Equal and local-load-sharing micromechanical models for collagens: Quantitative comparisons in response of non-diabetic and diabetic rat tissue

Acta Biomaterialia

Volumn 2, Issue 6, 2006, Pages 595-607

  Layton, Bradley E ^a   Sastry, Ann Marie ^a,b  

^a Drexel University   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Collagen; Diabetes; ECM; Mechanics; Nerve

Indexed keywords

BIOMECHANICS; COLLAGEN; CROSSLINKING; GLYCOSYLATION; MECHANICAL PERMEABILITY; STIFFNESS; STOCHASTIC MODELS; STOCHASTIC SYSTEMS; TISSUE; TISSUE ENGINEERING;

CHEMICAL CROSSLINKS; DIABETIC RATS; ECM; LOCAL LOAD SHARING; MICROMECHANICAL MODELLING; NERVE; NON LINEAR; QUANTITATIVE COMPARISON; RAT TISSUE; SHAPE PARAMETERS;

HISTOLOGY;

ADVANCED GLYCATION END PRODUCT; COLLAGEN FIBRIL; FIBRILLAR COLLAGEN;

ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; BIOMECHANICS; CONTROLLED STUDY; CORRELATION ANALYSIS; CROSS LINKING; DIABETES MELLITUS; FIBER; NONHUMAN; PERMEABILITY; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; QUANTITATIVE ANALYSIS; RAT; RIGIDITY; SCIATIC NERVE; STOCHASTIC MODEL;

EID: 33749521045     PISSN: 17427061     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.actbio.2006.05.013     Document Type: Article

References (85)

