Molecular analyses of dinosaur osteocytes support the presence of endogenous molecules

Published on Jan 1, 2013in Bone4.36
· DOI :10.1016/j.bone.2012.10.010
Mary H. Schweitzer25
Estimated H-index: 25
(NCSU: North Carolina State University),
Wenxia Zheng11
Estimated H-index: 11
(NCSU: North Carolina State University)
+ 1 AuthorsMarshall Bern42
Estimated H-index: 42
article i nfo The discovery of soft, transparent microstructures in dinosaur bone consistent in morphology with osteocytes was controversial. We hypothesize that, if original, these microstructures will have molecular features in com- mon with extant osteocytes. We present immunological and mass spectrometry evidence for preservation of proteins comprising extant osteocytes (Actin, Tubulin, PHEX, Histone H4) in osteocytes recovered from two non-avian dinosaurs. Furthermore, antibodies to DNA show localized binding to these microstructures, which also react positively with DNA intercalating stains propidium iodide (PI) and 4',6'-diamidino-2-phenylindole dihydrochloride (DAPI). Each antibody binds dinosaur cells in patterns similar to extant cells. These data are the first to support preservation of multiple proteins and to present multiple lines of evidence for material con- sistent with DNA in dinosaurs, supporting the hypothesis that these structures were part of the once living ani- mals. We propose mechanisms for preservation of cells and component molecules, and discuss implications for dinosaurian cellular biology.
  • References (85)
  • Citations (43)
📖 Papers frequently viewed together
126 Citations
124 Citations
105 Citations
78% of Scinapse members use related papers. After signing in, all features are FREE.
#1Edwin Alberto Cadena Rueda (NCSU: North Carolina State University)H-Index: 11
#2Mary H. Schweitzer (NCSU: North Carolina State University)H-Index: 25
article i nfo Here we describe variations in osteocytes derived from each of the three bone layers that comprise the turtle shell. We examine osteocytes in bone from four extant turtle species to form a morphological 'baseline' ,a nd then compare these with morphologies of osteocytes preserved in Cenozoic and Mesozoic fossils. Two different morphotypes of osteocytes are recognized: flattened-oblate osteocytes (FO osteocytes), which are particularly abundant in the internal cortex and lamellae of...
20 CitationsSource
#1Karine Lalonde (Concordia University)H-Index: 5
#2Alfonso Mucci (McGill University)H-Index: 55
Last. Yves Gélinas (Concordia University)H-Index: 31
view all 4 authors...
About one-fifth of organic carbon in sediments is bound to reactive iron phases, which are metastable over geological timescales and may therefore serve as a sink for the long-term storage of organic carbon. It is well known that solid iron phases can preserve organic carbon in soils, but it remains uncertain whether significant amounts of organic carbon can be preserved by iron in sediments. Yves Gelinas et al. study a range of freshwater and marine sediments and find that almost one-quarter of...
316 CitationsSource
The cytoskeleton is a system of intracellular filaments crucial for cell shape, division, and function in all three domains of life. The simple cytoskeletons of prokaryotes show surprising plasticity in composition, with none of the core filament-forming proteins conserved in all lineages. In contrast, eukaryotic cytoskeletal function has been hugely elaborated by the addition of accessory proteins and extensive gene duplication and specialization. Much of this complexity evolved before the last...
157 CitationsSource
#2Mary H. Schweitzer (MSU: Montana State University)H-Index: 25
Last. Joseph P. R. O. Orgel (IIT: Illinois Institute of Technology)H-Index: 21
view all 6 authors...
Eleven collagen peptide sequences recovered from chemical extracts of dinosaur bones were mapped onto molecular models of the vertebrate collagen fibril derived from extant taxa. The dinosaur peptides localized to fibril regions protected by the close packing of collagen molecules, and contained few acidic amino acids. Four peptides mapped to collagen regions crucial for cell-collagen interactions and tissue development. Dinosaur peptides were not represented in more exposed parts of the collage...
