Synchrotron imaging reveals bone healing and remodelling strategies in extinct and extant vertebrates

Journal of the Royal Society Interface

Volumn 11, Issue 96, 2014, Pages

  Anné, Jennifer ^a   Edwards, Nicholas P ^a   Wogelius, Roy A ^a   Tumarkin Deratzian, Allison R ^b   Sellers, William I ^a   Van Veelen, Arjen ^a   Bergmann, Uwe ^c   Sokaras, Dimosthenis ^d   Alonso Mori, Roberto ^d   Ignatyev, Konstantin ^e   Egerton, Victoria M ^a   Manning, Phillip L ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b Temple University   (United States)

^c SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^d SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^e DIAMOND LIGHT SOURCE LTD   (United Kingdom)

Author keywords

Archosaur; Bone; Fracture healing; Histology; SRS XRF

Indexed keywords

ANIMALS; CHEMICAL DETECTION; HISTOLOGY; MAPPING; SCANNING ELECTRON MICROSCOPY;

ARCHOSAUR; CHEMICAL SIGNATURES; FRACTURE HEALING; HISTOLOGICAL ANALYSIS; HISTOLOGICAL FEATURES; MORPHOLOGICAL OBSERVATIONS; PATHOLOGICAL TISSUE; SRS-XRF;

BONE;

BARIUM; CALCIUM; COPPER; IRON; LANTHANUM; STRONTIUM; TRACE ELEMENT; ZINC;

ALLOSAURUS FRAGILIS; ANIMAL TISSUE; ARCHOSAUR; ARTICLE; BONE GROWTH; BONE REMODELING; CATHARTES AURA; CONTROLLED STUDY; EXTINCT SPECIES; FOSSIL; FRACTURE HEALING; LIMIT OF DETECTION; NONHUMAN; SYNCHROTRON; SYNCHROTRON RADIATION; SYNCHROTRON RAPID SCANNING X RAY FLUORESCENCE; TRABECULAR BONE; X RAY FLUORESCENCE; ANATOMY AND HISTOLOGY; ANIMAL; BIRD; BONE; DINOSAUR; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BIRDS; BONE AND BONES; BONE REMODELING; DINOSAURS; FOSSILS; FRACTURE HEALING; SYNCHROTRONS;

EID: 84901396974     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2014.0277     Document Type: Article

References (51)

