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DNA Repair and Mutagenesis in Vertebrate Mitochondria: Evidence for Asymmetric DNA Strand Inheritance

Matkarimov, Bakhyt T., Saparbaev, Murat K.·2020·Advances in Experimental Medicine and Biology
DOI 10.1007/978-3-030-41283-8_6
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Figure 1 Schematic presentation of DNA damage induced by endogenous and exogenous factors. ( A ) Chemical structures of singular DNA base and sugar damages induced by oxygen free radicals. ( B ) Chemical structures of complex DNA damage having bulky and clustered characters.
Figure 1 Schematic presentation of DNA damage induced by endogenous and exogenous factors. ( A ) Chemical structures of singular DNA base and sugar damages induced by oxygen free radicals. ( B ) Chemical structures of complex DNA damage having bulky and clustered characters.CC-BY-NC-ND · From the PDF
Figure 2 The base excision repair (BER) and nucleotide incision repair (NIR): two alternative DNA repair pathways for oxidative damage to mitochondrial DNA. (1-5) Upstream and (6-9) downstream steps of the BER and NIR pathways. In BER, (1) human bi-functional DNA glycosylase/AP lyase, hNTHL1 excises 5-hydroxyuracil (5ohU) residue in DNA resulting in formation of a free 5ohU base and single-strand break in form of one nucleotide gap containing a 3 ′ -α , β -unsaturated aldehyde and a 5 ′ -phosphate; (2) the 3 ′ repair diesterase activity of human APE1 removes 3 ′ -blocking group to generate 3 ′ -OH terminus; (2) human mitochondrial monofunctional uracil-DNA glycosylase 1, UNG1 excises uracil (U) residue in DNA resulting in formation of a free U base and abasic site (AP); (4) APE1 cleaves duplex DNA at the 5 ′ of AP site yielding a single-strand break with a 3 ′ hydroxyl adjacent to a 5 ′ deoxyribosephosphate (5dRp); In NIR, (5) APE1 directly cleaves 5 ′ next to 5ohU base generating single-strand nick containing a 3 ′ -OH and a 5 ′ -phosphate with dangling base. (6) In the SP-BER pathway DNA polymerase γ insert a single nucleotide and removes the 5 ′ -dRp blocking residue, then DNA ligase III α seals the single-strand nick; (7-8) In the LP-BER and NIR pathways DNA polymerase γ initiates strand-displacement repair synthesis, coupled to DNA2- and FEN1-catalyzed cleavage of unannealed 5'-flap structures containing 5 ′ -dRp residue in BER and 5 ′ -dangling base in NIR pathway, respectively; (9) DNA ligase III α seals the single-strand nicks and restores genetic integrity of mtDNA.
Figure 2 The base excision repair (BER) and nucleotide incision repair (NIR): two alternative DNA repair pathways for oxidative damage to mitochondrial DNA. (1-5) Upstream and (6-9) downstream steps of the BER and NIR pathways. In BER, (1) human bi-functional DNA glycosylase/AP lyase, hNTHL1 excises 5-hydroxyuracil (5ohU) residue in DNA resulting in formation of a free 5ohU base and single-strand break in form of one nucleotide gap containing a 3 ′ -α , β -unsaturated aldehyde and a 5 ′ -phosphate; (2) the 3 ′ repair diesterase activity of human APE1 removes 3 ′ -blocking group to generate 3 ′ -OH terminus; (2) human mitochondrial monofunctional uracil-DNA glycosylase 1, UNG1 excises uracil (U) residue in DNA resulting in formation of a free U base and abasic site (AP); (4) APE1 cleaves duplex DNA at the 5 ′ of AP site yielding a single-strand break with a 3 ′ hydroxyl adjacent to a 5 ′ deoxyribosephosphate (5dRp); In NIR, (5) APE1 directly cleaves 5 ′ next to 5ohU base generating single-strand nick containing a 3 ′ -OH and a 5 ′ -phosphate with dangling base. (6) In the SP-BER pathway DNA polymerase γ insert a single nucleotide and removes the 5 ′ -dRp blocking residue, then DNA ligase III α seals the single-strand nick; (7-8) In the LP-BER and NIR pathways DNA polymerase γ initiates strand-displacement repair synthesis, coupled to DNA2- and FEN1-catalyzed cleavage of unannealed 5'-flap structures containing 5 ′ -dRp residue in BER and 5 ′ -dangling base in NIR pathway, respectively; (9) DNA ligase III α seals the single-strand nicks and restores genetic integrity of mtDNA.CC-BY-NC-ND · From the PDF
Figure 3 The model of mtDNA replication leading to asymmetrical DNA strand inheritance. ( 1 ) The mtDNA is anchored to inner membrane of mitochondria via interaction of D-loop region with a specific site in the membrane; ( 2 ) The asynchronous replication of leading Hstrand (blue arrow) at O H site proceeds unidirectionally to displace parental H-strand. When the O L site is exposed, the lagging L-strand (red arrow) replication initiates in opposite direction; ( 3 ) Replication of leading H-strand proceeds further and terminates at O H before the lagging L-strand reach this site. Premature termination of H-strand synthesis produces a hemicatenane: two-ring molecules mechanically interlocked via single-stranded linkage (Laurie et al. 1998); ( 4 ) Replication of lagging L-strand terminates at O L site to complete the formation of a double-stranded hemicatenane composed of two interlocked mtDNA molecules. The hemicatenane is unlinked by mitochondrial Toposiomerase III α to produce two separate mtDNA molecule one containing parental H-strand and the other parental Lstrand; ( 5 ) The mtDNA molecule containing old parental L-strand diffuses freely across mitochondrial matrix and may anchor to inner membrane through the expression of OXPHOS complex proteins (Lynch and Wang 1993); ( 6 ) The mtDNA molecule containing old parental H-strand stays attached to a specific site in the inner membrane and continues to replicate.
Figure 3 The model of mtDNA replication leading to asymmetrical DNA strand inheritance. ( 1 ) The mtDNA is anchored to inner membrane of mitochondria via interaction of D-loop region with a specific site in the membrane; ( 2 ) The asynchronous replication of leading Hstrand (blue arrow) at O H site proceeds unidirectionally to displace parental H-strand. When the O L site is exposed, the lagging L-strand (red arrow) replication initiates in opposite direction; ( 3 ) Replication of leading H-strand proceeds further and terminates at O H before the lagging L-strand reach this site. Premature termination of H-strand synthesis produces a hemicatenane: two-ring molecules mechanically interlocked via single-stranded linkage (Laurie et al. 1998); ( 4 ) Replication of lagging L-strand terminates at O L site to complete the formation of a double-stranded hemicatenane composed of two interlocked mtDNA molecules. The hemicatenane is unlinked by mitochondrial Toposiomerase III α to produce two separate mtDNA molecule one containing parental H-strand and the other parental Lstrand; ( 5 ) The mtDNA molecule containing old parental L-strand diffuses freely across mitochondrial matrix and may anchor to inner membrane through the expression of OXPHOS complex proteins (Lynch and Wang 1993); ( 6 ) The mtDNA molecule containing old parental H-strand stays attached to a specific site in the inner membrane and continues to replicate.CC-BY-NC-ND · From the PDF

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Authors
Matkarimov, B. T., & Saparbaev, M. K.
Venue
Advances in Experimental Medicine and Biology
Publisher
Springer International Publishing
Published
2020
Pages
77-100
ISSN
  • 0065-2598
  • 2214-8019
DOI
10.1007/978-3-030-41283-8_6
Cited by
18
References
19
Language
en
Licence
www.springer.com/tdm (tdm)

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