1. Hadley J., Malik N., and Meek K. Collagen as a model system to investigate the use of aspirin as an inhibitor of protein glycation and crosslinking. Micron 32 3 (2001) 307-315
2. Odetti P., Aragno I., Rolandi R., Garibaldi S., Valentini S., Cosso L., et al. Scanning force microscopy reveals structural alterations in diabetic rat collagen fibrils: role of protein glycation. Diabetes Metab Res Rev 16 2 (2000) 74-81
3. Sajithlal G.B., Chithra P., and Chandrakasan G. Advanced glycation end products induce crosslinking of collagen in vitro. Biochim Biophys Acta 1407 3 (1998) 215-224
4. Vasan S., Zhang X., Kapurniotu A., Bernhagen J., Teichberg S., Basgen J., et al. An agent cleaving glucose-derived protein crosslinks in vitro and in vivo. Nature 382 6588 (1996) 275-278
5. Yang S.Z., Litchfield J.E., and Baynes J.W. AGE-breakers cleave model compounds, but do not break Maillard crosslinks in skin and tail collagen from diabetic rats. Arch Biochem Biophys 412 1 (2003) 42-46
6. Zieman S.J., and Kass D.A. Advanced glycation endproduct crosslinking in the cardiovascular system: potential therapeutic target for cardiovascular disease. Drugs 64 5 (2004) 459-470
7. Reihsner R., Melling M., Pfeiler W., and Menzel E.J. Alterations of biochemical and two-dimensional biomechanical properties of human skin in diabetes mellitus as compared to effects of in vitro non-enzymatic glycation. Clin Biomech 15 5 (2000) 379-386
8. Reihsner R., and Menzel E.J. Two-dimensional stress-relaxation behavior of human skin as influenced by non-enzymatic glycation and the inhibitory agent aminoguanidine. J Biomech 31 11 (1998) 985-993
9. Macey L.R., Kana S.M., Jingushi S., Terek R.M., Borretos J., and Bolander M.E. Defects of early fracture-healing in experimental diabetes. J Bone Joint Surg Am 71 5 (1989) 722-733
10. Feldman E.L. Oxidative stress and diabetic neuropathy: a new understanding of an old problem. J Clin Invest 111 4 (2003) 431-433
11. Fu M.X., Wells-Knecht K.J., Blackledge J.A., Lyons T.J., Thorpe S.R., and Baynes J.W. Glycation, glycoxidation, and cross-linking of collagen by glucose. Kinetics, mechanisms, and inhibition of late stages of the Maillard reaction. Diabetes 43 5 (1994) 676-683
12. King R.H. The role of glycation in the pathogenesis of diabetic polyneuropathy. Mol Pathol 54 6 (2001) 400-408
13. Seyer J.M., Kang A.H., and Whitaker J.N. The characterization of Type I and Type III collagens from human peripheral nerve. Biochim Biophys Acta 492 (1977) 415-425
14. Fujii K., Tsuji M., and Murota K. Isolation of peripheral nerve collagen. Neurochem Res 11 10 (1986) 1439-1446
15. Dumanian G.A., McClinton M.A., and Brushart T.M. The effects of free fat grafts on the stiffness of the rat sciatic nerve and perineural scar. J Hand Surg-Am 24A 1 (1999) 30-36
16. Wang H., Layton B.E., and Sastry A.M. Nerve collagens from diabetic and nondiabetic Sprague-Dawley and biobreeding rats: an atomic force microscopy study. Diabetes Metabol Res Rev 19 4 (2003) 288-298
17. Layton B.E., Sastry A.M., Wang H., Sullivan K.A., Feldman E.L., Komorowski T.E., et al. Differences between collagen morphologies, properties and distribution in diabetic and normal biobreeding and Sprague-Dawley rat sciatic nerves. J Biomech 37 6 (2004) 879-888
18. Layton B.E., and Sastry A.M. A mechanical model for collagen fibril load sharing in peripheral nerve of diabetic and non-diabetic rats. ASME J Biomech Eng 126 (2004) 803-814
19. Abrams R.A., Butler J.M., Bodine-Fowler S., and Botte M.J. Tensile properties of the neurorrhaphy site in the rat sciatic nerve. J Hand Surg [Am] 23 3 (1998) 465-470
20. Wall E.J., Kwan M.K., Rydevik B.L., Woo S.L., and Garfin S.R. Stress relaxation of a peripheral nerve. J Hand Surg [Am] 16 5 (1991) 859-863
21. Sasaki N., and Odajima S. Stress-strain curve and Young's modulus of a collagen molecule as determined by the X-ray diffraction technique. J Biomech 29 5 (1996) 655-658
