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Lingner, J.

Publications and source records attributed to Lingner, J..

7 recordsLinked to original sources

Medulloblastoma-Associated KBTBD4 Mutations Disrupt PP2A-A Orphan Quality Control

Medulloblastoma, the most common malignant pediatric brain tumor, arises from developmental aberrations of cerebellar precursor cells. The CUL3-RING ubiquitin ligase adaptor KBTBD4 is recurrently mutated in medulloblastoma subgroups 3 and 4. While KBTBD4 mutations confer a gain-of-function phenotype leading to aberrant degradation of transcriptional repressors, endogenous targets of this E3 ligase remain unknown. Here, we identify the PP2A-A scaffolding subunit of the PP2A phosphatase as a CRL3KBTBD4 substrate. Using a combination of proteomics, cell biology, biochemical reconstitution, and cryo-EM structural analyses, we show that CRL3KBTBD4 mediates orphan quality control by targeting free PP2A-A for degradation to safeguard phosphatase activity. Loss of KBTBD4 or its mutation in medulloblastoma cause PP2A-A accumulation, hence affecting phospho-dependent signaling pathways in cancer development. Disease mutations in KBTBD4 thus elicit a dual phenotype: gain-of-function degradation of transcriptional repressors combined with loss of PP2A quality control, which dysregulates multiple signaling events implicated in cancer, including telomere length regulation.

cell biology↗

Rescue from pyridostatin-stabilized telomeric G-quadruplexes by DNA cleavage and microhomology-mediated end joining

G-quadruplexes are four-stranded nucleic acid structures that are formed by guanine rich sequences. They have been implicated to interfere with telomere maintenance, but their effects are not well understood at a molecular level. Here, we treat human cells with the G-quadruplex stabilizer and anti-cancer drug-candidate pyridostatin and characterize its effects on telomere replication and maintenance. We demonstrate that pyridostatin interferes with lagging strand DNA synthesis during semiconservative replication of telomeres. Pyridostatin impedes replication fork progression and triggers telomere cleavage events involving the Flap-endonuclease FEN1 and the nuclease-helicase DNA2. Telomeric protein composition analysis reveals pyridostatin-induced association of LIG3 with telomeres. This enzyme is involved in repair of DNA double strand breaks by microhomology-mediated end joining (MMEJ). Depletion of MMEJ-factors or their chemical inhibition enhances telomere loss events in pyridostatin-treated cells. Altogether, our data reveal a three-step mechanism in which pyridostatin-stabilized G-quadruplexes inhibit replication of lagging strand telomeres, which is overcome by FEN1/DNA2-mediated DNA cleavage and MMEJ-mediated DNA repair. The synthetic effects of pyridostatin and MMEJ inhibition on telomere maintenance may become exploitable in future anti-cancer therapies.

molecular biology↗

TERRA R-loops trigger a switch in telomere maintenance towards break-induced replication and PrimPol-dependent repair

TERRA long noncoding RNAs associate with telomeres post transcription through base-pairing with telomeric DNA forming R-loop structures. TERRA regulates telomere maintenance but its exact modes of action remain unknown. Here, we induce TERRA transcription and R-loop formation in telomerase-expressing cells and determine that TERRA R-loop formation requires non-redundant functions of the RAD51 DNA recombinase and its enhancer RAD51AP1. TERRA R-loops interfere with semiconservative DNA replication promoting telomere maintenance by a homology-directed repair (HDR) mechanism known as Break Induced Replication (BIR), which ensures telomere maintenance in ALT cancer cells. In addition, TERRA induced PrimPol-dependent repair, which can initiate DNA synthesis de novo downstream of replication obstacles. PrimPol acts in parallel to BIR for telomere maintenance of TERRA over-expressing cells promoting their survival. Similarly, we find that PrimPol depletion is synthetic lethal with BIR deficiency in U2OS ALT cancer cells. Therefore, in the absence of other ALT-typical telomeric chromatin changes, TERRA R-loops per se are sufficient to induce ALT-typical telomere repair mechanisms.

