Obesity affects collagen fibril diameter and mechanical properties of tendons in Zucker rats

Connective Tissue Research

Volumn 51, Issue 3, 2010, Pages 171-178

  Biancalana, Adriano ^a   Veloso, Lcioa ^a   Gomes, Laurecir ^a  

^a UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Biomechanics; Collagen Fibrils; Obesity; Tendon; Zucker

Indexed keywords

COLLAGEN FIBRIL; HYDROXYPROLINE; COLLAGEN;

ANIMAL TISSUE; ARTICLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FLEXOR TENDON; LEAN BODY WEIGHT; MALE; METABOLIC DISORDER; NONHUMAN; OBESITY; PROTEIN MODIFICATION; PROTEIN STRUCTURE; RAT; TENDON STRESS; TISSUE LEVEL; ZUCKER RAT; ANIMAL; CHEMISTRY; ENZYME IMMUNOASSAY; FORELIMB; GENETICS; MECHANICAL STRESS; METABOLISM; PATHOLOGY; PHYSIOLOGY; TENDON; TENSILE STRENGTH; ULTRASTRUCTURE;

ANIMALIA; RATTUS;

ANIMALS; COLLAGEN; EXTRACELLULAR MATRIX; FORELIMB; HYDROXYPROLINE; IMMUNOENZYME TECHNIQUES; MALE; OBESITY; RATS; RATS, ZUCKER; STRESS, MECHANICAL; TENDONS; TENSILE STRENGTH;

EID: 77954681746     PISSN: 03008207     EISSN: 16078438     Source Type: Journal    
DOI: 10.3109/03008200903191312     Document Type: Article

References (60)

