Mechanisms of soft tissue and protein preservation in Tyrannosaurus rex

Boatman, Elizabeth M.; Goodwin, Mark B.; Holman, Hoi-Ying N.; Fakra, Sirine; Zheng, Wenxia; Gronsky, Ronald; Schweitzer, Mary H.

doi:10.1038/s41598-019-51680-1

Title: Mechanisms of soft tissue and protein preservation in Tyrannosaurus rex

Abstract

Abstract The idea that original soft tissue structures and the native structural proteins comprising them can persist across geological time is controversial, in part because rigorous and testable mechanisms that can occur under natural conditions, resulting in such preservation, have not been well defined. Here, we evaluate two non-enzymatic structural protein crosslinking mechanisms, Fenton chemistry and glycation, for their possible contribution to the preservation of blood vessel structures recovered from the cortical bone of a Tyrannosaurus rex (USNM 555000 [formerly, MOR 555]). We demonstrate the endogeneity of the fossil vessel tissues, as well as the presence of type I collagen in the outermost vessel layers, using imaging, diffraction, spectroscopy, and immunohistochemistry. Then, we use data derived from synchrotron FTIR studies of the T. rex vessels to analyse their crosslink character, with comparison against two non-enzymatic Fenton chemistry- and glycation-treated extant chicken samples. We also provide supporting X-ray microprobe analyses of the chemical state of these fossil tissues to support our conclusion that non-enzymatic crosslinking pathways likely contributed to stabilizing, and thus preserving, these T. rex vessels. Finally, we propose that these stabilizing crosslinks could play a crucial role in the preservation of other microvascular tissues in skeletal elements from themore » Mesozoic.« less

Authors:

Boatman, Elizabeth M.; Goodwin, Mark B.; Holman, Hoi-Ying N.;

; Zheng, Wenxia; Gronsky, Ronald; Schweitzer, Mary H.

Publication Date:: 2019-10-30

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22), Scientific User Facilities Division (SC-22.3 )

OSTI Identifier:: 1619589

Alternate Identifier(s):: OSTI ID: 1581381

Grant/Contract Number:: AC02-05CH11231

Resource Type:: Published Article

Journal Name:: Scientific Reports

Additional Journal Information:: Journal Name: Scientific Reports Journal Volume: 9 Journal Issue: 1; Journal ID: ISSN 2045-2322

Publisher:: Nature Publishing Group

Country of Publication:: United Kingdom

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; palaeontology

Citation Formats


                    Boatman, Elizabeth M., Goodwin, Mark B., Holman, Hoi-Ying N., Fakra, Sirine, Zheng, Wenxia, Gronsky, Ronald, and Schweitzer, Mary H.. Mechanisms of soft tissue and protein preservation in Tyrannosaurus rex.  United Kingdom: N. p., 2019. 
Web.  doi:10.1038/s41598-019-51680-1.

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                    Boatman, Elizabeth M., Goodwin, Mark B., Holman, Hoi-Ying N., Fakra, Sirine, Zheng, Wenxia, Gronsky, Ronald, & Schweitzer, Mary H.. Mechanisms of soft tissue and protein preservation in Tyrannosaurus rex.  United Kingdom.  https://doi.org/10.1038/s41598-019-51680-1

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                    Boatman, Elizabeth M., Goodwin, Mark B., Holman, Hoi-Ying N., Fakra, Sirine, Zheng, Wenxia, Gronsky, Ronald, and Schweitzer, Mary H.. Wed .  
"Mechanisms of soft tissue and protein preservation in Tyrannosaurus rex".  United Kingdom.  https://doi.org/10.1038/s41598-019-51680-1.

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@article{osti_1619589,

  title        = {Mechanisms of soft tissue and protein preservation in Tyrannosaurus rex},

  author       = {Boatman, Elizabeth M. and Goodwin, Mark B. and Holman, Hoi-Ying N. and Fakra, Sirine and Zheng, Wenxia and Gronsky, Ronald and Schweitzer, Mary H.},

  abstractNote = {Abstract The idea that original soft tissue structures and the native structural proteins comprising them can persist across geological time is controversial, in part because rigorous and testable mechanisms that can occur under natural conditions, resulting in such preservation, have not been well defined. Here, we evaluate two non-enzymatic structural protein crosslinking mechanisms, Fenton chemistry and glycation, for their possible contribution to the preservation of blood vessel structures recovered from the cortical bone of a Tyrannosaurus rex (USNM 555000 [formerly, MOR 555]). We demonstrate the endogeneity of the fossil vessel tissues, as well as the presence of type I collagen in the outermost vessel layers, using imaging, diffraction, spectroscopy, and immunohistochemistry. Then, we use data derived from synchrotron FTIR studies of the T. rex vessels to analyse their crosslink character, with comparison against two non-enzymatic Fenton chemistry- and glycation-treated extant chicken samples. We also provide supporting X-ray microprobe analyses of the chemical state of these fossil tissues to support our conclusion that non-enzymatic crosslinking pathways likely contributed to stabilizing, and thus preserving, these T. rex vessels. Finally, we propose that these stabilizing crosslinks could play a crucial role in the preservation of other microvascular tissues in skeletal elements from the Mesozoic.},

