title: Biominerals--hierarchical nanocomposites: the example of bone.
abstract: Many organisms incorporate inorganic solids in their tissues to enhance their functional, primarily mechanical, properties. These mineralized tissues, also called biominerals, are unique organo-mineral nanocomposites, organized at several hierarchical levels, from nano- to macroscale. Unlike man-made composite materials, which often are simple physical blends of their components, the organic and inorganic phases in biominerals interface at the molecular level. Although these tissues are made of relatively weak components under ambient conditions, their hierarchical structural organization and intimate interactions between different elements lead to superior mechanical properties. Understanding basic principles of formation, structure, and functional properties of these tissues might lead to novel bioinspired strategies for material design and better treatments for diseases of the mineralized tissues. This review focuses on general principles of structural organization, formation, and functional properties of biominerals on the example the bone tissues.
authors.affiliation: Department of Oral Biology, University of Pittsburgh, Pittsburgh, PA, USA. ebeniash@pitt.edu
authors.forename: Elia
authors.initials: E
authors.lastname: Beniash
mesh_terms: D001672:Biocompatible Materials / Q000737:chemistry / Q000494:pharmacology*; D001696:Biomechanical Phenomena / Q000187:drug effects; D001842:Bone and Bones / Q000187:drug effects*; D002113:Calcification, Physiologic / Q000187:drug effects; D006801:Humans; D008903:Minerals / Q000737:chemistry / Q000494:pharmacology*; D053761:Nanocomposites / Q000737:chemistry* / Q000648:ultrastructure
chemical_list: D001672:Biocompatible Materials; D008903:Minerals
references.citation: J Biomech. 2002 Sep;35(9):1163-71
references.pmid: 12163306
references.citation: Bone. 1995 May;16(5):533-44
references.pmid: 7654469
references.citation: Cell Tissue Res. 1994 Dec;278(3):543-7
references.pmid: 7850864
references.citation: Chembiochem. 2005 Feb;6(2):304-14
references.pmid: 15678422
references.citation: J Struct Biol. 1998 Oct;123(2):162-8
references.pmid: 9843670
references.citation: Matrix Biol. 2009 May;28(4):221-9
references.pmid: 19348940
references.citation: Cells Tissues Organs. 2009;189(1-4):252-5
references.pmid: 18815439
references.citation: J Dent Res. 2001 Jun;80(6):1555-9
references.pmid: 11499512
references.citation: Nat Mater. 2006 Jan;5(1):52-5
references.pmid: 16341218
references.citation: Matrix Biol. 1997 Mar;15(8-9):545-54
references.pmid: 9138287
references.citation: Cryst Growth Des. 2008 Aug;8(8):3084-3090
references.pmid: 19662103
references.citation: J Biol Chem. 1996 Apr 12;271(15):9150-9
references.pmid: 8621567
references.citation: Calcif Tissue Int. 2004 Dec;75(6):494-501
references.pmid: 15455184
references.citation: Dev Biol. 2007 Mar 1;303(1):191-201
references.pmid: 17196192
references.citation: FASEB J. 2002 May;16(7):673-80
references.pmid: 11978731
references.citation: Nanotechnology. 2008 Sep 24;19(38):384008
references.pmid: 18843380
references.citation: J Microsc. 1992 Jun;166(Pt 3):329-41
references.pmid: 1322995
references.citation: Bone Miner. 1993 Aug;22(2):147-59
references.pmid: 8251766
references.citation: Biopolymers. 1971;10(12):2597-605
