Nuclear α Spectrin Differentially Affects Monoubiquitinated Versus Non-Ubiquitinated FANCD2 Function after DNA Interstrand Cross-Link Damage

Journal of Cellular Biochemistry

Volumn 117, Issue 3, 2016, Pages 671-683

  Zhang, Pan ^a,b   Sridharan, Deepa ^a,c   Lambert, Muriel W ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

DNA DAMAGE; DNA INTERSTRAND CROSS LINKS; DNA REPAIR; FANCD2; FANCONI ANEMIA; NON UBIQUITINATED FANCD2; NONERYTHROID ALPHA SPECTRIN; NUCLEAR SPECTRIN; XPF

Indexed keywords

CALPAIN; FANCONI ANEMIA GROUP D2 PROTEIN; FODRIN; CHROMATIN; DNA BINDING PROTEIN; FANCD2 PROTEIN, HUMAN; SPECTRIN; UBIQUITINATED PROTEIN; XERODERMA PIGMENTOSUM GROUP F PROTEIN;

ARTICLE; CELL NUCLEUS; CHROMATIN; CONTROLLED STUDY; DISSOCIATION; DNA CROSS LINKING; DNA DAMAGE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; UBIQUITINATION; CELL LINE; METABOLISM; PROTEIN TRANSPORT;

CELL LINE; CELL NUCLEUS; CHROMATIN; DNA DAMAGE; DNA-BINDING PROTEINS; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; HUMANS; PROTEIN TRANSPORT; SPECTRIN; UBIQUITINATED PROTEINS; UBIQUITINATION;

EID: 84955388133     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25352     Document Type: Article

References (51)

