Biominerals-hierarchical nanocomposites: The example of bone

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 3, Issue 1, 2011, Pages 47-69

  Beniash, Elia ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMBIENT CONDITIONS; BASIC PRINCIPLES; BIO-INSPIRED; BIOMINERALS; BONE TISSUE; FUNCTIONAL PROPERTIES; HIERARCHICAL LEVEL; INORGANIC PHASIS; INORGANIC SOLIDS; MACRO SCALE; MATERIAL DESIGNS; MINERALIZED TISSUE; MOLECULAR LEVELS; STRUCTURAL ORGANIZATION;

BIOMECHANICS; BONE; HISTOLOGY; NANOCOMPOSITES; PHASE INTERFACES;

MECHANICAL PROPERTIES;

ACID PROTEIN; COLLAGEN FIBRIL; INORGANIC COMPOUND; NANOCOMPOSITE; ORGANIC COMPOUND;

BIOMINERALIZATION; BONE MINERAL; BONE STRUCTURE; BONE TISSUE; CHEMICAL STRUCTURE; CRYSTALLIZATION; ENVIRONMENTAL TEMPERATURE; HUMAN; OSSIFICATION; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN STRUCTURE; REVIEW;

BIOCOMPATIBLE MATERIALS; BIOMECHANICS; BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; HUMANS; MINERALS; NANOCOMPOSITES;

EID: 78650632819     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.105     Document Type: Review

References (208)

1. Aizenberg J, Weaver JC, Thanawala MS, Sundar VC, Morse DE. Science 2005, 309:275-278.
2. Fratzl P, Gupta HS, Paschalis EP, Roschger P. J Mater Chem 2004, 14:2115-2123.
3. Fratzl P, Weinkamer R. Prog Mater Sci 2007, 52:1263-1334.
4. Weiner S, Wagner HD. Ann Rev Mater Sci 1998, 28:271-298.
5. Margolis HC, Beniash E, Fowler CE. J Dent Res 2006, 85:775-793.
6. Gilbert P, Abrecht M, Frazer BH. The organic-mineral interface in biominerals. Molecular Geomicrobiology. Vol. 59. Chantilly, VA: Mineralogical Soc America; 2005, 157-185.
7. Dove PM. Elements 2010, 6:37-42.
8. Weiner S, Dove PM. An overview of biomineralization processes and the problem of the vital effect. In: Dove PM, DeYoreo JJ, Weiner S, eds. Biomineralization. Vol. 54. Washington, DC: Mineralogical Society of America; 2003, 1-29.
9. Lowenstam HA. Science 1981, 211:1126-1131.
10. Weiner S, Addadi L. J Mater Chem 1997, 7:689-702.
11. Aizenberg J, Weiner S, Addadi L. Connect Tissue Res 2003, 44:20-25.
12. Belcher AM, Wu XH, Christensen RJ, Hansma PK, Stucky GD, Morse DE. Nature 1996, 381:56-58.
13. Falini G, Albeck S, Weiner S, Addadi L. Science 1996, 271:67-69.
14. Kwak SY, Wiedemann-Bidlack FB, Beniash E, Yamakoshi Y, Simmer JP, Litman A, Margolis HC. J Biol Chem 2009, 284:18972-18979.
15. Albeck S, Addadi L, Weiner S. Connect Tissue Res 1996, 35:365-370.
16. Moradian-Oldak J, Tan J, Fincham AG. Biopolymers 1998, 46:225-238.
17. Beniash E, Simmer JP, Margolis HC. J Struct Biol 2005, 149:182-190.
18. Fantner GE, Hassenkam T, Kindt JH, Weaver JC, Birkedal H, Pechenik L, Cutroni JA, Cidade GAG, Stucky GD, Morse DE. Nat Mater 2005, 4:612-616.
