On the electrical properties of collagen macromolecule solutions: Role of collagen-water interactions

Abstract Collagen is the most abundant protein of the extracellular matrix in connective tissue in the mammalians with potential applications in the coverage of cardiovascular prostheses, regenerative medicine, pharmaceutical industry, controlled drug delivery, and proliferation, migration and cellular differentiation. In this research, the electrical properties (conductivity and permittivity) of type I collagen solution with different concentrations were measured in the frequency range 10 kHz–5 MHz and electrical analysis of the measurement results was performed. Analysis shows that special interactions with water molecules have a significant effect on the electrical properties of collagen solutions beyond what is predicted considering the rules of physical composition, such as the Maxwell-Garnet model of mixing rules. Very small variations in the amount of collagen in water, significantly changed solution conductivity and dielectric permittivity. Finally, to simplify the representation of the impedance measurements and to better understanding of the electrical behavior of the solutions, an equivalent electrical circuit model was developed to describe the measured data. The results obtained from the fitted electrical model were in good agreement with the experimental results.

[1]  R. Raines,et al.  4-chloroprolines: synthesis, conformational analysis, and effect on the collagen triple helix. , 2008, Biopolymers.

[2]  Jan Feijen,et al.  Micromechanical testing of individual collagen fibrils. , 2006, Macromolecular bioscience.

[3]  M. Raghunath,et al.  The Collagen Suprafamily: From Biosynthesis to Advanced Biomaterial Development , 2018, Advanced materials.

[4]  A. Kumbharkhane,et al.  Dielectric relaxation studies of collagen - Surfactant complexes in aqueous buffer solution. , 2019, International journal of biological macromolecules.

[5]  Todd J. Freeborn,et al.  Fatigue-Induced Cole Electrical Impedance Model Changes of Biceps Tissue Bioimpedance , 2018, Fractal and Fractional.

[6]  S. Bhattacharya,et al.  Dielectrophoresis assisted impedance spectroscopy for detection of gold-conjugated amplified DNA samples , 2019, Sensors and Actuators B: Chemical.

[7]  P. Lyu,et al.  Enhanced mobility of organic thin film transistors by water absorption of collagen hydrolysate gate dielectric , 2013 .

[8]  Nathalie Gontard,et al.  A Review: Origins of the Dielectric Properties of Proteins and Potential Development as Bio-Sensors , 2016, Sensors.

[9]  M. Moradi,et al.  The Development of a Four-Electrode Bio-Impedance Sensor for Identification and Localization of Deep Pulmonary Nodules , 2018, Annals of Biomedical Engineering.

[10]  J. A. C. Paiva,et al.  On the piezoelectricity of anionic collagen films , 2002 .

[11]  Songjun Li,et al.  Sustained release of BSA from a novel drug delivery matrix -- bullfrog skin collagen film. , 2004, Macromolecular bioscience.

[12]  J. Eastoe,et al.  The amino acid composition of mammalian collagen and gelatin. , 1955, The Biochemical journal.

[13]  Hanmei Xu,et al.  Collagen from Marine Biological Sources and Medical Applications , 2018, Chemistry & biodiversity.

[14]  J. Schofield,et al.  Stress Relaxation Behavior of Wheat Dough, Gluten, and Gluten Protein Fractions , 2003 .

[15]  A. Warshel,et al.  Calculations of electrostatic interactions in biological systems and in solutions , 1984, Quarterly Reviews of Biophysics.

[16]  J. Spadavecchia,et al.  Supramolecular Self‐Assembly and Organization of Collagen at Solid/Liquid Interface: Effect of Spheroid‐ and Rod‐Shaped TiO2 Nanocrystals , 2019, Advanced Materials Interfaces.

[17]  K. Lewandowska,et al.  Chitosan blends containing hyaluronic acid and collagen. Compatibility behaviour , 2015 .

[18]  A. Sihvola.  Mixing Rules with Complex Dielectric Coefficients , 2000 .

[19]  M. R. Kumar,et al.  Controlled cell proliferation on an electrochemically engineered collagen scaffold. , 2012, Macromolecular bioscience.

[20]  Olivier Français,et al.  Analysis of pulsed electric field effects on cellular tissue with Cole–Cole model: Monitoring permeabilization under inhomogeneous electrical field with bioimpedance parameter variations , 2015 .

[21]  S J Wodak,et al.  Calculations of electrostatic properties in proteins. Analysis of contributions from induced protein dipoles. , 1987, Journal of molecular biology.

[22]  Won Chul Lee,et al.  Formation of Highly Aligned Collagen Nanofibers by Continuous Cyclic Stretch of a Collagen Hydrogel Sheet. , 2016, Macromolecular bioscience.

[23]  A. Sombra,et al.  On the dielectric behaviour of collagen-algal sulfated polysaccharide blends: effect of glutaraldehyde crosslinking. , 2006, Biophysical chemistry.

[24]  A. Bonincontro,et al.  A study of the dielectric properties of E. coli ribosomal RNA and proteins in solution. , 1997, Biophysical chemistry.

[25]  A. Sionkowska,et al.  Collagen–synthetic polymer interactions in solution and in thin films , 2009 .

[26]  Hyoung-Ihl Kim,et al.  Electrical impedance spectroscopy on a needle for safer Veress needle insertion during laparoscopic surgery , 2017 .

[27]  Yonggang Lv,et al.  Application of Collagen Scaffold in Tissue Engineering: Recent Advances and New Perspectives , 2016, Polymers.

[28]  M. Moradi,et al.  A New Bio-Impedance Forceps Sensor for Measuring Electrical Conductivity of the Biological Tissues , 2019, IEEE Sensors Journal.

[29]  E. Lattman,et al.  Experimental measurement of the effective dielectric in the hydrophobic core of a protein. , 1997, Biophysical chemistry.

[30]  Todd J. Freeborn,et al.  A Survey of Fractional-Order Circuit Models for Biology and Biomedicine , 2013, IEEE Journal on Emerging and Selected Topics in Circuits and Systems.

[31]  Sangyoon Lee,et al.  Effects of hydroxyl groups in polymeric dielectrics on organic transistor performance , 2006 .

[32]  Xiang Chen.  Theoretical electrical conductivity of hydrogen-bonded benzamide-derived molecules and single DNA bases , 2013, Journal of biological physics.

[33]  Benjamín Sánchez Terrones.  Broadband electrical impedance spectroscopy for dynamic electrical bio-impedance characterization , 2012 .

[34]  Igor Polikarpov,et al.  Average protein density is a molecular‐weight‐dependent function , 2004, Protein science : a publication of the Protein Society.

[35]  M. Gauza,et al.  Effect of water content on electrical conductivity of fish skin collagen , 2011 .