25 CitationsSource
#1Johan Lindgren (Lund University)H-Index: 22
#2Per Uvdal (Lund University)H-Index: 22
Last. Louis L. Jacobs (SMU: Southern Methodist University)H-Index: 34
view all 12 authors...
Low concentrations of the structural protein collagen have recently been reported in dinosaur fossils based primarily on mass spectrometric analyses of whole bone extracts. However, direct spectroscopic characterization of isolated fibrous bone tissues, a crucial test of hypotheses of biomolecular preservation over deep time, has not been performed. Here, we demonstrate that endogenous proteinaceous molecules are retained in a humerus from a Late Cretaceous mosasaur (an extinct giant marine liza...
33 CitationsSource
#1Philipp Schneider (ETH Zurich)H-Index: 20
#2Matias Meier (ETH Zurich)H-Index: 3
Last. Ralph Müller (ETH Zurich)H-Index: 90
view all 4 authors...
Osteocytes are the most abundant cells in bone and the only cells embedded in the bone mineral matrix. They form an extended, three-dimensional (3D) network, whose processes interconnecting the cell bodies reside in thin canals, the canaliculi. Together with the osteocyte lacunae, the canaliculi form the lacuno-canalicular network (LCN). As the negative imprint of the cellular network within bone tissue, the LCN morphology is considered to play a central role for bone mechanosensation and mechan...
101 CitationsSource
#1Sarah L. Dallas (UMKC: University of Missouri–Kansas City)H-Index: 17
#2Lynda F. Bonewald (UMKC: University of Missouri–Kansas City)H-Index: 80
Osteocytes are derived from osteoblasts and make up over 90% of the cells in bone. However, the mechanisms that control the differentiation of osteoblasts into osteocytes embedded in bone matrix are not well understood. With the recent developments of transgenic models for manipulating gene expression in osteocytes and of transgenic mice carrying lineage reporters for osteoblasts and osteocytes, unprecedented new insights are becoming possible. In this article we review recent advances, such as ...
169 CitationsSource
#1Dayong Guo (UMKC: University of Missouri–Kansas City)H-Index: 14
#2Lynda F. Bonewald (UMKC: University of Missouri–Kansas City)H-Index: 80
Osteocytes were the forgotten bone cell until the bone community could become convinced that these cells do serve an important role in bone function and maintenance. In this review we trace the history of osteocyte characterization and present some of the major observations that are leading to the conclusion that these cells are not passive placeholders residing in the bone matrix, but are indeed, major orchestrators of bone remodeling.
12 CitationsSource
#1Kayo Tanaka-Kamioka (IU: Indiana University)H-Index: 1
#2Hiroshi Kamioka (IU: Indiana University)H-Index: 1
Last. Soo Siang Lim (IU: Indiana University)H-Index: 3
view all 4 authors...
Osteocytes are derived from a select group of osteoblasts that have undergone a final differentiation. Due to their inaccessibility when embedded in the bone matrix, very little is known about the osteocyte cytoskeleton. This study provides an extensive analysis of the osteocyte cytoskeleton, based on the successful isolation of osteocytes from 16-day embryonic chick calvariae. We used OB7.3, a chicken osteocyte-specific monoclonal antibody, to confirm the osteocytic phenotype of the isolated ce...
142 CitationsSource
#1Marshall BernH-Index: 42
#2Brett S. PhinneyH-Index: 29
Last. David A. GoldbergH-Index: 27
view all 3 authors...
Asara et al. reported the detection of collagen peptides in a 68-million-year-old Tyrannosaurus rex bone by shotgun proteomics. This finding has been called into question as a possible statistical artifact. We reanalyze Asara et al.’s tandem mass spectra using a different search engine and different statistical tools. Our reanalysis shows a sample containing common laboratory contaminants, soil bacteria, and bird-like hemoglobin and collagen.