22. Pins G.D., Christiansen D.L., Patel R., and Silver F.H. Self-assembly of collagen fibers. Influence of fibrillar alignment and decorin on mechanical properties. Biophys J 73 4 (1997) 2164-2172
23. Harlow D.G., and Phoenix S.L. Chain-of-bundles probability model for strength of fibrous materials 2. Numerical study of convergence. J Compos Mater 12 July (1978) 314-334
24. Harlow D.G., and Phoenix S.L. Chain-of-bundles probability model for strength of fibrous materials 1. Analysis and conjectures. J Compos Mater 12 April (1978) 195-214
25. Danielson H.E. The statistical theory of the strength of bundles of threads. I. Proc Roy Soc (Lond A) 183 (1945) 405-435
26. Brownlee M. Glycation products and the pathogenesis of diabetic complications. Diabetes Care 15 12 (1992) 1835-1843
27. Makita Z., Vlassara H., Cerami A., and Bucala R. Immunochemical detection of advanced glycosylation end products in vivo. J Biol Chem 267 8 (1992) 5133-5138
28. Ahmed N., Argirov O.K., Minhas H.S., Cordeiro C.A.A., and Thornalley P.J. Assay of advanced glycation endproducts (AGEs): surveying AGEs by chromatographic assay with derivatization by 6-aminoquinolyl-N-hydroxysuccinimidyl-carbamate and application to N-epsilon-carboxymethyl-lysine- and N-epsilon-(1-carboxyethyl)lysine-modified albumin. Biochem J 364 (2002) 1-14
29. Vlassara H., and Palace M.R. Diabetes and advanced glycation endproducts. J Int Med 251 2 (2002) 87-101
30. Bai P., Phua K., Hardt T., Cernadas M., and Brodsky B. Glycation alters collagen fibril organization. Connect Tissue Res 28 1-2 (1992) 1-12
31. Benazzoug Y., Borchiellini C., Labat-Robert J., Robert L., and Kern P. Effect of high-glucose concentrations on the expression of collagens and fibronectin by fibroblasts in culture. Exp Gerontol 33 5 (1998) 445-455
32. Muona P., Peltonen J., Jaakkola S., and Uitto J. Increased matrix gene expression by glucose in rat neural connective tissue cells in culture. Diabetes 40 5 (1991) 605-611
33. Muona P., Jaakkola S., Zhang R.Z., Pan T.C., Pelliniemi L., Risteli L., et al. Hyperglycemic glucose concentrations up-regulate the expression of type VI collagen in vitro. Relevance to alterations of peripheral nerves in diabetes mellitus. Am J Pathol 142 5 (1993) 1586-1597
34. Muona P., Jaakkola S., Salonen V., and Peltonen J. Diabetes induces the formation of large diameter collagen fibrils in the sciatic nerves of BB rats. Matrix 9 1 (1989) 62-67
35. Bradley J.L., King R.H., Muddle J.R., and Thomas P.K. The extracellular matrix of peripheral nerve in diabetic polyneuropathy. Acta Neuropath 99 (2000) 539-546
36. Halme T., Vihersaari T., and Penttinen R. Lysyl oxidase activity and synthesis of desmosines in cultured human aortic cells and skin fibroblasts: comparison of cell lines from control subjects and patients with the Marfan syndrome or other annulo-aortic ectasia. Scand J Clin Lab Invest 46 1 (1986) 31-37
37. Yamauchi M., London R.E., Guenat C., Hashimoto F., and Mechanic G.L. Structure and formation of a stable histidine-based trifunctional cross-link in skin collagen. J Biol Chem 262 24 (1987) 11428-11434
38. Cooper M.E. Importance of advanced glycation end products in diabetes-associated cardiovascular and renal disease. Am J Hypertens 17 12 Pt 2 (2004) 31S-38S
39. Stitt A.W., Moore J.E., Sharkey J.A., Murphy G., Simpson D.A., Bucala R., et al. Advanced glycation end products in vitreous: Structural and functional implications for diabetic vitreopathy. Invest Ophthalmol Vis Sci 39 13 (1998) 2517-2523
40. Sensi M., Pricci F., Andreani D., and Di Mario U. Advanced nonenzymatic glycation endproducts (AGE): their relevance to aging and the pathogenesis of late diabetic complications. Diabetes Res 16 1 (1991) 1-9