1. Akkari YM, Bateman RL, Reifsteck C, Olson SB, Grompe M,. 2000. DNA replication is required to elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol Cell Biol 20: 8283-8289.
2. Al-Minawi AZ, Lee Y-F, Hakansson D, Johansson F, Lundin C, Saleh-Gohari N, Schultz N, Jenssen D, Bryant HE, Meuth M, Hinz JM, Helleday T,. 2009. The ERCC1/XPF endonuclease is required for completion of homologous recombination at DNA replication forks stalled by inter-strand cross-links. Nucleic Acids Res 37: 6400-6413.
3. Alpi AF, Patel KJ,. 2009. Monoubiquitylation in the Fanconi anemia DNA damage response pathway. DNA Repair 8: 430-435.
4. Bhagwat N, Olsen AL, Wang AT, Hanada K, Stuckert P, Kanaar R, D'Andrea A, Niedernhofer LJ, McHugh PJ,. 2009. XPF-ERCC1 participates in the Fanconi anemia pathway of cross-link repair. Mol Cel Biol 29: 6427-6437.
5. Bogliolo M, Lyakhovich A, Callen E, Castella M, Cappelli E, Ramirez MJ, Creus A, Marcos R, Kalb R, Neveling K, Schindler D, Surralles J,. 2007. Histone H2AX and Fanconi anemia FANCD2 function in the same pathway to maintain chromosome stability. EMBO J 26: 1340-1351.
6. de Oca RM, Andreassen PR, Margossian SP, Gregory RC, Taniguchi T, Wang X, Houghtaling S, Grompe M, D'Andrea AD,. 2000. Regulated interaction of the Fanconi anemia protein, FANCD2, with chromatin. Blood 105: 1003-1009.
7. de Winter JP, Joenje H,. 2009. The genetic and molecular basis of Fanconi anemia. Mutat Res 668: 11-19.
8. Garcia-Higuera I, Taniguchi T, Ganesan S, Meyn MS, Timmers C, Hejna J, Grompe M, d'Andrea AD,. 2001. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 7: 249-262.
9. Gregory RC, Tankguchi T, D'Andrea AD,. 2003. Regulation of the Fanconi anemia pathway by monoubiquitination. Semin Cancer Biol 13: 77-82.
10. Ho ATV, Scharer OD,. 2010. Translesion DNA synthesis polymerases in DNA interstrand crosslink repair. Environ Mol Mutatgen 51: 552-566.
11. Hussain S, Wilson JB, Blom W, Thompson LH, Sung P, Gordon SM, Kupfer GM, Joenje H, Mathew CG, Jones NJ,. 2006. Tetratricopeptide-motif-mediated interaction of FANCG with recombination proteins XRCC3 and BR CA2. DNA Repair 5: 629-640.
12. Kachnic LA, Li L, Fournier L, Willers H,. 2010. Fanconi anemia pathway revealed by cisplatin and oxaliplatin treatments. Cancer Lett 292: 73-79.
13. Kim H, D'Andrea AD,. 2012. Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev 26: 1393-1408.
14. Klein Douwel D, Boon RACM, Long DT, Szypowska AA, Raschle M, Walter JC, Knipscheer P,. 2014. XPF-ERCC1 acts in unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/S LX4. Mol Cell 54: 460-471.
15. Knipscheer P, Raschle M, Smogorzewska A, Enoiu M, Ho TV, Scharer OD, Elledge SJ, Walter JC,. 2009. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 326: 1698-1701.
16. Kottemann MC, Smogorzewska A,. 2013. Fanconi anaemia and the repair of Watson and Crick DNA crosslinks. Nature 493: 356-363.
17. Kumaresan KR, Hang B, Lambert MW,. 1995. Human endonucleolytic incision of DNA 3' and 5' to a site-directed psoralen monoadduct and interstrand cross-link. J Biol Chem 270: 30709-30716.
18. Kumaresan KR, Lambert MW,. 2000. Fanconi anemia, complementation group A, cells are defective in ability to produce incisions at sites of psoralen interstrand cross-links. Carcinogenesis 21: 741-751.
19. Kumaresan K, Sridharan D, McMahon L,. Lambert MW 2007. Deficiency in incisions produced by XPF at the site of a DNA interstrand cross-link in Fanconi anemia cells. Biochemistry 46: 14359-14368.
20. Lambert MW,. 2015. Functional significance of nuclear α spectrin. J Cell Biochem 116: 1816-1830.
21. Lambert MW, Tsongalis GJ, Lambert W, Hang B, Parrish DD,. 1992. Defective DNA endonuclease activities in Fanconi's anemia cells, complementation groups A and B. Mutat Res 273: 57-71.
22. Lambert MW, Tsongalis JT, Lambert WC, Parrish DD,. 1997. Correction of the DNA repair defect in Fanconi anemia complementation groups A and D cells. Biochem Biophys Res Commun 230: 687-591.
23. Lefferts JA, Lambert MW,. 2003. Fanconi anemia cell lines deficient in αII spectrin express normal levels of αII spectrin mRNA. Biochem Biophys Res Comm 307: 510-515.
24. Lefferts JA, Wang C, Sridharan D, Baralt M, Lambert MW,. 2009. The SH3 domain of αII spectrin is a target for the Fanconi anemia protein, FANCG. Biochemistry 48: 254-263.
25. Legerski RJ,. 2010. Repair of DNA interstrand cross-links during S phase of the mammalian cell cycle. Environ Mol Mutagen 51: 540-551.
26. Manadhar M, Voulware KS, Wood RD,. 2015. The ERCC1 and ERCC4 (XPF) genes and gene products. Gene 569: 153-161.
