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Thomas, Christoph ; Aller, Stephen G. ; Beis, Konstantinos ; Carpenter, Elisabeth P. ; Chang, Geoffrey ; Chen, Lei ; Dassa, Elie ; Dean, Michael ; Duong Van Hoa, Franck ; Ekiert, Damian ; Ford, Robert ; Gaudet, Rachelle ; Gong, Xin ; Holland, I. Barry ; Huang, Yihua ; Kahne, Daniel K. ; Kato, Hiroaki ; Koronakis, Vassilis ; Koth, Christopher M. ; Lee, Youngsook ; Lewinson, Oded ; Lill, Roland ; Martinoia, Enrico ; Murakami, Satoshi ; Pinkett, Heather W. ; Poolman, Bert ; Rosenbaum, Daniel ; Sarkadi, Balazs ; Schmitt, Lutz ; Schneider, Erwin ; Shi, Yigong ; Shyng, Show‐Ling ; Slotboom, Dirk Jan ; Tajkhorshid, Emad ; Tieleman, Dirk Peter ; Ueda, Kazumitsu ; Váradi, András ; Wen, Po‐Chao ; Yan, Nieng ; Zhang, Peng ; Zheng, Hongjin ; Zimmer, Jochen ; Tampé, Robert
Members of the ATP‐binding cassette (ABC) transporter superfamily translocate a broad spectrum of chemically diverse substrates. While their eponymous ATP‐binding cassette in the nucleotide‐binding domains (NBDs) is highly conserved, their transmembrane domains (TMDs) forming the translocation pathway exhibit distinct folds and topologies, suggesting that during evolution the ancient motor domains were combined with different transmembrane mechanical systems to orchestrate a variety of cellular processes. In recent years, it has become increasingly evident that the distinct TMD folds are best suited to categorize the multitude of ABC transporters. We therefore propose a new ABC transporter classification that is based on structural homology in the TMDs:
Haslinger, Denise ; Waltes, Regina ; Yousaf, Afsheen ; Lindlar, Silvia ; Schneider, Ines ; Lim, Chai K. ; Tsai, Meng-Miao ; Garvalov, Boyan K. ; Acker-Palmer, Amparo ; Krezdorn, Nicolas ; Rotter, Björn ; Acker, Till ; Guillemin, Gilles J. ; Fulda, Simone ; Freitag, Christine M. ; Geburtig-Chiocchetti, Andreas
Background: Altered neuronal development is discussed as the underlying pathogenic mechanism of autism spectrum disorders (ASD). Copy number variations of 16p11.2 have recurrently been identified in individuals with ASD. Of the 29 genes within this region, quinolinate phosphoribosyltransferase (QPRT) showed the strongest regulation during neuronal differentiation of SH-SY5Y neuroblastoma cells. We hypothesized a causal relation between this tryptophan metabolism-related enzyme and neuronal differentiation. We thus analyzed the effect of QPRT on the differentiation of SH-SY5Y and specifically focused on neuronal morphology, metabolites of the tryptophan pathway, and the neurodevelopmental transcriptome.
Methods: The gene dosage-dependent change of QPRT expression following Chr16p11.2 deletion was investigated in a lymphoblastoid cell line (LCL) of a deletion carrier and compared to his non-carrier parents. Expression of QPRT was tested for correlation with neuromorphology in SH-SY5Y cells. QPRT function was inhibited in SH-SY5Y neuroblastoma cells using (i) siRNA knockdown (KD), (ii) chemical mimicking of loss of QPRT, and (iii) complete CRISPR/Cas9-mediated knock out (KO). QPRT-KD cells underwent morphological analysis. Chemically inhibited and QPRT-KO cells were characterized using viability assays. Additionally, QPRT-KO cells underwent metabolite and whole transcriptome analyses. Genes differentially expressed upon KO of QPRT were tested for enrichment in biological processes and co-regulated gene-networks of the human brain.
Results: QPRT expression was reduced in the LCL of the deletion carrier and significantly correlated with the neuritic complexity of SH-SY5Y. The reduction of QPRT altered neuronal morphology of differentiated SH-SY5Y cells. Chemical inhibition as well as complete KO of the gene were lethal upon induction of neuronal differentiation, but not proliferation. The QPRT-associated tryptophan pathway was not affected by KO. At the transcriptome level, genes linked to neurodevelopmental processes and synaptic structures were affected. Differentially regulated genes were enriched for ASD candidates, and co-regulated gene networks were implicated in the development of the dorsolateral prefrontal cortex, the hippocampus, and the amygdala.