41. Tanaka S., Avigad G., Brodsky B., and Eikenberry E.F. Glycation induces expansion of the molecular packing of collagen. J Mol Biol 203 2 (1988) 495-505
42. Thornalley P.J., Battah S., Ahmed N., Karachalias N., Agalou S., Babaei-Jadidi R., et al. Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry. Biochem J 375 Pt 3 (2003) 581-592
43. Monnier V.M., Kohn R.R., and Cerami A. Accelerated age-related browning of human collagen in diabetes mellitus. Proc Natl Acad Sci USA 81 2 (1984) 583-587
44. Malik N.S., Moss S.J., Ahmed N., Furth A.J., Wall R.S., and Meek K.M. Ageing of the human corneal stroma: structural and biochemical changes. Biochim Biophys Acta 1138 3 (1992) 222-228
45. Araki N., Ueno N., Chakrabarti B., Morino Y., and Horiuchi S. Immunochemical evidence for the presence of advanced glycation end products in human lens proteins and its positive correlation with aging. J Biol Chem 267 15 (1992) 10211-10214
46. Meerwaldt R., Graaff R., Oomen P.H., Links T.P., Jager J.J., Alderson N.L., et al. Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia 47 7 (2004) 1324-1330
47. Nagaraj R.H., Sell D.R., Prabhakaram M., Ortwerth B.J., and Monnier V.M. High correlation between pentosidine protein cross-links and pigmentation implicates ascorbate oxidation in human lens senescence and cataractogenesis. Proc Natl Acad Sci USA 88 22 (1991) 10257-10261
48. Daniels H.E. The statistical theory of the strength of bundles of threads I. Proc R Soc Lond Ser A-Math Phys Sci 183 995 (1945) 405-435
49. Ushiki T., and Ide C. Three-dimensional organization of the collagen fibrils in the rat sciatic nerve as revealed by transmission- and scanning electron microscopy. Cell Tissue Res 260 1 (1990) 175-184
50. Pins G.D., Huang E.K., Christiansen D.L., and Silver F.H. Effects of static axial strain on the tensile properties and failure mechanisms of self-assembled collagen fibers. J Appl Polym Sci 63 11 (1997) 1429-1440
51. Parkinson J., Brass A., Canova G., and Brechet Y. The mechanical properties of simulated collagen fibrils. J Biomech 30 6 (1997) 549-554
52. Christiansen D.L., Huang E.K., and Silver F.H. Assembly of type I collagen: fusion of fibril subunits and the influence of fibril diameter on mechanical properties. Matrix Biol 19 5 (2000) 409-420
53. Hulmes D.J.S., Wess T.J., Prockop D.J., and Fratzl P. Radial packing, order, and disorder in collagen fibrils. Biophys J 68 5 (1995) 1661-1670
54. Hulmes D.J. Building collagen molecules, fibrils, and suprafibrillar structures. J Struct Biol 137 1-2 (2002) 2-10
55. Makita Z., Vlassara H., Cerami A., and Bucala R. Immunochemical detection of advanced glycosylation end products in vivo. J Biol Chem 267 8 (1992) 5133-5138
56. Bevington PR, Robinson DK. Data reduction and error analysis for the physical sciences. 3rd ed., vol. xi. Boston, MA: McGraw-Hill; 2003. 320 p.
57. Myers R.R., Costello M.L., and Powell H.C. Increased endoneurial fluid pressure in galactose neuropathy. Muscle Nerve 2 4 (1979) 299-303
58. Freeman J.W., and Silver F.H. Elastic energy storage in unmineralized and mineralized extracellular matrices (ECMs): a comparison between molecular modeling and experimental measurements. J Theor Biol 229 3 (2004) 371-381
59. Misof K., Rapp G., and Fratzl P. A new molecular model for collagen elasticity based on synchrotron X-ray scattering evidence. Biophys J 72 3 (1997) 1376-1381
60. Lorenzo A.C., and Caffarena E.R. Elastic properties, Young's modulus determination and structural stability of the tropocollagen molecule: a computational study by steered molecular dynamics. J Biomech 38 7 (2005) 1527-1533
61. Fass J.N., and Odde D.J. Tensile force-dependent neurite elicitation via anti-beta 1 integrin antibody-coated magnetic beads. Biophys J 85 1 (2003) 623-636
62. Ault H.K., and Hoffman A.H. A composite micromechanical model for connective tissues. 1. Theory. J Biomech Eng-Trans ASME 114 1 (1992) 137-141
