Applications of atomic force microscopy for the assessment of nanoscale morphological and mechanical properties of bone

Bone

Volumn 50, Issue 1, 2012, Pages 420-427

  Wallace, Joseph M ^a  

^a Indiana University Purdue University Indianapolis   (United States)

Author keywords

AFM; Collagen; Mineral; SPM; Structure function

Indexed keywords

CARBON NANOTUBE; COLLAGEN TYPE 1; DNA;

ATOMIC FORCE MICROSCOPY; BONE DEMINERALIZATION; BONE MINERAL; BONE MORPHOLOGY; HIGH RESOLUTION COMPUTER TOMOGRAPHY; HUMAN; MECHANICS; MORPHOLOGY; NANOANALYSIS; PIEZOELECTRICITY; REVIEW; SCANNING PROBE MICROSCOPY; STATIC ELECTRICITY;

BONE AND BONES; HUMANS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, SCANNING PROBE; RESEARCH; SURFACE PROPERTIES;

EID: 84455202277     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2011.11.008     Document Type: Review

References (64)

1. Lakes R. Materials with structural hierarchy. Nature 1993, 361(6412):511-515.
2. Ritchie R.O., Buehler M.J., Hansma P. Plasticity and toughness in bone. Phys Today 2009, 62:41-47.
3. Fratzl P., Gupta H.S., Paschalis E.P., Roschger P. Structure and mechanical quality of the collagen-mineral nano-composite in bone. J Mater Chem 2004, 14(14):2115-2123.
4. Gupta H.S., Wagermaier W., Zickler G.A., Raz-Ben Aroush D., Funari S.S., Roschger P., et al. Nanoscale deformation mechanisms in bone. Nano Lett 2005, 5(10):2108-2111.
5. Silverman S.R., Fuyat R.K., Weiser J.D. Quantitative determination of calcite associated with carbonate-bearing apatites. Am Mineral 1952, 37:211-222.
6. Paschalis E.P., Verdelis K., Doty S.B., Boskey A.L., Mendelsohn R., Yamauchi M. Spectroscopic characterization of collagen cross-links in bone. J Bone Miner Res 2001, 16(10):1821-1828.
7. Mendelsohn R., Hassankhani A., DiCarlo E., Boskey A. FT-IR microscopy of endochondral ossification at 20 spatial resolution. Calcif Tissue Int 1989, 44(1):20-24.
8. Timlin J.A., Carden A., Morris M.D. Chemical microstructure of cortical bone probed by Raman transects. Appl Spectrosc 1999, 53(11):1429-1435.
9. Wallace J.M., Golcuk K., Morris M.D., Kohn D.H. Inbred strain-specific response to biglycan deficiency in the cortical bone of C57BL6/129 and C3H/He mice. J Bone Miner Res 2009, 24(6):1002-1012.
10. Thurner P.J., Chen C.G., Ionova-Martin S., Sun L., Harman A., Porter A., et al. Osteopontin deficiency increases bone fragility but preserves bone mass. Bone 2010, 46:1564-1573.
11. Gupta H.S., Seto J., Wagermaier W., Zaslansky P., Boesecke P., Fratzl P. Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc Natl Acad Sci U S A 2006, 103(47):17741-17746.
12. Giraud-Guille M.M. Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif Tissue Int 1988, 42(3):167-180.
13. Weiner S., Arad T., Sabanay I., Traub W. Rotated plywood structure of primary lamellar bone in the rat: orientations of the collagen fibril arrays. Bone 1997, 20(6):509-514.
14. Morris V.J., Kirby A.R., Gunning A.P. Atomic force microscopy for biologists 1999, Imperial College Press, Norwich, UK.
15. Eaton P., West P. Atomic Force Microscopy 2010, Oxford Univ Press.
16. Schmalz G. Uber Glatte und Ebenheit als physikalisches und physiologishes Problem 1929.
17. Becker H. Apparatus for measuring surface irregularities 1955.
18. Young R., Ward J., Scire F. The topografiner: an instrument for measuring surface microtopography. Rev Sci Instrum 1972, 43(7):999-1011.
19. Binnig G., Rohrer H., Gerber C., Weibel E. Surface studies by scanning tunneling microscopy. Phys Rev Lett 1982, 49(1):57-61.
20. Binnig G., Quate C.F., Gerber C. Atomic force microscope. Phys Rev Lett 1986, 56(9):930-933.
21. Braga P.C., Ricci D. Atomic force microscopy: biomedical methods and applications 2004, Humana Pr Inc.
22. Thurner P.J. Atomic force microscopy and indentation force measurement of bone. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2009, 1(6):624-649.