1. James, P.T., Leach, R., Kalamara, E., and Shayeghi, M. (2001). The worldwide obesity epidemic. Obes. Res., 9, S228-S233.
2. Visscher, T.L.S., and Seidell, J.C. (2001). The public health impact of obesity. Annu. Rev. Public Health, 22, 355-375.
3. Kuczmarski, R., Flegal, K., Campbell, S., and Johnson, C. (1994). Increasing prevalence of overweight among US adults. J. Am. Med. Assoc., 272, 205-211.
4. WHO. (2000). Obesity, preventing and managing the global epidemic. Report of a WHO consultation. WHO technical report series 894. Geneva, World Health Organization.
5. Kopelman, P.G. (2000). Obesity as a medical problem. Nature, 404, 635-643.
6. Phillips, M.S., Liu, Q., Hammond, H.A., Dugan, V., Hey, P.J., Caskey, C.J., and Hess, J.F. (1996). Leptin receptormissense mutation in the fatty Zucker rat. Nat. Genet., 13, 18-19.
7. Bray, G.A. (1977). The Zucker-fat rat, a review. Fed. Proc., 36, 148-153.
8. Friedman, J.M., and Halaas, J.L. (1998). Leptin and the regulation of body weight in mammals. Nature, 395, 763-770.
9. Kopelman, P.G. (1994). Causes and consequences of obesity. Med. Int., 22, 385-388.
10. Sorof, J., and Daniels, S. (2002). Obesity hypertension in children, a problem of epidemic proportions. Hypertension, 40, 441-447.
11. James, W.P. (1995). A public health approach to the problem of obesity. Int. J. Obes. Relat. Metab. Disord., 3, 37-45.
12. J́ozsa, L.G., and Kannus, P. (1997). Strucutre and metabolism of normal tendons. In Human Tendons, Anatomy, Physiology and Pathology, pp. 46-95, 1st edn. Champaign, IL, Human Kinetics.
13. Parry, D.A.D., Barnes, G.R.G., and Craig, A.S. (1978b). A comparison of the size distribution of collagen fibrils in connective tissues as a function of age and a possible relation between fibril size distribution and mechanical properties. Proc. R. Soc. Lond. B. Biol. Sci., 203, 305-321.
14. Liu, S.H.,Yang, R.S., Shaikh, R., and Lane, J.M. (1995).Collagen in tendon, ligament and bone healing. Clin. Orthop. Relat. Res., 318, 265-278.
15. Van Der Rest, M., and Garrone, R. (1991). Collagen family of proteins. FASEB J., 5, 2814-2823.
16. Zhang, G.,Young, B.B., Ezura,Y., Favata, M., Soslowsky, L.J., Chakravarti, S., and Birk, D.E. (2005). Development of tendon structure and function, regulation of collagen fibrillogenesis. J. Musculoskelet. Neuronal Interact., 5, 5-21.
17. Vogel, K.G., and Koob, T.J. (1989). Structural specialization in tendons under compression. Int. Rev. Cytol., 115, 267-293.
18. Woo, S.L., Ritter,M.A., Amiel, D., Sanders,M., Gomez, M.A., Kuei, S.C., Garfin, S.R., andAkeson,W.H. (1980). The biomechanical and biochemical properties of swine tendons long-term effects of exercise on the digital extensors. Connect. Tissue Res., 7, 177-183.
19. Curwin, S.L., Vailas, A.C., and Wood, J. (1988). Immature tendon adaptation to strenuous exercise. J. Appl. Physiol., 65, 2297-2301.
20. Vidal, B.C., and Carvalho, H.F. (1990). Aggregational state and molecular order of tendons as a function of age. Matrix, 10, 48-57.
21. Birk, D.E., Nurminskaya, M.V., and Zycband, E.I. (1995). Collagen fibrillogenesis in situ, fibril segments undergo post-depositional modifications resulting in linear and lateral growth duringmatrix development. Dev. Dyn., 202, 229-243.
22. Gillard, G.C., Reilly, H.C., Bell-Booth, P.G., and Flint, M.H. (1979). The influence of mechanical forces on the glycosaminoglycans content of the rabbit flexor digitorum profundus tendon. Connect. Tissue Res., 7, 37-46.
23. Vidal, B.C. (1993). Cell and extracellular matrix interaction, a feedback theory based on molecular order recognition-adhesion events. Rev. Fac. Ciên. Med. Unicamp, 4, 11-14.
24. Esquisatto, M.A.M., Joazeiro, P.P., Pimentel, E.R., and Gomes, L. (2007). The effect of age on the structure and composition of rat tendon fibrocartilage. Cell Biol. Int., 31, 570-577.
25. Cherdchutham, W., Meershoek, L.S., van Weeren, P.R., and Barneveld, A. (2001). Effects of exercise on biomechanical properties of the superficial digital flexor tendon in foals. Am. J. Vet. Res., 62, 1859-1864.
26. Nakagaki, W.R., Biancalana A., Benevides, G.P., and Gomes, L. (2007). Biomechanical and biochemical properties of chicken calcaneal tendon under effect of age and nonforced active exercise. Connect. Tissue Res., 48, 219-228.
27. Frank, C., McDonald, D., Bray, D., Bray, R., Rangayyan, R., Chimich, D., and Shrive, N. (1992). Collagen fibril diameters in the healing adult rabbit medial collateral ligament. Connect. Tissue Res., 27, 251-263.
28. Benevides, G.P., Pimentel, E.R., Toyama, M.H., Novello, J.C., Marangoni, S., and Gomes, L. (2004). Biochemical and biomechanical analysis of tendons of caged and penned chickens. Connect. Tissue Res., 45, 206-215.
29. Covizi, D.Z., Felisbino, S.L., Gomes, L., Pimentel, E.R., and Carvalho, H.F. (2001). Regional adaptations in three rat tendons. Tissue & Cell, 33, 483-490.
30. Flint, M.H., Craig, A.S., Reilly, H.C., Gillard, G.C., and Parry, D.A.D. (1984). Collagen fibril diameters and glycosaminoglycan content of skins-indices of tissue maturity and function. Connect. Tissue Res., 13, 69-81.
31. Lindsey, J., Edwards, J., Allen, E., and Helen, L. (2005). Effect of exercise on age-related changes in collagen fibril diameter distributions in the common digital extensor tendons of young horses. Am. J. Vet. Res., 66, 564-568.
