XPF-ERCC1 protects liver, kidney and blood homeostasis outside the canonical excision repair pathways


Autoři: Lee Mulderrig aff001;  Juan I. Garaycoechea aff002
Působiště autorů: MRC Laboratory of Molecular Biology, Cambridge Biomedical Campus, Francis Crick Avenue, Cambridge, United Kingdom aff001;  Hubrecht Institute–KNAW, University Medical Center Utrecht, Uppsalalaan, CT Utrecht, Netherlands aff002
Vyšlo v časopise: XPF-ERCC1 protects liver, kidney and blood homeostasis outside the canonical excision repair pathways. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008555
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008555

Souhrn

Loss of the XPF-ERCC1 endonuclease causes a dramatic phenotype that results in progeroid features associated with liver, kidney and bone marrow dysfunction. As this nuclease is involved in multiple DNA repair transactions, it is plausible that this severe phenotype results from the simultaneous inactivation of both branches of nucleotide excision repair (GG- and TC-NER) and Fanconi anaemia (FA) inter-strand crosslink (ICL) repair. Here we use genetics in human cells and mice to investigate the interaction between the canonical NER and ICL repair pathways and, subsequently, how their joint inactivation phenotypically overlaps with XPF-ERCC1 deficiency. We find that cells lacking TC-NER are sensitive to crosslinking agents and that there is a genetic interaction between NER and FA in the repair of certain endogenous crosslinking agents. However, joint inactivation of GG-NER, TC-NER and FA crosslink repair cannot account for the hypersensitivity of XPF-deficient cells to classical crosslinking agents nor is it sufficient to explain the extreme phenotype of Ercc1-/- mice. These analyses indicate that XPF-ERCC1 has important functions outside of its central role in NER and FA crosslink repair which are required to prevent endogenous DNA damage. Failure to resolve such damage leads to loss of tissue homeostasis in mice and humans.

Klíčová slova:

Cloning – Cross-linking – DNA repair – Flow cytometry – Hematopoietic stem cells – Kidneys – Nucleases – Tissue repair


Zdroje

1. Lindahl T. Instability and decay of the primary structure of DNA. Nature. 1993;362: 709–15. doi: 10.1038/362709a0 8469282

2. Marteijn JA, Lans H, Vermeulen W, Hoeijmakers JHJ. Understanding nucleotide excision repair and its roles in cancer and ageing. Nat Rev Mol Cell Biol. 2014;15: 465–81. doi: 10.1038/nrm3822 24954209

3. Klein Douwel D, Boonen RACM, Long DT, Szypowska AA, Räschle M, Walter JC, et al. XPF-ERCC1 acts in Unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/SLX4. Mol Cell. 2014;54: 460–71. doi: 10.1016/j.molcel.2014.03.015 24726325

4. Hodskinson MRG, Silhan J, Crossan GP, Garaycoechea JI, Mukherjee S, Johnson CM, et al. Mouse SLX4 is a tumor suppressor that stimulates the activity of the nuclease XPF-ERCC1 in DNA crosslink repair. Mol Cell. 2014;54: 472–84. doi: 10.1016/j.molcel.2014.03.014 24726326

5. Langevin F, Crossan GP, Rosado I V., Arends MJ, Patel KJ. Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice. Nature. 2011;475: 53–59. doi: 10.1038/nature10192 21734703

6. Garaycoechea JI, Crossan GP, Langevin F, Mulderrig L, Louzada S, Yang F, et al. Alcohol and endogenous aldehydes damage chromosomes and mutate stem cells. Nature. 2018;553: 171–177. doi: 10.1038/nature25154 29323295

7. Pontel LB, Rosado I V., Burgos-Barragan G, Garaycoechea JI, Yu R, Arends MJ, et al. Endogenous formaldehyde is a hematopoietic stem cell genotoxin and metabolic carcinogen. Mol Cell. 2015;60: 177–188. doi: 10.1016/j.molcel.2015.08.020 26412304

8. Knipscheer P, Räschle M, Smogorzewska A, Enoiu M, Ho TV, Schärer OD, et al. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science. 2009;326: 1698–701. doi: 10.1126/science.1182372 19965384

