Niculescu A B, Le-Niculescu H, Levey D F, Phalen P L, Dainton H L, Roseberry K, Niculescu E M, Niezer J O, Williams A, Graham D L, Jones T J, Venugopal V, Ballew A, Yard M, Gelbart T, Kurian S M, Shekhar A, Schork N J, Sandusky G E, Salomon D R
Department of Psychiatry, Indiana University School of Medicine, Indianapolis, IN, USA.
Stark Neuroscience Research Institute, Indiana University School of Medicine, Indianapolis, IN, USA.
Mol Psychiatry. 2017 Sep;22(9):1250-1273. doi: 10.1038/mp.2017.128. Epub 2017 Aug 15.
Suicide remains a clear, present and increasing public health problem, despite being a potentially preventable tragedy. Its incidence is particularly high in people with overt or un(der)diagnosed psychiatric disorders. Objective and precise identification of individuals at risk, ways of monitoring response to treatments and novel preventive therapeutics need to be discovered, employed and widely deployed. We sought to investigate whether blood gene expression biomarkers for suicide (that is, a 'liquid biopsy' approach) can be identified that are more universal in nature, working across psychiatric diagnoses and genders, using larger cohorts than in previous studies. Such markers may reflect and/or be a proxy for the core biology of suicide. We were successful in this endeavor, using a comprehensive stepwise approach, leading to a wealth of findings. Steps 1, 2 and 3 were discovery, prioritization and validation for tracking suicidality, resulting in a Top Dozen list of candidate biomarkers comprising the top biomarkers from each step, as well as a larger list of 148 candidate biomarkers that survived Bonferroni correction in the validation step. Step 4 was testing the Top Dozen list and Bonferroni biomarker list for predictive ability for suicidal ideation (SI) and for future hospitalizations for suicidality in independent cohorts, leading to the identification of completely novel predictive biomarkers (such as CLN5 and AK2), as well as reinforcement of ours and others previous findings in the field (such as SLC4A4 and SKA2). Additionally, we examined whether subtypes of suicidality can be identified based on mental state at the time of high SI and identified four potential subtypes: high anxiety, low mood, combined and non-affective (psychotic). Such subtypes may delineate groups of individuals that are more homogenous in terms of suicidality biology and behavior. We also studied a more personalized approach, by psychiatric diagnosis and gender, with a focus on bipolar males, the highest risk group. Such a personalized approach may be more sensitive to gender differences and to the impact of psychiatric co-morbidities and medications. We compared testing the universal biomarkers in everybody versus testing by subtypes versus personalized by gender and diagnosis, and show that the subtype and personalized approaches permit enhanced precision of predictions for different universal biomarkers. In particular, LHFP appears to be a strong predictor for suicidality in males with depression. We also directly examined whether biomarkers discovered using male bipolars only are better predictors in a male bipolar independent cohort than universal biomarkers and show evidence for a possible advantage of personalization. We identified completely novel biomarkers (such as SPTBN1 and C7orf73), and reinforced previously known biomarkers (such as PTEN and SAT1). For diagnostic ability testing purposes, we also examined as predictors phenotypic measures as apps (for suicide risk (CFI-S, Convergent Functional Information for Suicidality) and for anxiety and mood (SASS, Simplified Affective State Scale)) by themselves, as well as in combination with the top biomarkers (the combination being our a priori primary endpoint), to provide context and enhance precision of predictions. We obtained area under the curves of 90% for SI and 77% for future hospitalizations in independent cohorts. Step 5 was to look for mechanistic understanding, starting with examining evidence for the Top Dozen and Bonferroni biomarkers for involvement in other psychiatric and non-psychiatric disorders, as a mechanism for biological predisposition and vulnerability. The biomarkers we identified also provide a window towards understanding the biology of suicide, implicating biological pathways related to neurogenesis, programmed cell death and insulin signaling from the universal biomarkers, as well as mTOR signaling from the male bipolar biomarkers. In particular, HTR2A increase coupled with ARRB1 and GSK3B decreases in expression in suicidality may provide a synergistic mechanistical corrective target, as do SLC4A4 increase coupled with AHCYL1 and AHCYL2 decrease. Step 6 was to move beyond diagnostics and mechanistical risk assessment, towards providing a foundation for personalized therapeutics. Items scored positive in the CFI-S and subtypes identified by SASS in different individuals provide targets for personalized (psycho)therapy. Some individual biomarkers are targets of existing drugs used to treat mood disorders and suicidality (lithium, clozapine and omega-3 fatty acids), providing a means toward pharmacogenomics stratification of patients and monitoring of response to treatment. Such biomarkers merit evaluation in clinical trials. Bioinformatics drug repurposing analyses with the gene expression biosignatures of the Top Dozen and Bonferroni-validated universal biomarkers identified novel potential therapeutics for suicidality, such as ebselen (a lithium mimetic), piracetam (a nootropic), chlorogenic acid (a polyphenol) and metformin (an antidiabetic and possible longevity promoting drug). Finally, based on the totality of our data and of the evidence in the field to date, a convergent functional evidence score prioritizing biomarkers that have all around evidence (track suicidality, predict it, are reflective of biological predisposition and are potential drug targets) brought to the fore APOE and IL6 from among the universal biomarkers, suggesting an inflammatory/accelerated aging component that may be a targetable common denominator.
