Nanoscale structure of type I collagen fibrils: Quantitative measurement of D-spacing

Biotechnology Journal

Volumn 8, Issue 1, 2013, Pages 117-126

  Erickson, Blake ^a,b   Fang, Ming ^a,b   Wallace, Joseph M ^c   Orr, Bradford G ^a,b   Les, Clifford M ^d   Banaszak Holl, Mark M ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c Indiana University Purdue University Indianapolis   (United States)

^d HENRY FORD HOSPITAL   (United States)

Author keywords

2D fast fourier transform; Atomic force microscopy; Collagen fibril; D spacing

Indexed keywords

2D FAST FOURIER TRANSFORMS; CLINICAL APPLICATION; COLLAGEN FIBRILS; COMPLEMENTARY METHODS; D-SPACING; DATA SAMPLING; DISEASE MODELS; GENE KNOCKOUT; INSTRUMENT CALIBRATIONS; MORPHOLOGICAL FEATURES; NANO SCALE; NANOSCALE STRUCTURE; OSTEOGENESIS IMPERFECTA; QUANTITATIVE MEASUREMENT; QUANTITATIVE METHOD; STATISTICALLY SIGNIFICANT DIFFERENCE; STRUCTURAL INFORMATION; TYPE I COLLAGEN;

ATOMIC FORCE MICROSCOPY; COLLAGEN; ELECTRON MICROSCOPY; FAST FOURIER TRANSFORMS; TISSUE; TISSUE ENGINEERING;

NANOTECHNOLOGY;

COLLAGEN TYPE 1; ESTROGEN; NANOMATERIAL;

AGING; ANIMAL EXPERIMENT; ARTICLE; ATOMIC FORCE MICROSCOPY; COLLAGEN TYPE 1 D PERIODIC SPACING; ELECTRON MICROSCOPY; ESTROGEN DEFICIENCY; FEMALE; FOURIER TRANSFORMATION; GENE INACTIVATION; NONHUMAN; OSTEOGENESIS IMPERFECTA; PRIORITY JOURNAL; PROTEIN STRUCTURE; RADIATION SCATTERING; TISSUE ENGINEERING;

ANALYSIS OF VARIANCE; ANIMALS; COLLAGEN TYPE I; FEMALE; FOURIER ANALYSIS; MICROSCOPY, ATOMIC FORCE; NANOTECHNOLOGY; OVARIECTOMY; PROTEIN CONFORMATION; SHEEP; SKIN;

EID: 84871749972     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201200174     Document Type: Article

References (50)