1. Chinsamy-Turan A. 2005 The microstructure of dinosaur bone: deciphering biology with fine-scale techniques. Baltimore, MD: The John Hopkins University Press.
2. Currey J. 2002 Bones: structure and biomechanics. Princeton, NJ: Princeton University Press.
3. de Ricqlés A. 1974 Evolution of endothermy: histological evidence. Evol. Theor. 1, 51-80.
4. Tumarkin-Deratzian AR, Vann DV, Dodson P. 2006 Bone surface texture as an ontogenetic indicator in long bones of the Canada goose Branta Canadensis (Anseriformes: Anatidae). Zool. J. Linn. Soc. Lond. 148, 133-168. (doi:10.1111/j.1096-3642.2006.00232.x)
5. Madsen J. 1976 Allosaurus fragilis: a revised osteology. Utah Geol. Surv. Bull. 109, 1-163.
6. Goodwin MB, Grant PG, Bench G, Holyrod P. 2007 Elemental composition and diagenetic alteration of dinosaur bone: distinguishing micron-scale spatial and compositional heterogeneity using PIXE. Palaeogeogr. Palaeoclimatol. Palaeoecol. 23, 458-476. (doi:10.1016/j.palaeo.2007.06.017)
7. Trueman CN, Tuross N. 2002 Trace elements in recent and fossil bone apatite. Rev. Mineral. Geochem. 48, 489-521. (doi:10.2138/rmg.2002.48.13)
8. Wopenka B, Pasteris J. 2005 A mineralogical perspective on the apatite in bone. Mater. Sci. Eng. C 25, 131-143. (doi:10.1016/j.msec.2005.01.008)
9. Fricke HC, Rogers RR. 2000 Multiple taxon-multiple locality approach to providing oxygen isotope evidence for warm-blooded theropod dinosaurs. Geology 28, 799-802. (doi:10.1130/0091-7613(2000)28〈799:MTLATP〉2.0.CO;2)
10. Herwartz D, Tütken T, Jochum KP, Sander PM. 2012 Rare earth element systematics of fossil bone revealed by LA-ICPMS analysis. Geochim. Cosmochim. Acta 103, 161-183. (doi:10.1016/j.gca.2012.10.038)
11. Kocsis L, Trueman CN, Palmer MR. 2010 Protracted diagenetic alteration of REE contents in fossil bioapatites: direct evidence for Lu-Hf isotope systematics. Geochim. Cosmochim. Acta 74, 6077-6092. (doi:10.1016/j.gca.2010.08. 007)
12. Kohn MJ, Moses RJ. 2013 Trace element diffusivities in bone rule out simple diffusive uptake during fossilization but explain in vivo uptake and release. Proc. Natl Acad. Sci. USA 10, 419-422. (doi:10.1073/pnas.1209513110)
13. Kohn M. 2008 Models of diffusion-limited uptake of trace elements in fossils and rates of fossilization. Geochim. Cosmochim. Acta 72, 3758-3770. (doi:10.1016/j.gca.2008.05.045)
14. Edwards NP, Barden H, van Dongen BE, Manning PL, Larson P, Bergmann U, Sellers WI, Wogelius RA. 2011 Infra-red mapping resolves soft-tissue preservation in 50 million year old reptile skin. Proc. R. Soc. B 278, 3209-3218. (doi:10.1098/rspb.2011.0135)
15. Stankiewicz BA, Briggs DEG, Evershed RP, Flannery MB, Wuttke M. 1997 Preservation of chitin in 25-million-year-old fossils. Science 276, 1541-1543. (doi:10.1126/science.276.5318.1541)
16. Vitek NS, Vinther J, Schiffbauer JD, Briggs DEG, Prum RO. 2013 Exceptional three-dimensional preservation and coloration of an originally iridescent fossil feather from the middle Eocene messel oil shale. Paläontol. Z. 87, 493-503. (doi:10.1007/s12542-013-0173-5)
17. Bergmann U, Morton RW, Manning PL, Sellers WI, Farrar S, Huntley KG, Wogelius RA, Larson P. 2010 Archaeopteryx feathers and bone chemistry fully revealed via synchrotron imaging. Proc. Natl Acad. Sci. USA 107, 9060-9065. (doi:10.1073/pnas.1001569107)
18. Bergmann U, Manning PL, Wogelius RA. 2012 Chemical mapping of paleontological and archaeological artefacts using synchrotron x-rays. Ann. Rev. Anal. Chem. 5, 361-389. (doi:10.1146/annurev-anchem-062011-143019)
19. Wogelius RA et al. 2011 Trace metals as biomarkers for eumelanin pigment in the fossil record. Science 333, 1622-1626. (doi:10.1126/science.1205748)
20. Edwards NP et al. 2014 Leaf metallome preserved over 50 million years. Metallomics 6, 774-782. (doi:10.1039/C3MT00242J)
21. Straight W, Davis G, Skinner C, Haims A, McClennan B, Tanke D. 2009 Bone lesions in Hadrosaurus: computed tomographic imaging as a guide for paleohistolological and stable-isotope analysis. J. Vertebr. Paleontol. 29, 315-325. (doi:10.1671/039.029.0211)
22. Skinner HCW. 2005 Mineralogy of bone. In Essentials of medical geology (eds O Selinus et al.), pp. 667-693. Burlington, MA: Elsevier Academic Press.
23. Pasteris J, Wopenka B, Freeman J, Rogers K, Valsami-Jones E, van der Houwen J, Silva M. 2004 Lack of OH in nanocrystalline apatite as a function of degree of atomic order: implications for bone and biomaterials. Biomaterials 25, 229-238. (doi:10.1016/S0142-9612(03)00487-3)
24. Carter D, Beaupré G. 2001 Skeletal function and form: mechanobiology of skeletal development, aging, and regeneration. New York, NY: Cambridge University Press.
25. Waldron T. 2009 Paleopathology. New York, NY: Cambridge University Press.
