The structure and function of normally mineralizing avian tendons

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 133, Issue 4, 2002, Pages 1135-1157

  Landis, William J ^a   Silver, Frederick H ^b  

^a Northeastern Ohio Medical University   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Biomechanics; Elastic modulus; Matrix vesicles; Mineralization; Strain; Stress; Tendon; Type I collagen

Indexed keywords

CALCIUM; COLLAGEN TYPE 1; PROTEOGLYCAN;

ACHILLES TENDON; BIOMECHANICS; CONFERENCE PAPER; EXTRACELLULAR MATRIX; FOWL; GASTROCNEMIUS MUSCLE; HIP; LEG; LOCOMOTION; MELEAGRIS GALLOPAVO; MINERALIZATION; MUSCLE FUNCTION; NONHUMAN; TENDON; TURKEY (BIRD);

ANIMALIA; AVES; MELEAGRIS GALLOPAVO;

EID: 0036901730     PISSN: 10956433     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1095-6433(02)00248-9     Document Type: Conference Paper

References (124)

1. Abdalla O. Ossification and mineralization in the tendons of the chicken (Gallus domesticus). J. Anat. 129:1979;351-359.
2. Alexander R.M. Animal Mechanics. Second ed: 1983;Blackwell Scientific, Oxford, United Kingdom.
3. Alexander R.M. Elastic energy stores in running vertebrates. A. Zool. 24:1984;85-94.
4. Ali S.Y. Analysis of matrix vesicles and their role in the calcification of epiphyseal cartilage. Fed. Proc. 35:1976;135-142.
5. Anderson H.C. Vesicles associated with calcification in the matrix of epiphyseal cartilage. J. Cell Biol. 41:1969;59-72.
6. Anderson H.C. Mineralization by matrix vesicles. Scan. Electron Microsc. 2:1984;953-964.
7. Arsenault A.L. Crystal-collagen relationships in calcified turkey leg tendons visualized by selected-area dark field electron microscopy. Calcif. Tissue Int. 43:1988;202-212.
8. Bernard G.W., Pease D.C. An electron microscopic study of initial intramembranous osteogenesis. Am. J. Anat. 125:1969;271-290.
9. Berthet-Colominas C., Miller A., White S.W. Structural study of the calcifying collagen in turkey leg tendons. J. Mol. Biol. 134:1979;431-445.
10. Bianco P., Fisher L., Young M., Termine J., Gehron Robey P. Expression and localization of the two small proteoglycans biglycan and decorin in developing human skeletal and non-skeletal tissues. J. Histochem. Cytochem. 38:1990;1549-1563.
11. Bonucci E. Fine structure and histochemistry of calcifying globules in epiphyseal cartilage. Z. Zellforsch. Mikroskop. Anat. 103:1970;192-217.
12. Boudreau N.J., Jones P.L. Extracellular matrix and integrin signaling: The shape of things to come. Biochem. J. 339:1999;481-488.
13. Breen E.C. Mechanical strain increases type I collagen expression in pulmonary fibroblasts. J. Appl. Physiol. 88:2000;203-209.
14. Carmeliet G., Nys G., Bouillon R. Microgravity reduces the differentiation of human osteoblastic MG-63 cells. J. Bone Miner. Res. 12:1997;786-794.
15. Chen-Izu Y., Moreno A.P., Spangler R.A. Opposing gates model for voltage gating of gap junction channel. Am. J. Physiol. 281:2001;C1604-C1613.
16. Christoffersen J.C., Landis W.J. A contribution with review to the description of mineralization of bone and other calcified tissues in vivo. Anat. Rec. 230:1991;435-450.
17. Collet P., Uebelhart D., Vico L., Moro L., Hartmann D., Roth M. Effects of 1- and 6-month spaceflight on bone mass area and biochemistry in two humans. Bone. 20:1997;547-551.
18. Cooper R.R., Misol S. Tendon and ligament insertion. A light and electron microscopic study. J. Bone Joint Surg. Am. 52A:1970;1-20.
19. D'Andrea P., Vittur F. Gap junctions mediate intercellular calcium signaling in cultured articular chondrocytes. Cell Calcium. 20:1996;389-397.
20. 2+ waves in mechanically stimulated articular chondrocytes. Biorheology. 37:2000;75-83.
