One-Dimensional Viscoelastic Behavior of Fibroblast Populated Collagen Matrices

[+] Author and Article Information
Jessica E. Wagenseil

Department of Cell Biology and Physiology, Washington University School of Medicine, 660 S. Euclid, CB 8228, St. Louis, MO 63110e-mail: Jessica.Wagenseil@cellbio.wustl.edu

Tetsuro Wakatsuki

Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, 660 S. Euclid Ave., St. Louis, MO 63110e-mail: wakatsuk@biochem.wustl.edu

Ruth J. Okamoto

Departments of Mechanical and Biomedical Engineering, Washington University, One Brookings Dr., St. Louis, MO 63130e-mail: rjo@me.wustl.edu

George I. Zahalak

Department of Mechanical Engineering, Washington University, One Brookings Dr., St. Louis, MO 63130

Elliot L. Elson

Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, 660 S. Euclid Ave., St. Louis, MO 63110e-mail: elson@biochem.wustl.edu

J Biomech Eng 125(5), 719-725 (Oct 09, 2003) (7 pages) doi:10.1115/1.1614818 History: Received July 15, 2002; Revised April 18, 2003; Online October 09, 2003
Copyright © 2003 by ASME
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Bell,  E., Ivarsson,  B., and Merrill,  C., 1979, “Production of a Tissue-Like Structure by Contraction of Collagen Lattices by Human Fibroblasts of Different Proliferative Potential In Vitro,” Proc. Natl. Acad. Sci. U.S.A., 76, pp. 1274–1278.
Auger,  F. A., Rouabhia,  M., Goulet,  F., Berthod,  F., Moulin,  V., and Germain,  L., 1998, “Tissue-Engineered Human Skin Substitutes From Collagen-Populated Hydrated Gels: Clinical and Findamental Applications,” Med. Biol. Eng. Comput., 36, pp. 801–812.
Huang,  D., Chang,  T. R., Aggarwal,  A., Lee,  R. C., and Ehrlich,  H. P., 1993, “Mechanisms and Dynamics of Mechanical Strengthening in Ligament-Equivalent Fibroblast-Populated Collagen Matrices,” Ann. Biomed. Eng., 21, pp. 289–305.
Seliktar,  D., Black,  R. A., Vito,  R. P., and Nerem,  R. M., 2000, “Dynamic Mechanical Conditioning of Collagen-Gel Blood Vessel Constructs Induces Remodeling In Vitro,” Ann. Biomed. Eng., 28, pp. 351–362.
Butler,  D. L., Goldstein,  S. A., and Guilak,  F., 2000, “Functional Tissue Engineering: The Role of Biomechanics,” J. Biomech. Eng., 122, pp. 570–575.
Fung, Y. C., 1993, Biomechanics: Mechanical Properties of Living Tissues, Springer-Verlag, New York, pp. 41, 46, 262–263, 270–272, 301.
Fung,  Y. C., Fronek,  K., and Patitucci,  P., 1979, “Pseudoelasticity of Arteries and the Choice of its Mathematical Expression,” Am. J. Physiol., 237, pp. H620–H631.
Emery,  J. L., Omens,  J. H., and McCulloch,  A. D., 1997, “Strain Softening in the Rat Left Ventricular Myocardium,” J. Biomech. Eng., 119, pp. 6–12.
Gregersen,  H., Emery,  J. L., and McCulloch,  A. D., 1998, “History-Dependent Mechanical Behavior of Guinea-Pig Small Intestine,” Ann. Biomed. Eng., 26, pp. 850–858.
Wakatsuki,  T., Kolodney,  M. S., Zahalak,  G. I., and Elson,  E. L., 2000, “Cell Mechanics Studied by a Reconstituted Model Tissue,” Biophys. J., 79, pp. 2353–2368.
Zahalak,  G., Wagenseil,  J., Wakatsuki,  T., and Elson,  E., 2000, “A Cell-Based Constitutive Relation for Bio-Artificial Tissues,” Biophys. J., 79, pp. 2369–2381.
Girton,  T. S., Oegema,  T. R., and Tranquillo,  R. T., 1999, “Exploiting Glycation to Stiffen and Strengthen Tissue Equivalents for Tissue Engineering,” J. Biomed. Mater. Res., 46, pp. 87–92.
Vawter,  D. L., Fung,  Y. C., and West,  J. B., 1978, “Elasticity of Excised Dog Lung Parenchyma,” J. Appl. Physiol., 45, pp. 261–269.
McElhaney,  J. H., 1966, “Dynamic Response of Bone and Muscle Tissue,” J. Appl. Physiol., 21, pp. 1231–1236.
Pinto,  J. G., and Fung,  Y. C., 1973, “Mechanical Properties of the Heart Muscle in the Passive State,” J. Biomech., 6, pp. 597–616.
Kang,  T., Resar,  J., and Humphrey,  J. D., 1995, “Heat-Induced Changes in the Mechanical Behavior of Passive Coronary Arteries,” ASME J. Biomech. Eng., 117, pp. 86–93.
May-Newman,  K., and Yin,  F. C. P., 1995, “Biaxial Mechanical Behavior of Excised Porcine Mitral Valve Leaflets,” Am. J. Physiol., 269, pp. H1319–H1327.
Takamizawa,  K., and Hayashi,  K., 1987, “Strain Energy Density Function and Uniform Strain Hypothesis for Arterial Mechanics,” J. Biomech., 20, pp. 7–17.
Johnson,  M., and Beatty,  M., 1993, “The Mullins Effect in Uniaxial Extension and its Influence on the Transverse Vibration of a Rubber String,” Continuum Mech. Thermodyn., 5, pp. 83–115.
Kolodney,  M. S., and Elson,  E. L., 1993, “Correlation of Myosin Light Chain Phosphorylation With Isometric Contraction of Fibroblasts,” J. Biol. Chem., 268, pp. 23850–23855.
Holzapfel,  G. A., Gasser,  T. C., and Stadler,  M., 2002, “A Structural Model for the Viscoelastic Behavior of Arterial Walls: Continuum Formulation and Finite-Element Analysis,” European Journal of Mechanics a-Solids,21, pp. 441–463.
Barocas,  V. H., and Tranquillo,  R. T., 1997, “An Anisotropic Biphasic Theory of Tissue-Equivalent Mechanics: The Interplay Among Cell Traction, Fibrillar Network Deformation, Fibril Alignment, and Cell Contact Guidance,” ASME J. Biomech. Eng., 119, pp. 137–145.
Ozerdem,  B., and Tozeren,  A., 1995, “Physical Response of Collagen Gels to Tensile Strain,” J. Biomech. Eng., 117, pp. 397–401.
Roeder,  B. A., Kokini,  K., Sturgis,  J. E., Robinson,  J. P., and Voytik-Harbin,  S. L., 2002, “Tensile Mechanical Properties of Three-Dimensional Type I Collagen Extracellular Matrices With Varied Microstructure,” J. Biomech. Eng., 124, pp. 214–222.
Tower,  T. T., Neidert,  M. R., and Tranquillo,  R. T., 2002, “Fiber Alignment Imaging During Mechanical Testing of Soft Tissues,” Ann. Biomed. Eng., 30, pp. 1221–1233.
Eastwood,  M., Porter,  R., Khan,  U., McGrouther,  G., and Brown,  R., 1996, “Quantitative Analysis of Collagen Gel Contractile Forces Generated by Dermal Fibroblast and the Relationship to Cell Morphology,” J. Cell Physiol., 166, pp. 33–42.
Eastwood,  M., McGrouther,  D. A., and Brown,  R. A., 1994, “A Culture Force Monitor for Measurement of Contraction Forces Generated in Human Dermal Fibroblast Cultures: Evidence for Cell-Matrix Mechanical Signalling,” Biochim. Biophys. Acta, 1201, pp. 186–192.