  doi          = {10.1038/s41598-019-51680-1},

  journal      = {Scientific Reports},

  number       = 1,

  volume       = 9,

  place        = {United Kingdom},

  year         = {2019},

  month        = {10}

}

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Title: Mechanisms of soft tissue and protein preservation in Tyrannosaurus rex

Abstract

Citation Formats

Synchrotron infrared imaging of advanced glycation endproducts (AGEs) in cardiac tissue from mice fed high glycemic diets journal, January 2013

Infrared spectroscopy of proteins journal, September 2007

Comparative genomics of elastin: Sequence analysis of a highly repetitive protein journal, September 2007

A Basic Mathematical Simulation of the Chemical Degradation of Ancient Collagen journal, March 1995

Enzymatic and nonenzymatic cross‐linking of collagen and elastin journal, April 1992

Virtual histology by means of high-resolution X-ray CT journal, December 2008

Glutaraldehyde as a crosslinking agent for collagen-based biomaterials journal, August 1995

Microspectroscopic Evidence of Cretaceous Bone Proteins journal, April 2011

Mechanisms of maturation and ageing of collagen journal, December 1998

Molecular evolution of fibrillar collagen in chordates, with implications for the evolution of vertebrate skeletons and chordate phylogeny journal, July 2006

Fabrication and characterization of cross-linked gelatin electro-spun nano-fibers journal, January 2010

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Fe2+-Catalyzed non-enzymatic glycosylation alters collagen conformation during AGE-collagen formation in vitro journal, December 2007

Elastin in Large Artery Stiffness and Hypertension journal, January 2012

Soft tissue and cellular preservation in vertebrate skeletal elements from the Cretaceous to the present journal, November 2006

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Enzymatic Hydroxylation of Proline and Lysine in Protocollagen journal, March 1967

Protein Glycation, Diabetes, and Aging journal, January 2001

Infrared spectroscopy used to evaluate glycosylation of proteins journal, January 2006

Soft-Tissue Vessels and Cellular Preservation in Tyrannosaurus rex journal, March 2005

Generation of Free Oxygen Radicals and the Toxicity of Hemoglobin Solutions journal, January 1990

Comparative study of some physico-chemical characteristics of osteoporotic and normal human femur heads journal, August 2007

Iron release, oxidative stress and erythrocyte ageing2 2Guest Editor: Mario Comporti 3 3This article is part of a series of reviews on “Iron and Cellular Redox Status.” The full list of papers may be found on the homepage of the journal. journal, April 2002

Hierarchical Structure and Nanomechanics of Collagen Microfibrils from the Atomistic Scale Up journal, February 2011

Cross-Linking in Collagen and Elastin journal, June 1984

Type I and Type III Collagen Interactions during Fibrillogenesis journal, February 1990

Oxidative deamination of lysine residue in plasma protein of diabetic rats: Novel mechanism via the Maillard reaction journal, October 2002

Discerning the Subfibrillar Structure of Mineralized Collagen Fibrils: A Model for the Ultrastructure of Bone journal, September 2013

Bone protects proteins over thousands of years: Extraction, analysis, and interpretation of extracellular matrix proteins in archeological skeletal remains journal, January 2003

Effect of pH on the Formation of Goethite and Hematite from Ferrihydrite journal, January 1983

The role of nonenzymatic glycosylation, transition metals, and free radicals in the formation of collagen aggregates journal, August 1991

Fibres and cellular structures preserved in 75-million–year-old dinosaur specimens journal, June 2015

Feasibility of Spectroscopic Characterization of Algal Lipids: Chemometric Correlation of NIR and FTIR Spectra with Exogenous Lipids in Algal Biomass journal, July 2010

Elastin biosynthesis: The missing link in tissue-engineered blood vessels journal, July 2006

Testing the Hypothesis of Biofilm as a Source for Soft Tissue and Cell-Like Structures Preserved in Dinosaur Bone journal, February 2016

Increased resistance of crosslinked cornea against enzymatic digestion journal, January 2004

Effects of pH on bone calcium and proton fluxes in vitro journal, August 1983

The long-term survival of bone: the role of bioerosion journal, August 2002

Diabetes induces compositional, structural and functional alterations on rat skeletal soleus muscle revealed by FTIR spectroscopy: a comparative study with EDL muscle journal, January 2010