19. Bajaj D, Arola DD. Biomaterials 2009, 30:4037-4046.
20. Baldassarri M, Margolis HC, Beniash E. J Dent Res 2008, 87:645-649.
21. He G, Dahl T, Veis A, George A. Nat Mater 2003, 2:552-558.
22. Weiner S, Addadi L. Trends Biochem Sci 1991, 16:252-256.
23. Colfen H, Mann S. Angew Chem Int Ed Engl 2003, 42:2350-2365.
24. Beniash E, Aizenberg J, Addadi L, Weiner S. Proc R Soc Lond Ser B 1997, 264:461-465.
25. Beniash E, Metzler RA, Lam RSK, Gilbert P. J Struct Biol 2009, 166:133-143.
26. Mahamid J, Sharir A, Addadi L, Weiner S. Proc Natl Acad Sci U S A 2008, 105:12748-12753.
27. Weiner S. J Struct Biol 2008, 163:229-234.
28. Weiner S, Sagi I, Addadi L. Science 2005, 309:1027-1028.
29. Antonietti M, Breulmann M, Goltner CG, Colfen H, Wong KKW, Walsh D, Mann S. Chem Eur J 1998, 4:2493-2500.
30. Green D, Walsh D, Mann S, Oreffo ROC. Bone 2002, 30:810-815.
31. Hartgerink JD, Beniash E, Stupp SI. Science 2001, 294:1684-1688.
32. Heuer AH, Fink DJ, Laraia VJ, Arias JL, Calvert PD, Kendall K, Messing GL, Blackwell J, Rieke PC, Thompson DH. Science 1992, 255:1098-1105.
33. Mann S, Ozin GA. Nature 1996, 382:313-318.
34. Huo QS, Margolese DI, Ciesla U, Feng PY, Gier TE, Sieger P, Leon R, Petroff PM, Schuth F, Stucky GD. Nature 1994, 368:317-321.