references.pmid: 5126529
references.citation: Bone. 2004 Mar;34(3):443-53
references.pmid: 15003792
references.citation: Nat Genet. 2006 Nov;38(11):1310-5
references.pmid: 17033621
references.citation: Calcif Tissue Int. 1996 Dec;59(6):474-9
references.pmid: 8939774
references.citation: Biomaterials. 2009 Aug;30(23-24):4037-46
references.pmid: 19427691
references.citation: Proc Natl Acad Sci U S A. 2010 Apr 6;107(14):6316-21
references.pmid: 20308589
references.citation: J Microsc. 1999 Jul;195(Pt 1):58-63
references.pmid: 10444302
references.citation: Calcif Tissue Int. 1992 May;50(5):391-6
references.pmid: 1596774
references.citation: J Biol Chem. 2005 Apr 15;280(15):15362-9
references.pmid: 15657053
references.citation: Bone. 1999 Sep;25(3):287-93
references.pmid: 10495132
references.citation: J Biol Chem. 1993 Jun 15;268(17):12624-30
references.pmid: 8509401
references.citation: Biochem Biophys Res Commun. 2001 Jan 19;280(2):460-5
references.pmid: 11162539
references.citation: J Biol Chem. 2003 Jul 4;278(27):24874-80
references.pmid: 12721295
references.citation: Nano Lett. 2005 Oct;5(10):2108-11
references.pmid: 16218747
references.citation: J Struct Biol. 2002 Jan-Feb;137(1-2):2-10
references.pmid: 12064927
references.citation: Bone. 1997 Jun;20(6):509-14
references.pmid: 9177863
references.citation: Connect Tissue Res. 2003;44 Suppl 1:184-8
references.pmid: 12952195
references.citation: J Dent Res. 2001 Jan;80(1):321-6
references.pmid: 11269723
references.citation: J Am Chem Soc. 2002 Jan 9;124(1):32-9
references.pmid: 11772059
references.citation: J Struct Biol. 2009 May;166(2):133-43
references.pmid: 19217943
references.citation: J Struct Biol. 1999 Jun 30;126(3):241-55
references.pmid: 10475685
references.citation: J Cell Biochem. 1998;72 Suppl 30-31(S30-31):83-91
references.pmid: 29345818
references.citation: Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):17741-6
references.pmid: 17095608
references.citation: J Biol Chem. 1999 Dec 17;274(51):36083-8
references.pmid: 10593890
references.citation: J Biol Chem. 2004 Mar 19;279(12):11649-56
references.pmid: 14699165
references.citation: Science. 1992 Feb 28;255(5048):1098-105
references.pmid: 1546311
references.citation: J Biol Chem. 2000 Jul 21;275(29):21801-4
references.pmid: 10823816
references.citation: Comp Biochem Physiol A Mol Integr Physiol. 2002 Dec;133(4):1135-57
references.pmid: 12485697
references.citation: Connect Tissue Res. 1996;35(1-4):365-70
references.pmid: 9084676
references.citation: Int J Biochem Cell Biol. 2003 Sep;35(9):1301-5
references.pmid: 12798343
references.citation: Proc Natl Acad Sci U S A. 1989 Dec;86(24):9822-6
references.pmid: 2602376
references.citation: Nat Mater. 2005 Aug;4(8):612-6
references.pmid: 16025123
references.citation: J Mech Behav Biomed Mater. 2009 Aug;2(4):348-54
references.pmid: 19627841
references.citation: Bone. 1997 Oct;21(4):305-11
references.pmid: 9315333
references.citation: Nano Lett. 2007 Aug;7(8):2491-8
references.pmid: 17645366
references.citation: Langmuir. 2007 Oct 23;23(22):11200-5
references.pmid: 17880251
references.citation: Clin Oral Implants Res. 2003 Jun;14(3):251-62
references.pmid: 12755774
references.citation: Bone. 2009 Jun;44(6):1111-20
references.pmid: 19437610
references.citation: Cell. 2007 Aug 10;130(3):456-69
references.pmid: 17693256
