Lack of mitochondrial topoisomerase i (TOP1mt) impairs liver regeneration

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 36, 2015, Pages 11282-11287

  Khiati, Salim ^a   Baechler, Simone A ^a   Factor, Valentina M ^a   Zhang, Hongliang ^a   Huang, Shar Yin N ^a   Rosa, Ilaria Dalla ^a   Sourbier, Carole ^a   Neckers, Leonard ^a   Thorgeirsson, Snorri S ^a   Pommier, Yves ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cell proliferation; Liver regeneration; Mitochondrial DNA replication; Mitochondrial homeostasis; Mitochondrial topoisomerase I

Indexed keywords

CARBON TETRACHLORIDE; DNA TOPOISOMERASE; GLUTATHIONE; MITOCHONDRIAL DNA; MITOCHONDRIAL TOPOISOMERASE 1; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOMA CELL LINE; CELL DIVISION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME DEFICIENCY; FIBROBLAST; HOMEOSTASIS; HUMAN; HUMAN CELL; LIVER CELL; LIVER REGENERATION; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEADY STATE; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; GENE INACTIVATION; GENETICS; HCT 116 CELL LINE; KNOCKOUT MOUSE; LIVER MITOCHONDRION; MAMMALIAN EMBRYO; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; TOXIC HEPATITIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ANIMALS; BLOTTING, WESTERN; CARBON TETRACHLORIDE; CELL PROLIFERATION; CELLS, CULTURED; CHEMICAL AND DRUG INDUCED LIVER INJURY; DNA TOPOISOMERASES, TYPE I; DNA, MITOCHONDRIAL; EMBRYO, MAMMALIAN; FIBROBLASTS; GENE KNOCKOUT TECHNIQUES; GLUTATHIONE; HCT116 CELLS; HEPATOCYTES; HUMANS; LIVER REGENERATION; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA, LIVER; REACTIVE OXYGEN SPECIES;

EID: 84941130373     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1511016112     Document Type: Article

References (39)