35. Palmer LC, Newcomb CJ, Kaltz SR, Spoerke ED, Stupp SI. Chem Rev 2008, 108:4754-4783.
36. Espinosa HD, Rim JE, Barthelat F, Buehler MJ. Prog Mater Sci 2009, 54:1059-1100.
37. Liao SS, Cui FZ, Zhang W, Feng QL. J Biomed Mater Res B Appl Biomater 2004, 69B:158-165.
38. Tan J, Saltzman WM. Biomaterials 2004, 25:3593-3601.
39. Veis A. Rev Mineral Geochem 2003, 54:249-289.
40. Fratzl P. Nat Mater 2008, 7:610-612.
41. Prockop DJ, Fertala A. J Struct Biol 1998, 122:111-118.
42. Brodsky B, Ramshaw JAM. Matrix Biol 1997, 15:545-554.
43. Brodsky B, Shah NK. FASEB J 1995, 9:1537-1546.
44. Kadler KE, Holmes DF, Trotter JA, Chapman JA. Biochem J 1996, 316:1-11.
45. Kuznetsova N, Leikin S. J Biol Chem 1999, 274:36083-36088.
46. Hulmes DJS. J Struct Biol 2002, 137:2-10.
47. Chapman JA. Connect Tissue Res 1974, 2:137-150.
48. Ou-Yang H, Paschalis EP, Mayo WE, Boskey AL, Mendelsohn R. J Bone Miner Res 2001, 16:893-900.
49. Landis WJ, Hodgens KJ, Arena J, Song MJ, McEwen BF. Microsc Res Tech 1996, 33:192-202.
50. Ziv V, Weiner S. Connect Tissue Res 1994, 30:165-175.
51. Grabner B, Landis WJ, Roschger P, Rinnerthaler S, Peterlik H, Klaushofer K, Fratzl P. Bone 2001, 29:453-457.
52. Tesch W, Eidelman N, Roschger P, Goldenberg F, Klaushofer K, Fratzl P. Calcif Tissue Int 2001, 69:147-157.
53. Camacho NP, Rinnerthaler S, Paschalis EP, Mendelsohn R, Boskey AL, Fratzl P. Bone 1999, 25:287-293.
54. Huang S-J, Tsai Y-L, Lee Y-L, Lin C-P, Chan JCC. Chem Mater 2009, 21:2583-2585.
55. Christian J, Thea W, Wolfgang M-Z, Matthias E. Magn Reson Chem 2006, 44:573-580.
56. Cazalbou S, Combes C, Eichert D, Rey C, Glimcher MJ. J Bone Miner Metab 2004, 22:310-317.
57. Tang R, Wang L, Orme CA, Bonstein T, Bush PJ, Nancollas GH. Angew Chem Int Ed Engl 2004, 43:2697-2701.
58. Wang L, Nancollas GH, Henneman ZJ, Klein E, Weiner S. Biointerphases 2006, 1:106-111.
59. Traub W, Arad T, Weiner S. Proc Natl Acad Sci U S A 1989, 86:9822-9826.
60. Weiner S, Traub W. FASEB J 1992, 6:879-885.
61. Su X, Sun K, Cui FZ, Landis WJ. Bone 2003, 32:150-162.
62. Landis WJ, Silver FH. Cells Tissues Organs 2009, 189:20-24.
63. Sang-Hoon R, Jae Do L, Junzo T. J Am Ceram Soc 2000, 83:2890-2892.
64. Elangovan S, Margolis HC, Oppenheim FG, Beniash E. Langmuir 2007, 23:11200-11205.
65. Johnston N, Krimm S. Biopolymers 1971, 10:2597-2605.
66. Olszta MJ, Cheng X, Jee SS, Kumar R, Kim Y-Y, Kaufman MJ, Douglas EP, Gower LB. Mater Sci Eng R Rep 2007, 58:77-116.
67. Bonar LC, Lees S, Mook HA. J Mol Biol 1985, 181:265-270.
68. Landis WJ, Hodgens KJ, Song MJ, Arena J, Kiyonaga S, Marko M, Owen C, McEwen BF. J Struct Biol 1996, 117:24-35.
69. Prostak KS, Lees S. Calcif Tissue Int 1996, 59:474-479.
70. Lees S, Prostak KS, Ingle VK, Kjoller K. Calcif Tissue Int 1994, 55:180-189.
71. Kinney JH, Pople JA, Driessen CH, Breunig TM, Marshall GW, Marshall SJ. J Dent Res 2001, 80:1555-1559.
72. Tong W, Glimcher MJ, Katz JL, Kuhn L, Eppell SJ. Calcif Tissue Int 2003, 72:592-598.
73. Su XW, Feng QL, Cui FZ, Zhu XD. Connect Tissue Res 1997, 36:271-286.
74. Berglundh T, Abrahamsson I, Lang NP, Lindhe J. Clin Oral Implants Res 2003, 14:251-262.
75. Lacroix D, Prendergast PJ. J Biomech 2002, 35:1163-1171.
76. Ziv V, Wagner HD, Weiner S. Bone 1996, 18:417-428.
77. Landis WJ, Silver FH. Comp Biochem Physiol A Mol Integr Physiol 2002, 133:1135-1157.
78. Weiner S, Traub W, Wagner HD. J Struct Biol 1999, 126:241-255.
79. Yamamoto T, Domon T, Takahashi S, Islam N, Suzuki R. Anat Embryol (Berl) 2000, 202:25-30.
80. Weiner S, Arad T, Sabanay I, Traub W. Bone 1997, 20:509-514.
81. Qin C, Baba O, Butler WT. Crit Rev Oral Biol Med 2004, 15:126-136.
82. Mackie EJ. Int J Biochem Cell Biol 2003, 35:1301-1305.
83. Nanci A. Ten Cate's Oral Histology: Development, Structure, and Function. 7th ed. St. Luis: Mosby: 2008, 411.
84. Dimuzio MT, Veis A. J Biol Chem 1978, 253:6845-6852.
85. Beniash E, Traub W, Veis A, Weiner S. J Struct Biol 2000, 132:212-225.
86. Goldberg M, Rapoport O, Septier D, Palmier K, Hall R, Embery G, Young M, Ameye L. Connect Tissue Res 2003, 44:184-188.