9. Ahmad A, Robinson AR, Duensing A, van Drunen E, Beverloo HB, Weisberg DB, et al. ERCC1-XPF Endonuclease Facilitates DNA Double-Strand Break Repair. Mol Cell Biol. 2008;28: 5082–5092. doi: 10.1128/MCB.00293-08 18541667

10. Bradford PT, Goldstein AM, Tamura D, Khan SG, Ueda T, Boyle J, et al. Cancer and neurologic degeneration in xeroderma pigmentosum: long term follow-up characterises the role of DNA repair. J Med Genet. 2011;48: 168–76. doi: 10.1136/jmg.2010.083022 21097776

11. Laugel V. Cockayne syndrome: the expanding clinical and mutational spectrum. Mech Ageing Dev. 2013;134: 161–70. doi: 10.1016/j.mad.2013.02.006 23428416

12. Kutler DI, Singh B, Satagopan J, Batish SD, Berwick M, Giampietro PF, et al. A 20-year perspective on the International Fanconi Anemia Registry (IFAR). Blood. 2003;101: 1249–56. doi: 10.1182/blood-2002-07-2170 12393516

13. Niedernhofer LJ, Garinis GA, Raams A, Lalai AS, Robinson AR, Appeldoorn E, et al. A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis. Nature. 2006;444: 1038–43. doi: 10.1038/nature05456 17183314

14. Jaspers NGJ, Raams A, Silengo MC, Wijgers N, Niedernhofer LJ, Robinson AR, et al. First reported patient with human ERCC1 deficiency has cerebro-oculo-facio-skeletal syndrome with a mild defect in nucleotide excision repair and severe developmental failure. Am J Hum Genet. 2007;80: 457–66. doi: 10.1086/512486 17273966

15. Kashiyama K, Nakazawa Y, Pilz DT, Guo C, Shimada M, Sasaki K, et al. Malfunction of nuclease ERCC1-XPF results in diverse clinical manifestations and causes Cockayne syndrome, xeroderma pigmentosum, and Fanconi anemia. Am J Hum Genet. 2013;92: 807–19. doi: 10.1016/j.ajhg.2013.04.007 23623389

16. McWhir J, Selfridge J, Harrison DJ, Squires S, Melton DW. Mice with DNA repair gene (ERCC-1) deficiency have elevated levels of p53, liver nuclear abnormalities and die before weaning. Nat Genet. 1993;5: 217–24. doi: 10.1038/ng1193-217 8275084

17. Weeda G, Donker I, de Wit J, Morreau H, Janssens R, Vissers CJ, et al. Disruption of mouse ERCC1 results in a novel repair syndrome with growth failure, nuclear abnormalities and senescence. Curr Biol. 1997;7: 427–39. Available: http://www.ncbi.nlm.nih.gov/pubmed/9197240 doi: 10.1016/s0960-9822(06)00190-4 9197240

18. Tian M, Shinkura R, Shinkura N, Alt FW. Growth retardation, early death, and DNA repair defects in mice deficient for the nucleotide excision repair enzyme XPF. Mol Cell Biol. 2004;24: 1200–5. doi: 10.1128/MCB.24.3.1200-1205.2004 14729965

19. Selfridge J, Hsia KT, Redhead NJ, Melton DW. Correction of liver dysfunction in DNA repair-deficient mice with an ERCC1 transgene. Nucleic Acids Res. 2001;29: 4541–50. doi: 10.1093/nar/29.22.4541 11713303

20. Prasher JM, Lalai AS, Heijmans-Antonissen C, Ploemacher RE, Hoeijmakers JHJ, Touw IP, et al. Reduced hematopoietic reserves in DNA interstrand crosslink repair-deficient Ercc1-/- mice. EMBO J. 2005;24: 861–871. doi: 10.1038/sj.emboj.7600542 15692571

21. Cho JS, Kook SH, Robinson AR, Niedernhofer LJ, Lee BC. Cell autonomous and nonautonomous mechanisms drive hematopoietic stem/progenitor cell loss in the absence of DNA repair. Stem Cells. 2013;31: 511–525. doi: 10.1002/stem.1261 23097336

22. de Vries A, van Oostrom CT, Hofhuis FM, Dortant PM, Berg RJ, de Gruijl FR, et al. Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature. 1995;377: 169–73. doi: 10.1038/377169a0 7675086