21. Davis M.J., Donovitz J.A., Hood J.D. Stretch-activated single-channel whole cell currents in vascular smooth muscle cells. Am. J. Physiol. 262:1992;C1083-C1088.
22. Diamond S.L., Sachs F., Sigurdson W.J. Mechanically induced calcium mobilization in cultured endothelial cells is dependent on actin and phospholipase. Arterioscler. Thromb. 14:1994;2000-2006.
23. Durrant L.A., Archer C.W., Benjamin M., Ralphs J.R. Organization of the chondrocyte cytoskeleton and its response to changing mechanical conditions in organ culture. J. Anat. 194:1999;343-353.
24. Eastwood M., Mudera V.C., McGrouther D.A., Brown R.A. Effect of precise mechanical loading on fibroblast populated collagen lattices: Morphological changes. Cell Motil. Cytoskeleton. 40:1998;13-21.
25. Elefteriou F., Exposito J.Y., Garrone R., Lethias C. Binding of tenascin-X to decorin. FEBS Lett. 495:2001;44-77.
26. Ezura Y., Chakravarti S., Oldberg A., Chervoneva I., Birk D.E. Differential expression of lumican and fibromodulin regulates collagen fibrillogenesis in developing mouse tendons. J. Cell Biol. 151:2000;779-787.
27. Glimcher M.J. Recent studies of the mineral phase in bone and its possible linkage to the organic matrix by protein-bound phosphate bonds. Phil. Trans. Roy. Soc. Lond. B304:1984;479-508.
28. Glimcher M.J., Brickley-Parsons D., Kossiva D. Phosphopeptides and γ-carboxyglutamic acid-containing peptides in calcified turkey tendon: Their absence in uncalcified tendon. Calcif. Tissue Int. 27:1979;281-284.
29. Glimcher M.J., Hodge A.J., Schmitt F.O. Macromolecular aggregation states in relation to mineralization: The collagen-hydroxyapatite system as studied in vitro. Proc. Natl. Acad. Sci. USA. 43:1957;860-867.
30. Glimcher M.J., Krane S.M. The organization and structure of bone, and the mechanism of calcification. Ramachandran G.N., Gould B.S. Biology of Collagen. Treatise on Collagen. IIB:1968;68-251 Academic Press, New York.
31. Guignandon A., Usson Y., Laroche N., Lafrage-Proust M.H., Sabido O., Alexandre C., Vico L. Effects of intermittent or continuous gravitational stresses on cell-matrix adhesion: Quantitative analysis of focal contacts in osteoblastic ROS 17/2.8 cells. Exp. Cell Res. 10:1997;66-75.
32. Guilak F. Compression-induced changes in the shape and volume of the chondrocyte nucleus. J. Biomech. 28:1995;1529-1541.
33. Hodge A.J., Petruska J.A. Recent studies with the electron microscope on ordered aggregates of the tropocollagen macromolecule. Ramachandran G.N. Aspects of Protein Structure. 1963;289-300 Academic Press, New York.
34. Hohling H.J., Barckhaus R.H., Krefting E.R. Hard tissue formation in collagen-rich systems - Calcium-phosphate nucleation and organic matrix. Trends Biochem. Sci. 5:1980;8-11.
35. Hsu H.H., Anderson H.C. Evidence of the presence of a specific ATPase responsible for ATP-initiated calcification by matrix vesicles isolated from cartilage and bone. J. Biol. Chem. 271:1996;26383-26388.
36. Ingber D. Integrins as mechanochemical transducers. Curr. Opin. Cell. Biol. 3:1991;841-848.
37. Ingber D.E. Tensegrity: The architectural basis of cellular mechanotransduction. Annu. Rev. Physiol. 59:1997;575-599.
38. Ingber D. How cells (might) sense microgravity. Fed. Am. Soc. Exp. Biol. J. 13:1999;S3-S15.
39. Iozzo R.V. The family of the small leucine-rich proteoglycans: Key regulators of matrix assembly and cellular growth. Crit. Rev. Biochem. Mol. Biol. 32:1997;141-174.
40. Johnson L.C. Mineralization of turkey leg tendon. I. Histology and histochemistry of mineralization. Sognnaes R.F. Calcification in Biological Systems. 1960;117-128 American Association for the Advancement of Science, Washington, DC.
41. Jorgensen N.R., Henriksen Z., Brot C., Riksen E.F., Sorensen O.H., Civitelli R., Steinberg T.H. Human osteoblastic cells propagate intercellular calcium signals by two different mechanisms. J. Bone Miner. Res. 15:2000;1024-1032.