87. Septier D, Hall RC, Lloyd D, Embery G, Goldberg M. Histochem J 1998, 30:275-284.
88. Weinstock M, Leblond CP. J Cell Biol 1974, 60:92-127.
89. Ameye L, Aria D, Jepsen K, Oldberg AKE, Xu T, Young MF. FASEB J 2002, 16:673-680.
90. Ameye L, Young MF. Glycobiology 2002, 12:107R-116R.
91. Embery G, Hall R, Waddington R, Septier D, Goldberg M. Crit Rev Oral Biol Med 2001, 12:331-349.
92. Haruyama N, Sreenath TL, Suzuki S, Yao X, Wang Z, Wang Y, Honeycutt C, Iozzo RV, Young MF, Kulkarni AB. Matrix Biol 2009, 28:129-136.
93. Keene DR, San Antonio JD, Mayne R, McQuillan DJ, Sarris G, Santoro S, Iozzo RV. J Biol Chem 2000, 275:21801-21804.
94. Neame PJ, Kay CJ, McQuillan DJ, Beales MP, Hassell JR. Cell Mol Life Sci 2000, 57:859-863.
95. Weber IT, Harrison RW, Iozzo RV. J Biol Chem 1996, 271:31767-31770.
96. Milan AM, Sugars RV, Embery G, Waddington RJ. Calcif Tissue Int 2005, 76:127-135.
97. Plate U, Hohling HJ, Reimer L, Barckhaus RH, Wienecke R, Wiesmann HP, Boyde A. J Microsc 1992, 166:329-341.
98. Dallas SL, Veno PA, Rosser JL, Barragan-Adjemian C, Rowe DW, Kalajzic I, Bonewald LF. Cells Tissues Organs 2009, 189:6-11.
99. Irie K, Ejiri S, Sakakura Y, Shibui T, Yajima T. J Histochem Cytochem 2008, 56:561-567.
100. Mahamid J, Aichmayer B, Shimoni E, Ziblat R, Li C, Siegel S, Paris O, Fratzl P, Weiner S, Addadi L. Proc Natl Acad Sci U S A 2010, 107:6316-6321.
101. Landis WJ, Glimcher MJ. J Ultrastruct Res 1982, 78:227-268.
102. Wu LNY, Genge BR, Dunkelberger DG, LeGeros RZ, Concannon B, Wuthier RE. J Biol Chem 1997, 272:4404-4411.
103. Saito T, Arsenault AL, Yamauchi M, Kuboki Y, Crenshaw MA. Bone 1997, 21:305-311.
104. Hunter GK, Poitras MS, Underhill TM, Grynpas MD, Goldberg HA. J Biomed Mater Res 2001, 55:496-502.
105. Deshpande AS, Beniash E. Cryst Growth Des 2008, 8:3084-3090.
106. Boskey AL. J Cell Biochem 1998, 72:83-91.
107. Gorski J. Calcif Tissue Int 1992, 50:391-396.
108. Fisher LW, Torchia DA, Fohr B, Young MF, Fedarko NS. Biochem Biophys Res Commun 2001, 280:460-465.
109. George A, Sabsay B, Simonian PA, Veis A. J Biol Chem 1993, 268:12624-12630.
110. Stetler-Stevenson WG, Veis A. Biochemistry 1983, 22:4326-4335.
111. George A, Veis A. Chem Rev 2008, 108:4670-4693.
112. Gotliv B-A, Kessler N, Sumerel JL, Morse DE, Tuross N, Addadi L, Weiner S. Chembiochem 2005, 6:304-314.
113. Stetler-Stevenson W, Veis A. Calcif Tissue Int 1987, 40:97-102.
114. Goldberg HA, Warner KJ, Li MC, Hunter GK. Connect Tissue Res 2001, 42:25-37.
115. Hunter GK, Hauschka PV, Poole AR, Rosenberg LC, Goldberg HA. Biochem J 1996, 317:59-64.
116. Atkinson RA, Evans JS, Hauschka PV, Levine BA, Meats R, Triffitt JT, Virdi AS, Williams RJP. Eur J Biochem 1995, 232:515-521.
