Abstract
This study assessed genetically based differences in intrinsic material properties of both cortical and cancellous bone in adult females of three inbred mouse strains [C57BL/6J (B6), DBA/2J (D2), C3H/HeJ (C3)]. These mouse strains have previously been shown to differ in bone mineral content (BMC) and density (BMD). Distal femoral cancellous bone and midshaft cortical bone in femurs and tibias were assessed for intrinsic material properties using nanoindentation technique. The intrinsic material properties tested were modulus (Eb) and hardness (H) of the midshaft femoral and tibial cortical bone cross sections and of cancellous bone in the distal femur. Both femoral and tibial cortical bone intrinsic material properties were different among the three inbred mouse strains. Femoral modulus and tibial hardness in cortical bone and hardness in cancellous bone were either greatest or showed greater trends in C3 mice as compared to both D2 and B6. Cancellous bone modulus was similar among the three mouse strains. With the exception of the D2 mice, the femoral and tibial cortical modulus were similar within each mouse strain. The tibial cortical modulus was smaller than the femoral cortical modulus for D2 mouse strain. The cortical hardness was greater in tibiae compared with that in femora within each mouse strain. The nanoindentation data suggest that cortical and cancellous intrinsic material properties are influenced by the genetic background of the inbred mouse strains. The inbred mouse strain-related intrinsic material property phenotype can be used to locate responsible quantitative trait loci (QTLs) in future studies of recombinant inbred mouse strains.
Similar content being viewed by others
References
Slemenda CW, Christian JC, Williams CJ, Norton JA, Johnston CC (199l) Genetic determinants of bone mass in adult women: a re-evaluation of the twin model and the potential importance of gene interaction on heritability estimates. J Bone Miner Res 6:561–567
Slemenda CW, Turner CH, Peacock M, Christian JC, Sorbel J, Hui SL, Johnston CC Jr (l996) The genetics of proximal femur geometry, distribution of bone mass and bone mineral density. Osteoporos Int 6:178–182
CW Slemenda JC Christian T Reed TK Reister CJ Williams CC Johnston (1992) ArticleTitleLong-term bone loss in men: effects of genetic and environmental factors Ann Intern Med 117 IssueID4 286–291 Occurrence Handle1:STN:280:By2A2cvhsFA%3D Occurrence Handle1637023
DM Smith WE Nance KW Kang JC Christian CC Johnston SuffixJr (1973) ArticleTitleGenetic factors in determining bone mass J Clin Invest 52 2800–2808 Occurrence Handle1:STN:280:CSuD387msVA%3D Occurrence Handle4795916
J Dequeker J Nijs A Verstraeten P Geusens G Gevers (1987) ArticleTitleGenetic determinants of bone mineral content at the spine and radius: a twin study Bone 8 IssueID4 207–209 Occurrence Handle10.1016/8756-3282(87)90166-9 Occurrence Handle1:STN:280:BieC1czotFY%3D Occurrence Handle3446256
FH Glorieux (2001) ArticleTitleOsteogenesis imperfecta A disease of the osteoblast. Lancet 358 suppl S45
RD Little JP Carulli RG Mastro ParticleDel J Dupuis M Osborne C Folz et al. (2002) ArticleTitleA mutation in the LDL receptor-related protein 5 gene results in the autosomal dominant high-bone-mass trait Am J Hum Genet 70 IssueID1 11–19 Occurrence Handle10.1086/338450 Occurrence Handle1:CAS:528:DC%2BD38XlvVKhtw%3D%3D Occurrence Handle11741193
NA Pocock JA Eisman JL Hopper MG Yeates PN Sambrook S Eberl (1987) ArticleTitleGenetic determinants of bone mass in adults: a twin study J Clin Invest 80 706–710 Occurrence Handle1:STN:280:BiiA3cfotVM%3D Occurrence Handle3624485
RF Klein SR Mitchell TJ Phillips JK Belknap ES Orwoll (1998) ArticleTitleQuantitative trait loci affecting peak bone mineral density in mice J Bone Miner Res 13 1648–1656 Occurrence Handle1:CAS:528:DyaK1cXntFKru78%3D Occurrence Handle9797472
RF Klein KA Vartanian LD Skinner RJ Turner GB Pelz AS Carlos JK Belknap M Shea ES Orwoll (2000) ArticleTitleBone size and density are regulated by distinct chromosomal regions J Bone Miner Res 15 IssueIDSuppl 1 S186
CH Turner YF Hsieh R Müller ML Bouxsein CJ Rosen ME McCrann LR Donahue WG Beamer (2001) ArticleTitleVariation in bone biomechanical properties and microstructure in B × H recombinant inbred mice J Bone Miner Res 16 IssueID2 206–213 Occurrence Handle1:STN:280:DC%2BD3M3ht1Wntg%3D%3D Occurrence Handle11204420
MP Akhter DM Cullen EA Pedersen DB Kimmel RR Recker (1998) ArticleTitleBone response to in vivo mechanical loading in two breeds of mice Calcif Tissue Int 63 442–449 Occurrence Handle10.1007/s002239900554 Occurrence Handle1:CAS:528:DyaK1cXntFSjsbY%3D Occurrence Handle9799831
MP Akhter JK Otero UT Iwaniec DM Cullen RR Recker (2003) ArticleTitleGenetic variation in vertebral biomechanics and histomorphometry in mice JMNI . .