63. Ault H.K., and Hoffman A.H. A composite micromechanical model for connective tissues. 2. Application to rat tail tendon and joint capsule. J Biomech Eng-Trans ASME 114 1 (1992) 142-146
64. Toby E.B., Rotramel J., Jayaraman G., and Struthers A. Changes in the stress relaxation properties of peripheral nerves after transection. J Hand Surg [Am] 24 4 (1999) 694-699
65. Hurschler C., Loitz-Ramage B., and Vanderby Jr. R. A structurally based stress-stretch relationship for tendon and ligament. J Biomech Eng 119 4 (1997) 392-399
66. Parry D.A. The molecular and fibrillar structure of collagen and its relationship to the mechanical properties of connective tissue. Biophys Chem 29 1-2 (1988) 195-209
67. Roeder B.A., Kokini K., Sturgis J.E., Robinson J.P., and Voytik-Harbin S.L. Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure. J Biomech Eng 124 2 (2002) 214-222
68. Haut R.C., and Little R.W. Constitutive equation for collagen fibers. J Biomech 5 5 (1972) 423-430
69. Hoger A. The elasticity tensor of a transversely isotropic hyperelastic material with residual stress. J Elasticity 42 2 (1996) 115-132
70. Kolowrocki K. Asymptotic approach to reliability evaluation of rope transportation system. Reliab Eng Syst Saf 71 1 (2001) 57-64
71. Perry R.J. Estimating strength of the Williamsburg Bridge suspension cables. Am Stat 52 3 (1998) 211-217
72. Hurschler C., LoitzRamage B., and Vanderby R. A structurally based stress-stretch relationship for tendon and ligament. J Biomech Eng-Trans ASME 119 4 (1997) 392-399
73. Liao J., Yang L., Grashow J., and Sacks M.S. Molecular orientation of collagen in intact planar connective tissues under biaxial stretch. Acta Biomater 1 1 (2005) 45-54
74. Pradhan S., Chakrabarti B.K., and Hansen A. Crossover behavior in a mixed-mode fiber bundle model. Phys Rev E 71 3 (2005)
75. Hidalgo R.C., Moreno Y., Kun F., and Herrmann H.J. Fracture model with variable range of interaction. Phys Rev E 65 4 (2002)
76. Galbraith J.A., Thibault L.E., and Matteson D.R. Mechanical and electrical responses of the squid giant-axon to simple elongation. J Biomech Eng-Trans ASME 115 1 (1993) 13-22
77. Wall E.J., Massie J.B., Kwan M.K., Rydevik B.L., Myers R.R., and Garfin S.R. Experimental stretch neuropathy - changes in nerve-conduction under tension. J Bone Joint Surg-Br 74 1 (1992) 126-129
78. Ogata K., and Naito M. Blood-flow of peripheral-nerve effects of dissection, stretching and compression. J Hand Surg-Br Eur 11B 1 (1986) 10-14
79. Driscoll P.J., Glasby M.A., and Lawson G.M. An in vivo study of peripheral nerves in continuity: biomechanical and physiological responses to elongation. J Orthop Res 20 2 (2002) 370-375
80. Takahara K., Sato Y., Okazawa K., Okamoto N., Noda A., Yaoi Y., et al. Complete primary structure of human collagen alpha 1 (V) chain. J Biol Chem 266 20 (1991) 13124-13129
81. Traub W., and Steinmann B. Structural study of a mutant type I collagen from a patient with lethal osteogenesis imperfecta containing an intramolecular disulfide bond in the triple-helical domain. FEBS Lett 198 2 (1986) 213-216
82. Rainey J.K., and Goh M.C. A statistically derived parameterization for the collagen triple-helix. Protein Sci 11 11 (2002) 2748-2754
83. Ottani V., Martini D., Franchi M., Ruggeri A., and Raspanti M. Hierarchical structures in fibrillar collagens. Micron 33 7-8 (2002) 587-596
84. Ushiki T., and Ide C. Three-dimensional architecture of the endoneurium with special reference to the collagen fibril arrangement in relation to nerve fibers. Arch Histol Japon 49 5 (1986) 553-563
85. Puxkandl R., Zizak I., Paris O., Keckes J., Tesch W., Bernstorff S., et al. Viscoelastic properties of collagen: synchrotron radiation investigations and structural model. Philos Trans R Soc Lond B Biol Sci 357 1418 (2002) 191-197