1. Bonawitz ND, Clayton DA, Shadel GS (2006) Initiation and beyond: Multiple functions of the human mitochondrial transcription machinery. Mol Cell 24(6):813-825.
2. Champoux JJ (2001) DNA topoisomerases: Structure, function, and mechanism. Annu Rev Biochem 70:369-413.
3. Pommier Y (2013) Drugging topoisomerases: Lessons and challenges. ACS Chem Biol 8(1):82-95.
4. Pommier Y, Leo E, Zhang H, Marchand C (2010) DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem Biol 17(5):421-433.
5. Zhang H, et al. (2014) Increased negative supercoiling of mtDNA in TOP1mt knockout mice and presence of topoisomerases IIα and IIβ in vertebrate mitochondria. Nucleic Acids Res 42(11):7259-7267.
6. Zhang H, et al. (2001) Human mitochondrial topoisomerase I. Proc Natl Acad Sci USA 98(19):10608-10613.
7. Dalla Rosa I, et al. (2009) Adaptation of topoisomerase I paralogs to nuclear and mitochondrial DNA. Nucleic Acids Res 37(19):6414-6428.
8. Zhang H, Pommier Y (2008) Mitochondrial topoisomerase I sites in the regulatory D-loop region of mitochondrial DNA. Biochemistry 47(43):11196-11203.
9. Sobek S, et al. (2013) Negative regulation of mitochondrial transcription by mitochondrial topoisomerase I. Nucleic Acids Res 41(21):9848-9857.
10. Medikayala S, Piteo B, Zhao X, Edwards JG (2011) Chronically elevated glucose compromises myocardial mitochondrial DNA integrity by alteration of mitochondrial topoisomerase function. Am J Physiol Cell Physiol 300(2):C338-C348.
11. Douarre C, et al. (2012) Mitochondrial topoisomerase I is critical for mitochondrial integrity and cellular energy metabolism. PLoS One 7(7):e41094.
12. Lee S, Kim S, Sun X, Lee JH, Cho H (2007) Cell cycle-dependent mitochondrial biogenesis and dynamics in mammalian cells. Biochem Biophys Res Commun 357(1): 111-117.
13. Böhm F, Köhler UA, Speicher T, Werner S (2010) Regulation of liver regeneration by growth factors and cytokines. EMBO Mol Med 2(8):294-305.
14. Mao SA, Glorioso JM, Nyberg SL (2014) Liver regeneration. Transl Res 163(4):352-362.
15. Durand F, et al. (2002) Auxiliary liver transplantation for fulminant hepatitis B: Results from a series of six patients with special emphasis on regeneration and recurrence of hepatitis B. Liver Transpl 8(8):701-707.
16. Manibusan MK, Odin M, Eastmond DA (2007) Postulated carbon tetrachloride mode of action: A review. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 25(3): 185-209.
17. Khiati S, et al. (2014) Mitochondrial topoisomerase I (top1mt) is a novel limiting factor of Doxorubicin cardiotoxicity. Clinical Cancer Res 20(18):4873-4881.
18. Uemitsu N, Nakayoshi H (1984) Evaluation of liver weight changes following a single oral administration of carbon tetrachloride in rats. Toxicol Appl Pharmacol 75(1):1-7.
19. Zoppoli G, et al. (2011) Coordinated regulation of mitochondrial topoisomerase IB with mitochondrial nuclear encoded genes and MYC. Nucleic Acids Res 39(15): 6620-6632.
20. Moraes CT (2001) What regulates mitochondrial DNA copy number in animal cells? Trends Genet 17(4):199-205.
21. Shadel GS, Clayton DA (1997) Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem 66:409-435.
22. Shimuzu M, Morita S, Yamano T, Yamada A (1989) Relationship between hepatic glutathione content and carbon tetrachloride-induced hepatotoxicity in vivo. Toxicol Lett 47(1):95-102.
23. Park CB, et al. (2007) MTERF3 is a negative regulator of mammalian mtDNA transcription. Cell 130(2):273-285.
24. Buchet K, Godinot C (1998) Functional F1-ATPase essential in maintaining growth and membrane potential of human mitochondrial DNA-depleted rho degrees cells. J Biol Chem 273(36):22983-22989.
25. Kao CY, Factor VM, Thorgeirsson SS (1996) Reduced growth capacity of hepatocytes from c-myc and c-myc/TGF-alpha transgenic mice in primary culture. Biochem Biophys Res Commun 222(1):64-70.
26. Wanson JC, Drochmans P, Mosselmans R, Ronveaux MF (1977) Adult rat hepatocytes in primary monolayer culture. Ultrastructural characteristics of intercellular contacts and cell membrane differentiations. J Cell Biol 74(3):858-877.
27. Dalla Rosa I, et al. (2014) Mapping topoisomerase sites in mitochondrial DNA with a poisonous mitochondrial topoisomerase I (Top1mt). J Biol Chem289(26):18595-18602.
28. Meyer RR, Simpson MV (1969) DNA biosynthesis in mitochondria. Differential inhibition of mitochondrial and nuclear DNA polymerases by the mutagenic dyes ethidium bromide and acriflavin. Biochem Biophys Res Commun 34(2):238-244.
29. Leibowitz RD (1971) The effect of ethidium bromide on mitochondrial DNA synthesis and mitochondrial DNA structure in HeLa cells. J Cell Biol 51(1):116-122.
30. Guerrieri F, et al. (1995) Correlation between rat liver regeneration and mitochondrial energy metabolism. Biochim Biophys Acta 1272(2):95-100.
31. Russell AP, Foletta VC, Snow RJ, Wadley GD (2014) Skeletal muscle mitochondria: A major player in exercise, health and disease. Biochim Biophys Acta 1840(4):1276-1284.
32. Gonzalvez F, et al. (2013) Barth syndrome: Cellular compensation of mitochondrial dysfunction and apoptosis inhibition due to changes in cardiolipin remodeling linked to tafazzin (TAZ) gene mutation. Biochim Biophys Acta 1832(8):1194-1206.
33. Diaz F, Moraes CT (2008) Mitochondrial biogenesis and turnover. Cell Calcium 44(1): 24-35.
34. Wang Y, Lyu YL, Wang JC (2002) Dual localization of human DNA topoisomerase IIIalpha to mitochondria and nucleus. Proc Natl Acad Sci USA 99(19):12114-12119.
35. Wu J, Feng L, Hsieh TS (2010) Drosophila topo IIIalpha is required for the maintenance of mitochondrial genome and male germ-line stem cells. Proc Natl Acad Sci USA 107(14):6228-6233.
36. Medja F, et al. (2009) Development and implementation of standardized respiratory chain spectrophotometric assays for clinical diagnosis. Mitochondrion 9(5):331-339.
37. Yang Y, et al. (2010) UOK 262 cell line, fumarate hydratase deficient (FH-/FH-) hereditary leiomyomatosis renal cell carcinoma: in Vitro and in vivo model of an aberrant energy metabolic pathway in human cancer. Cancer Genet Cytogenet 196(1): 45-55.
38. Cong L, et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819-823.
39. Loiseau D, et al. (2007) Mitochondrial coupling defect in Charcot-Marie-Tooth type 2A disease. Ann Neurol 61(4):315-323.