23. Lin D.C., Dimitriadis E.K., Horkay F. Robust strategies for automated AFM force curve analysis-I. Non-adhesive indentation of soft, inhomogeneous materials. J Biomech Eng 2007, 129:430-440.
24. Butt H.J., Cappella B., Kappl M. Force measurements with the atomic force microscope: technique, interpretation and applications. Surf Sci Rep 2005, 59(1-6):1-152.
25. Hameroff S.R., Simic Krstic J., Kelley M.F., Voelker M.A., He J.D., Dereniak E.L., et al. Scanning tunneling microscopy of biopolymers: conditions for microtubule stabilization. J Vac Sci Technol A Vac Surf Films 1989, 7(4):2890-2894.
26. Chernoff E.A.G., Chernoff D.A. Atomic force microscope images of collagen fibers. J Vac Sci Technol A Vac Surf Films 1992, 10(4):596-599.
27. Sasaki T., Debari K., Hasemi M. Measurement of Howship's resorption lacunae by a scanning probe microscope system. J Electron Microsc 1993, 42(5):356-359.
28. Debari K., Sasaki T., Udagawa N., Rifkin B. An ultrastructural evaluation of the effects of cysteine-proteinase inhibitors on osteoclastic resorptive functions. Calcif Tissue Int 1995, 56(6):566-570.
29. Hassenkam T., Jorgensen H.L., Lauritzen J.B. Mapping the imprint of bone remodeling by atomic force microscopy. Anat Rec A Discov Mol Cell Evol Biol 2006, 288(10):1087-1094.
30. Bozec L., Groot J., Odlyha M., Nicholls B., Nesbitt S., Flanagan A., et al. Atomic force microscopy of collagen structure in bone and dentine revealed by osteoclastic resorption. Ultramicroscopy 2005, 105(1-4):79-89.
31. Barragan-Adjemian C., Nicolella D., Dusevich V., Dallas M., Eick J., Bonewald L. Mechanism by which MLO-A5 late osteoblasts/early osteocytes mineralize in culture: similarities with mineralization of lamellar bone. Calcif Tissue Int 2006, 79(5):340-353.
32. Reilly G.C., Knapp H.F., Stemmer A., Niederer P., Knothe Tate M.L. Investigation of the morphology of the lacunocanalicular system of cortical bone using atomic force microscopy. Ann Biomed Eng 2001, 29(12):1074-1081.
33. Knapp H.F., Stemmer A., Reilly G.C., Niederer P., Tate M.L.K. Development of preparation methods for and insights obtained from atomic force microscopy of fluid spaces in cortical bone. Scanning 2002, 24(1):25-33.
34. Lin Y., Xu S. AFM analysis of the lacunar canalicular network in demineralized compact bone. J Microsc 2010, 241(3):291-302.
35. Eppell S.J., Tong W., Katz J.L., Kuhn L., Glimcher M.J. Shape and size of isolated bone mineralites measured using atomic force microscopy. J Orthop Res 2001, 19(6):1027-1034.
36. Tong W., Glimcher M., Katz J., Kuhn L., Eppell S. Size and shape of mineralites in young bovine bone measured by atomic force microscopy. Calcif Tissue Int 2003, 72(5):592-598.
37. Weiner S., Traub W. Bone structure: from angstroms to microns. FASEB J 1992, 6(3):879-885.
38. Kindt JH, Fantner GE, Thurner PJ, Schitter G, Hansma PK, editors. A new technique for imaging Mineralized Fibrils on Bovine Trabecular Bone Fracture Surfaces by Atomic Force Microscopy 2005: Warrendale, Pa.; Materials Research Society; 1999.
39. Sasaki N., Tagami A., Goto T., Taniguchi M., Nakata M., Hikichi K. Atomic force microscopic studies on the structure of bovine femoral cortical bone at the collagen fibril-mineral level. J Mater Sci Mater Med 2002, 13(3):333-337.
40. Mineralised tissues as nanomaterials: analysis by atomic force microscopy. IEEE Proceedings - Nanobiotechnology 2005, L. Bozec, J. de Groot, M. Odlyha, B. Nicholls, M.A. Horton (Eds.).
41. 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(3):227-236.
42. El Feninat F., Ellis T.H., Sacher E., Stangel I. Moisture-dependent renaturation of collagen in phosphoric acid etched human dentin. J Biomed Mater Res 1998, 42(4):549-553.
43. Ge J., Cui F.Z., Wang X., Wang Y. New evidence of surface mineralization of collagen fibrils in wild type zebrafish skeleton by AFM and TEM. Mater Sci Eng C 2007, 27(1):46-50.
44. Baranauskas V., Garavello-Freitas I., Jingguo Z., Cruz-Höfling M.A. Observation of the bone matrix structure of intact and regenerative zones of tibias by atomic force microscopy. J Vac Sci Technol A Vac Surf Films 2001, 19(4):1042-1045.