Grahic Jump Location
(a) Average experimental force-stretch curves for the seventh stretch to 1.20 λmax at each stretch rate (N≥10 for each rate). Error bars are not shown for clarity. (b) Average peak force and hysteresis for the seventh stretch to 1.20 λmax at each stretch rate. * =significantly different from all other rates, #=significantly different from 0.10 and 1.0 mm/s (ANOVA, Fisher’s PLSD, p<.05). Error bars=1 SD.
Grahic Jump Location
(a) First five force-stretch curves for a representative FPCM. Stretch rate=0.10 mm/s, continuous cycling. The largest difference in FPCM force-stretch behavior is seen between the first and subsequent stretches to the same λmax for all test protocols. (b) Average peak force and hysteresis for four FPCMs stretched for 80 cycles to 1.20 λmax at 0.10 mm/s. Continuous cycling, except one hour rest period after stretch 41 and two to five minute rest periods after stretches 21 and 61. Similar trends were seen in four additional FPCMs and in other protocols with constant λmax. Error bars=1 SD.
Grahic Jump Location
Force-stretch curves for a representative FPCM stretched to increasing λmax. Stretch rate=0.10 mm/s, rest period=5 min. Similar curves were obtained for six additional FPCMs.
Grahic Jump Location
(a) Representative peak forces for one FPCM stretched with different rest periods between cycles to 1.20 λmax at 0.10 mm/s. The hysteresis is not shown, but also depended on the rest period (percent change shown in b). Similar trends were seen in five additional FPCMs and in other protocols (i.e., Fig. 2(b), one hour rest period after stretch 41). Initial, final, pre and post force values for the one hour rest period are shown for the percent change calculation in b. (b) Mean relative percent change in peak force and hysteresis following the protocol shown in a for three FPCMs. Percent change was calculated from the peak forces and hysteresis for subsequent stretches (as demonstrated in a for the forces) using the equation presented in the text. Error bars=1 SD.
Grahic Jump Location
(a) Peak forces for a representative FPCM stretched to different λmax. Stretch rate=0.10 mm/s, continuous cycling except 45-min rest period after stretch 50. Peak force declines with each stretch during 10 preconditioning by overstretch cycles to 1.25 λmax, then reaches a steady state for the following cycles to lower λmax. Similar trends were seen in 11 additional FPCMs. (b) Force-stretch curves for stretches 51–90 for the same FPCM shown in a. Note the consistent shape of the force-stretch curve when cycles are performed in order of decreasing λmax (unlike cycles to increasing λmax in Fig. 3).




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