go back to reference Drott C, Lonnroth C, Lundholm K. Protein synthesis, myosin ATPase activity and myofibrillar protein composition in hearts from tumour-bearing rats and mice. Biochem J. 1989;264:191–8.PubMedCentralPubMed Drott C, Lonnroth C, Lundholm K. Protein synthesis, myosin ATPase activity and myofibrillar protein composition in hearts from tumour-bearing rats and mice. Biochem J. 1989;264:191–8.PubMedCentralPubMed
52.
go back to reference Bradshaw AD, Baicu CF, Rentz TJ, Van Laer AO, Bonnema DD, Zile MR. Age-dependent alterations in fibrillar collagen content and myocardial diastolic function: role of SPARC in post-synthetic procollagen processing. Am J Physiol Heart Circ Physiol. 2010;298:H614–22.PubMedCentralPubMedCrossRef Bradshaw AD, Baicu CF, Rentz TJ, Van Laer AO, Bonnema DD, Zile MR. Age-dependent alterations in fibrillar collagen content and myocardial diastolic function: role of SPARC in post-synthetic procollagen processing. Am J Physiol Heart Circ Physiol. 2010;298:H614–22.PubMedCentralPubMedCrossRef
53.
go back to reference Hunter RJ, Patel VB, Miell JP, Wong HJ, Marway JS, Richardson PJ, et al. Diarrhea reduces the rates of cardiac protein synthesis in myofibrillar protein fractions in rats in vivo. J Nutr. 2001;131:1513–9.PubMed Hunter RJ, Patel VB, Miell JP, Wong HJ, Marway JS, Richardson PJ, et al. Diarrhea reduces the rates of cardiac protein synthesis in myofibrillar protein fractions in rats in vivo. J Nutr. 2001;131:1513–9.PubMed
54.
go back to reference Bertini I, Luchinat C, Turano P, Battaini G, Casella L. The Magnetic Properties of Myoglobin as Studied by NMR Spectroscopy. Chemistry. 2003;9:2316–22.PubMedCrossRef Bertini I, Luchinat C, Turano P, Battaini G, Casella L. The Magnetic Properties of Myoglobin as Studied by NMR Spectroscopy. Chemistry. 2003;9:2316–22.PubMedCrossRef
55.
56.
go back to reference Riveros-Moreno V, Wittenberg JB. The Self-Diffusion Coefficients of Myoglobin and Hemoglobin in Concentrated Solutions. J Biol Chem. 1972;247:895–901.PubMed Riveros-Moreno V, Wittenberg JB. The Self-Diffusion Coefficients of Myoglobin and Hemoglobin in Concentrated Solutions. J Biol Chem. 1972;247:895–901.PubMed
57.
go back to reference Swaanenburg JC, Visser-VanBrummen PJ, DeJongste MJ, Tiebosch AT. The content and distribution of troponin I, troponin T, myoglobin, and alpha-hydroxybutyric acid dehydrogenase in the human heart. Am J Clin Pathol. 2001;115:770–7.PubMedCrossRef Swaanenburg JC, Visser-VanBrummen PJ, DeJongste MJ, Tiebosch AT. The content and distribution of troponin I, troponin T, myoglobin, and alpha-hydroxybutyric acid dehydrogenase in the human heart. Am J Clin Pathol. 2001;115:770–7.PubMedCrossRef
58.
go back to reference Naito A, Nagao T, Obata M, Shindo Y, Okamoto M, Yokoyama S, et al. Dynorphin induced magnetic ordering in lipid bilayers as studied by (31)P NMR spectroscopy. Biochim Biophys Acta. 2002;1558:34–44.PubMedCrossRef Naito A, Nagao T, Obata M, Shindo Y, Okamoto M, Yokoyama S, et al. Dynorphin induced magnetic ordering in lipid bilayers as studied by (31)P NMR spectroscopy. Biochim Biophys Acta. 2002;1558:34–44.PubMedCrossRef
59.
go back to reference Sachs HG, Colgan JA, Lazarus ML. Ultrastructure of the aging myocardium: A morphometric approach. Am J Anat. 1977;150:63–71.PubMedCrossRef Sachs HG, Colgan JA, Lazarus ML. Ultrastructure of the aging myocardium: A morphometric approach. Am J Anat. 1977;150:63–71.PubMedCrossRef
60.