Conclusions: In this study, QPRT was causally related to in vitro neuronal differentiation of SH-SY5Y cells and affected the regulation of genes and gene networks previously implicated in ASD. Thus, our data suggest that QPRT may play an important role in the pathogenesis of ASD in Chr16p11.2 deletion carriers.
Rothenburger, Tamara ; Thomas, Dominique Jeanette ; Schreiber, Yannick ; Wratil, Paul Robin ; Pflantz, Tamara ; Knecht, Kirsten M. ; Digianantonio, Katie ; Temple, Joshua ; Schneider, Constanze ; Baldauf, Hanna-Mari ; McLaughlin, Katie-May ; Rothweiler, Florian ; Bilen, Berna ; Farmand, Samira ; Bojkova, Denisa ; Costa, Rui ; Ferreirós Bouzas, Nerea ; Geisslinger, Gerd ; Oellerich, Thomas ; Xiong, Yong ; Keppler, Oliver Till ; Wass, Mark N. ; Michaelis, Martin ; Cinatl, Jindrich
Background: SAMHD1 mediates resistance to anti-cancer nucleoside analogues, including cytarabine, decitabine, and nelarabine that are commonly used for the treatment of leukaemia, through cleavage of their triphosphorylated forms. Hence, SAMHD1 inhibitors are promising candidates for the sensitisation of leukaemia cells to nucleoside analogue-based therapy. Here, we investigated the effects of the cytosine analogue CNDAC, which has been proposed to be a SAMHD1 inhibitor, in the context of SAMHD1. Methods: CNDAC was tested in 13 acute myeloid leukaemia (AML) cell lines, in 26 acute lymphoblastic leukaemia (ALL) cell lines, ten AML sublines adapted to various antileukaemic drugs, 24 single cell-derived clonal AML sublines, and primary leukaemic blasts from 24 AML patients. Moreover, 24 CNDAC-resistant sublines of the AML cell lines HL-60 and PL-21 were established. The SAMHD1 gene was disrupted using CRISPR/Cas9 and SAMHD1 depleted using RNAi, and the viral Vpx protein. Forced DCK expression was achieved by lentiviral transduction. SAMHD1 promoter methylation was determined by PCR after treatment of genomic DNA with the methylation-sensitive HpaII endonuclease. Nucleoside (analogue) triphosphate levels were determined by LC-MS/MS. CNDAC interaction with SAMHD1 was analysed by an enzymatic assay and by crystallisation. Results: Although the cytosine analogue CNDAC was anticipated to inhibit SAMHD1, SAMHD1 mediated intrinsic CNDAC resistance in leukaemia cells. Accordingly, SAMHD1 depletion increased CNDAC triphosphate (CNDAC-TP) levels and CNDAC toxicity. Enzymatic assays and crystallisation studies confirmed CNDAC-TP to be a SAMHD1 substrate. In 24 CNDAC-adapted acute myeloid leukaemia (AML) sublines, resistance was driven by DCK (catalyses initial nucleoside phosphorylation) loss. CNDAC-adapted sublines displayed cross-resistance only to other DCK substrates (e.g. cytarabine, decitabine). Cell lines adapted to drugs not affected by DCK or SAMHD1 remained CNDAC sensitive. In cytarabine-adapted AML cells, increased SAMHD1 and reduced DCK levels contributed to cytarabine and CNDAC resistance. Conclusion: Intrinsic and acquired resistance to CNDAC and related nucleoside analogues are driven by different mechanisms. The lack of cross-resistance between SAMHD1/ DCK substrates and non-substrates provides scope for next-line therapies after treatment failure.