26. Ferguson C, Alpern E, Miclau T, Helms J. 1999 Does fracture repair recapitulate embryonic skeletal formation? Mech. Dev. 87, 57-66. (doi:10.1016/S0925-4773(99)00142-2)
27. Shapiro F. 2008 Bone development and its relation to fracture repair. The role of mesenchymal osteoblasts and surface osteoblasts. Eur. Cells Mater. 15, 53-76. (Pubitemid 351958405)
28. Pritchard JJ, Ruzicka AJ. 1950 Comparison of fracture repair in the frog, lizard, and rat. J. Anat. 84, 236-261.
29. Raftery A. 2011 Reptile orthopaedic medicine and surgery. J. Exot. Pet Med. 20, 107-116. (doi:10.1053/j.jepm.2011.02.005)
30. Beatty B, Rothschild B. 2009 Paleopathologies are features of an organism and its interaction with the environment and should not be treated like organisms unto themselves. Hist. Biol. 21, 229-233. (doi:10.1080/ 08912960903469711)
31. Barbara A, Delannoy P, Denis BG, Marie PG. 2004 Normal matrix mineralization induced by strontium renelate in MC3T3-E1 osteogenic cells. Metabolis 53, 532-537. (doi:10.1016/j.metabol.2003.10.022)
32. Bonnelye E, Chabadel A, Saltel F, Jurdic P. 2008 Dual effect of strontium ranelate: stimulation of osteoblast differentiation and inhibition of osteoclast formation and resorption in vitro. Bone 42, 129-138. (doi:10.1016/j.bone.2007.08.043)
33. Yuan X, Wang J, Zhu X, Zhang Z, Ai Y, Sun G, Wang Z, Liu G. 2011 Effect of copper on levels of collagen and alkaline phosphatase activity from chondrocytes in newborn piglets in vitro. Biol. Trace Elem. Res. 144, 597-605. (doi:10.1007/s12011-011-9151-5)
34. Yamaguchi M. 2010 Role of nutritional zinc in the prevention of osteoporosis. Mol. Cell. Biochem. 338, 241-254. (doi:10.1007/s11010-009-0358-0)
35. Lowe NM, Fraser WD, Jackson MJ. 2002 Is there a potential therapeutic value of copper and zinc for osteoporosis? Proc. Nutr. Soc. 61, 181-185. (doi:10.1079/PNS2002154)
36. Gomez S, Rizzo R, Pozzi-Mucelli M, Bonucci E, Vittur F. 1999 Zinc mapping in bone tissues by histochemistry and synchrotron radiation-induced X-ray emission: correlation with the distribution of alkaline phosphates. Bone 25, 33-38. (doi:10.1016/S8756-3282(99)00102-7)
37. Haumont S. 1961 Distribution of zinc in bone tissue. J. Histochem. Cyctochem. 9, 141-145. (doi:10.1177/9.2.141)
38. Rucker RB, Konsonen T, Clegg MS, Mitchell AE, Rucker BR, Uriu-Hare JY, Keen CL. 1998 Copper, lysyl oxidase, and extracellular matrix protein crosslinking. Am. J. Clin. Nutr. 67(Suppl.), 996S-1002S. (Pubitemid 28198823)
39. Brown Jr GE, Strurchio NC. 2002 An overview of synchrotron radiation applications to low temperature geochemistry and environmental science. Rev. Mineral. Geochem. 49, 1-115. (doi:10.2138/gsrmg.49.1.1)
40. Morton RW, Witherspoon KC. 1993 Elemental X-ray imaging of fossils. Adv. X-Ray Anal. 36, 97-104.
41. Chinsamy A, Raath MA. 1992 Preparation of fossil bone for histological examination. Palaeontol. Afr. 29, 39-44.
42. Abramoff MD, Magelhaes PJ, Ram SJ. 2004 Image processing with IMAGEJ. Biophotonics Int. 11, 36-42.
43. Chinga G, Syverud K. 2007 Quantification of paper mass distributions within local picking areas. Nord. Pulp Pap. Res. J. 22, 441-446. (doi:10.3183/NPPRJ-2007-22-04-p441-446)
44. Solé VA, Papillon E, Cotte M, Walter Ph, Susini J. 2007 A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra. Spectrochim. Acta B 62, 63-68. (doi:10.1016/j.sab.2006.12.002)
45. Ravel B, Newville M. 2005 Athena, Artemis, Hephaestus: data analysis for x-ray absorption spectroscopy using IFEFFIT. J. Synchrotron Radiat. 12, 537-541. (doi:10.1107/S0909049505012719)
46. Sandström M, Jalilehvand F, Damain E, Fors Y, Gelius U, Jones M, Salomé M. 2005 Sulphur accumulation in the timbers of King Henry VIII's warship Mary Rose: a pathway in the sulphur cycle of conservation concern. Proc. Natl Acad. Sci. USA 102, 14 165-14 170. (doi:10.1073/pnas.0504490102)
47. Parslow JLF, Jefferies DJ, French MC. 1972 Ingested pollutants in puffins and their eggs. Bird Study 19, 18-33. (doi:10.1080/00063657209476321)
48. Tang Y, Chappell HF, Dove MT, Reeder RJ, Lee YJ. 2009 Zinc incorporation into hydroxylapatite. Biomaterials 30, 2864-2872. (doi:10.1016/j.biomaterials. 2009.01.043)
49. Suarez C, Macpherson G, González L, Grandstaff G. 2010 Heterogeneous rare earth element (REE) patterns and concentrations in a fossil bone: implications for the use of REE in vertebrate taphonomy and fossilization history. Geochim. Cosmochim. Acta 74, 2970-2988. (doi:10.1016/j.gca.2010.02.023)
50. Bilbey S. 1998 Cleveland-Lloyd dinosaur quarry: age, stratigraphy, and depositional environments. Mod. Geol. 22, 87-120.
51. Gates T. 2005 The late Jurassic Cleveland-Lloyd dinosaur quarry as a drought-induced assemblage. Palaios 20, 363-375. (doi:10.2110/palo.2003.p03-22)