23. Cheng NC, van de Vrugt HJ, van der Valk MA, Oostra AB, Krimpenfort P, de Vries Y, et al. Mice with a targeted disruption of the Fanconi anemia homolog Fanca. Hum Mol Genet. 2000;9: 1805–11. doi: 10.1093/hmg/9.12.1805 10915769

24. Río P, Segovia JC, Hanenberg H, Casado JA, Martínez J, Göttsche K, et al. In vitro phenotypic correction of hematopoietic progenitors from Fanconi anemia group A knockout mice. Blood. 2002;100: 2032–9. Available: http://www.ncbi.nlm.nih.gov/pubmed/12200363 12200363

25. Sladek FM, Munn MM, Rupp WD, Howard-Flanders P. In vitro repair of psoralen-DNA cross-links by RecA, UvrABC, and the 5’-exonuclease of DNA polymerase I. J Biol Chem. 1989;264: 6755–65. Available: http://www.ncbi.nlm.nih.gov/pubmed/2708342 2708342

26. Van Houten B, Gamper H, Holbrook SR, Hearst JE, Sancar A. Action mechanism of ABC excision nuclease on a DNA substrate containing a psoralen crosslink at a defined position. Proc Natl Acad Sci U S A. 1986;83: 8077–81. doi: 10.1073/pnas.83.21.8077 3534882

27. McHugh PJ, Sones WR, Hartley JA. Repair of intermediate structures produced at DNA interstrand cross-links in Saccharomyces cerevisiae. Mol Cell Biol. 2000;20: 3425–33. doi: 10.1128/mcb.20.10.3425-3433.2000 10779332

28. Sarkar S, Davies AA, Ulrich HD, McHugh PJ. DNA interstrand crosslink repair during G1 involves nucleotide excision repair and DNA polymerase ζ. EMBO J. 2006;25: 1285–1294. doi: 10.1038/sj.emboj.7600993 16482220

29. Muniandy PA, Thapa D, Thazhathveetil AK, Liu S, Seidman MM. Repair of laser-localized DNA interstrand cross-links in G1 phase mammalian cells. J Biol Chem. 2009;284: 27908–17. doi: 10.1074/jbc.M109.029025 19684342

30. Enoiu M, Jiricny J, Schärer OD. Repair of cisplatin-induced DNA interstrand crosslinks by a replication-independent pathway involving transcription-coupled repair and translesion synthesis. Nucleic Acids Res. 2012;40: 8953–8964. doi: 10.1093/nar/gks670 22810206

31. Hill R, Crossan GP. DNA crosslink repair safeguards genomic stability during pre-meiotic germ cell development. Nat Genet. 2019.

32. Parmar K, Kim J, Sykes SM, Shimamura A, Stuckert P, Zhu K, et al. Hematopoietic stem cell defects in mice with deficiency of Fancd2 or Usp1. Stem Cells. 2010;28: 1186–95. doi: 10.1002/stem.437 20506303

33. Garaycoechea JI, Crossan GP, Langevin F, Daly M, Arends MJ, Patel KJ. Genotoxic consequences of endogenous aldehydes on mouse haematopoietic stem cell function. Nature. 2012;489: 571–575. doi: 10.1038/nature11368 22922648

34. Kamimae-Lanning AN, Goloviznina NA, Kurre P. Fetal origins of hematopoietic failure in a murine model of Fanconi anemia. Blood. 2013;121: 2008–2012. doi: 10.1182/blood-2012-06-439679 23315168

35. Domenech C, Maillard L, Rousseau A, Guidez F, Petit L, Pla M, et al. Studies in an early development window unveils a severe HSC defect in both murine and human Fanconi Anemia. Stem cell reports. 2018;11: 1075–1091. doi: 10.1016/j.stemcr.2018.10.001 30449320

36. Huang JC, Zamble DB, Reardon JT, Lippard SJ, Sancar A. HMG-domain proteins specifically inhibit the repair of the major DNA adduct of the anticancer drug cisplatin by human excision nuclease. Proc Natl Acad Sci U S A. 1994;91: 10394–8. doi: 10.1073/pnas.91.22.10394 7937961

37. Cheng G, Shi Y, Sturla SJ, Jalas JR, McIntee EJ, Villalta PW, et al. Reactions of formaldehyde plus acetaldehyde with deoxyguanosine and DNA: formation of cyclic deoxyguanosine adducts and formaldehyde cross-links. Chem Res Toxicol. 2003;16: 145–52. doi: 10.1021/tx025614r 12588185