Beamer WG, Donahue LR, Rosen CJ, Baylink DJ (l996) Genetic variability in adult bone density among inbred strains of mice. Bone 18:397–403
Y Kodama HP Dimai J Wegedal M Sheng R Malpe S Kutilek W Beamer LR Donahue C Rosen DJ Baylink J Farley (1999) ArticleTitleCortical tibial bone volume in two strains of mice: Effects of sciatic neurectomy and genetic regulation of bone response to mechanical loading Bone 25 IssueID2 183–190 Occurrence Handle10.1016/S8756-3282(99)00155-6 Occurrence Handle1:STN:280:DyaK1MzotlartA%3D%3D Occurrence Handle10456383
Pedersen EA, Akhter MP, Cullen DM, Kimmel DB, Recker RR (l999) Bone response to in vivo mechanical loading in C3/HeJ mice. Calcif Tissue Int 65:41–46
CH Turner Y Hsieh R Muller ML Bouxsein DJ Baylink CJ Rosen MD Grynpas LR Donahue WG Beamer (2000) ArticleTitleGenetic regulation of cortical and trabecular bone strength and microstructure in inbred strains of mice Bone Miner Res 15 IssueID6 1126–1131 Occurrence Handle1:STN:280:DC%2BD3cvmtFaltQ%3D%3D
MP Akhter UT Iwaniec MA Covey DM Cullen DB Kimmel RR Recker (2000) ArticleTitleGenetic variations in bone density, histomorphometry, and strength in mice Calcif Tissue Int 67 IssueID1 68–74 Occurrence Handle10.1007/s002230001144 Occurrence Handle10908416
Q Chen JY Rho Z Fan SJF Laulederkind R Raghow (2003) ArticleTitleCongenital lack of COX-2 affects mechanical and geometric properties of bone in mice Calcif Tissue Int 73 387–392 Occurrence Handle10.1007/s00223-002-0009-x Occurrence Handle1:CAS:528:DC%2BD3sXos1als7s%3D Occurrence Handle12874706
T Jamsa JY Rho Z Fan CA MacKay SC Marks SuffixJr J Tuukkanen (2002) ArticleTitleMechanical properties in long bones of rat osteopetrotic mutations J Biomech 35 IssueID2 161–165 Occurrence Handle10.1016/S0021-9290(01)00203-2 Occurrence Handle11784534
Oliver WC, Pharr GM (l992) An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J Mater Res 7:1564–1583
JY Rho JD Currey P Zioupos GM Pharr (2001) ArticleTitleThe anisotropic Young’s modulus of equine secondary osteones and intershtial bone determined by nanoindentation J Exp Biol 204 IssueIDPt 10 l775–1781
JY Rho M Roy GM Pharr (2000) ArticleTitleComments on “Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur” J Biomech 33 IssueID10 1335–1337 Occurrence Handle10.1016/S0021-9290(99)00228-6 Occurrence Handle1:STN:280:DC%2BD3cvnt1OgtQ%3D%3D Occurrence Handle11023378
JY Rho ME Roy TY Tsui GM Pharr (1999) ArticleTitleElastic properties of microstructural components of human bone tissue as measured by nanoindentation J Biomed Mater Res 45 IssueID1 48–54 Occurrence Handle10.1002/(SICI)1097-4636(199904)45:1<48::AID-JBM7>3.0.CO;2-5 Occurrence Handle1:CAS:528:DyaK1MXhtVWrs7c%3D Occurrence Handle10397957
JY Rho TY Tsui GM Pharr (1997) ArticleTitleElastic properties of human cortical and trabecular lamellar bone measured by nanoindentation Biomaterials 18 IssueID20 1325–1330 Occurrence Handle10.1016/S0142-9612(97)00073-2 Occurrence Handle1:CAS:528:DyaK2sXntVSlurc%3D Occurrence Handle9363331
JY Rho P Zioupos JD Currey GM Pharr (1999) ArticleTitleVariations in the individual thick lamellar properties within osteons by nanoindentation Bone 25 IssueID3 295–300 Occurrence Handle10.1016/S8756-3282(99)00163-5 Occurrence Handle1:STN:280:DyaK1Mvitlehtg%3D%3D Occurrence Handle10495133
ME Roy SK Nishimoto JY Rho SK Bhattacharya JS Lin GM Pharr (2001) ArticleTitleCorrelations between osteocalcin content, degree of mineralization, and mechanical properties of C. carpio rib bone J Biomed Mater Res 54 IssueID4 547–553 Occurrence Handle10.1002/1097-4636(20010315)54:4<547::AID-JBM110>3.3.CO;2-U Occurrence Handle1:CAS:528:DC%2BD3MXmtFWnuw%3D%3D Occurrence Handle11426600