molecular biology↗

The Human Telomeric Proteome During Telomere Replication

Telomere shortening can cause detrimental diseases and contribute to aging. It occurs due to the end replication problem in cells lacking telomerase. Furthermore, recent studies revealed that telomere shortening can be attributed to difficulties of the semi-conservative DNA replication machinery to replicate through the bulk of telomeric DNA repeats. To investigate telomere replication in a comprehensive manner, we develop QTIP-iPOND, which enables purification of proteins that associate with telomeres specifically during replication. We identify in addition to the core replisome a large number of proteins that associate with telomere replication forks and validate their importance. We find that POT1 is depleted, whereas histone H1 is specifically enriched, at telomere replication forks. Our work reveals the dynamic changes of the telomeric proteome during replication, providing a valuable resource of telomere replication proteins. To our knowledge, this is the first study that examines the replisome at a specific region of the genome.

biochemistry↗

RADX Sustains POT1 Function at Telomeres to Counteract RAD51 Binding, which Triggers Telomere Fragility

The 3 terminal DNA extensions at chromosome ends can become engaged into multiple biochemical reactions during DNA replication, telomerase-mediated telomere extension, homology directed DNA repair, nucleolytic processing and DNA damage checkpoint activation. To keep these activities in check, telomeric 3 overhangs can be hidden in t-loop structures or they associate with specialized proteins such as POT1. Here, we explore the telomeric microenvironment using a proximity-dependent labeling approach and identify the oligonucleotide/oligosaccharide-binding (OB)-fold containing protein RADX. RADX binds single-stranded telomeric DNA throughout the cell cycle along with POT1, suppressing accumulation of fragile telomeres, which are indicative of telomere replication defects. Telomere fragility in POT1 and RADX double-depleted cells was due to accumulation of the RAD51 recombinase at telomeres. RADX also supports DNA damage signaling at POT1-depleted telomeres counteracting RAD51 binding. Thus, RADX represents next to POT1 a second OB-fold containing single-strand telomere binding protein sustaining telomere protection.

molecular biology↗

Human POT1 Prevents Severe Telomere Instability Induced by Homology Directed DNA Repair

The evolutionarily conserved POT1 protein binds single stranded G-rich telomeric DNA and has been implicated in contributing to telomeric DNA maintenance and the suppression of DNA damage checkpoint signaling. Here, we explore human POT1 function through genetics and proteomics discovering that the complete absence of POT1 leads to severe telomere maintenance defects that had not been anticipated from previous depletion studies. Conditional deletion of POT1 in HEK293E cells gives rise to rapid telomere elongation and length heterogeneity, branched telomeric DNA structures, telomeric R-loops and telomere fragility. We determine the telomeric proteome upon POT1-loss implementing an improved telomeric chromatin isolation protocol. We identify a large set of proteins involved in nucleic acid metabolism that engage with telomeres upon POT1-loss. Inactivation of the homology directed repair machinery suppresses POT1-loss mediated telomeric DNA defects. Our results unravel as major function of human POT1 the suppression of telomere instability induced by homology directed repair.

molecular biology↗

SMCHD1 Promotes ATM-dependent DNA Damage Signaling and Repair of Uncapped Telomeres

SMCHD1 (structural maintenance of chromosomes flexible hinge domain containing protein 1) has been implicated in X-chromosome inactivation, imprinting and DNA damage repair. Mutations in SMCHD1 can also cause facioscapulohumoral muscular dystrophy. More recently, SMCHD1 has also been detected as component of telomeric chromatin. Here, we identify requirements of SMCHD1 for DNA damage signaling and non-homologous end joining (NHEJ) at unprotected telomeres. Co-depletion of SMCHD1 with TRF2 reduced the rate of 3 overhang removal in time course experiments and the number of telomere end fusions. In SMCHD1 deficient cells, the formation of ATM pS1981, {gamma}H2AX and 53BP1 containing telomere dysfunction induced foci (TIFs) were diminished indicating defects in checkpoint signaling. Strikingly, removal of TPP1 and subsequent activation of ATR signaling rescued telomere fusion events in TRF2-depleted SMCHD1 knockout cells. Together, these data indicate that SMCHD1 depletion reduces telomere fusions in TRF2-depleted cells due to defects in ATM-dependent DNA checkpoint signaling. SMCHD1 mediates DNA damage signaling activation upstream of ATM phosphorylation at uncapped telomeres.

molecular biology↗