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The Downstream Targets of Complex I Dysfunction in Bipolar Disorder
Helena Kyunghee Kim
A thesis submitted in conformity with the requirements for the degree of PhD
Graduate Department of Pharmacology and Toxicology
2011; Srinivasan et al., 2006; Srinivasan, Spence, Pandi-Perumal, Brown, & Cardinali, 2011). These
findings suggest that melatonin may be efficacious as an adjunct in BD by improving complex I
function and decreasing oxidative stress. In fact, patients with BD were found to have genetic
variations in the melatonin gene (Etain et al., 2012), further suggesting that melatonin may have
positive effects on the treatment of BD. Moreover, melatonin was found to decrease metabolic
effects of antipsychotic medications such as increased blood pressure or weight gain in patients with
BD, demonstrating that melatonin is safe to use as an adjunct for the treatment of BD and that it may
have multiple beneficial effects (Romo-Nava et al., 2014). Hence, a randomized clinical trial
examining the effect of melatonin as an adjunct on symptom severity, cognitive decline, complex I
dysfunction and oxidative stress may be beneficial for the development of better treatments for BD.
To summarize, I first re-examined microarray studies measuring mRNA levels of complex I
subunits in patients with BD or SCZ, and determined that patients with BD have lower levels of
subunits that are involved in the process of electron transfer, suggesting that they may be more
susceptible to increased leakage of electrons and greater generation of ROS. I also confirmed lower
levels of complex I and its subunit, NDUFS7, in the post-mortem brain of patients with BD. After
confirming that complex I dysfunction in BD is likely to contribute to increased oxidative stress, I
aimed to extend on a previous study identifying the mitochondria and the synapse as two targets of
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oxidative stress in the frontal cortex of patients with BD. To examine the mitochondria as a target of
complex I dysfunction, I examined activation of the NLRP3-inflammasome, a marker of complex I
dysfunction and mitochondrial production of ROS, and found that the activation of the NLRP3-
inflammasome is increased in the post-mortem frontal cortex of patients with BD, demonstrating the
mitochondria as a potential downstream target of complex I dysfunction in BD. The next study
aimed to examine the second potential target, the synapse, by focusing on the dopaminergic synapse
as dopamine dysregulation is known to underlie mania. This study demonstrated the synapse as a
potential target of complex I dysfunction in BD, as oxidative modifications to the dopaminergic
synapse were found to be altered in the post-mortem prefrontal cortex from patients with BD.
Downstream targets of complex I dysfunction were further examined using cell models, allowing us
to directly inhibit the electron transfer process in complex I with rotenone. Using cell models, I
could also examine the effect of lithium, which is uniquely used for the treatment of BD and can be
used to examine if alterations produced by rotenone may be relevant to BD pathology. Complex I
dysfunction produced by rotenone increased protein nitration and oxidation, and increased
methylation and hydroxymethylation of DNA. These alterations were decreased with lithium pre-
treatment, suggesting that downstream effects of complex I dysfunction may have important
pathological roles in BD. While much remains to be explored in the role of complex I dysfunction in
the pathophysiology of BD, these studies suggest that examining complex I defect and its
downstream pathways may increase our understanding of the different systems that are involved in
BD, and potentially reveal novel targets that can be used to improve therapeutic interventions.
139
7. CONCLUSIONS
The overall aim of my PhD was to elucidate downstream targets of complex I dysfunction in
BD. Our review of microarray studies examining complex I subunits in psychiatric disorders
revealed that the differentiating factor between BD and schizophrenia is the downregulation of
complex I subunits specifically involved in the process of electron transfer in BD, suggesting that
patients with BD may be more vulnerable to the generation of oxidative stress. We then confirmed
complex I dysfunction in post-mortem brains of patients with BD, where patients with BD were
found to have lower levels of complex I, but not other members of the electron transport chain, and
also lower levels of NDUFS7, a complex I subunit that is critical for the electron transfer process.
After confirming complex I dysfunction in the frontal cortex of patients with BD, we aimed to
extend on a recent study published from our group, identifying the mitochondria and the synapse as
targets of oxidative stress in the post-mortem brain of patients with BD. I first examined the
mitochondria as a potential downstream target of complex I dysfunction in BD by measuring a
marker of mitochondrial oxidative stress, the NLRP3-inflamamsome, in the post-mortem frontal
cortex. Patients with BD were found to have increased activation of the NLRP3-inflammasome,
demonstrating the mitochondria as a potential downstream target of complex I dysfunction in BD. I
then examined the synapse as a downstream target of complex I defect by examining oxidative
modifications to the dopaminergic synapse, as dopamine dysregulation is known to underlie mania.
Results showed altered levels of oxidation and nitration in areas immunoreactive for markers of the
dopamine synapse, suggesting that complex I dysfunction may also target the synapse in BD. To
further examine downstream effects of complex I dysfunction, we used cell models, allowing us to
directly inhibit the electron transfer process in complex I using rotenone. We also examined the
effect of lithium, as it is uniquely used for the treatment of BD and can aid us in determining if
alterations occurring due to complex I inhibition with rotenone may be relevant to BD pathology.
140
Results revealed that complex I dysfunction produced by rotenone causes an increase in protein
oxidation and nitration and methylation and hydroxymethylation of DNA, suggesting that complex I
defect in the electron transfer process can directly cause potentially pathological alterations
downstream. Importantly, lithium pre-treatment was able to decrease these alterations caused by
rotenone, suggesting that consequences of complex I dysfunction may have pathological
implications in BD.
Our findings in post-mortem brain and cell models suggest that complex I dysfunction and its
downstream targets have important roles in the pathophysiology of BD. In vitro and animal studies
have shown that complex I dysfunction can lead to other downstream alterations as well (Beal, 2002;
Halliwell, 1992). Of interest, oxidative stress from complex I defect can increase intracellular
calcium levels (Persson et al., 2013; L. S. Zheng, Ishii, Zhao, Kondo, & Sasahara, 2013), which has
been consistently reported in patients with BD (Dubovsky et al., 1994; Perova et al., 2010; Perova,
Wasserman, Li, & Warsh, 2008), suggesting that complex I dysfunction may have multiple effects in
BD. Future directions include confirmation of these findings using different techniques. For
example, while DAT and TH immunoreactive regions were found to be targets of oxidative
modifications using FRET, most likely representing alterations of DAT and TH themselves,
confirming this using a biochemical technique, such as co-immunoprecipitation would help solidify
the dopaminergic synapse as a downstream target of complex I dysfunction. Furthermore, as
identification of biomarkers in BD is of great interest, examining whether markers of complex I
dysfunction, such as the NLRP3-inflammasome, can be measured in peripheral cells from patients
with BD may yield interesting results. This will also allow us to confirm our findings using a larger
sample, increasing the generalizability of the results. Also, using animal models to confirm the
findings of our studies using neuroblastoma cells and primary neurons would allow for the validation
of the identified mechanisms in a more complex system. Lastly, as lithium was demonstrated to be
141
effective in preventing downstream effects of complex I inhibition through its ability to improve
complex I functioning, examining the effect of other reagents that were shown to improve complex I
activity as an adjunct may contribute to developing better treatments for BD.
142
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Oxidation and nitration in dopaminergic areas of the prefrontal cortex from patients with bipolar disorder and schizophrenia
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