Tendon and ligament fibrillar crimps give rise to left-handed helices of collagen fibrils in both planar and helical crimps

Journal of Anatomy

Volumn 216, Issue 3, 2010, Pages 301-309

  Franchi, Marco ^a   Ottani, Vittoria ^a   Stagni, Rita ^a   Ruggeri, Alessandro ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Collagen handedness; Fibrillar crimp; Helical crimps; Ligament; Planar crimps; Tendon

Indexed keywords

COLLAGEN FIBER;

ACHILLES TENDON; ANIMAL TISSUE; ARTICLE; FEMALE; FLEXOR TENDON; LEFT HANDEDNESS; LIGAMENT; MUSCLE FIBRIL; MUSCLE FORCE; MUSCLE STRETCHING; MUSCLE TONE; MUSCLE TRAINING; NONHUMAN; POLARIZATION MICROSCOPY; PRIORITY JOURNAL; PROTEIN STRUCTURE; RAT; SCANNING ELECTRON MICROSCOPY; TAIL; TENDON; THREE DIMENSIONAL IMAGING; TISSUE STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; FEMALE; FIBRILLAR COLLAGENS; LIGAMENTS; MICROSCOPY, ELECTRON, SCANNING; RATS; RATS, SPRAGUE-DAWLEY; TENDONS; TENSILE STRENGTH;

RATTUS;

EID: 77949632785     PISSN: 00218782     EISSN: 14697580     Source Type: Journal    
DOI: 10.1111/j.1469-7580.2009.01188.x     Document Type: Article

References (68)