Beyer, Mandy ; Romanski, Annette ; Al-Hassan, M. Mustafa ; Pons, Miriam ; Büchler, Iris ; Vogel, Anja ; Pautz, Andrea ; Sellmer, Andreas ; Schneider, Günter ; Bug, Gesine ; Krämer, Oliver Holger
Therapy of acute myeloid leukemia (AML) is unsatisfactory. Histone deacetylase inhibitors (HDACi) are active against leukemic cells in vitro and in vivo. Clinical data suggest further testing of such epigenetic drugs and to identify mechanisms and markers for their efficacy. Primary and permanent AML cells were screened for viability, replication stress/DNA damage, and regrowth capacities after single exposures to the clinically used pan-HDACi panobinostat (LBH589), the class I HDACi entinostat/romidepsin (MS-275/FK228), the HDAC3 inhibitor RGFP966, the HDAC6 inhibitor marbostat-100, the non-steroidal anti-inflammatory drug (NSAID) indomethacin, and the replication stress inducer hydroxyurea (HU). Immunoblotting was used to test if HDACi modulate the leukemia-associated transcription factors β-catenin, Wilms tumor (WT1), and myelocytomatosis oncogene (MYC). RNAi was used to delineate how these factors interact. We show that LBH589, MS-275, FK228, RGFP966, and HU induce apoptosis, replication stress/DNA damage, and apoptotic fragmentation of β-catenin. Indomethacin destabilizes β-catenin and potentiates anti-proliferative effects of HDACi. HDACi attenuate WT1 and MYC caspase-dependently and -independently. Genetic experiments reveal a cross-regulation between MYC and WT1 and a regulation of β-catenin by WT1. In conclusion, reduced levels of β-catenin, MYC, and WT1 are molecular markers for the efficacy of HDACi. HDAC3 inhibition induces apoptosis and disrupts tumor-associated protein expression.
Pirkis, Jane ; Gunnell, David ; Shin, Sangsoo ; Del Pozo-Banos, Marcos ; Arya, Vikas ; Analuisa Aguilar, Pablo ; Appleby, Louis ; Yasir Arafat, S. M. ; Arensman, Ella ; Ayuso-Mateos, Jose Luis ; Pal Singh Balhara, Yatan ; Bantjes, Jason ; Baran, Anna ; Behera, Chittaranjan ; Bertolote, Jose ; Borges, Guilherme ; Bray, Michael ; Brečić, Petrana ; Caine, Eric ; Calati, Raffaella ; Carli, Vladimir ; Castelpietra, Giulio ; Fong Chan, Lai ; Chang, Shu-Sen ; Colchester, David ; Coss-Guzmán, Maria ; Crompton, David ; Ćurković, Marko ; Dandona, Rakhi ; De Jaegere, Eva ; De Leo, Diego ; Deisenhammer, Eberhard A. ; Dwyer, Jeremy ; Erlangsen, Annette ; Faust, Jeremy S. ; Fornaro, Michele ; Fortune, Sarah ; Garrett, Andrew ; Gentile, Guendalina ; Gerstner, Rebekka ; Gilissen, Renske ; Gould, Madelyn ; Kumar Gupta, Sudhir ; Hawton, Keith ; Holz, Franziska ; Kamenshchikov, Iurii ; Kapur, Navneet ; Kasal, Alexandr ; Khan, Murad ; Kirtley, Olivia J. ; Knipe, Duleeka ; Kõlves, Kairi ; Kölzer, Sarah C. ; Krivda, Hryhorii ; Leske, Stuart ; Madeddu, Fabio ; Marshall, Andrew ; Memon, Anjum ; Mittendorfer-Rutz, Ellenor ; Nestadt, Paul ; Neznanov, Nikolay ; Niederkrotenthaler, Thomas ; Nielsen, Emma ; Nordentoft, Merete ; Oberlerchner, Herwig ; O’Connor, Rory C. ; Papsdorf, Rainer ; Partonen, Timo ; Phillips, Michael R. ; Platt, Steve ; Portzky, Gwendolyn ; Psota, Georg ; Qin, Ping ; Radeloff, Daniel ; Reif, Andreas ; Reif-Leonhard, Christine ; Rezaeian, Mohsen ; Román-Vázquez, Nayda ; Roskar, Saska ; Rozanov, Vsevolod ; Sara, Grant ; Scavacini, Karen ; Schneider, Barbara ; Semenova, Natalia ; Sinyor, Mark ; Tambuzzi, Stefano ; Townsend, Ellen ; Ueda, Michiko ; Wasserman, Danuta ; Webb, Roger T. ; Winkler, Petr ; Yip, Paul S. F. ; Zalsman, Gil ; Zoja, Riccardo ; John, Ann ; Spittal, Matthew J.