117. Evans JS, Chan SI. Biopolymers 1994, 34:507-527.
118. Evans JS. Curr Opin Colloid Interface Sci 2003, 8:48-54.
119. Delak K, Collino S, Evans JS. Biochemistry 2009, 48:3669-3677.
120. Delak K, Harcup C, Lakshminarayanan R, Sun Z, Fan YW, Moradian-Oldak J, Evans JS. Biochemistry 2009, 48:2272-2281.
121. He G, Gajjeraman S, Schultz D, Cookson D, Qin CL, Butler WT, Hao JJ, George A. Biochemistry 2005, 44:16140-16148.
122. Li JH, Olton D, Lee D, Kumta PN, Sfeir C. Cells Tissues Organs 2009, 189:252-255.
123. Aggeli A, Nyrkova IA, Bell M, Harding R, Carrick L, McLeish TCB, Semenov AN, Boden N. Proc Natl Acad Sci U S A 2001, 98:11857-11862.
124. Nelson R, Sawaya MR, Balbirnie M, Madsen AO, Riekel C, Grothe R, Eisenberg D. Nature 2005, 435:773-778.
125. Serpell LC. Biochim Biophys Acta 2000, 1502:16-30.
126. Beniash E, Hartgerink JD, Storrie H, Stendahl JC, Stupp SI. Acta Biomaterialia 2005, 1:387-397.
127. Adams J, Fantner GE, Fisher LW, Hansma PK. Nanotechnology 2008, 19:384008-340015.
128. Fujisawa R, Kuboki Y. Calcif Tissue Int 1992, 51:438-442.
129. Stetler-Stevenson W, Veis A. Calcif Tissue Int 1986, 38:135-141.
130. Di Lullo GA, Sweeney SM, Korkko J, Ala-Kokko L, San Antonio JD. J Biol Chem 2002, 277:4223-4231.
131. He G, George A. J Biol Chem 2004, 279:11649-11656.
132. Dahl T, Sabsay B, Veis A. J Struct Biol 1998, 123:162-168.
133. Tye CE, Hunter GK, Goldberg HA. J Biol Chem 2005, 280:13487-13492.
134. Silverman L, Boskey AL. Calcif Tissue Int 2004, 75:494-501.
135. Wang L, Nancollas GH. Chem Rev 2008, 108:4628-4669.
136. He G, Ramachandran A, Dahl T, George S, Schultz D, Cookson D, Veis A, George A. J Biol Chem 2005, 280:33109-33114.
137. Burke EM, Guo Y, Colon L, Rahima M, Veis A, Nancollas GH. Colloids Surf B Biointerfaces 2000, 17:49-57.
138. Grohe B, O'Young J, Ionescu DA, Lajoie G, Rogers KA, Karttunen M, Goldberg HA, Hunter GK. J Am Chem Soc 2007, 129:14946-14951.
139. Chien YC, Masica DL, Gray JJ, Nguyen S, Vali H, McKee MD. J Biol Chem 2009, 284:23491-23501.
140. Heywood BR, Mann S. Adv Mater 1994, 6:9-20.
141. Aizenberg J, Black AJ, Whitesides GM. Nature 1999, 398:495-498.
142. Boskey AL, Maresca M, Ullrich W, Doty SB, Butler WT, Prince CW. Bone Miner 1993, 22:147-159.
143. Tartaix PH, Doulaverakis M, George A, Fisher LW, Butler WT, Qin C, Salih E, Tan M, Fujimoto Y, Spevak L, et al. J Biol Chem 2004, 279:18115-18120.
144. Tsuji T, Onuma K, Yamamoto A, Iijima M, Shiba K. Proc Natl Acad Sci U S A 2008, 105:16866-16870.
145. Aizenberg J, Lambert G, Addadi L, Weiner S. Adv Mater 1996, 8:222-226.
146. Crane NJ, Popescu V, Morris MD, Steenhuis P, Ignelzi MA. Bone 2006, 39:434-442.
147. Cross K, Huq N, O'Brien-Simpson N, Perich J, Attard T, Reynolds E. Int J Pept Res Ther 2007, 13:479-495.
148. Cross KJ, Huq NL, Palamara JE, Perich JW, Reynolds EC. J Biol Chem 2005, 280:15362-15369.
149. Shechter A, Glazer L, Cheled S, Mor E, Weil S, Berman A, Bentov S, Aflalo ED, Khalaila I, Sagi A. Proc Natl Acad Sci U S A 2008, 105:7129-7134.