Bacterial colonization patterns of intact Pinus sylvestris mycorrhizospheres in dry pine forest soil: an electron microscopy study journal, November 1997

Abnormalities of Basement Membrane on Blood Vessels and Endothelial Sprouts in Tumors journal, November 2003

Bacterial collagen-like proteins that form triple-helical structures journal, June 2014

A role for iron and oxygen chemistry in preserving soft tissues, cells and molecules from deep time journal, January 2014

Quantification of carbohydrates in fruit juices using FTIR spectroscopy and multivariate analysis journal, January 2011

Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage. journal, October 1993

Ferritin: a cytoprotective antioxidant strategem of endothelium. journal, September 1992

Actin and tropomyosin variants in smooth muscles. Dependence on tissue type. journal, December 1984

Proteome degradation in fossils: investigating the longevity of protein survival in ancient bone: Proteome degradation in fossils journal, February 2014

Processing of type I collagen gels using nonenzymatic glycation journal, January 2009

Crosslinked α-elastin biomaterials: towards a processable elastin mimetic scaffold journal, March 2005

Probing non-enzymatic glycation of type I collagen: A novel approach using Raman and infrared biophotonic methods journal, June 2013

Biomolecular Characterization and Protein Sequences of the Campanian Hadrosaur B. canadensis journal, April 2009

Fourier transform infrared evaluation of microscopic scarring in the cardiomyopathic heart: Effect of chronic AT1 suppression journal, May 2003

Enhanced physicochemical properties of collagen by using EDC/NHS-crosslinking journal, October 2012

Evidence of preserved collagen in an Early Jurassic sauropodomorph dinosaur revealed by synchrotron FTIR microspectroscopy journal, January 2017

Collagenous proteins of blood vessels. journal, November 1986

Rho GTPases and the Actin Cytoskeleton journal, January 1998

Mechanisms, Pathophysiology, and Therapy of Arterial Stiffness journal, May 2005

Changes in biomechanical properties, composition of collagen and elastin, and advanced glycation endproducts of the rat aorta in relation to age journal, December 1996

Analysis of type I and IV collagens by FT-IR spectroscopy and imaging for a molecular investigation of skeletal muscle connective tissue journal, October 2006

Mechanical design in arteries journal, December 1999

Structure-function Relationships in the Evolution of Elastin journal, July 1982

Lipid peroxidation and endothelial cell injury: implications in atherosclerosis journal, January 1988

Cardiac Blood pH as a Possible Indicator of Postmortem Interval journal, November 1988

Synchrotron infrared imaging of advanced glycation endproducts (AGEs) in cardiac tissue from mice fed high glycemic diets
journal, January 2013

Infrared spectroscopy of proteins
journal, September 2007

Comparative genomics of elastin: Sequence analysis of a highly repetitive protein
journal, September 2007

A Basic Mathematical Simulation of the Chemical Degradation of Ancient Collagen
journal, March 1995

Enzymatic and nonenzymatic cross‐linking of collagen and elastin
journal, April 1992

Virtual histology by means of high-resolution X-ray CT
journal, December 2008

Glutaraldehyde as a crosslinking agent for collagen-based biomaterials
journal, August 1995

Microspectroscopic Evidence of Cretaceous Bone Proteins
journal, April 2011

Mechanisms of maturation and ageing of collagen
journal, December 1998

Molecular evolution of fibrillar collagen in chordates, with implications for the evolution of vertebrate skeletons and chordate phylogeny
journal, July 2006

Fabrication and characterization of cross-linked gelatin electro-spun nano-fibers
journal, January 2010

Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus
journal, September 2009

Fe2+-Catalyzed non-enzymatic glycosylation alters collagen conformation during AGE-collagen formation in vitro
journal, December 2007

Elastin in Large Artery Stiffness and Hypertension
journal, January 2012

Soft tissue and cellular preservation in vertebrate skeletal elements from the Cretaceous to the present
journal, November 2006

Structure of Type I and Type III Heterotypic Collagen Fibrils: An X-Ray Diffraction Study
journal, January 2002

Enzymatic Hydroxylation of Proline and Lysine in Protocollagen
journal, March 1967

Protein Glycation, Diabetes, and Aging
journal, January 2001

Infrared spectroscopy used to evaluate glycosylation of proteins
journal, January 2006

Soft-Tissue Vessels and Cellular Preservation in Tyrannosaurus rex
journal, March 2005

Generation of Free Oxygen Radicals and the Toxicity of Hemoglobin Solutions
journal, January 1990

Comparative study of some physico-chemical characteristics of osteoporotic and normal human femur heads
journal, August 2007