references.citation: J Mol Biol. 1985 Jan 20;181(2):265-70
references.pmid: 3981637
references.citation: J Mol Biol. 1997 Jul 11;270(2):275-84
references.pmid: 9236128
references.citation: Crit Rev Oral Biol Med. 2004 Jun 04;15(3):126-36
references.pmid: 15187031
references.citation: Nature. 1996 Aug 1;382(6590):448-52
references.pmid: 8684484
references.citation: Calcif Tissue Int. 1992 Dec;51(6):438-42
references.pmid: 1451011
references.citation: J Struct Biol. 1996 Jul-Aug;117(1):24-35
references.pmid: 8776885
references.citation: Cells Tissues Organs. 2009;189(1-4):20-4
references.pmid: 18703872
references.citation: Biochemistry. 1983 Aug 30;22(18):4326-35
references.pmid: 6414510
references.citation: J Biol Chem. 2004 Apr 30;279(18):18115-20
references.pmid: 14769788
references.citation: Nature. 2005 Jun 9;435(7043):773-8
references.pmid: 15944695
references.citation: Biochemistry. 2009 Apr 28;48(16):3669-77
references.pmid: 19344178
references.citation: Bone. 2006 Sep;39(3):434-42
references.pmid: 16627026
references.citation: Bone. 2002 Jun;30(6):810-5
references.pmid: 12052446
references.citation: Chem Rev. 2008 Nov;108(11):4670-93
references.pmid: 18831570
references.citation: J Biomed Mater Res B Appl Biomater. 2004 May 15;69(2):158-65
references.pmid: 15116405
references.citation: Science. 1981 Mar 13;211(4487):1126-31
references.pmid: 7008198
references.citation: Biochem J. 1996 Jul 1;317 ( Pt 1):59-64
references.pmid: 8694787
references.citation: Crit Rev Oral Biol Med. 2001;12(4):331-49
references.pmid: 11603505
references.citation: J Bone Miner Res. 2005 Dec;20(12):2169-77
references.pmid: 16294270
references.citation: Biophys J. 2000 Oct;79(4):1737-46
references.pmid: 11023882
references.citation: Connect Tissue Res. 2003;44 Suppl 1:20-5
references.pmid: 12952169
references.citation: Matrix Biol. 1994 Aug;14(4):337-45
references.pmid: 7827757
references.citation: J Biomed Mater Res. 2001 Jun 15;55(4):496-502
references.pmid: 11288077
references.citation: Calcif Tissue Int. 1987 Feb;40(2):97-102
references.pmid: 3105840
references.citation: J Ultrastruct Res. 1982 Mar;78(3):227-68
references.pmid: 7045386
references.citation: Bone. 1996 May;18(5):417-28
references.pmid: 8739899
references.citation: J Biol Chem. 1996 Dec 13;271(50):31767-70
references.pmid: 8943211
references.citation: J Bone Miner Metab. 2004;22(4):310-7
references.pmid: 15221488
references.citation: Trends Biochem Sci. 1991 Jul;16(7):252-6
references.pmid: 1926334
references.citation: J Struct Biol. 2000 Dec;132(3):212-25
references.pmid: 11243890
references.citation: J Biol Chem. 1978 Oct 10;253(19):6845-52
references.pmid: 690128
references.citation: Cells Tissues Organs. 2005;181(3-4):144-53
references.pmid: 16612080
references.citation: Biopolymers. 1998 Oct 5;46(4):225-38
references.pmid: 9715666
references.citation: FASEB J. 1995 Dec;9(15):1537-46
references.pmid: 8529832
references.citation: Connect Tissue Res. 1997;36(3):271-86
references.pmid: 9512895
references.citation: J Biol Chem. 2009 Jun 19;284(25):17092-17101
references.pmid: 19414589
references.citation: Biochim Biophys Acta. 2000 Jul 26;1502(1):16-30
references.pmid: 10899428
references.citation: J Cell Biol. 1974 Jan;60(1):92-127
references.pmid: 4129079
references.citation: Connect Tissue Res. 1994;30(3):165-75