150. Aizenberg J, Lambert G, Weiner S, Addadi L. J Am Chem Soc 2002, 124:32-39.
151. Bradt J-H, Mertig M, Teresiak A, Pompe W. Chem Mater 1999, 11:2694-2701.
152. Ling YF, Rios HF, Myers ER, Lu YB, Feng JQ, Boskey AL. J Bone Miner Res 2005, 20:2169-2177.
153. Ducy P, Desbois C, Boyce B, Pinero G, Story B, Dunstan C, Smith E, Bonadio J, Goldstein S, Gundberg C, et al. Nature 1996, 382:448-452.
154. Boskey AL, Gadaleta S, Gundberg C, Doty SB, Ducy P, Karsenty G. Bone 1998, 23:187-196.
155. Boskey AL, Young MF, Kilts T, Verdelis K. Cells Tissues Organs 2005, 181:144-153.
156. Boskey AL, Moore DJ, Amling M, Canalis E, Delany AM. J Bone Miner Res 2003, 18:1005-1011.
157. Boskey AL, Spevak L, Paschalis E, Doty SB, McKee MD. Calcif Tissue Int 2002, 71:145-154.
158. Lu YB, Ye L, Yu SB, Zhang SB, Xie YX, McKee MD, Li YC, Kong J, Eick JD, Dallas SL, et al. Dev Biol 2007, 303:191-201.
159. Suzuki S, Sreenath T, Haruyama N, Honeycutt C, Terse A, Cho A, Kohler T, Müller R, Goldberg M, Kulkarni AB. Matrix Biol 2009, 28:221-229.
160. Sreenath T, Thyagarajan T, Hall B, Longenecker G, D'Souza R, Hong S, Wright JT, MacDougall M, Sauk J, Kulkarni AB. J Biol Chem 2003, 278:24874-24880.
161. Malaval L, Wade-Gueye NM, Boudiffa M, Fei J, Zirngibl R, Chen F, Laroche N, Roux J-P, Burt-Pichat B, Duboeuf F. J Exp Med 2008, 205:1145-1153.
162. Feng JQ, Ward LM, Liu SG, Lu YB, Xie YX, Yuan BZ, Yu XJ, Rauch F, Davis SI, Zhang SB, et al. Nat Genet 2006, 38:1310-1315.
163. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY. Cell 2007, 130:456-469.
164. Zhang W, Liao SS, Cui FZ. Chem Mater 2003, 15:3221-3226.
165. Fratzl P, Paris O, Klaushofer K, Landis WJ. J Clin Invest 1996, 97:396-402.
166. Landis WJ. Bone 1995, 16:533-544.
167. Traub W, Arad T, Vetter U, Weiner S. Matrix Biol 1994, 14:337-345.
168. Bella J, Eaton M, Brodsky B, Berman HM. Science 1994, 266:75-81.
169. McBride DJ, Choe V, Shapiro JR, Brodsky B. J Mol Biol 1997, 270:275-284.
170. Arnold S, Plate U, Wiesmann HP, Stratmann U, Kohl H, Höhling H. J Microsc 1999, 195:58-63.
171. Plate U, Arnold S, Reimer L, Hohling HJ, Boyde A. Cell Tissue Res 1994, 278:543-547.
172. Toroian D, Lim JE, Price PA. J Biol Chem 2007, 282:22437-22447.
173. Gower LB. Chem Rev 2008, 108:4551-4627.
174. Landis WJ, Song MJ, Leith A, McEwen L, McEwen BF. J Struct Biol 1993, 110:39-54.
175. Ofir PBY, Govrin-Lippman R, Garti N, Furedi-Milhofer H. Cryst Growth Des 2004, 4:177-183.
176. Price PA, Toroian D, Lim JE. J Biol Chem 2009, 284:17092-17101.
177. Ji B, Gao H. J Mech Phys Solids 2004, 52:1963-1990.
178. Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2006, 436.