42. Karimbux N.Y., Nishimura I. Temporal and spatial expressions of type XII collagen in the remodeling periodontal ligament during experimental tooth movement. J. Dent. Res. 73:1995;313-318.
43. Katz E.P., Li S.-T. The intermolecular space of reconstituted collagen fibrils. J. Mol. Biol. 73:1973a;351-369.
44. Katz E.P., Li S.-T. Structure and function of bone collagen fibrils. J. Mol. Biol. 80:1973b;1-15.
45. Keene D.R., Lunstrum G.P., Morris N.P., Stoddard D.W., Burgeson R.E. Two type XII-like collagens localize to the surface of banded collagen fibrils. J. Cell Biol. 113:1991;971-978.
46. Keene D.R., San Antonio J.D., Mayne R., McQuillan D.J., Sarris G., Santoro S.A., Iozzo R.V. Decorin binds near the C terminus of type I collagen. J. Biol. Chem. 275:2000;21801-21804.
47. Kessler D., Dethlefsen S., Haase I., Plomann M., Hirche F., Krieg T., Eckes B. Fibroblasts in mechanically stressed collagen lattices assume a 'synthetic' phenotype. J. Biol. Chem. 276:2001;36375-36385.
48. Khachigian L.M., Resnick N., Gimbrone M.A. Jr., Tucker C. Nuclear factor-κB interacts functionally with the platelet-derived growth-B chain shear-stress response element in vascular endothelial cells exposed to shear stress. J. Clin. Invest. 96:1995;1169-1175.
49. Kirber M.T., Walsh J.V., Singer J.J. Stretch-activated ion channels in smooth muscle: A mechanism for the initiation of stretch-induced contraction. Pflugers Arch. 412:1988;339-345.
50. Kirsch T., Nah H.D., Demuth D.R., Harrison G., Golub E.E., Adams S.L., Pacifici M. Annexin V-mediated calcium flux across membranes is dependent on the lipid composition: Implications for cartilage mineralization. Biochemistry. 36:1997;3359-3367.
51. Kirsch T., Harrison G., Golub E.E., Nah H.D. The roles of annexins and types II and X collagen in matrix vesicle-mediated mineralization of growth plate cartilage. J. Biol. Chem. 275:2000;35577-35583.
52. Ko K.S., Arora P.D., McCulloch C.A. Cadherins mediate intercellular mechanical signaling in fibroblasts by activation of stretch-sensitive calcium permeable channels. J. Biol. Chem. 276:2001;35967-35977.
53. Laher I., van Breemen C., Bevan J.A. Stretch-dependent calcium uptake associated with myogenic tone in rabbit facial vein. Circ. Res. 63:1988;669-672.
54. Landis W.J. Temporal sequences of mineralization in calcifying turkey leg tendon. Butler W.T. The Chemistry and Biology of Mineralized Tissues. 1985;360-363 Ebsco Media, Birmingham, AL.
55. Landis W.J. A study of calcification in the leg tendons from the domestic turkey. J. Mol. Struct. Res. 94:1986;217-238.
56. Landis W.J. The strength of a calcified tissue depends in part on the molecular structure and organization of its constituent mineral crystals in their organic matrix. Bone. 16:1995;533-544.
57. Landis W.J. Mineral characterization in calcifying tissues: atomic, molecular and macromolecular perspectives. Connect. Tissue Res. 34:1996;239-246.
58. Landis W.J. An overview of vertebrate mineralization with emphasis on collagen-mineral interaction. Gravitational Space Biol. Bull. 12:1999;15-26.
59. Landis W.J., Arsenault A.L. Vesicle- and collagen-mediated calcification in the turkey leg tendon. Connect. Tissue Res. 22:1989;39-42.
60. Landis W.J., Song M.J. Initial mineral deposition in calcifying tendon characterized by high voltage electron microscopy and three-dimensional graphic imaging. J. Struct. Biol. 107:1991;116-127.
61. Landis W.J., Paine M.C., Hodgens K.J., Glimcher M.J. Matrix vesicles in embryonic chick bone: Considerations of their identification, number, distribution, and possible effects on calcification of extracellular matrices. J. Ultrastruct. Mol. Struct. Res. 95:1986;142-163.