61.
go back to reference Kensler RW. The mammalian cardiac muscle thick filament: Crossbridge arrangement. J Struct Biol. 2005;149:303–12.PubMedCrossRef Kensler RW. The mammalian cardiac muscle thick filament: Crossbridge arrangement. J Struct Biol. 2005;149:303–12.PubMedCrossRef
62.
go back to reference Pollard TD. Structure and polymerization of Acanthamoeba myosin-II filaments. J Cell Biol. 1982;95:816–25.PubMedCrossRef Pollard TD. Structure and polymerization of Acanthamoeba myosin-II filaments. J Cell Biol. 1982;95:816–25.PubMedCrossRef
63.
go back to reference Atkinson SJ, Stewart M. Molecular basis of myosin assembly: coiled-coil interactions and the role of charge periodicities. J Cell Sci Suppl. 1991;14:7–10.PubMedCrossRef Atkinson SJ, Stewart M. Molecular basis of myosin assembly: coiled-coil interactions and the role of charge periodicities. J Cell Sci Suppl. 1991;14:7–10.PubMedCrossRef
65.
go back to reference McLachlan AD, Stewart M. The 14-fold periodicity in α-tropomyosin and the interaction with actin. J Mol Biol. 1976;103:271–98.PubMedCrossRef McLachlan AD, Stewart M. The 14-fold periodicity in α-tropomyosin and the interaction with actin. J Mol Biol. 1976;103:271–98.PubMedCrossRef
66.
go back to reference Gunning P, editor. Tropomyosin. Austin, TX: Springer Science + Business Media; 2008. New York, NY; Landes Bioscience. Gunning P, editor. Tropomyosin. Austin, TX: Springer Science + Business Media; 2008. New York, NY; Landes Bioscience.
67.
go back to reference Pauling L, Corey RB. Compound Helical Configurations of Polypeptide Chains: Structure of Proteins of the [alpha]-Keratin Type. Nature. 1953;171:59–61.PubMedCrossRef Pauling L, Corey RB. Compound Helical Configurations of Polypeptide Chains: Structure of Proteins of the [alpha]-Keratin Type. Nature. 1953;171:59–61.PubMedCrossRef
68.
go back to reference Likhtenshtein GI, Yamauchi J, Nakatsuji S, Tamura R, Smirnov AI. Nitroxides Applications in Chemistry, Biomedicine, and Materials Science. Hoboken: Wiley-VCH Imprint, John Wiley & Sons, Incorporated; 2008. Likhtenshtein GI, Yamauchi J, Nakatsuji S, Tamura R, Smirnov AI. Nitroxides Applications in Chemistry, Biomedicine, and Materials Science. Hoboken: Wiley-VCH Imprint, John Wiley & Sons, Incorporated; 2008.
69.
go back to reference Allen TH, Krzywicki HJ, Roberts JE. Density, fat, water and solids in freshly isolated tissues. J Appl Physiol. 1959;14:1005–8.PubMed Allen TH, Krzywicki HJ, Roberts JE. Density, fat, water and solids in freshly isolated tissues. J Appl Physiol. 1959;14:1005–8.PubMed
Metadata
Title
Magnetic susceptibility anisotropy of myocardium imaged by cardiovascular magnetic resonance reflects the anisotropy of myocardial filament α-helix polypeptide bonds
Authors
Russell Dibb
Yi Qi
Chunlei Liu
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Journal of Cardiovascular Magnetic Resonance / Issue 1/2015
Electronic ISSN: 1532-429X
DOI
https://doi.org/10.1186/s12968-015-0159-4

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