Iron release, oxidative stress and erythrocyte ageing2 2Guest Editor: Mario Comporti 3 3This article is part of a series of reviews on “Iron and Cellular Redox Status.” The full list of papers may be found on the homepage of the journal.
journal, April 2002

Hierarchical Structure and Nanomechanics of Collagen Microfibrils from the Atomistic Scale Up
journal, February 2011

Cross-Linking in Collagen and Elastin
journal, June 1984

Type I and Type III Collagen Interactions during Fibrillogenesis
journal, February 1990

Oxidative deamination of lysine residue in plasma protein of diabetic rats: Novel mechanism via the Maillard reaction
journal, October 2002

Discerning the Subfibrillar Structure of Mineralized Collagen Fibrils: A Model for the Ultrastructure of Bone
journal, September 2013

Bone protects proteins over thousands of years: Extraction, analysis, and interpretation of extracellular matrix proteins in archeological skeletal remains
journal, January 2003

Effect of pH on the Formation of Goethite and Hematite from Ferrihydrite
journal, January 1983

The role of nonenzymatic glycosylation, transition metals, and free radicals in the formation of collagen aggregates
journal, August 1991

Fibres and cellular structures preserved in 75-million–year-old dinosaur specimens
journal, June 2015

Feasibility of Spectroscopic Characterization of Algal Lipids: Chemometric Correlation of NIR and FTIR Spectra with Exogenous Lipids in Algal Biomass
journal, July 2010

Elastin biosynthesis: The missing link in tissue-engineered blood vessels
journal, July 2006

Testing the Hypothesis of Biofilm as a Source for Soft Tissue and Cell-Like Structures Preserved in Dinosaur Bone
journal, February 2016

Increased resistance of crosslinked cornea against enzymatic digestion
journal, January 2004

Effects of pH on bone calcium and proton fluxes in vitro
journal, August 1983

The long-term survival of bone: the role of bioerosion
journal, August 2002

Diabetes induces compositional, structural and functional alterations on rat skeletal soleus muscle revealed by FTIR spectroscopy: a comparative study with EDL muscle
journal, January 2010

Bacterial colonization patterns of intact Pinus sylvestris mycorrhizospheres in dry pine forest soil: an electron microscopy study
journal, November 1997

Abnormalities of Basement Membrane on Blood Vessels and Endothelial Sprouts in Tumors
journal, November 2003

Bacterial collagen-like proteins that form triple-helical structures
journal, June 2014

A role for iron and oxygen chemistry in preserving soft tissues, cells and molecules from deep time
journal, January 2014

Quantification of carbohydrates in fruit juices using FTIR spectroscopy and multivariate analysis
journal, January 2011

Endothelial-cell heme uptake from heme proteins: induction of sensitization and desensitization to oxidant damage.
journal, October 1993

Ferritin: a cytoprotective antioxidant strategem of endothelium.
journal, September 1992

Actin and tropomyosin variants in smooth muscles. Dependence on tissue type.
journal, December 1984

Proteome degradation in fossils: investigating the longevity of protein survival in ancient bone: Proteome degradation in fossils
journal, February 2014

Processing of type I collagen gels using nonenzymatic glycation
journal, January 2009

Crosslinked α-elastin biomaterials: towards a processable elastin mimetic scaffold
journal, March 2005

Probing non-enzymatic glycation of type I collagen: A novel approach using Raman and infrared biophotonic methods
journal, June 2013

Biomolecular Characterization and Protein Sequences of the Campanian Hadrosaur B. canadensis
journal, April 2009

Fourier transform infrared evaluation of microscopic scarring in the cardiomyopathic heart: Effect of chronic AT1 suppression
journal, May 2003

Enhanced physicochemical properties of collagen by using EDC/NHS-crosslinking
journal, October 2012

Evidence of preserved collagen in an Early Jurassic sauropodomorph dinosaur revealed by synchrotron FTIR microspectroscopy
journal, January 2017

Collagenous proteins of blood vessels.
journal, November 1986

Rho GTPases and the Actin Cytoskeleton
journal, January 1998

Mechanisms, Pathophysiology, and Therapy of Arterial Stiffness
journal, May 2005

Changes in biomechanical properties, composition of collagen and elastin, and advanced glycation endproducts of the rat aorta in relation to age
journal, December 1996

Analysis of type I and IV collagens by FT-IR spectroscopy and imaging for a molecular investigation of skeletal muscle connective tissue
journal, October 2006

Mechanical design in arteries
journal, December 1999

Structure-function Relationships in the Evolution of Elastin
journal, July 1982

Lipid peroxidation and endothelial cell injury: implications in atherosclerosis
journal, January 1988

Cardiac Blood pH as a Possible Indicator of Postmortem Interval
journal, November 1988