62. Landis W.J., Moradian-Oldak J., Weiner S. Topographic imaging of mineral and collagen in the calcifying turkey tendon. Connect. Tissue Res. 25:1991;181-196.
63. Landis W.J., Hodgens K.J., McKee M.D., et al. Extracellular vesicles of calcifying turkey leg tendon characterized by immunocytochemistry and high voltage electron microscopic tomography and 3-D graphic image reconstruction. Bone Miner. 17:1992a;237-241.
64. Landis W.J., Hodgens K., Song M.J., Arena J., Kiyonaga S., McEwen B. Mineral and collagen interaction during calcification. Slavkin H., Price P. Chemistry and Biology of Mineralized Tissues. 1992b;211-219 Elsevier Science, New York.
65. Landis W.J., Song M.J., Leith A., McEwen L., McEwen B. Mineral and organic matrix interaction in normally calcifying tendon visualized in three dimensions by high voltage electron microscopic tomography and graphic image reconstruction. J. Struct. Biol. 110:1993;39-54.
66. Landis W.J., LiBrizzi J.J., Dunn M.G., Silver F.H. A study of the relationship between mineral content and mechanical properties of turkey gastrocnemius tendon. J. Bone Miner. Res. 10:1995;859-867.
67. Landis W.J., Hodgens K.J., Arena J., Song M.J., McEwen B.F. The structural relation between collagen and mineral in bone as determined by high voltage electron microscopic tomography. Microsc. Res. Technol. 33:1996a;192-202.
68. Landis W.J., Hodgens K.J., Song M.J., et al. Mineralization of collagen occurs on fibril surfaces: Evidence from conventional and high voltage electron microscopy and three-dimensional imaging. J. Struct. Biol. 117:1996b;24-35.
69. Landis W.J., Hodgens K.J., Block D., Toma C.D., Gerstenfeld L.C. Spaceflight effects on cultured embryonic chick bone cells. J. Bone Miner. Res. 15:2000;1099-1112.
70. Lees S., Prostak K.S., Ingle V.K., Kjoller K. The loci of mineral in turkey leg tendon as seen by atomic force microscopy and electron microscopy. Calcif. Tissue Int. 55:1994;180-189.
71. Likens R.C., Piez K.A., Kunde M.L. Mineralization of turkey leg tendon. III. Chemical nature of the protein and mineral phases. Sognnaes R.F. Calcification in Biological Systems. 1960;143-149 American Association for the Advancement of Science, Washington, DC.
72. Maitland M.E., Arsenault A.L. A correlation between the distribution of biological apatite and amino acid sequence of type I collagen. Calcif. Tissue Int. 48:1991;341-352.
73. McEwen B.F., Song M.J., Landis W.J. Quantitative determination of the mineral distribution in different collagen zones of calcifying tendon using high voltage electron microscopic tomography. J. Computer-Assist. Microsc. 3:1992;201-210.
74. Moradian-Oldak J., Weiner S., Addadi L., Landis W.J., Traub W. Electron diffraction study of individual crystals of bone, mineralized tendon and synthetic apatite. Connect. Tissue Res. 25:1991;219-228.
75. Morey-Holton E.R., Whalen R.T., Arnaud S.B., van der Meulen M.C. The skeleton and its adaptation to gravity. Fregly M.J., Blatteis C.M. Microgravity. Handbook of Physiology: Environmental Physiology. Section 4: The gravitational environment. 1:1996;691-720 Oxford University Press, New York.
76. Mosler E., Folkhard W., Knorzer E., Nemetschek-Gansler H., Nemetschek T., Koch M.H. Stress-induced molecular arrangement in tendon collagen. J. Mol. Biol. 182:1985;589-596.
77. Mudera V.C., Pleass R., Eastwood M., et al. Molecular responses of human dermal fibroblasts to dual cues: Contact guidance and mechanical load. Cell Motil. Cytoskeleton. 45:2000;1-9.
78. Nakayama K. Calcium-dependent contractile activation of cerebral artery produced by quick stretch. Am. J. Physiol. 242:1982;H760-H768.
79. Nylen M.J., Scott D.B., Mosley V.M. Mineralization of turkey leg tendon. II. Collagen-mineral relations as revealed by electron and x-ray microscopy. Sognnaes R.F. Calcification in Biological Systems. 1960;129-142 American Association for the Advancement of Science, Washington, DC.