Background: Predicted increases in suicide were not generally observed in the early months of the COVID-19 pandemic. However, the picture may be changing and patterns might vary across demographic groups. We aimed to provide a timely, granular picture of the pandemic's impact on suicides globally.
Methods: We identified suicide data from official public-sector sources for countries/areas-within-countries, searching websites and academic literature and contacting data custodians and authors as necessary. We sent our first data request on 22nd June 2021 and stopped collecting data on 31st October 2021. We used interrupted time series (ITS) analyses to model the association between the pandemic's emergence and total suicides and suicides by sex-, age- and sex-by-age in each country/area-within-country. We compared the observed and expected numbers of suicides in the pandemic's first nine and first 10-15 months and used meta-regression to explore sources of variation.
Findings: We sourced data from 33 countries (24 high-income, six upper-middle-income, three lower-middle-income; 25 with whole-country data, 12 with data for area(s)-within-the-country, four with both). There was no evidence of greater-than-expected numbers of suicides in the majority of countries/areas-within-countries in any analysis; more commonly, there was evidence of lower-than-expected numbers. Certain sex, age and sex-by-age groups stood out as potentially concerning, but these were not consistent across countries/areas-within-countries. In the meta-regression, different patterns were not explained by countries’ COVID-19 mortality rate, stringency of public health response, economic support level, or presence of a national suicide prevention strategy. Nor were they explained by countries’ income level, although the meta-regression only included data from high-income and upper-middle-income countries, and there were suggestions from the ITS analyses that lower-middle-income countries fared less well.
Interpretation: Although there are some countries/areas-within-countries where overall suicide numbers and numbers for certain sex- and age-based groups are greater-than-expected, these countries/areas-within-countries are in the minority. Any upward movement in suicide numbers in any place or group is concerning, and we need to remain alert to and respond to changes as the pandemic and its mental health and economic consequences continue.
Haenisch, Frieder ; Cooper, Jason D. ; Reif, Andreas ; Kittel-Schneider, Sarah ; Steiner, Johann ; Leweke, F. Markus ; Rothermundt, Matthias ; Beveren, Nico J. M. van ; Crespo-Facorro, Benedicto ; Niebuhr, David W. ; Cowan, David N. ; Weber, Natalya S. ; Yolken, Robert H. ; Penninx, Brenda W. J. H. ; Bahn, Sabine
Highlights
• A panel of 20 biomarkers was identified capable of differentiating BD patients from controls.
• Excellent discrimination between established BD patients and controls.
• Good to excellent discrimination between misdiagnosed BD patients and first onset MDD patients.
• Fair to good discrimination between pre-diagnostic BD patients and controls.
• Study demonstrates the potential utility of a protein biomarker panel as a diagnostic test for BD.
Abstract
Background: Bipolar disorder (BD) is a costly, devastating and life shortening mental disorder that is often misdiagnosed, especially on initial presentation. Misdiagnosis frequently results in ineffective treatment. We investigated the utility of a biomarker panel as a diagnostic test for BD.
Methods and findings: We performed a meta-analysis of eight case-control studies to define a diagnostic biomarker panel for BD. After validating the panel on established BD patients, we applied it to undiagnosed BD patients. We analysed 249 BD, 122 pre-diagnostic BD, 75 pre-diagnostic schizophrenia and 90 first onset major depression disorder (MDD) patients and 371 controls. The biomarker panel was identified using ten-fold cross-validation with lasso regression applied to the 87 analytes available across the meta-analysis studies.
We identified 20 protein analytes with excellent predictive performance [area under the curve (AUC) ⩾ 0.90]. Importantly, the panel had a good predictive performance (AUC 0.84) to differentiate 12 misdiagnosed BD patients from 90 first onset MDD patients, and a fair to good predictive performance (AUC 0.79) to differentiate between 110 pre-diagnostic BD patients and 184 controls. We also demonstrated the disease specificity of the panel.
Conclusions: An early and accurate diagnosis has the potential to delay or even prevent the onset of BD. This study demonstrates the potential utility of a biomarker panel as a diagnostic test for BD.