32. Tohyama, H., and Yasuda, K. (2000). The effects if stress enhancement on the extracellular matrix and fibroblasts in the patellar tendon. J. Biomech., 33, 559-565.
33. Gupte, C.M., Smith, A., Jamieson, N., Bull, A.M.J., Thomas, R.W. D., and Amis, A.A. (2002). Meniscofemoral ligaments-structural and material properties. J. Biomech., 35, 1623-1629.
34. Stegemann, H., and Stalder, K. (1967). Determination of hydroxyproline. Clin. Chim. Acta, 18, 267-273.
35. Nielsen, H.M., Skalicky, M., and Viidik, A. (1998). Influence of physical exercise on aging rats. III. Life-long exercise modifies the aging changes of the mechanical properties of limb muscle tendons. Mech. Ageing Dev., 100, 243-260.
36. Buchanan, C.I., and Marsh, R.L. (2001). Effects of long-term exercise on the biomechanical properties of the Achilles tendon of guinea fowl. J. Appl. Physiol., 90, 164-171.
37. Viidik, S. (1969). Tensile strength properties of Achilles tendon systems in trained and untrained rabbits. Acta Orthop. Scand., 40, 261-272.
38. Rosager, S., Aagaard, P., Dyhre-Poulsen, P., Neergaard, K., Kjaer, M., and Magnusson, S.P. (2002). Load-displacement properties of the human triceps surae aponeurosis and tendon in runners and non-runners. Scand. J. Med. Sci. Sports., 12, 90-98.
39. Viidik, A. (1996). Tendons and ligaments. In Extracellular matrix, tissue function, W.D. Comper (ed.), pp. 303-327. Amsterdam, The Netherlands: Harwood Academic Publishers.
40. Birk, D.E., and Mayne, R. (1997). Localization of collagen types I, III and V during tendon development. Changes in collagen types I and III are correlated with changes in fibril diameter. Eur. J. Cell Biol., 72, 352-361.
41. Parry, D.A.D. (1988). The molecular and fibrillar structure of collagen and its relationship to the mechanical properties of connective tissue. Biophys. Chem., 29, 195-209.
42. Haut, R.C., Lancaster, R.L., and DeCamp, C.E. (1992). Mechanical properties of the canine patellar tendon, some correlations with age and the content of collagen. J. Biomech., 25, 163-173.
43. Silver, F.H., Christiansen, D.L., Snowhill, P.B., and Chen, Y. (2000). Role of storage on changes in the mechanical properties of tendon and selfassembled collagen fibers. Connect. Tissue Res., 41, 155-164.
44. Culav, E.M., Clarck, C.H., and Merrilees, M.J. (1999). Connective tissue, matrix composition and its relevance to physical therapy. Phys. Ther., 79, 308-319.
45. Nakagawa, Y., Totsuka, M., Sato, T., Fukuda, Y., and Hirota, K. (1989). Effect of disuse on the ultrastructure of the Achilles tendon in rats. Eur. J. Appl. Physiol., 59, 239-242.
46. Eriksen, H.A., Pajala, A., Leppilahti, J., and Risteli, J. (2002). Increased content of type III collagen at the rupture site of human Achilles tendon. J. Orthop. Res., 20, 1352-1357.
47. Parry, D.A.D., Craig, A.S., and Barnes, G.R.G. (1978a). Tendon and ligament from the horse, an ultrastructural study of collagen fibrils and elastic fibres as a function of age. Proc. R. Soc. Lond. B. Biol. Sci., 203, 293-303.
48. Evanko, S.P., and Vogel, K.G. (1990). Ultrastructure and proteoglycan composition in the developing fibrocartilaginous regions of bovine tendon. Matrix, 10, 420-436.
49. Shino, K., Oakes, B.W., Horibe, S., Nakata, K., and Nakamura, N. (1995). Collagen fibril populations in human anterior cruciate ligament allografts. Am. J. Sports Med., 23, 203-209.
50. Fleischmajer,R., Perlish, J.S., Burgeson, R.E., Shaikh-Bahai, E., and Timpl, R. (1990). Type I and type III collagen interactions during fibrillogenesis. Ann. NY Acad. Sci., 580, 161-175.
51. Birk, D.E., Fitch, J.M., Babiarz, J.P., Doane, K.J., and Linsenmayer, T.E. (1990). Collagen fibrillogenesis in vitro, interaction of types I and V collagen regulates fibril diameter. J. Cell Sci., 95, 649-657.
52. Patterson-Kane, J.C., Wilson, A.M., Firth, E.C., Parry, D.A.D. and Goodship, A.E. (1997). Comparison of collagen fibril populations in the superficial digital flexor tendons of exercised and nonexercised thoroughbreds. Equine Vet. J., 29, 121-125.
53. Strocchi, R., Pasquale,V., and Guizzardi, S. (1991).Human Achilles tendon, morphological and morphometric variations as a function of age. Foot Ankle, 12, 100-104.
54. Derwin, K.A., Soslowsky, L.J., Kimura, J.H., and Plaas, A.H. (2001). Proteoglycans and glycosaminoglycan fine structure in the mouse tail tendon fascicle. J. Orthop. Res., 19, 269-277.
55. Lavagnino, M., Arnoczky, S.P., Frank, K., and Tian, T. (2005). Collagen fibril diameter distribution does not reflect changes in the mechanical properties of in vitro stress-deprived tendons. J. Biomech., 38, 69-75.
56. Shadwick, R.E. (1990). Elastic energy storage in tendons, mechanical differences related to function and age. J. Appl. Physiol., 68, 1033-1040.
57. Rahmouni, K., and Haynes, W.G. (2001). Leptin signaling pathways in the central nervous system, interactions between neuropeptide Y and melanocortins. BioEssays, 23, 1095-1099.
58. Muoio, D.M., Dohm, G.L., Fiedorek Jr., F.T., Tapscott, E.B., and Coleman, R.A. (1997). Leptin directly alters lipid partitioning in skeletal muscle. Diabetes, 46, 1360-1363.
59. Reidy, S.P., and Weber, J.M. (2000). Leptin, an essential regulator of lipid metabolism. Comp. Biochem. Physiol., 125, 285-297.
60. Steinberg, G.R., Parolin,M.L., Heigenhauser, G.J.F., andDyck, D.J. (2002). Leptin increases FA oxidation in lean but not obese human skeletal muscle, evidence of peripheral leptin resistance. Am. J. Physiol., 28, E187-E192.