179. Du C, Cui FZ, Zhang W, Feng QL, Zhu XD, Groot KD. J Biomed Mater Res 2000, 50:518-527.
180. Kavukcuoglu NB, Patterson-Buckendahl P, Mann AB. J Mech Behav Biomed Mater 2009, 2:348-354.
181. Akkus O, Adar F, Schaffler MB. Bone 2004, 34:443-453.
182. Gao H, Ji B, JÃger IL, Arzt E, Fratzl P. Proc Natl Acad Sci U S A 2003, 100:5597-5600.
183. Wopenka B, Pasteris JD. Mater Sci Eng C 2005, 25:131-143.
184. Almer JD, Stock SR. J Struct Biol 2007, 157:365-370.
185. White SN, Luo W, Paine ML, Fong H, Sarikaya M, Snead ML. J Dent Res 2001, 80:321-326.
186. Ruys AJ, Wei M, Sorrell CC, Dickson MR, Brandwood A, Milthorpe BK. Biomaterials 1995, 16:409-415.
187. Giri B, Tadano S, Fujisaki K, Sasaki N. Bone 2009, 44:1111-1120.
188. Currey JD, Foreman J, Laketi I, Mitchell J, Pegg DE, Reilly GC. J Orthop Res 1997, 15:111-117.
189. Currey JD. Osteoporos Int 2003, 14:29-36.
190. Fratzl P, Misof K, Zizak I, Rapp G, Amenitsch H, Bernstorff S. J Struct Biol 1998, 122:119-122.
191. Puxkandl R, Zizak I, Paris O, Keckes J, Tesch W, Bernstorff S, Purslow P, Fratzl P. Philos Trans R Soc Lond B Biol Sci 2002, 357:191-197.
192. McCutchen CW. J Theor Biol 1975, 51:51-58.
193. Maciel KT, Carvalho RM, Ringle RD, Preston CD, Russell CM, Pashley DH. J Dent Res 1996, 75:1851-1858.
194. Lees S, Tao NJ, Lindsay SM. Connect Tissue Res 1990, 24:187-205.
195. Jäger I, Fratzl P. Biophys J 2000, 79:1737-1746.
196. Gupta HS, Seto J, Wagermaier W, Zaslansky P, Boesecke P, Fratzl P. Proc Natl Acad Sci U S A 2006, 103:17741-17746.
197. Gao H. Int J Fracture 2006, 138:101-137.
198. Gupta HS, Wagermaier W, Zickler GA, Raz-Ben Aroush D, Funari SS, Roschger P, Wagner HD, Fratzl P. Nano Lett 2005, 5:2108-2111.
199. Thompson JB, Kindt JH, Drake B, Hansma HG, Morse DE, Hansma PK. Nature 2001, 414:773-776.
200. Fantner GE, Adams J, Turner P, Thurner PJ, Fisher LW, Hansma PK. Nano Lett 2007, 7:2491-2498.
201. Peterlik H, Roschger P, Klaushofer K, Fratzl P. Nat Mater 2006, 5:52-55.
202. Liu D, Wagner HD, Weiner S. J Mater Sci Mater Med 2000, 11:49-60.
203. Ebacher V, Wang R. Adv Funct Mater 2009, 19:57-66.
204. Kamat S, Su X, Ballarini R, Heuer AH. Nature 2000, 405:1036-1040.
205. Politi Y, Arad T, Klein E, Weiner S, Addadi L. Science 2004, 306:1161-1164.
206. Weiss IM, Tuross N, Addadi L, Weiner S. J Exp Zool 2002, 293:478-491.
207. Killian CE, Wilt FH. J Biol Chem 1996, 271:9150-9159.
208. Aizenberg J, Fratzl P. Adv Mater 2009, 21:387-388.