45. Baranauskas V., Garavello I., Jingguo Z., Cruz-Höfling M.A. Analyses of regenerative bone matrix of rat tibia after laser photo-excitation by SEM and AFM. Appl Surf Sci 2005, 248(1-4):492-498.
46. Thalhammer S., Heckl W.M., Zink A., Nerlich A.G. Atomic force microscopy for high resolution imaging of collagen fibrils-a new technique to investigate collagen structure in historic bone tissues. J Archaeol Sci 2001, 28(10):1061-1068.
47. Wallace J.M., Chen Q.S., Fang M., Erickson B., Orr B.G., Holl M.M.B. Type I collagen exists as a distribution of nanoscale morphologies in teeth, bones, and tendons. Langmuir 2010, 26(10):7349-7354.
48. Wallace J.M., Erickson B., Les C.M., Orr B.G., Holl M.M.B. Distribution of type I collagen morphologies in bone: relation to estrogen depletion. Bone 2010, 46(5):1349-1354.
49. 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 Biol 2011, 173:146-152.
50. Thompson J.B., Kindt J.H., Drake B., Hansma H.G., Morse D.E., Hansma P.K. Bone indentation recovery time correlates with bond reforming time. Nature 2001, 414(6865):773-776.
51. Fantner G.E., Hassenkam T., Kindt J.H., Weaver J.C., Birkedal H., Pechenik L., et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat Mater 2005, 4(8):612-616.
52. Hansma P.K., Fantner G.E., Kindt J.H., Thurner P.J., Schitter G., Turner P.J., et al. Sacrificial bonds in the interfibrillar matrix of bone. J Musculoskelet Neuronal Interact 2005, 5(4):313-315.
53. Fantner G.E., Adams J., Turner P., Thurner P.J., Fisher L.W., Hansma P.K. Nanoscale ion mediated networks in bone: osteopontin can repeatedly dissipate large amounts of energy. Nano Lett 2007, 7(8):2491-2498.
54. Fantner G.E., Birkedal H., Kindt J.H., Hassenkam T., Weaver J.C., Cutroni J.A., et al. Influence of the degradation of the organic matrix on the microscopic fracture behavior of trabecular bone. Bone 2004, 35(5):1013-1022.
55. Hassenkam T., Fantner G.E., Cutroni J.A., Weaver J.C., Morse D.E., Hansma P.K. High-resolution AFM imaging of intact and fractured trabecular bone. Bone 2004, 35(1):4-10.
56. Fantner G.E., Rabinovych O., Schitter G., Thurner P., Kindt J.H., Finch M.M., et al. Hierarchical interconnections in the nano-composite material bone: fibrillar cross-links resist fracture on several length scales. Compos Sci Technol 2006, 66(9):1205-1211.
57. Kindt J.H., Thurner P.J., Lauer M.E., Bosma B.L., Schitter G., Fantner G.E., et al. In situ observation of fluoride-ion-induced hydroxyapatite-collagen detachment on bone fracture surfaces by atomic force microscopy. Nanotechnology 2007, 18(135012):1-8.
58. Thurner P.J., Oroudjev E., Jungmann R., Kreutz C., Kindt J.H., Schitter G., et al. Imaging of bone ultrastructure using atomic force microscopy. Modern Research and Educational Topics in Microscopy 2007, 37-48. (Journal Article).
59. Grant C.A., Brockwell D.J., Radford S.E., Thomson N.H. Effects of hydration on the mechanical response of individual collagen fibrils. Appl Phys Lett 2008, 92(233902):1-3.
60. Tai K., Dao M., Suresh S., Palazoglu A., Ortiz C. Nanoscale heterogeneity promotes energy dissipation in bone. Nat Mater 2007, 6(6):454-462.
61. Cueru L., sfarghiu A.T., Bala Y., Depalle B., Berthier Y., Follet H. Mechanical and physicochemical multiscale analysis of cortical bone. Comput Methods Biomech Biomed Engin 2011, 14(sup1):223-225.
62. Minary-Jolandan M., Yu M.F. Uncovering nanoscale electromechanical heterogeneity in the subfibrillar structure of collagen fibrils responsible for the piezoelectricity of bone. ACS Nano 2009, 3(7):1859-1863.
63. Halperin C., Mutchnik S., Agronin A., Molotskii M., Urenski P., Salai M., et al. Piezoelectric effect in human bones studied in nanometer scale. Nano Lett 2004, 4(7):1253-1256.
64. Kelly G.M., Kilpatrick J.I., van Es M.H., Weafer P.P., Prendergast P.J., Jarvis S.P. Bone cell elasticity and morphology changes during the cell cycle. J Biomech 2011, 44(8):1484-1490.