Mechanisms of DNA Replication, Chromosome Compaction, and Chromosome Unlinking

NIH RePORTER · NIH · R35 · $1,028,611 · view on reporter.nih.gov ↗

Abstract

Summary Accurate transmission of the genetic information requires complete duplication of the chromosomal DNA each cell division cycle. The orderly progression of replication forks is challenged by encounters with template damage, slow moving and arrested RNA polymerases, and frozen DNA-protein complexes that stall the fork. Stalled forks are foci for genomic instability that causes genetic alterations and can give rise to cancer. Stalled forks must be remodeled/repaired and replication restarted/continued in order to maintain genomic stability. We have developed an Escherichia coli DNA replication system that allows us to analyze the consequences of collision of the replisome with leading-strand template damage and with which we can model all aspects of replisome stalling in vitro. In this proposal we investigate the integrated network of responses to DNA damage that the bacterium uses to preserve genomic integrity. We ask: (i) how do stalled forks contribute to induction of the DNA damage (SOS) response? (ii) What is the mechanism of the UmuDC DNA replication checkpoint elaborated by the SOS response? (iii) What are the dynamics of exchange between DNA polymerase IV and DNA polymerase III during replisome-mediated trans-lesion bypass? And (iv), how do replisomes overcome collisions with RNA polymerases that are themselves stalled by DNA template damage. We will begin to apply our expertise to address these questions using human replication proteins and are also expanding our analyses by using single molecule approaches. Coordinating the structural organization of chromosomes is essential for DNA replication, transcription, and chromosome segregation during cell division. Failure to achieve proper chromosomal organization during separation can result in DNA breakage, leading to an uneven distribution of the genetic material to the next generation. Chromosomal organization involves two principal mechanisms: topological maintenance and protein-mediated packaging of the DNA. The former prevents entanglement by regulating the topology of the DNA, resolving unwanted catenanes and knots. The latter shapes the conformation of chromosomes, increasing the efficiency of any particular macromolecular transaction. Our analyses focus on the interaction between the cellular condesin, MukB, and the cellular decatenase topoisomerase IV that we discovered and that we have shown to be required for proper chromosome compaction and segregation. We ask: (i) what is the role of the MukB accessory proteins MukE and MukF and MukB ATP hydrolysis in chromosome compaction? (ii) What are the DNA-MukB-Topo IV structures that are formed that lead to chromosome compaction? (iii) How do defects in chromosome compaction affect DNA metabolic processes such as DNA repair? And (iv) how does the presumptive bacterial cohesin, RecN, function in double-strand break repair and daughter-strand gap repair?

Key facts

NIH application ID
10129200
Project number
5R35GM126907-04
Recipient
SLOAN-KETTERING INST CAN RESEARCH
Principal Investigator
KENNETH J MARIANS
Activity code
R35
Funding institute
NIH
Fiscal year
2021
Award amount
$1,028,611
Award type
5
Project period
2018-04-01 → 2023-03-31