1. Fratzl, P. (Ed.), Collagen: Structure and Mechanics, Springer, New York 2008.
2. Kadler, K. E., Holmes, D. F., Trotter, J. A., Chapman, J. A., Collagen fibril formation. Biochem. J. 1996, 316, 1-11.
3. Kadler, K. E., Baldock, C., Bella, J., Boot-Hanford, R. P., Collagens at a glance. J. Cell Sci. 2007, 120, 1955-1958.
4. Canty, E. G., Kadler, K. E., Procollagen trafficking, processing and fibrillogenesis. J. Cell Sci. 2005, 118, 1341-1353.
5. Bear, R. S., Long x-ray diffraction spacing of collagen. J. Am. Chem. Soc. 1942, 64, 727.
6. Schmitt, F. O., Hall, C. E., Jakus, M. A., Electron microscope investigations of the structure of collagen. J. Cell. Comp. Phys. 1942, 20, 11-33.
7. Hodge, A. J., Petruska, J. A., Recent studies with the electron microscope on ordered aggregates of the tropocollagen molecule, in: Ramachandran, G. N. (Ed.), Aspects of Protein Structure, Academic Press, New York 1963, p. 289.
8. Bigi, A., Koch, M. H. J., Panzavolta, S., Roveri, N., Rubini, K., Structural aspects of the calcification process of lower vertebrate collagen. Connect. Tissue Res. 2000, 41, 37-43.
9. Fraser, R. D. B., MacRae, T. P., Miller, A., Suzuki, E., Molecular conformation and packing in collagen fibrils. J. Mol. Biol. 1983, 167, 497-521.
10. Eikenberry, E. F., Brodsky, B., Parry, D. A. D., Collagen fibril morphology in developing chick metatarsal tendons: I. X-ray diffraction studies. Int. J.Biol. Macromol. 1982, 4, 322-328.
11. Brodsky, B., Eikenberry, E. F., Characterization of fibrous forms of collagen. Methods Enzymol. 1982, 82(PtA), 127-174.
12. Chapman, J. A., Tzaphlidou, M., Meek, K. M., Kadler, K. E., The collagen fibril - a model system for studying the staining and fixation of a protein. Electron Microsc. Rev. 1990, 3, 143-182.
13. Lin, A. C., Goh, M. C., Investigating the ultrastructure of fibrous long spacing collagen by parallel atomic force and transmission electron microscopy. Proteins 2002, 49, 378-384.
14. Arsenault, A. L., Image analysis of mineralized and non-mineralized type I collagen fibrils. J. Electron Microsc. Tech. 1991, 18, 262-268.
15. Orgel, J., Irving, T. C., Miller, A., Wess, T. J., Microfibrillar structure of type I collagen in situ. Proc. Natl. Acad. Sci. USA 2006, 103, 9001-9005.
16. Hulmes, D. J. S., Wess, T. J., Prockop, D. J., Fratzl, P., Radial packing, order, and disorder in collagen fibrils. Biophys. J. 1995, 68, 1661-1670.
17. Hulmes, D. J. S., Miller, A., Quasi-hexagonal molecular packing in collagen fibrils. Nature 1979, 282, 878-880.
18. Fraser, R. D. B., MacRae, T. P., Miller, A., Molecular packing in type I collagen fibrils. J. Mol. Biol. 1987, 193, 115-125.
19. Orgel, J. P. R. O., Miller, A., Irving, T. C., Fischetti, R. F. et al., The in situ supermolecular structure of type I collagen. Structure 2001, 9, 1061-1069.
20. Trus, B. L., Piez, K. A., Compressed microfibril models of the native collagen fibril. Nature 1980, 286, 300-301.
21. Piez, K. A., Trus, B. L., A new model for packing of type-I collagen molecules in the native fibril. Biosci. Rep. 1981, 1, 801-810.
22. Gautieri, A., Vesentini, S., Redaelli, A., Buehler, M. J., Hierarchical structure and nanomechanics of collagen microfibrils from the atomistic scale up. Nano Lett. 2011, 11, 757-766.
23. Wallace, J. M., Chen, Q., Fang, M., Erickson, B. et al., Type I collagen exists as a distribution of nanoscale morphologies in teeth, bones, and tendons. Langmuir 2010, 26, 7349-7354.
24. Wallace, J. M., Erickson, B., Les, C. M., Orr, B. G., Banaszak Holl, M. M., Distribution of type I collagen morphologies in bone: Relation to estrogen depletion in bone. Bone 2010, 46, 1349-1354.
25. Fang, M., Liroff, K. G., Turner, A. S., Les, C. M. et al., Estrogen depletion results in nanoscale morphology changes in dermal collagen. J. Invest. Dermatol. 2012, 132, 1791-1797.
26. Wallace, J. M., Orr, B. G., Marini, J. C., Banaszak Holl, M. M., Nanoscale morphology of type I collagen is altered in the Brtl mouse model of osteogenesis imperfecta. J. Struct. Biology 2011, 173, 146-152.
27. Fratzl, P., Fratzlzelman, N., Klaushofer, K., Collagen packing and mineralization - an X-ray-scattering investigation of turkey leg tendon. Biophys. J. 1993, 64, 260-266.