80. Osol G., Laher I., Cipolla M. Protein kinase C modulates basal myogenic tone in resistance arteries from the cerebral circulation. Circ. Res. 68:1991;359-367.
81. Osol G., Laher I., Kelly M. Myogenic tone is coupled to phospholipase C and G protein activation in small cerebral arteries. Am. J. Physiol. 265:1993;H415-H420.
82. Paterlini M.G., Nemethy G., Scheraga H.A. The energy of formation of internal loops in triple-helical collagen polypeptides. Biopolymers. 35:1995;607-619.
83. Redini F. Structure and regulation of proteoglycan expression in articular cartilage. Pathol. Biol. 49:2001;364-375.
84. Resnick N., Collins T., Atkinson W., Bonthron D.T. Jr., Dewey C.F. Jr., Gimbron M.A. Jr. Platelet-derived growth factor B chain promoter contains a cis-acting fluid shear-stress-responsive element. Proc. Natl. Acad. Sci. USA. 90:1993;4591-4595.
85. Roberts T.J., Marsh R.L., Weyand P.G., Taylor C.R. Muscular force in running turkeys: The economy of minimizing work. Science. 275:1997;113-115.
86. Robinson R.A. An electron-microscope study of the crystalline inorganic component of bone and its relationship to the organic matrix. J. Bone Joint Surg. 34:1952;389-434.
87. Robinson R.A., Watson M.L. Collagen-crystal relationships in bone as seen in the electron microscope. Anat. Rec. 114:1952;383-410.
88. Sachs F. Mechanical transduction by membrane ion channels: A mini review. Mol. Cell. Biochem. 104:1991;57-60.
89. Schiller P.C., D'Ippolito G., Brambilla R., Roos B.A., Howard G.A. Inhibition of gap-junctional communication induces the trans-differentiation of osteoblasts to an adipocytic phenotype in vitro. J. Biol. Chem. 276:2001;14133-14138.
90. Scott J.E. The nomenclature of glycosaminoglycans and proteoglycans. Glycoconj. J. 10:1993;419-421.
91. Scott J.E., Orford C.R. Dermatan sulphate-rich proteoglycan associates with rat tail-tendon collagen at the d band in the gap region. Biochem. J. 197:1981;213-216.
92. Shadwick R.E. Elastic energy storage in tendons: Mechanical differences related to function and age. J. Appl. Physiol. 68:1990;1033-1040.
93. Sibonga J.D., Zhang M., Evans G.L., Westerlind K.C., Cavolina J., Morey-Holton E., Turner R.T. Effects of spaceflight and simulated weightlessness on longitudinal bone growth. Bone. 27:2000;535-540.
94. Silver F.H. Biological Materials: Structure, Mechanical Properties and Modeling of Soft Tissues. 1987;New York University Press, New York.
95. Silver F.H., Christiansen D., Snowhill P.B., Chen Y., Landis W.J. The role of mineral in the storage of elastic energy in turkey tendons. Biomacromolecules. 1:2000a;180-185.
96. Silver F.H., Christiansen D.L., Snowhill P., Chen Y. Role of storage on changes in the mechanical properties of tendon and self-assembled collagen fibers. Connect. Tissue Res. 41:2000b;155-164.
97. Silver F.H., Bradica G., Tria A. Viscoelastic behavior of osteoarthritic cartilage. Connect. Tissue Res. 42:2001a;223-233.
98. Silver F.H., Christiansen D.L., Snowhill P.B., Chen Y. Transition from viscous to elastic-based dependency of mechanical properties of self-assembled type I collagen fibers. J. Appl. Polymer Sci. 79:2001b;134-142.
99. Silver F.H., Freeman J.W., DeVore D. Viscoelastic properties of human skin and processed dermis. Skin Res. Technol. 7:2001c;18-23.
100. Silver F.H., Freeman J.W., Horvath I., Landis W.J. Molecular basis for elastic energy storage in mineralized tendon. Biomacromolecules. 2:2001d;750-756.
101. Silver F.H., Bradica G., Tria A. Elastic energy storage in human articular cartilage: Estimation of the elastic spring constant for type II collagen and changes associated with osteoarthritis. Matrix Biol. 21:2002a;129-137.
102. Silver, F.H., Ebrahimi, A., Snowhill, P.B., 2002b. Viscoelastic properties of self-assembled type I collagen fibers: Molecular basis of elastic and viscous behaviors. Connect. Tissue Res., in press.
