DITYROSINE AS A BIOMARKER OF FREE RADICAL INDUCED OXIDATIVE DAMAGE IN DISEASES OF AGEING

Короткий опис

Originality Statement
‘I hereby declare that this submission is my own work and to the best of my
knowledge it contains no materials previously published or written by another
person, or substantial proportions of material which have been accepted for the
award of any other degree or diploma at UNSW or any other educational
institution, except where due acknowledgement is made in the thesis. Any
contribution made to the research by others, with whom I have worked at
UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that
the intellectual content of this thesis is the product of my own work, except to
the extent that assistance from others in the project's design and conception or
in style, presentation and linguistic expression is acknowledged.’
Signed ……………………………………………..............
Date ……………………………………………..............
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Abstract
Dityrosine (o,o’-dityrosine), an oxidation product of tyrosine produced by reaction
between tyrosyl radicals, is becoming established as a biomarker of free radical
oxidative protein damage in vivo. Attempts to measure o,o’-dityrosine concentrations
in various physiological and pathological systems using different analytical
technologies have produced varied and often contradictory results. o,o’-Dityrosine
concentrations in urine, plasma, cerebrospinal fluid (CSF) and brain tissue varying over
three orders of magnitude have been reported, together with inconsistent claims of
significant o,o’-dityrosine elevation in several ageing-related pathologies. Some of
these findings have contributed to the implication of free radical activity in the
pathology of several neurodegenerative disorders, vascular and ocular abnormalities and
in phagocyte response to infection.
The aim of this study was to test the hypothesis that o,o’-dityrosine levels are elevated
in ageing and ageing-related disease due to increases in free radical activity, reduced
antioxidant defenses or accumulation of oxidative damage products. The study also
aims to determine the utility of o,o’-dityrosine measurement as an index of oxidative
damage, identify the erroneous information reported in literature and elucidate possible
explanations for the apparent inconsistencies.
An assay for the quantification of o,o’-dityrosine in urine and protein hydrolysates was
developed using capillary HPLC with electrospray tandem quadrupole mass
spectrometry (HPLC-MS/MS). The assay was highly specific for o,o’-dityrosine and
has the highest absolute sensitivity for o,o’-dityrosine of any method reported to date,
with a detection limit of 3 femtomoles of o,o’-dityrosine on-column. Urine samples
from volunteers of different age and from hospital patients with various pathologies
were analyzed. Protein hydrolysates from the plasma of healthy control subjects,
Alzheimer’s and stroke patients were analyzed, together with hydrolysates of
postmortem tissue from the brains of Alzheimer’s and control subjects.
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The data obtained show that urinary o,o’-dityrosine level is elevated in states of acute
infection and inflammation, but does not correlate with age or chronic disease. Protein
o,o’-dityrosine levels in plasma did not vary with disease state. Protein o,o’-dityrosine
in four sections of Alzheimer’s brain was not significantly different from control
sections. o,o’-Dityrosine was present in human plasma and tissue proteins at
approximately 5-35 residues per million tyrosine residues, and in normal urine at 5-25
μmol/mol creatinine or 20-200 nM. Most of the discrepancies in the literature relate to
inadequate specificity of the analytical method. Interpretation of published data with
critical appraisal of measurement technology specificity is essential in developing an
accurate understanding of the role of free radicals in ageing and disease.
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Acknowledgements
Firstly I would like to express my sincere thanks and deep appreciation to my
Supervisor, Associate Professor George Smythe, for encouraging me to begin a PhD,
for all his ideas, guidance, constant support and encouragement throughout my
candidature at UNSW. George has been, and continues to be a first-class scientific
mentor for me in my development as a research scientist, with unfailing patience and
dedication to me as his student and friend.
I would like to express my thanks and appreciation to Associate Professor Michael
Guilhaus, Director of the BMSF at UNSW for all his encouragement and for allowing
me the time and resources to complete my PhD at the BMSF. Michael’s counsel,
enthusiasm, and technical advice have been invaluable throughout my studies.
My sincere thanks to my Co-Supervisor, Professor Michael J. Davies, Deputy Director
of the Heart Research Institute, Sydney, for all his guidance and encouragement. I
would especially like to thank him for his help in arranging samples for this study and
for his helpful critique of my manuscripts.
I would also like to express my gratitude to my Co-Supervisor, Dr. Vimal Kapoor for
all his help in getting my PhD studies started, for all his encouragement and for
allowing me to freely use the facilities in his laboratory.
Special thanks to my friend and co-worker, Ms Anne Poljak for her collaboration on the
analysis of plasma and tissue samples, for all her advice and assistance with method
development and all her hard work with ethics documentation, sample cataloging,
dissecting and weighing. Anne’s collaboration and willingness to share material and
expertise has been pivotal to the success of this study.
I would also like to thank Professor Perminder Sachdev, School of Psychiatry, UNSW
for all his help in obtaining samples and ethics approval for this study. Thanks also to
Professor Alicia Jenkins, St Vincent’s Hospital, University of Melbourne for providing
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pathological urine samples and assistance with ethics approval. My thanks to Dr. Gilles
Guillemin, School of Medical Sciences, UNSW for providing cultured neuroblastoma
cells, and to Professor Catriona McLean, National Neural Tissue Resource Facility,
Monash University, Melbourne for providing sections of human brain tissue.
My special thanks and appreciation to Miss Justyna Maria Czarna, PhD student of the
Statens Serum Institut and University of Odense, Denmark, for all her hard work on
GC-MS tyrosine measurement of the plasma hydrolysates for this study whilst she was
a Visiting Fellow at UNSW. Justyna also helped in developing sample preparation
techniques for o,o’-dityrosine measurement of plasma hydrolysates and hydrolysed all
of the plasma samples for this study. My thanks to Mr. Thuan Thai for assisting Justyna
with this very hard work.
I would like to express my appreciation to Miss Ivana Solaja, former honors student of
the School of Medical Sciences (SOMS), for allowing me access to her treated neuronal
cells and for providing me with background information on her experiments. Thanks to
Miss Tharusha Jayasena, Student of SOMS, for preparing fresh control and peroxidetreated
neuronal cells.
I would like to acknowledge the assistance and support I have received from all of my
colleagues and fellow students at the BMSF and SOMS, my sincere thanks to everyone.
In Particular I would like to thank Dr. Mark Raftery for all his excellent advice on
analytical techniques, construction of capillary columns and instrument specifics of the
TSQ 7000 mass spectrometer. My special thanks to Dr. Ross Grant and Mrs. Sonia
Bustamante for their assistance with urinary creatinine measurements. Thanks to Dr.
Valerie Wasinger for her help in adapting a conventional electropray ion source to
accept integrated-tip capillary columns. Thanks also to Jones Chen, Summer Student of
the BMSF, who performed initial development work on the synthesis and purification
of our o,o’-dityrosine standard and analyzed this material by GC-MS.
I would like to thank Agilent Technologies for their loan of an LC MSD Trap mass
spectrometer and for donation of a semi-preparative HPLC column. Thanks to
Phenomenex Inc. for their gift of Jupiter C18 packing material. I would also like to
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thank Mr. Mark Obrien, of Thermo Australia for all his help with the Thermo TSQ
7000 mass spectrometer which has worked consistently well throughout the project.
Finally, I would like to thank all of my family for their support and encouragement
throughout my PhD candidature, In particular my wife, Adis for all her love, patience
and loyalty and my son, Adrian Paul, for his love and understanding of my need for
time to work and study. Born in the first months of this work, Adrian has been an
enduring, unquestioning source of love, support and encouragement. Moving forward
from thesis submission, it is my foremost intention to spend more time with you,
Adrian, you are so very precious to me.
This work was supported in part by grants from the Australian Government Systemic
Infrastructure Initiative and Major National Research Facilities Program (UNSW node
of the Australian Proteome Analysis Facility) and by the UNSW Capital Grants
Scheme.
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ix