references.pmid: 8039384
references.citation: Proc Natl Acad Sci U S A. 2003 May 13;100(10):5597-600
references.pmid: 12732735
references.citation: Nature. 2000 Jun 29;405(6790):1036-40
references.pmid: 10890440
references.citation: Nature. 2001 Dec 13;414(6865):773-6
references.pmid: 11742405
references.citation: J Bone Miner Res. 2001 May;16(5):893-900
references.pmid: 11341334
references.citation: Histochem J. 1998 Apr;30(4):275-84
references.pmid: 9610819
references.citation: Biochemistry. 2005 Dec 13;44(49):16140-8
references.pmid: 16331974
references.citation: Proc Natl Acad Sci U S A. 2008 Nov 4;105(44):16866-70
references.pmid: 18957547
references.citation: Anat Embryol (Berl). 2000 Jul;202(1):25-30
references.pmid: 10926092
references.citation: Science. 2005 Aug 12;309(5737):1027-8
references.pmid: 16099970
references.citation: Biochem J. 1996 May 15;316 ( Pt 1):1-11
references.pmid: 8645190
references.citation: Nat Mater. 2008 Aug;7(8):610-2
references.pmid: 18654582
references.citation: Bone. 2001 Nov;29(5):453-7
references.pmid: 11704498
references.citation: J Struct Biol. 2008 Sep;163(3):229-34
references.pmid: 18359639
references.citation: Eur J Biochem. 1995 Sep 1;232(2):515-21
references.pmid: 7556201
references.citation: J Struct Biol. 2005 Feb;149(2):182-90
references.pmid: 15681234
references.citation: J Biol Chem. 2005 Sep 30;280(39):33109-14
references.pmid: 16046405
references.citation: Bone. 2003 Feb;32(2):150-62
references.pmid: 12633787
references.citation: J Biol Chem. 2009 Aug 28;284(35):23491-501
references.pmid: 19581305
references.citation: J Histochem Cytochem. 2008 Jun;56(6):561-7
references.pmid: 18319272
references.citation: Proc Natl Acad Sci U S A. 2001 Oct 9;98(21):11857-62
references.pmid: 11592996
references.citation: J Biol Chem. 2007 Aug 3;282(31):22437-47
references.pmid: 17562713
references.citation: J Theor Biol. 1975 May;51(1):51-8
references.pmid: 1142784
references.citation: J Am Chem Soc. 2007 Dec 5;129(48):14946-51
references.pmid: 17994739
references.citation: Chem Rev. 2008 Nov;108(11):4754-83
references.pmid: 19006400
references.citation: Angew Chem Int Ed Engl. 2004 May 10;43(20):2697-701
references.pmid: 18629994
references.citation: Matrix Biol. 2009 Apr;28(3):129-36
references.pmid: 19379665
references.citation: Proc Natl Acad Sci U S A. 2008 May 20;105(20):7129-34
references.pmid: 18480260
references.citation: J Biol Chem. 1997 Feb 14;272(7):4404-11
references.pmid: 9020163
references.citation: Connect Tissue Res. 1990;24(3-4):187-205
references.pmid: 2376122
references.citation: J Biomed Mater Res. 2000 Jun 15;50(4):518-27
references.pmid: 10756310
references.citation: Biomaterials. 1995 Mar;16(5):409-15
references.pmid: 7662827
references.citation: Science. 2005 Jul 8;309(5732):275-8
references.pmid: 16002612
references.citation: Proc Natl Acad Sci U S A. 2008 Sep 2;105(35):12748-53
references.pmid: 18753619
references.citation: J Exp Zool. 2002 Oct 1;293(5):478-91
references.pmid: 12486808
references.citation: Science. 2001 Nov 23;294(5547):1684-8
references.pmid: 11721046
references.citation: J Mater Sci Mater Med. 2000 Jan;11(1):49-60
references.pmid: 15348099
references.citation: J Biol Chem. 2002 Feb 8;277(6):4223-31
references.pmid: 11704682
references.citation: Biointerphases. 2006 Sep;1(3):106-11
references.pmid: 20408623