1. Atkinson TS, Ewers BJ, Haut RC. The tensile and stress relaxation responses of human patellar tendon varies with specimen cross-sectional area. J Biomech 1999, 32:907-914.
2. Benjamin M, Kaiser E, Milz S. Structure-function relationships in tendons: a review. J Anat 2008, 212:211-228.
3. Bozec L, van der Heijden G, Horton M. Collagen fibrils: nanoscale ropes. Biophys J 2007, 92:70-75.
4. Brodsky B, Persikov AV. Molecular structure of the collagen triple helix. Adv Protein Chem 2005, 70:301-359.
5. de Campos Vidal B. Crimp as a part of a helical structure. C R Acad Sci III 1995, 318:173-178.
6. de Campos Vidal B. Image analysis of tendon helical superstructure using interference and polarized light microscopy. Micron 2003, 34:423-432.
7. de Campos Vidal B, Mello ML. Structural organization of collagen fibers in chordae tendineae as assessed by optical anisotropic properties and Fast Fourier transform. J Struct Biol 2009, 167:166-175.
8. Canty EC, Kadler KE. Procollagen trafficking, processing and fibrillogenesis. J Cell Sci 2005, 118:1341-1353.
9. Chen JM, Kung CE, Feairheller SH. An energic evaluation of a " Smith" collagen microfibril model. J Protein Chem 1991, 10:535-552.
10. Cribb AM, Scott JE. Tendon response to tensile stress: an ultrastructural investigation of collagen: proteoglycan interactions in stressed tendon. J Anat 1995, 187:423-428.
11. Diamant J, Keller A, Baer E. Collagen: ultrastructure and its relation to mechanical properties as a function of ageing. Proc R Soc Lond B Biol Sci 1972, 180:293-315.
12. Doillon CJ, Dunn MG, Bender E. Collagen fiber formation in repair tissue: development of strength and toughness. Coll Relat Res 1985, 5:481-492.
13. Elliott DH. Structure and function of mammalian tendon. Biol Rev Camb Philos Soc 1965, 40:392-421.
14. Evans JH, Barbenel JC. Structural and mechanical properties of tendon related to function. Equine Vet J 1975, 7:1-8.
15. Franchi M, Fini M, Quaranta M. Crimp morphology in relaxed and stretched rat Achilles tendon. J Anat 2007, 210:1-7.
16. Franchi M, Raspanti M, Dell'Orbo C. Different crimp patterns in collagen fibrils relate to the subfibrillar arrangement. Connect Tissue Res 2008, 49:85-91.
17. Fraser RDB, Trus BL. Molecular mobility in the gap regions of type I collagen fibrils. J Mol Biol 1986, 6:221-226.
18. Fraser RDB, MacRae TP, Miller A. Molecular conformation and packing in collagen fibrils. J Mol Biol 1986, 167:497-521.
19. Fratzl P, Misof K, Zizak I. Fibrillar structure and mechanical properties of collagen. J Struct Biol 1997, 122:119-122.
20. Freed AD, Doehring TC. Elastic model for crimped collagen fibrils. J Biomech Eng 2005, 127:587-593.
21. Gathercole LJ, Keller A. Crimp morphology in the fibreforming collagens. Matrix 1991, 11:214-234.
22. Grytz R, Meschke G. Constitutive modelling of crimped collagen fibrils in soft tissues. J Mech Behav Biomed Mater 2009, 2:522-533.
23. Gutsmann T, Fantner GE, Venturoni M. Evidence that collagen fibrils in tendons are inhomogenously structures in a tubelike manner. Biophys J 2003, 84:2593-2598.
24. Hansen KA, Weiss JA, Barton JK. Recruitment of tendon crimp with applied tensile strain. J Biomech Eng 2002, 124:72-77.
25. Hart RA, Woo SL, Newton PO. Ultrastructural morphometry of anterior cruciate and medial collateral ligaments: an experimental study in rabbits. J Orthop Res 1992, 10:96-103.
26. Hess GP, Cappiello WL, Poole RM. Prevention and treatment of overuse tendon injuries. Sports Med 1989, 8:371-384.
27. Holmes DF, Gilpin CJ, Baldock C. Corneal collagen fibril structure in three dimensions: structural insights into fibril assembly, mechanical properties, and tissue organization. Proc Natl Acad Sci U S A 2001, 98:7307-7312.
28. Hongo C, Noguchi K, Okuyama K. Repetitive interactions observed in the crystal structure of a collagen-model peptide, [(Pro-Pro-Gly)9]3. J Biochem 2005, 138:135-144.
29. Hulmes DJS. Building collagen molecules, fibrils, and suprafibrillar structures. J Struct Biol 2002, 137:2-10.
30. Jozsa L, Kannus P. Histopathological findings in spontaneous tendon ruptures. Scand J Med Sci Sports 1997, 7:113-118.
31. Jozsa L, Kannus P, Balint JB. Three-dimensional ultrastructure of human tendons. Acta Anat 1991, 142:306-312.
32. Kadler KE, Holmes DF, Trotter JA. Collagen fibril formation. Biochem J 1996, 316:1-11.
33. Kannus P. Structure of the tendon connective tissue. Scand J Med Sci Sports 2000, 10:312-320.
34. Kastelic J, Palley I, Baer E. A structural mechanical model for tendon crimping. J Biomech 1980, 13:887-893.
