Identification of Low-molecular-weight Vitellogenin 1 (Vg1)-like Proteins As Nucleotide Excision Repair (NER) Factors in Developing Zebrafish (Danio Rerio) Using a Transcription-based DNA Repair Assay

Overview

Journal Fish Physiol Biochem

Specialty Biochemistry

Date 2017 Jan 12

PMID 28074418

Citations 1

Authors

Yung-Chi Shen

Todd Hsu

Li-Bin Ling

Wen-Chian You

Chia-Wei Liu

Affiliations

Soon will be listed here.

Abstract

Nucleotide excision repair (NER) removes helix-distorting DNA lesions such as UV-induced pyrimidine dimers and cisplatin-induced strand crosslinking. Our earlier studies have identified low-molecular-weight proteins homologous to the 150-kDa vitellogenin 1 (Vg1) as UV-damaged DNA-binding factors expressed in developing zebrafish (Danio rerio). This present study explored if Vg1-like proteins also participated in NER in zebrafish. Immunoblot analysis of affinity-captured 12 h post-fertilization (hpf) zebrafish extract proteins showed a transient binding of a 30-kDa Vg1-like polypeptide to UV-damaged DNA. A transcription-based in vitro repair assay revealed a significant up-regulation of UVC or cisplatin-suppressed transcriptional activity of a marker cDNA driven by a SP6 RNA polymerase-regulated promotor after incubating the damaged plasmid with the extracts of 12 hpf embryos or 96 hpf larvae. The up-regulation of UV or cisplatin-suppressed transcription was abolished in the presence of a monoclonal anti-zebrafish Vg1 antibody. The differential sensitivity of UV-induced repair in 12 and 96 hpf zebrafish extracts to exogenous ATP suggested a development-dependent expression of Vg1-like NER factors. A T endonuclease V digestion assay showed no inhibition of the anti-Vg1 antibody on the excision of UV-induced cyclobutane pyrimidine dimers. Our results identified the participation of Vg1-like factors in NER in developing zebrafish, and these factors may function at post-incison steps of NER.

Citing Articles

DNA repair genes play a variety of roles in the development of fish embryos.

Dey A, Flajshans M, Psenicka M, Gazo I Front Cell Dev Biol. 2023; 11:1119229.

PMID: 36936683 PMC: 10014602. DOI: 10.3389/fcell.2023.1119229.

References

Radany E, Friedberg E . A pyrimidine dimer-DNA glycosylase activity associated with the v gene product of bacterophage T4. Nature. 1980; 286(5769):182-5. DOI: 10.1038/286182a0. View

Guo C, Tang T, Friedberg E . SnapShot: nucleotide excision repair. Cell. 2010; 140(5):754-4.e1. DOI: 10.1016/j.cell.2010.02.033. View

Gillet L, Scharer O . Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev. 2006; 106(2):253-76. DOI: 10.1021/cr040483f. View

Qiao Y, Spitz M, Guo Z, Hadeyati M, Grossman L, Kraemer K . Rapid assessment of repair of ultraviolet DNA damage with a modified host-cell reactivation assay using a luciferase reporter gene and correlation with polymorphisms of DNA repair genes in normal human lymphocytes. Mutat Res. 2002; 509(1-2):165-74. DOI: 10.1016/s0027-5107(02)00219-1. View

Zeng Z, Richardson J, Verduzco D, Mitchell D, Patton E . Zebrafish have a competent p53-dependent nucleotide excision repair pathway to resolve ultraviolet B-induced DNA damage in the skin. Zebrafish. 2010; 6(4):405-15. PMC: 2804931. DOI: 10.1089/zeb.2009.0611. View

Sugasawa K, Okamoto T, Shimizu Y, Masutani C, Iwai S, Hanaoka F . A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 2001; 15(5):507-21. PMC: 312644. DOI: 10.1101/gad.866301. View

Wang H, Tan J, Emelyanov A, Korzh V, Gong Z . Hepatic and extrahepatic expression of vitellogenin genes in the zebrafish, Danio rerio. Gene. 2005; 356:91-100. DOI: 10.1016/j.gene.2005.03.041. View

Sugasawa K, Okuda Y, Saijo M, Nishi R, Matsuda N, Chu G . UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell. 2005; 121(3):387-400. DOI: 10.1016/j.cell.2005.02.035. View

Vichi P, Coin F, Renaud J, Vermeulen W, Hoeijmakers J, Moras D . Cisplatin- and UV-damaged DNA lure the basal transcription factor TFIID/TBP. EMBO J. 1998; 16(24):7444-56. PMC: 1170344. DOI: 10.1093/emboj/16.24.7444. View

10.

Groche D, Rashkovetsky L, Falchuk K, Auld D . Subunit composition of the zinc proteins alpha- and beta-lipovitellin from chicken. J Protein Chem. 2000; 19(5):379-87. DOI: 10.1023/a:1026487414167. View

11.

Amacher S . Emerging gene knockout technology in zebrafish: zinc-finger nucleases. Brief Funct Genomic Proteomic. 2008; 7(6):460-4. PMC: 2722258. DOI: 10.1093/bfgp/eln043. View

12.

Lai Y, Hsieh F, Hsu T . Affinity isolation and mass spectral analysis of 1,10-phenanthroline (OP)-stimulated UV-damaged-DNA binding proteins expressed in zebrafish (Danio rerio) embryos. Fish Physiol Biochem. 2012; 38(4):1117-1129. DOI: 10.1007/s10695-011-9598-5. View

13.

Hanawalt P, Spivak G . Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol. 2008; 9(12):958-70. DOI: 10.1038/nrm2549. View

14.

Tong Y, Shan T, Poh Y, Yan T, Wang H, Lam S . Molecular cloning of zebrafish and medaka vitellogenin genes and comparison of their expression in response to 17beta-estradiol. Gene. 2004; 328:25-36. DOI: 10.1016/j.gene.2003.12.001. View

15.

Fortier S, Yang X, Wang Y, Bennett R, Strauss P . Base excision repair in early zebrafish development: evidence for DNA polymerase switching and standby AP endonuclease activity. Biochemistry. 2009; 48(23):5396-404. PMC: 2731577. DOI: 10.1021/bi900253d. View

16.

Tang J, Chu G . Xeroderma pigmentosum complementation group E and UV-damaged DNA-binding protein. DNA Repair (Amst). 2003; 1(8):601-16. PMC: 2894533. DOI: 10.1016/s1568-7864(02)00052-6. View

17.

Kang T, Reardon J, Sancar A . Regulation of nucleotide excision repair activity by transcriptional and post-transcriptional control of the XPA protein. Nucleic Acids Res. 2011; 39(8):3176-87. PMC: 3082913. DOI: 10.1093/nar/gkq1318. View

18.

Koberle B, Grimaldi K, Sunters A, Hartley J, Kelland L, Masters J . DNA repair capacity and cisplatin sensitivity of human testis tumour cells. Int J Cancer. 1997; 70(5):551-5. DOI: 10.1002/(sici)1097-0215(19970304)70:5<551::aid-ijc10>3.0.co;2-g. View

19.

Montorzi M, Falchuk K, Vallee B . Vitellogenin and lipovitellin: zinc proteins of Xenopus laevis oocytes. Biochemistry. 1995; 34(34):10851-8. DOI: 10.1021/bi00034a018. View

20.

Kimmel C, Ballard W, Kimmel S, Ullmann B, Schilling T . Stages of embryonic development of the zebrafish. Dev Dyn. 1995; 203(3):253-310. DOI: 10.1002/aja.1002030302. View