Table of Contents
Chapter 1 – Introduction 1
1.1 Research hypothesis and aims 1
1.2 Free radicals 1
1.3 Literature review – structure and coverage 3
1.4 Early experiments on free radical-mediated protein oxidation (in vitro) 6
1.5 Free radicals in biological materials 10
1.6 The free radical theory of ageing 11
1.7 o,o’-Dityrosine – early work 14
1.8 o,o’-Dityrosine as a marker of free radical activity in biological systems 16
1.9 Experiments in this study 35
Chapter 2 – Urinary o,o’-Dityrosine Assay 37
2.1 Experimental rationale 37
2.2 Materials and methods 38
2.21 Materials 38
2.22 Standards 38
2.23 Urine samples 41
2.24 Sample processing 42
2.25 Capillary chromatography 42
2.26 Quantitative mass spectrometry 47
2.27 Calibration curves 49
2.28 Validation 49
2.29 Data manipulation and statistics 51
2.3 Assay – results and discussion 51
2.31 Purification of o,o’-dityrosine standard material 51
2.32 Purity analysis of o,o’-dityrosine-d4 57
2.33 Standard calibration curves, limits of quantification and detection 62
2.34 Validation 66
2.35 Discussion 68
2.4 Urine samples from healthy subjects – results and discussion 79
x
2.41 Results 79
2.42 Discussion 84
2.5 Pathological urine samples – results and discussion 86
2.51 Results 86
2.52 Discussion 99
Chapter 3 – Measuring o,o’-Dityrosine in Plasma Hydrolysates 112
3.1 Experimental rationale 112
3.2 Materials and methods 112
3.21 Materials 112
3.22 Subjects and plasma samples 113
3.23 Hydrolysis 114
3.24 Measuring tyrosine in plasma protein hydrolysates 115
3.25 o,o’-Dityrosine analysis 119
3.3 Results 122
3.4 Discussion 123
Chapter 4 – Measuring o,o’-Dityrosine in Brain Tissue Hydrolysates 130
4.1 Experimental rationale 130
4.2 Materials and methods 130
4.21 Samples 130
4.3 Results 132
4.4 Discussion 136
Chapter 5 – o,o’-Dityrosine in Cultured Neuronal Cell Hydrolysates 144
5.1 Experimental rationale 144
5.2 Materials and methods 146
5.21 Materials 146
5.22 Cell culture 146
5.23 Treatments 146
5.24 Preparation for hydrolysis 148
5.3 Results 148
5.4 Discussion 149
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Chapter 6 – Study Conclusions 151
6.1 Assay 151
6.2 o,o’-Dityrosine analysis of urine samples 152
6.3 Urinary o,o’-dityrosine and ageing 152
6.4 Urinary o,o’-dityrosine and disease 153
6.5 Protein-bound plasma o,o’-dityrosine levels 154
6.6 Should we measure urinary, or plasma o,o’-dityrosine? 154
6.7 o,o’-Dityrosine measurement in Alzheimer’s brain tissue 155
6.8 Cultured neuronal cells subject to Fenton oxidation 156
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