28. Fang, M., Liroff, G. K., Turner, A. S., Les, C. M. et al., Estrogen Depletion results in nanoscale morphology changes in dermal collagen J. Invest. Dermatol. 2012, 132, 1791-1797.
29. Habelitz, S., Balooch, M., Marshall, S. J., Balooch, G., Marshall, G. W., In situ atomic force microscopy of partially demineralized human dentin collagen fibrils. J. Struct. Biol. 2002, 138, 227-236.
30. Hassenkam, T., Fantner, G. E., Cutroni, J. A., Weaver, J. C. et al., High-resolution AFM imaging of intact and fractured trabecular bone. Bone 2004, 35, 4-10.
31. Baranauskas, V., Garavello-Freitas, I., Jingguo, Z., Cruz-Hofling, M. A., Observation of the bone matrix structure of intact and regenerative zones of tibias by atomic force microscopy. J. Vacuum Sci. Technol. A 2001, 19, 1042-1045.
32. Kindt, J. H., Thurner, P. J., Lauer, M. E., Bosma, B. L. et al., In situ observation of fluoride-ion-induced hydroxyapatite-collagen detachment on bone fracture surfaces by atomic force microscopy. Nanotechnology 2007, 135102.
33. Cremer, C., Kaufman, R., Gunkel, M., Pres, S. et al., Superresolution imaging of biological nanostructures by spectral precision distance microscopy. Biotechnol. J. 2011, 6, 1037-1051.
34. Wallace, J. M., Applications of atomic force microscopy for the assessment of nanoscale morphological and mechanical properties of bone. Bone 2012, 50, 420-427.
35. Buehler, M. J., Keten, S., Ackbarow, T., Theoretical and computational hierarchical nanomechanics of protein materials: Deformation and fracture. Prog. Mater. Sci. 2008, 53, 1101-1241.
36. Mogilner, I. G., Ruderman, G., Grigera, J. R., Collagen stability, hydration and native state. J. Mol. Graphics Model. 2002, 21, 209-213.
37. Price, R. I., Lees, S., Kirschner, D. A., X-ray diffraction analysis of tendon collagen at ambient and cryogenic temperatures: Role of hydration. Int. J. Biol. Macromol. 1997, 20, 23-33.
38. Habelitz, S., Balooch, M., Marshall, S. J., Balooch, G., Marshall, G. W. Jr., In situ atomic force microscopy of partially demineralized human dentin collagen fibrils. J. Struct. Biol. 2002, 138, 227-236.
39. Brodsky, B., Eikenberry, E. F., Cassidy, K., An unusual collagen periodicity in skin. Biochim. Biophys. Acta 1980, 621, 162-166.
40. Sasaki, N., Shukunami, N., Matsushima, N., Izumi, Y., Time-resolved X-ray diffraction from tendon collagen during creep using synchrotron radiation. J. Biomech. 1999, 32, 285-292.
41. Puxkandl, R., Zizak, I., Paris, O., Keckes, J. et al., Viscoelastic properties of collagen: Synchrotron radiation investigations and structural model. Philos. Trans. R. Soc. B Biol.Sci. 2002, 357, 191-197.
42. Gupta, H. S., Zioupos, P., Fracture of bone tissue: The 'hows' and the 'whys'. Med. Eng. Phys. 2008, 30, 1209-1226.
43. Drits, V. A., Eberl, D. D., Srodon, J., XRD measurement of mean thickness, thickness distribution and strain for illite and illite-smectite crystallites by the Bertaut-Warren-Averbach technique. Clays Clay Miner. 1998, 46, 38-50.
44. Haczynski, J., Tarkowski, R., Jarzabek, K., Slomczynska, M. et al., Human cultured skin fibroblasts express estrogen receptor alpha and beta. Int. J. Mol. Med. 2002, 10, 149-153.
45. Dimitrios J, H., Ioannis I, A., Bone remodeling. Ann. N. Y. Acad. Sci. 2006, 1092, 385-396.
46. Brincat, M. P., Baron, Y. M., Galea, R., Estrogens and the skin. Climacteric 2005, 8, 110-123.
47. Brincat, M., Moniz, C. J., Studd, J. W. W., Long-term effects of the menopause and sex hormones on skin thickness. Br. J. Obstet. Gynaecol. 1985, 92, 256-259.
48. Chang, S.-W., Shefelbine, S. J., Buehler, M. J., Structural and mechanical differences between collagen homo- and heterotrimers: Relevance for the molecular origin of brittle bone disease. Biophys. J. 2012, 102, 640-648.
49. Lee, K. H., Kuczera, K., Banaszak Holl, M. M., The severity of osteogenesis imperfecta: A comparison to the relative free energy differences of collagen model peptides. Biopolymers 2011, 95, 182-193.
50. Gautieri, A., Uzel, S., Vesentini, S., Redaelli, A., Buehler, M. J., Molecular and mesoscale mechanisms of osteogenesis imperfecta disease in collagen fibrils. Biophys. J. 2009, 97, 857-865.