references.citation: Connect Tissue Res. 1974;2(2):137-50
references.pmid: 4138005
references.citation: Biochemistry. 2009 Mar 17;48(10):2272-81
references.pmid: 19236004
references.citation: J Dent Res. 1996 Nov;75(11):1851-8
references.pmid: 9003231
references.citation: Science. 2004 Nov 12;306(5699):1161-4
references.pmid: 15539597
references.citation: Angew Chem Int Ed Engl. 2003 May 30;42(21):2350-65
references.pmid: 12783497
references.citation: Bone. 1998 Sep;23(3):187-96
references.pmid: 9737340
references.citation: J Orthop Res. 1997 Jan;15(1):111-7
references.pmid: 9066534
references.citation: Calcif Tissue Int. 2005 Feb;76(2):127-35
references.pmid: 15549638
references.citation: Connect Tissue Res. 2001;42(1):25-37
references.pmid: 11696986
references.citation: J Clin Invest. 1996 Jan 15;97(2):396-402
references.pmid: 8567960
references.citation: Cells Tissues Organs. 2009;189(1-4):6-11
references.pmid: 18728354
references.citation: Magn Reson Chem. 2006 Jun;44(6):573-80
references.pmid: 16395729
references.citation: J Dent Res. 2006 Sep;85(9):775-93
references.pmid: 16931858
references.citation: J Biol Chem. 2005 Apr 8;280(14):13487-92
references.pmid: 15703183
references.citation: Biopolymers. 1994 Apr;34(4):507-27
references.pmid: 8186362
references.citation: Glycobiology. 2002 Sep;12(9):107R-16R
references.pmid: 12213783
references.citation: Philos Trans R Soc Lond B Biol Sci. 2002 Feb 28;357(1418):191-7
references.pmid: 11911776
references.citation: Calcif Tissue Int. 1986 Mar;38(3):135-41
references.pmid: 3011229
references.citation: Biomaterials. 2004 Aug;25(17):3593-601
references.pmid: 15020133
references.citation: Nat Mater. 2003 Aug;2(8):552-8
references.pmid: 12872163
references.citation: J Exp Med. 2008 May 12;205(5):1145-53
references.pmid: 18458111
references.citation: J Biol Chem. 2009 Jul 10;284(28):18972-9
references.pmid: 19443653
references.citation: Calcif Tissue Int. 2002 Aug;71(2):145-54
references.pmid: 12073157
references.citation: Science. 1994 Oct 7;266(5182):75-81
references.pmid: 7695699
references.citation: Chem Rev. 2008 Nov;108(11):4628-69
references.pmid: 18816145
references.citation: J Struct Biol. 1993 Jan-Feb;110(1):39-54
references.pmid: 8494671
references.citation: Calcif Tissue Int. 2001 Sep;69(3):147-57
references.pmid: 11683529
references.citation: Microsc Res Tech. 1996 Feb 1;33(2):192-202
references.pmid: 8845518
references.citation: Cell Mol Life Sci. 2000 May;57(5):859-63
references.pmid: 10892350
references.citation: J Bone Miner Res. 2003 Jun;18(6):1005-11
references.pmid: 12817752
references.citation: FASEB J. 1992 Feb 1;6(3):879-85
references.pmid: 1740237
references.citation: J Struct Biol. 1998;122(1-2):119-22
references.pmid: 9724612
references.citation: Calcif Tissue Int. 1994 Sep;55(3):180-9
references.pmid: 7987731
references.citation: Chem Rev. 2008 Nov;108(11):4551-627
references.pmid: 19006398
references.citation: J Dent Res. 2008 Jul;87(7):645-9
references.pmid: 18573984
references.citation: Calcif Tissue Int. 2003 May;72(5):592-8
references.pmid: 12724830
references.citation: Acta Biomater. 2005 Jul;1(4):387-97
references.pmid: 16701820
references.citation: J Struct Biol. 2007 Feb;157(2):365-70
references.pmid: 17055741
references.citation: J Struct Biol. 1998;122(1-2):111-8
references.pmid: 9724611