27. Mathew CG,. 2006. Fanconi anaemia genes and susceptibility to cancer. Oncogene 25: 5875-5884.
28. McMahon LW, Sangerman J, Goodman SR, Kumaresan K, Lambert MW,. 2001. Human alpha spectrin II and the FANCA, FANCC, and FANCG proteins bind to DNA containing psoralen interstrand cross-links. Biochemistry 40: 7025-7034.
29. McMahon LW, Walsh CE, Lambert MW,. 1999. Human α spectrin II and the Fanconi anemia proteins FANCA and FANCC interact to form a nuclear complex. J Biol Chem 274: 32904-32980.
30. McMahon LW, Zhang P, Sridharan DM, Lefferts JA, Lambert MW,. 2009. Knockdown of αII spectrin in normal human cells by siRNA leads to chromosomal instability and decreased DNA interstrand cross-link repair. Biochem Biophys Res Commun 381: 288-293.
31. Moldovan G-L, D'Andrea A,. 2009. How the Fanconi anemia pathway guards the genome. Ann Rev Genet 43: 223-249.
32. Park W-H, Margossian S, Horwitz AA, Simons AM, D'Andrea AD, Parvin JD,. 2005. Direct DNA binding activity of the Fanconi anemia D2 protein. J Biol Chem 280: 23593-23598.
33. Raghunandan M, Chaudhury I, Kellich SL, Hanenberg H, Soebeck A,. 2015. FANCD2, FANCJ and BRCA2 cooperate to promote replication fork recovery independently of the Fanconi anemia complex. Cell Cycle 143: 342-353.
34. Raschle M, Knipsheer P, Enoiu M, Angelov T, Sun J, Griffith JD, Ellenberger TE, Scharer OD, Walter JC,. 2008. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134: 969-980.
35. Sareen A, Chaudhury I, Adams N, Sobeck A,. 2012. Fanconi anemia proteins FANCD2 and FANCI exhibit different DNA damage responses during S-phase. Nucleic Acids Res 40: 8425-8439.
36. Seki S, Ohzeki M, Uchiada A, Hirano S, Matsushita N, Kitao H, Oda T, Yamashita T, Kashihara N, Tsubahara A, Takata M, Ishiai M,. 2007. A requirement of FancL and FancD2 monoubiquitination in DNA repair. Genes to Cells 12: 299-310.
37. Sobeck A, Stone S, Hoatlin ME,. 2007. DNA structure-induced recruitment and activation of the Fanconi anemia pathway protein FAN CD2. Mol Cell Biol 27: 4283-4292.
38. Sridharan D, Brown M, Lambert WC, McMahon LW, Lambert MW,. 2003. Nonerythroid alpha II spectrin is required for recruitment of FANCA and XPF to nuclear foci induced by DNA interstrand cross-links. J Cell Sci 116: 823-835.
39. Sridharan DM, McMahon LW, Lambert MW,. 2006. αII-Spectrin interacts with five groups of functionally important proteins in the nucleus. Cell Biol Intl 30: 866-878.
40. Taniguchi T, D'Andrea AD,. 2006. Molecular pathogenesis of Fanconi anemia: Recent progress. Blood 107: 4223-4233.
41. Thompson LH, Hinz JM,. 2009. Cellular and molecular consequences of defective Fanconi anemia proteins in replication-coupled DNA repair: Mechanistic insights. Mutat Res 668: 54-72.
42. Walden H, Deans AJ,. 2014. The Fanconi anemia DNA repair pathway: Structural and functinal insights into a complex disorder. Ann Rev Biophys 43: 257-278.
43. Wang W,. 2007. Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nat Rev Genet 8: 735-748.
44. Wang X, Andreassen PR, D'Andrea AD,. 2004. Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol Cell Biol 24: 5850-5862.
45. Wang C, Lambert MW,. 2010. The Fanconi anemia protein, FANCG, binds to the ERCC1-XPF endonuclease via its tetratricopeptide repeats and the central domain of ER CC1. Biochemistry 49: 5560-5569.
46. Wilson JB, Blom E, Cunningham R, Xiao Y, Kupfer GM, Jones NJ,. 2010. Several tetratricopeptide repeat (TPR) motifs of FANCG are required for assembly of the BRCA2/D1-D2-G-X3 complex, FANCD2 monoubiquitylation and phleomycin resistance. Mutat Res 689: 12-20.
47. Wilson JB, Yamamoto K, Marriott AS, Hussain S, Sung P, Hoatlin ME, Mathew CG, Takata M, Thompson LH, Kupfer GM, Jones NJ,. 2008. FANCG promotes formation of a newly identified protein complex containing BRCA2, FANCD2 and XR CC3. Oncogene 27: 3641-3652.
48. Yuan F, Hokayem JE, Zhou W, Zhang Y,. 2009. FANCI protein binds to DNA and interacts with FANCD2 to recognize branched structures. J Biol Chem 284: 24443-24452.
49. Zhang P, Herbig U, Coffman F, Lambert MW,. 2013. Non-erythroid alpha spectrin prevents telomere dysfunction after DNA interstrand cross-link damage. Nucleic Acids Res 41: 5321-5340.
50. Zhang P, Sridharan D, Lambert MW,. 2010. Knockdown of μ-calpain in Fanconi anemia, FA-A, cells by siRNA restores αII spectrin levels and corrects chromosomal instability and defective DNA interstrand cross-link repair. Biochemistry 49: 5570-5581.
51. Zhang J, Walter JC,. 2014. Mechanism and regulation of incisions during DNA interstrand cross-link repair. DNA Repair 19: 135-142.