38. Kuykendall JR, Bogdanffy MS. Efficiency of DNA-histone crosslinking induced by saturated and unsaturated aldehydes in vitro. Mutat Res. 1992;283: 131–6. doi: 10.1016/0165-7992(92)90145-8 1381490

39. Cheo DL, Ruven HJT, Meira LB, Hammer RE, Burns DK, Tappe NJ, et al. Characterization of defective nucleotide excision repair in XPC mutant mice. Mutat Res. 1997;374: 1–9. doi: 10.1016/s0027-5107(97)00046-8 9067411

40. van der Horst GT, van Steeg H, Berg RJ, van Gool AJ, de Wit J, Weeda G, et al. Defective transcription-coupled repair in Cockayne syndrome B mice is associated with skin cancer predisposition. Cell. 1997;89: 425–35. doi: 10.1016/s0092-8674(00)80223-8 9150142

41. Barnhoorn S, Uittenboogaard LM, Jaarsma D, Vermeij WP, Tresini M, Weymaere M, et al. Cell-autonomous progeroid changes in conditional mouse models for repair endonuclease XPG deficiency. PLoS Genet. 2014;10: e1004686. doi: 10.1371/journal.pgen.1004686 25299392

42. Ghezraoui H, Oliveira C, Becker JR, Bilham K, Moralli D, Anzilotti C, et al. 53BP1 cooperation with the REV7-shieldin complex underpins DNA structure-specific NHEJ. Nature. 2018;560: 122–127. doi: 10.1038/s41586-018-0362-1 30046110

43. Bellelli R, Borel V, Logan C, Svendsen J, Cox DE, Nye E, et al. Polε Instability Drives Replication Stress, Abnormal Development, and Tumorigenesis. Mol Cell. 2018;70: 707–721.e7. doi: 10.1016/j.molcel.2018.04.008 29754823

44. Furuta T, Ueda T, Aune G, Sarasin A, Kraemer KH, Pommier Y. Transcription-coupled nucleotide excision repair as a determinant of cisplatin sensitivity of human cells. Cancer Res. 2002;62: 4899–4902. 12208738

45. Bennardo N, Cheng A, Huang N, Stark JM. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 2008;4: e1000110. doi: 10.1371/journal.pgen.1000110 18584027

46. Al-Minawi AZ, Saleh-Gohari N, Helleday T. The ERCC1/XPF endonuclease is required for efficient single-strand annealing and gene conversion in mammalian cells. Nucleic Acids Res. 2008;36: 1–9. doi: 10.1093/nar/gkm888 17962301

47. Motycka TA, Bessho T, Post SM, Sung P, Tomkinson AE. Physical and functional interaction between the XPF/ERCC1 endonuclease and hRad52. J Biol Chem. 2004;279: 13634–9. doi: 10.1074/jbc.M313779200 14734547

48. Ishiai M, Kimura M, Namikoshi K, Yamazoe M, Yamamoto K, Arakawa H, et al. DNA cross-link repair protein SNM1A interacts with PIAS1 in nuclear focus formation. Mol Cell Biol. 2004;24: 10733–41. doi: 10.1128/MCB.24.24.10733-10741.2004 15572677

49. Wang AT, Sengerová B, Cattell E, Inagawa T, Hartley JM, Kiakos K, et al. Human SNM1A and XPF-ERCC1 collaborate to initiate DNA interstrand cross-link repair. Genes Dev. 2011;25: 1859–70. doi: 10.1101/gad.15699211 21896658

50. Verhagen-Oldenampsen JHE, Haanstra JR, van Strien PMH, Valkhof M, Touw IP, von Lindern M. Loss of Ercc1 Results in a Time- and Dose-Dependent Reduction of Proliferating Early Hematopoietic Progenitors. Anemia. 2012;2012: 1–9. doi: 10.1155/2012/783068 22701168

51. Compe E, Egly J-M. TFIIH: when transcription met DNA repair. Nat Rev Mol Cell Biol. 2012;13: 343–54. doi: 10.1038/nrm3350 22572993

