Sunday, July 9, 2017

5. Novel insights into RAD51 activity and regulation during homologous recombination and DNA replication


Stephen K. Godin, Meghan R. Sullivan, Kara A. Bernstein. Review paper. 2016. 

IR induces DSB
MMS induces replicative stress

This paper focuses on understanding the homologous recombination under Rad51 regulation. Rad51 filament formation/presynaptic filament/nucleoprotein formation is well regulated to avoid unnecessary recombination and genomic instability.

In budding yeast, the Rad51 regulators include Rad51 mediators, scRad52, 2xRad51 paralogues, scRad55 and scRAd57. In budding yeast (sc), Rad51 regulators help to overcome the barrier by replication protein A (RPA) coating the 3' overhanging ssDNA after the resection. However the RPA removal mechanism is not clearly understood.

Human Rad51 paralogues form 3 complexes. The BCDX2 complex is composed of hRAD52B, hRAD51C, hRAD51D and hXRCC2. The XC3 complex is composed of hRAD51C and hXRCC3. Shu complex is composed of the hSWSAP1 (one of the RAD51 paralogues)  and the hSWS1.

scRAD52 is analogous to hBRAC2 in their sequences so it plays similar role in RAD51 foci formation, but hRAD52 also exists in human

scRAD51 containing Walker A and Walker B ATP binding motifs that only bind ATP-bound ssDNA. There are other anti-recombinase proteins that prevent the illegitimate HR to ensure that RAD51 filament is only formed at the DNAdamage sites in order to avoid excess recombination and DNA instability.

When the scRAD51 filament is established, the strand invasion can start on dsDNA to search for homologous stretch of DNA. Once scRad51 filament passes 15-nucleotide threshold, it stops sampling another dsDNA and becomes committed to the replication based on the target dsDNA. Then, scRAD51 was dissembled by scRAD54 to allow the invasion of DNA polymerase to the heteroduplex to extend the invading ssDNA up to 1700 bp. In human, hRAD54 was also known to direct hRAD51 invasion and disassemble hRAD51 from the ssDNA to allow DNA pol to start its job.



In the simplest form of repair, synthesis dependent strand annealing (SDSA) or double Holliday junction (DHJ) or break-induced replication (BIR) can take over the role to produce cross-over or non-cross-over products as represented in the diagram.


























DNA lesions can initiate homologous recombination at the replication fork by stalling the DNA or inhibiting the progression of the replication fork. Each lesion is repaired by a different mechanism. Her we focus on HR at stalled replication fork. DNA alkylating agent methylmethane sulfonate (MMS) can result in DNA lesion that requires HR to DNA repair. During HR, a X-structure was formed by scRAD51 and accumulates in the absence of scSGS1. Interstingly, HR in MMS-induced DNA lesion occurs at gapped ssDNA but not free ssDNA ends. 
  
















hRAD51C and hRAD51 were considered as Fanconi anemia but truncated hXRCC2 was also detected in this disorder. 

Mouse KO models have resulted in embryonic lethality, making our understanding of mammalian RAD51 paralogues limited to specific cell lines. Disruption in any RAD51 paralogues can result in chromosomal instabiloty, increases in MMC sensitivity, and decreases in cell survival.

In human cell lines, osteosarcoma U2OS and breast cancer MCF7, the BCDX2 and CX3 perform different functions at different stages in HR. BCDX2 is important for upstream of hRAD51 filament formation while CX3 is essential for downstream hRAD51 foci formation in response to IR. Depletion of either BCDX2 or CX3 complex caused a decease in HR at an Depletion of both BCDX2 and CX3 complexes did not yield additive effect on levels of hRAD51 filament formation.

Recruitment of hBRCA2 is independent of both BCDX2 and CX3 during IR-induced HR (because PALB2 and BRCA2 forms a complex at the damage sites (Park et al., 2014)), BUT hBRCA2 is epistatic (needed) for RAD51 paralogues to accumulate at the DSB. RAD51 paralogues are not epistatic with hRAD52, which performs a different function from BRCA2 does. Depletion of hRAD52 with hXRCC3 caused synthetic lethality and decreased HR rates, saying that hRAD52 and hRAD51 paralogues function in different pathways [So hRAD52 does not promote HR which is RAD51 dependent????? When does hBRCA2 and hRAD52 compete in repairing damaged DNA????]

RAD51 paralogues respond to damaged replication fork by performing these functions:
     "1) Protect nascent ssDNA at stalled forks from resection
       2) Prevent replication fork collapse 
       3) Facilitate replication restart"

Shu complex is an obligate heterotetramer comprised of scShu2, scShu1, scCsm2, and scPsy3. Disruption of any Shu components will result in increase sensitivity in replication fork stalling. The Shu complex is likely to act upstream of hRAD54, suggesting that this complex may play a role in hRAD51 filament formation. The scCsm2 and scPsy3 were crystalized and found to mediate the Shu complex in binding DNA and are structural scRad51 even though it does not share much sequence homology with scRAD51. The Shu complex interacts with the scRad1 filament machinery via Rad55-Rad57 bridge in presence of scRad52. Since scSrs2 interacts with the ATPase domain of scRad51, causing ARRP to hydrolyze, leading to the inability of scRad51 to bind to DNA,  scRad55-Rad57 can directly prevent scSrs2 from destablizing Rad51 filament in vitro. These results present a direct role for the Shu complex in scRad51 filament formation. 

"hRAD51C and hXRCC3 were found to assemble into an additional complex that is scaffolded by hPALP2, termed the "HR complex" comprised of hPALP2, hRAD51C, hRAD51, hBRCA2 and hXRCC3 (Park et al., 2014)." Heterozygous mutations in hPALB2, hBRCA2, and hRAD51C can lead to hereditary breast and ovarian cancers because of the lost WT copy. Homozygous mutations in hPALP2 (FANCN), hBRCA2 (FANCD1), and hRAD51C (FANCO) can lead to FA condition. 

IR-induce DSB causes disruption in hRAD51 which will inhibit HR pathway and promotes NHEJ pathway. tumors with disrupted hRAD51 can be targeted by PARP inhibition. However, mutation in hRAD51 in combination with PARPi can result in collapsing replication fork and activation of error-prone NHEJ pathway which can increase cell death. Therefore, clinical practice need to consider if using PARPi is safe to treat breast and ovarian cancers. 




















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