CH Turner JY Rho Y Takano TY Tsui GM Pharr (1999) ArticleTitleThe elastic properties of trabecular and cortical bone tissues are similar: results from two microscopic measurement techniques J Biomech 32 IssueID4 437–441 Occurrence Handle10.1016/S0021-9290(98)00177-8 Occurrence Handle1:STN:280:DyaK1M3ivVShsQ%3D%3D Occurrence Handle10213035
PK Zysset XE Guo CE Hoffler KE Moore SA Goldstein (1999) ArticleTitleElastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur J Biomech 32 IssueID10 1005–1012 Occurrence Handle10.1016/S0021-9290(99)00111-6 Occurrence Handle1:STN:280:DyaK1MvgsVCrug%3D%3D Occurrence Handle10476838
Zysset PK, Guo XE, Hoffler CE, Moore KE, Goldstein SA (l998) Mechanical properties of human trabecular bone lamellae quantified by nanoindentation. Technol Health care 6(5–6):429–432
JG Swadener JY Rho GM Pharr (2001) ArticleTitleEffects of anisotropy on elastic moduli measured by nanoindentation in human tibial cortical bone J Biomed Mater Res 57 IssueID1 108–112 Occurrence Handle10.1002/1097-4636(200110)57:1<108::AID-JBM1148>3.0.CO;2-6 Occurrence Handle1:CAS:528:DC%2BD3MXlsVehu7o%3D Occurrence Handle11416856
Z Fan JG Swadener JY Rho ME Rho GM Pharr (2002) ArticleTitleAnisotropic Properties of human tibial cortical bone measured by nanoindentation J Orthop Res 20 806–810 Occurrence Handle10.1016/S0736-0266(01)00186-3 Occurrence Handle1:STN:280:DC%2BD38vhsV2gtg%3D%3D Occurrence Handle12168671
Z Fan JY Rho (2003) ArticleTitleThe effects of viscoelasticity and time-dependent plasticity to nanoindentation measurement of a human cortical bone J Biomed Mater Res 67A IssueID1 208–214 Occurrence Handle10.1002/jbm.a.10027 Occurrence Handle1:CAS:528:DC%2BD3sXotF2mtrc%3D Occurrence Handle14517878
S Hengsberger A Kulik PH Zysset (2002) ArticleTitleNanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions Bone 30 IssueID1 178–184 Occurrence Handle10.1016/S8756-3282(01)00624-X Occurrence Handle1:STN:280:DC%2BD38%2FmvVWntA%3D%3D Occurrence Handle11792582
M Zidi L Carpentier A Chateauminois F Sidoroff (2000) ArticleTitleQuantitative analysis of the micro-indentation behavior of fiber-reinforced composite: development and validation of an analytical model Composite Sci Techno 60 429–437 Occurrence Handle10.1016/S0266-3538(99)00143-8
MCH Meulen ParticleVan der KJ Jepsen B Mikie (2001) ArticleTitleUnderstanding bone strength: size isn’t everything Bone 29 101–104 Occurrence Handle10.1016/S8756-3282(01)00491-4 Occurrence Handle11502469
ME Levenston GS Beaupre MCH Meulen ParticleVan der (1994) ArticleTitleImproved method for analysis of whole bone torsion tests J Bone Miner Res 9 1459–1465 Occurrence Handle1:STN:280:ByqC3MjlvV0%3D Occurrence Handle7817831
Roy ME, Rho JY, Tsui TY, Evans ND, Pharr GM (l999) Mechanical and morphological variation of the lumbar vertebral cortical and trabecular bone. J Biomed Mater Res 44:191–197
Y Kodama Y Umemura S Nagasawa WG Beamer LR Donahue CR Rosen DJ Baylink JR Farley (2000) ArticleTitleExercise and mechanical loading increase periosteal bone formation and whole bone strength in C57BL/6J mice but not in C3H/HeJ mice Calcif tissue Int 66 IssueID4 298–306 Occurrence Handle10.1007/s002230010060 Occurrence Handle1:CAS:528:DC%2BD3cXivVChu78%3D Occurrence Handle10742449
Acknowledgments
We thank Dr. Marcel Roy for his help in performing nanoindentation tests, and Andy Lund and Nick Glass their help in editing. This study was partially supported by the LB595 Nebraska State Funds.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Akhter, M.P., Fan, Z. & Rho, J.Y. Bone Intrinsic Material Properties in Three Inbred Mouse Strains. Calcif Tissue Int 75, 416–420 (2004). https://doi.org/10.1007/s00223-004-0241-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00223-004-0241-7