自杀仍然是一个明显、当前且日益严重的公共卫生问题,尽管它是一个潜在可预防的悲剧。其发病率在患有明显或未被诊断出的精神疾病的人群中尤其高。需要发现、采用并广泛应用客观且精确的风险个体识别方法、监测治疗反应的方式以及新型预防性治疗手段。我们试图研究是否能够识别出更具普遍性的自杀血液基因表达生物标志物(即一种“液体活检”方法),该方法适用于各种精神疾病诊断和不同性别,且使用比以往研究更大的队列。此类标志物可能反映自杀的核心生物学特征和/或作为其替代指标。我们通过全面的逐步方法成功达成了这一目标,得出了大量研究结果。步骤1、2和3分别是发现、筛选优先级和验证追踪自杀倾向的生物标志物,最终得到了一个由每个步骤的顶级生物标志物组成的“十二强”候选生物标志物列表,以及在验证步骤中通过邦费罗尼校正的148个候选生物标志物的更大列表。步骤4是在独立队列中测试“十二强”列表和经邦费罗尼校正的生物标志物列表对自杀意念(SI)和未来自杀相关住院治疗的预测能力,从而识别出全新的预测生物标志物(如CLN5和AK2),同时也强化了我们以及该领域其他人之前的研究发现(如SLC4A4和SKA2)。此外,我们研究了是否可以根据高自杀意念时的精神状态识别出自杀倾向的亚型,并确定了四种潜在亚型:高度焦虑型、情绪低落型、混合型和非情感型(精神病型)。这些亚型可能描绘出在自杀生物学特征和行为方面更具同质性的个体群体。我们还研究了一种更具个性化的方法,根据精神疾病诊断和性别进行划分,重点关注双相情感障碍男性这一最高风险群体。这种个性化方法可能对性别差异以及精神疾病共病和药物治疗的影响更为敏感。我们比较了在所有人中测试通用生物标志物、按亚型测试以及按性别和诊断进行个性化测试的情况,结果表明亚型和个性化方法能够提高对不同通用生物标志物预测的精确性。特别是,LHFP似乎是抑郁症男性自杀倾向的有力预测指标。我们还直接研究了仅使用男性双相情感障碍患者发现的生物标志物在男性双相情感障碍独立队列中是否比通用生物标志物更具预测性,并证明了个性化可能具有的优势。我们识别出了全新的生物标志物(如SPTBN1和C7orf73),并强化了先前已知的生物标志物(如PTEN和SAT1)。为了进行诊断能力测试,我们还研究了作为预测指标的表型测量工具,如应用程序(用于自杀风险(CFI - S,自杀倾向的收敛功能信息)以及用于焦虑和情绪(SASS,简化情感状态量表)),以及它们与顶级生物标志物的组合(该组合是我们预先设定的主要终点),以提供背景信息并提高预测的精确性。在独立队列中,我们获得了自杀意念的曲线下面积为90%,未来住院治疗自杀相关情况的曲线下面积为77%。步骤5是寻求机制理解,首先检查“十二强”和经邦费罗尼校正的生物标志物参与其他精神和非精神疾病的证据,以此作为生物易感性和脆弱性的一种机制。我们识别出的生物标志物还为理解自杀生物学特征提供了一个窗口,从通用生物标志物中暗示了与神经发生、程序性细胞死亡和胰岛素信号传导相关的生物途径,以及从男性双相情感障碍生物标志物中暗示了mTOR信号传导。特别是,在自杀倾向中HTR2A表达增加同时ARRB1和GSK3B表达降低可能提供一个协同的机制校正靶点,SLC4A4表达增加同时AHCYL1和AHCYL2表达降低也是如此。步骤6是超越诊断和机制风险评估,为个性化治疗奠定基础。在不同个体中CFI - S得分呈阳性的项目以及SASS识别出的亚型为个性化(心理)治疗提供了靶点。一些个体生物标志物是用于治疗情绪障碍和自杀倾向的现有药物(锂盐、氯氮平和ω - 3脂肪酸)的靶点,这为患者的药物基因组学分层和治疗反应监测提供了一种方法。此类生物标志物值得在临床试验中进行评估。对“十二强”和经邦费罗尼验证的通用生物标志物的基因表达生物特征进行生物信息学药物重新利用分析,识别出了自杀倾向的新型潜在治疗药物,如依布硒仑(一种锂模拟物)、吡拉西坦(一种益智药)、绿原酸(一种多酚)和二甲双胍(一种抗糖尿病药物且可能具有促进长寿的作用)。最后,基于我们的数据总体情况以及该领域迄今为止的证据,一个收敛功能证据评分突出了具有全面证据(追踪自杀倾向、预测自杀倾向、反映生物易感性且是潜在药物靶点)的生物标志物,在通用生物标志物中,APOE和IL6脱颖而出,表明炎症/加速衰老成分可能是一个可靶向的共同特征。