52. Fousteri M, Vermeulen W, van Zeeland AA, Mullenders LHF. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol Cell. 2006;23: 471–82. doi: 10.1016/j.molcel.2006.06.029 16916636

53. Sarker AH, Tsutakawa SE, Kostek S, Ng C, Shin DS, Peris M, et al. Recognition of RNA polymerase II and transcription bubbles by XPG, CSB, and TFIIH: insights for transcription-coupled repair and Cockayne Syndrome. Mol Cell. 2005;20: 187–98. doi: 10.1016/j.molcel.2005.09.022 16246722

54. Ito S, Kuraoka I, Chymkowitch P, Compe E, Takedachi A, Ishigami C, et al. XPG stabilizes TFIIH, allowing transactivation of nuclear receptors: implications for Cockayne syndrome in XP-G/CS patients. Mol Cell. 2007;26: 231–43. doi: 10.1016/j.molcel.2007.03.013 17466625

55. Kamileri I, Karakasilioti I, Sideri A, Kosteas T, Tatarakis A, Talianidis I, et al. Defective transcription initiation causes postnatal growth failure in a mouse model of nucleotide excision repair (NER) progeria. Proc Natl Acad Sci U S A. 2012;109: 2995–3000. doi: 10.1073/pnas.1114941109 22323595

56. Le May N, Mota-Fernandes D, Vélez-Cruz R, Iltis I, Biard D, Egly JM. NER Factors Are Recruited to Active Promoters and Facilitate Chromatin Modification for Transcription in the Absence of Exogenous Genotoxic Attack. Mol Cell. 2010;38: 54–66. doi: 10.1016/j.molcel.2010.03.004 20385089

57. Chatzinikolaou G, Apostolou Z, Aid-Pavlidis T, Ioannidou A, Karakasilioti I, Papadopoulos GL, et al. ERCC1-XPF cooperates with CTCF and cohesin to facilitate the developmental silencing of imprinted genes. Nat Cell Biol. 2017;19: 421–432. doi: 10.1038/ncb3499 28368372

58. Le May N, Fradin D, Iltis I, Bougnères P, Egly JM. XPG and XPF Endonucleases Trigger Chromatin Looping and DNA Demethylation for Accurate Expression of Activated Genes. Mol Cell. 2012;47: 622–632. doi: 10.1016/j.molcel.2012.05.050 22771116

59. Shiomi N, Kito S, Oyama M, Matsunaga T, Harada Y-N, Ikawa M, et al. Identification of the XPG Region That Causes the Onset of Cockayne Syndrome by Using Xpg Mutant Mice Generated by the cDNA-Mediated Knock-In Method. Mol Cell Biol. 2004;24: 3712–3719. doi: 10.1128/MCB.24.9.3712-3719.2004 15082767

60. Tian M, Jones DA, Smith M, Shinkura R, Alt FW. Deficiency in the Nuclease Activity of Xeroderma Pigmentosum G in Mice Leads to Hypersensitivity to UV Irradiation. Mol Cell Biol. 2004;24: 2237–2242. doi: 10.1128/MCB.24.6.2237-2242.2004 14993263

61. DiGiovanna JJ, Kraemer KH. Shining a light on xeroderma pigmentosum. J Invest Dermatol. 2012;132: 785–96. doi: 10.1038/jid.2011.426 22217736

62. van der Pluijm I, Garinis GA, Brandt RMC, Gorgels TGMF, Wijnhoven SW, Diderich KEM, et al. Impaired genome maintenance suppresses the growth hormone—insulin-like growth factor 1 axis in mice with Cockayne syndrome. PLoS Biol. 2007;5: e2. doi: 10.1371/journal.pbio.0050002 17326724

63. Jaarsma D, van der Pluijm I, de Waard MC, Haasdijk ED, Brandt R, Vermeij M, et al. Age-related neuronal degeneration: Complementary roles of nucleotide excision repair and transcription-coupled repair in preventing neuropathology. PLoS Genet. 2011;7: 6–8. doi: 10.1371/journal.pgen.1002405 22174697

64. Pace P, Johnson M, Tan WM, Mosedale G, Sng C, Hoatlin M, et al. FANCE: the link between Fanconi anaemia complex assembly and activity. EMBO J. 2002;21: 3414–23. doi: 10.1093/emboj/cdf355 12093742

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2020 Číslo 4

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!

×