35. Kure M, Araki K, Ogata T. Scanning tunneling microscopic study of osmium-impregnated collagen. J Electron Microsc 1995, 44:207-211.
36. Lanir Y. Structure-strength relations in mammalian tendon. Biophys J 1978, 24:541-554.
37. Learch H. Ueber der aufbau des sehnengewebes. Gegenbaurs Morphol Jahrb 1950, 90:192-205.
38. Lo IK, Marchuk LL, Leatherbarrow KE. Collagen fibrillogenesis and mRNA levels in the maturing rabbit medial collateral ligament and patellar tendon. Connect Tissue Res 2004, 45:11-22.
39. Lujan TJ, Underwood CI, Henninger HB. Effect of dermatan sulfate glycosaminoglycans on the quasi-static material properties of the human medial collateral ligament. J Orthop Res 2007, 25:894-903.
40. Lujan TJ, Underwood CJ, Jacobs NT. Contribution of glycosaminoglycans to viscoelastic tensile behavior of human ligament. J Appl Physiol 2009, 106:423-431.
41. Nicholls SP, Gathercole J, Shah JS. Morphology of human plamaris longus tendon. Ann Rheum Dis 1984, 43:477-482.
42. Niven H, Baer E, Hiltner A. Organization of collagen fibers in rat tail tendon at the optical microscope level. Coll Relat Res 1982, 2:131-142.
43. Orgel JP, Irving TC, Miller A. Microfibrillar structure of type I collagen in situ. Proc Natl Acad Sci U S A 2006, 103:9001-9005.
44. Ottani V, Raspanti M, Ruggeri A. Collagen structure and functional implications. Micron 2001, 32:251-260.
45. Ottani V, Martini D, Franchi M. Hierarchical structures in fibrillar collagens. Micron 2002, 33:587-596.
46. Parry DA, Barnes GR, Craig AS. 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 1978, 203:305-321.
47. Pins GD, Christiansen DL, Patel R. Self-assembly of collage fibers. Influence of fibrillar alignment and decorin on mechanical properties. Biophys J 1997, 73:2164-2172.
48. Puxkandl R, Zizak I, Paris O. Viscoelastic properties of collagen: synchontron radiation investigations and structural model. Philos Trans R Soc Lond B Biol Sci 2002, 357:191-197.
49. Raspanti M, Manelli A, Franchi M. The 3D structure of crimps in the rat Achilles tendon. Matrix Biol 2005, 24:503-507.
50. Reale E, Benazzo F, Ruggeri A. Differences in the microfibrillar arrangement of collagen fibrils. Distribution and possible significance. J Submicrosc Cytol 1981, 13:135-143.
51. van der Rest M, Garrone R. Collagen family of proteins. FASEB J 1991, 5:2814-2823.
52. Rigby BJ, Hirai N, Spikes JD. The mechanical properties of rat tail tendon. J Gen Physiol 1959, 43:265-283.
53. Robinson PS, Lin TW, Reynolds PR. Strain-rate sensitive mechanical properties of tendon fascicles from mice with genetically engineered alterations in collagen and decorin. J Biomech Eng 2004, 126:252-257.
54. Rowe RW. The structure of rat tail tendon. Connect Tissue Res 1985a, 14:9-20.
55. Rowe RW. The structure of rat tail tendon fascicles. Connect Tissue Res 1985b, 14:21-30.
56. Ruggeri A, Benazzo F, Reale E. Collagen fibrils with straight and helicoidal microfibrils: a freeze-fracture and thin-section study. J Ultrastruct Res 1979, 68:101-108.
57. Scott JE. Proteodermatan and proteokeratan sulphate (decorin, lumican/fibromodulin) proteins are horseshoe shaped. Implications for their interactions with collagens. Biochemistry (Mosc) 1996, 35:8795-8799.
58. Screen HR, Bader DL, Lee DA. Local strain measurement within tendon. Strain 2004a, 40:157-163.
59. Screen HR, Lee DA, Bader DL. An investigation into the effects of the hierarchical structure of tendon fascicles on micromechanical properties. Proc Inst Mech Eng H 2004b, 218:109-119.
60. Silver FH, Freeman JW, Seehra GP. Collagen self-assembly and the development of tendon mechanical properties. J Biomech 2003, 36:1529-1553.
61. Stolinski C. Disposition of collagen fibrils in human tendons. J Anat 1995, 186:577-583.
62. Verzar F. Aging of the collagen fiber. Int Rev Connect Tissue Res 1964, 2:243-300.
63. Viidik A. Simultaneous mechanical and light microscopic studies of collagen fibers. Z Anat Entwicklungsgesch 1972, 136:204-212.
64. Viidik A, Ekholm R. Light and electron microscopic studies of collagen fibers under strain. Z Anat Entwicklungsgesch 1968, 127:154-164.
65. Viidik A, Nielsen HM, Skalicky M. Influence of physical exercise on aging rats. II. Life-long exercise delays aging of tail tendon collagen. Mech Ageing Dev 1996, 88:139-148.
66. Wess TJ, Hammersley AP, Wess L. A consensus model for molecular packing of type I collagen. J Struct Biol 1998, 122:92-100.
67. Woo SLY, Debski RE, Withrow JD. Biomechanics of knee ligaments. Am J Sports Med 1999, 27:533-543.
68. Yannas I, Huang C. Fracture of tendon collagen. J Polym Sci A-2 Polym Phys 1972, 10:577-X.