103. Silver, F.H., Freeman, J.W., Seehra, G.P., 2002c. Collagen self-assembly and development of matrix mechanical properties. J. Biomech., in press.
104. Silver F.H., Horvath I., Foran D.J. Mechanical implications of the domain structure of fibril forming collagens: Comparison of the molecular and fibrillar flexibility of α-chains found in types I, II and III collagen. J. Theor. Biol. 216:2002d;243-254.
105. Silver F.H., Seehra P., Freeman J.W. Viscoelastic properties of young and old human dermis: Evidence that elastic energy storage occurs in the flexible regions of collagen and elastin. J. Appl. Polymer Sci. 86:2002e;1978-1985.
106. Siperko L.M., Landis W.J. Aspects of mineral structure in normally calcifying avian tendon. J. Struct. Biol. 135:2001;313-320.
107. Takeichi M. The cadherins: Cell-cell adhesion molecules controlling animal morphogenesis. Development. 102:1988;639-655.
108. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 251:1991;1451-1455.
109. Traub W., Arad T., Weiner S. Three-dimensional ordered distribution of crystals in turkey tendon collagen fibers. Proc. Natl. Acad. Sci. USA. 86:1989;9822-9826.
110. Traub W., Arad T., Weiner S. Growth of mineral crystals in turkey tendon collagen fibers. Connect. Tissue Res. 28:1992;99-111.
111. Vandenburgh H., Chromiak J., Shansky J., Del Tatto M., Lemaire J. Space travel directly induces skeletal muscle atrophy. Fed. Am. Soc. Exp. Biol. J. 13:1999;1031-1038.
112. Vogel K.G., Ordog A., Pogany G., Olah J. Proteoglycans in the compressed region of human tibialis posterior tendon and in ligaments. J. Orthop. Res. 11:1993;68-77.
113. Webb C.M., Zaman G., Mosley J.R., Tucker R.P., Lanyon L.E., Mackie E.J. Expression of tenascin-C in bones responding to mechanical load. J. Bone Miner. Res. 12:1997;52-58.
114. Weiner S., Price P.A. Disaggregation of bone into crystals. Calcif. Tissue Int. 39:1986;365-375.
115. Weiner S., Traub W. Organization of hydroxyapatite crystals within collagen fibrils. FEBS Lett. 206:1986;262-266.
116. Weiner S., Traub W. Crystal size and organization in bone. Connect. Tissue Res. 21:1989;259-265.
117. Westerlind K.C., Turner R.T. The skeletal effects of spaceflight in growing rats: Tissue specific alterations in mRNA levels for TGF-β J. Bone Miner. Res. 10:1995;843-848.
118. White S.W., Hulmes D.J.S., Miller A., Timmins P.A. Collagen-mineral axial relationship in calcified turkey leg tendon by x-ray and neutron diffraction. Nature. 266:1977;421-425.
119. Wilda M., Bachner D., Just W., Geerkens C., Kraus P., Vogel W., Hameister H. A comparison of the expression pattern of five genes of the family of small leucine-rich proteoglycans during mouse development. J. Bone Miner. Res. 15:2000;2187-2196.
120. Wu J.J., Eyre D.R., Landis W.J. Cross-linking and the calcification of bone and tendon collagens. Trans. Orthop. Res. Soc. 12:1987;313.
121. Wuthier R. Proposed mechanism of matrix vesicle formation and vesicle-mediated mineralization. Ascenzi A., Bonucci E., de Bernard B. Matrix Vesicles. Proceedings of the Third International Conference on Matrix Vesicles. 1981;103-109 Wichtig Editore srl, Milan, Italy.
122. Xu Y., Gurusiddappa S., Rich R.L., et al. Multiple binding sites in collagen type I for the integrins α1β1 and α2β1. J. Biol. Chem. 275:2000;38981-38989.
123. Yamauchi M., Katz E.P., Otsubo K., Teraoka K., Mechanic G.L. Cross-linking and stereospecific structure of collagen in mineralized and nonmineralized skeletal tissues. Connect. Tissue Res. 21:1989;159-169.
124. Yang X.C., Sachs F. @ 'Mechanically sensitive, non-selective cation channels. Siemen D., Hescheler J. Nonselective cation channels: Pharmacoloy, Physiology, and Biophysics. 1993;79-92 Springer-Verlag, Heidelberg.