44 CitationsSource
Cited By43
#1Aaron J. van der Reest (U of A: University of Alberta)H-Index: 2
#2Philip J. Currie (U of A: University of Alberta)H-Index: 52
Abstract In recent years, several papers have claimed that soft tissue can preserve within bone matrix of extinct vertebrates, some dating back over 100 million years. Work conducted on specimens from Montana suggested sediment type may influence preservation of original tissues and proteins. An alternative hypothesis is that soft tissue preservation may be linked to the time that a specimen is exposed to the environment prior to burial. The time of exposure can be estimated by the degree of dis...
#1Alida M. Bailleul (CAS: Chinese Academy of Sciences)H-Index: 8
#2Wenxia Zheng (NCSU: North Carolina State University)H-Index: 11
Last. Mary H. Schweitzer (NCSU: North Carolina State University)H-Index: 25
view all 6 authors...
1 CitationsSource
#1Renxing Liang (Princeton University)H-Index: 1
#2Maggie C. Y. Lau (CAS: Chinese Academy of Sciences)H-Index: 17
Last. Tullis C. Onstott (Princeton University)H-Index: 51
view all 5 authors...
#1Aurore Canoville (NCSU: North Carolina State University)H-Index: 11
#2Mary H. SchweitzerH-Index: 25
Last. Lindsay E. Zanno (NCSU: North Carolina State University)H-Index: 17
view all 3 authors...
Medullary bone (MB) is a sex-specific tissue produced by female birds during the laying cycle, and it is hypothesized to have arisen within Avemetatarsalia, possibly outside Avialae. Over the years...
#1Brian Thomas (University of Liverpool)
#2Stephen Taylor (University of Liverpool)H-Index: 73
ABSTRACTIntroduction: Despite an extensive published literature, skepticism over the claim of original biochemicals including proteins preserved in the fossil record persists and the issue remains ...
#1Alexander W.A. Kellner (UFRJ: Federal University of Rio de Janeiro)H-Index: 25
#1Alexander W.A. Kellner (AmeriCorps VISTA)H-Index: 10
Last. Marina B. Soares (AmeriCorps VISTA)
view all 2 authors...
#1Alida M. Bailleul (CAS: Chinese Academy of Sciences)H-Index: 8
#2Jingmai K. O’Connor (CAS: Chinese Academy of Sciences)H-Index: 26
Last. Mary H. SchweitzerH-Index: 25
view all 3 authors...
In the mid-19th century, the discovery that bone microstructure in fossils could be preserved with fidelity provided a new avenue for understanding the evolution, function, and physiology of long extinct organisms. This resulted in the establishment of paleohistology as a subdiscipline of vertebrate paleontology, which has contributed greatly to our current understanding of dinosaurs as living organisms. Dinosaurs are part of a larger group of reptiles, the Archosauria, of which there are only t...
1 CitationsSource
#1Hans D. HallenH-Index: 21
#2Brandon J. N. LongH-Index: 1
#1Mary H. SchweitzerH-Index: 25
#2Elena R. Schroeter (NCSU: North Carolina State University)H-Index: 9
Last. Wenxia Zheng (NCSU: North Carolina State University)H-Index: 11
view all 4 authors...
Molecular studies have contributed greatly to our understanding of evolutionary processes that act upon virtually every aspect of living organisms. However, these studies are limited with regard to extinct organisms, particularly those from the Mesozoic because fossils pose unique challenges to molecular workflows, and because prevailing wisdom suggests no endogenous molecular components can persist into deep time. Here, the power and potential of a molecular approach to Mesozoic fossils is disc...
1 CitationsSource
#1Paul V. Ullmann (Rowan University)H-Index: 2
#2Suraj H. Pandya (Drexel University)H-Index: 1
Last. Ron Nellermoe (Concordia College)H-Index: 2
view all 3 authors...
Abstract Recovery of soft tissues and cells from fossil bones is becoming increasingly common, with structures morphologically consistent with vertebrate osteocytes, blood vessels, fibrous/collagenous matrix, and potential intravascular contents now recognized from specimens dating back to the Permian. However, it largely remains unclear how bone tissue structure, early diagenetic regimes, and many other taphonomic variables influence or control the preservation potential of soft tissues in vert...
1 CitationsSource