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Central and Peripheral Molecular Profiling of Sex Differences in Schizophrenia, Major Depressive Disorder, and Controls

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Central and Peripheral Molecular Profiling of Sex Differences in Schizophrenia, Major Depressive Disorder, and Controls Central and peripheral molecular profiling of sex differences in schizophrenia, major depressive disorder, and controls Jordan Marion Ramsey Churchill College May 2015 This dissertation is submitted for the degree of Doctor of Philosophy To my family. Acknowledgements This thesis would not have been possible without the support of my supervisor, Prof Sabine Bahn. She provided me with guidance and interesting projects and funded me during the last couple months of my PhD. Her support has been crucial for my PhD work and career development. Most of the funding for my PhD was from the Edmonton Churchill Scholarship. In addition to their generous funding, the encouragement I received from my fellow Edmonton Churchill Scholars during my time here has been invaluable. I would also like to thank the Cambridge Commonwealth Trust for their support. Dr Emanuel Schwarz gave me the first taste for working in this field and helped me through my first research projects on serum molecular sex differences and sex-dependent differences in schizophrenia. His creative take on this work inspired me to keep learning and coming up with new ideas. Dr Jason Cooper took me under his wing and my thesis would not be what it is without his insightful comments and discussions of all chapters in this thesis. I learned an immense amount in a short period with his help and he has helped to shape me as a scientist. He continues to support me and my career, give me confidence in my work, and continuously looks out for my best interests. I cannot thank him enough for that. I would also like to thank all other members of the Bahn lab (past and present). This work would not have been possible without our collaborators: Nico JM van Beveren, F Markus Leweke, Matthias Rothermundt, Bernhard Bogerts, Johann Steiner, and Brenda Penninx. Microarray data used in this thesis was made available by the Stanley Medical Research Institute (SMRI), Harvard Brain Tissue Resource Centre, Jacqueline de Belleroche (Imperial College London, dataset GSE17612 deposited in the Gene Expression Omnibus (GEO)), and Elizabeth A Thomas (The Scripps Research Institute, dataset GSE21138 deposited in the GEO). I am very grateful to all patients and controls who participated in these studies. Finally, I would like to give my heartfelt thanks to all my friends and family who supported me throughout my PhD and put up with me while I was writing up. Churchill College has been a home away from home during my time here. I have shared some truly lovely times with my housemates Ana, Hugo, Tim, and Matt and my Aussies Ryan, Jess, and Ash. My Mom and Dad have always been there for me in any way they can be, as have my brother, Hart and sister, Elizabeth. I would also like to thank my confidante Krista and partner Dave. I expect a lot from him and he always does his best to deliver, all the while keeping me a sane, balanced, and better person. Declaration and Statement of Length The work in this thesis is entirely my own, except where stated in the Acknowledgements or elsewhere in the text. This thesis, in its entirety or in part, has not been submitted for any other degree, diploma, or qualification at any university or other institution. This text does not exceed the 65,000 word limit and does not contain more than 150 figures, as required by the Degree Committee of Engineering. Cambridge, United Kingdom, May 2015 Publications arising from this work J. M. Ramsey, E. Schwarz, P.C. Guest, N.J.M. van Beveren, F.M. Leweke, M. Rothermundt, B. Bogerts, J. Steiner, L. Ruta, S. Baron-Cohen, S. Bahn, Molecular sex differences in human serum. PLOS ONE. 7, e51504 (2012). J. M. Ramsey, E. Schwarz, P.C. Guest, N.J.M. van Beveren, F.M. Leweke, M. Rothermundt, B. Bogerts, J. Steiner, S. Bahn, Distinct molecular phenotypes in male and female schizophrenia patients. PLOS ONE. 8, e78729 (2013). J. M. Ramsey, E. Schwarz, P.C. Guest, N.J.M. van Beveren, F.M. Leweke, M. Rothermundt, B. Bogerts, J. Steiner, S. Bahn, EPA-1234 – Distinct molecular phenotypes in male and female schizophrenia patients. Eur. Psychiatry. 29, 1 (2014). J. M. Ramsey, S. Bahn, P. 8. b. 023 Overlapping and distinct sex-specific serum molecular profiles in schizophrenia, depression, bipolar disorder, and Asperger syndrome. Eur. Neuropsychopharmacol. 24, S746–S747 (2014). Abstract Schizophrenia and major depressive disorder (MDD) are disabling, poorly understood conditions with inadequate diagnostic and therapeutic technologies. They are characterized by clinical and epidemiological heterogeneity between male and female patients. Females have a higher prevalence of MDD, and in schizophrenia males have a higher incidence, earlier onset, more negative symptoms, and a worse prognosis and response to antipsychotic medication in schizophrenia. A better understanding of sex differences in these patients is needed to provide insight into biological mechanisms in these conditions and develop better diagnostic tools and therapies for males and females. This thesis sought to examine molecular sex differences in control subjects and in schizophrenia and MDD patients by profiling serum and prefrontal cortex (PFC) brain tissue. Multiplex immunoassay and microarray technologies were used to measure concentrations of proteins and small molecules in serum and gene expression in brain, respectively. Extensive differences in serum molecular concentrations were found between males and females experiencing a menstrual cycle, using oral contraceptives, and after menopause. These were involved in immune, metabolic, and endocrine processes and may play a role in driving sex differences in susceptibility and other characteristics of mental disorders. Furthermore, the hypothalamic-pituitary-gonadal (HPG) axis was altered in MDD and first onset, antipsychotic naive schizophrenia patients. Biological processes involving response to steroid hormone stimulus and estradiol were enriched among differentially expressed genes in the PFC in schizophrenia. However, investigation of sex-dependent differences in PFC gene expression in schizophrenia was limited by the small number of female samples available. Finally, higher serum concentrations of a number of immune and inflammatory molecules were associated with MDD and schizophrenia in males only and this may have consequences for immune hypotheses of these disorders. The research undertaken in this thesis has advanced the understanding of the mechanisms potentially involved in schizophrenia and MDD in males and females. Furthermore, sex and female hormonal status should routinely be taken into account during design and analysis of psychiatric molecular data to increase the reproducibility of such studies. This research shows that failing to consider these in biomarker studies can result in a high proportion of false positive findings and obscure important sex-dependent markers of mental disorders. Contents Chapter 1 Introduction .................................................................................................... 1 1.1 The burden and challenges of mental disorders ...................................................... 1 1.2 Sex ......................................................................................................................... 3 1.2.1 Endocrine and nervous systems ...................................................................... 3 1.2.2 Other systems .................................................................................................. 7 1.3 Gender .................................................................................................................... 9 1.4 Diagnosis of mental disorders ............................................................................... 10 1.5 Research tools in mental disorders ....................................................................... 11 1.6 Major depressive disorder (MDD) ......................................................................... 12 1.6.1 Criteria for diagnosis ...................................................................................... 13 1.6.2 Course and treatment .................................................................................... 14 1.6.3 Risk factors .................................................................................................... 14 1.6.4 Pathology ....................................................................................................... 15 1.6.5 Hypotheses .................................................................................................... 16 1.7 Sex and gender differences in MDD ..................................................................... 18 1.7.1 Hypotheses and pathology............................................................................. 18 1.8 Schizophrenia ....................................................................................................... 21 1.8.1 Criteria for diagnosis ...................................................................................... 22 1.8.2 Course and treatment .................................................................................... 23 1.8.3 Risk factors .................................................................................................... 24 1.8.4 Pathology ....................................................................................................... 24 1.8.5 Hypotheses .................................................................................................... 25 1.9 Sex and gender differences in schizophrenia .......................................................
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