Molecular pathogenesis of fanconi anemia

International Journal of Hematology

Volumn 75, Issue 2, 2002, Pages 123-128

  Taniguchi, Toshiyasu ^a   D'Andrea, Alan D ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

BRCA1; Checkpoint; DNA repair; Fanconi anemia; Ubiquitin

Indexed keywords

BRCA1 PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; FANCC PROTEIN, HUMAN; FANCD2 PROTEIN, HUMAN; FANCONI ANEMIA GROUP C PROTEIN; FANCONI ANEMIA PROTEIN; NUCLEAR PROTEIN;

APLASTIC ANEMIA; AUTOSOMAL RECESSIVE INHERITANCE; CANCER SUSCEPTIBILITY; CELLULAR DISTRIBUTION; CHROMOSOME BREAKAGE; CLINICAL FEATURE; DEVELOPMENTAL DISORDER; DNA CROSS LINKING; DNA DAMAGE; FANCONI ANEMIA; GENETIC COMPLEMENTATION; HUMAN; HYPERSENSITIVITY; NONHUMAN; ONSET AGE; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVIEW; UBIQUITINATION; ANIMAL; FEMALE; GENETICS; MALE; METABOLISM;

ANIMALS; BRCA1 PROTEIN; CELL CYCLE PROTEINS; DNA DAMAGE; DNA-BINDING PROTEINS; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP C PROTEIN; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; FANCONI ANEMIA COMPLEMENTATION GROUP PROTEINS; FEMALE; HUMANS; MALE; NUCLEAR PROTEINS; PROTEINS;

EID: 0036463957     PISSN: 09255710     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02982016     Document Type: Review

References (82)

1. D'Andrea AD, Grompe M. Molecular biology of Fanconi anemia: implications for diagnosis and therapy. Blood. 1997;90:1725-1736.
2. Butturini A, Gale RP, Verlander PC, Adler-Brecher B, Gillio A, Auerbach AD. Hematologic abnormalities in Fanconi anemia. An International Fanconi Anemia Registry study. Blood. 1994;84:1650-1655.
3. Alter BP. Fanconi's anemia and malignancies. Am J Hematol. 1996;53:99-110.
4. Jacobs P, Karabus C. Fanconi's anemia. A family study with 20-year follow-up including associated breast pathology. Cancer. 1984;54:1850-1853.
5. Auerbach AD, Rogatko A, Schroeder-Kurth TM. International Fanconi Anemia Registry: relation of clinical symptoms to diepoxybutane sensitivity. Blood. 1989;73:391-396.
6. Joenje H, Arwert F, Eriksson AW, de Koning H, Oostra AB. Oxygen-dependence of chromosomal aberrations in Fanconi's anaemia. Nature. 1981;290:142-143.
7. Schindler D, Hoehn H. Fanconi anemia mutation causes cellular susceptibility to ambient oxygen. Am J Hum Genet. 1988;43:429-435.
8. Whitney MA, Royle G, Low MJ, et al. Germ cell defects and hematopoietic hypersensitivity to gamma-interferon in mice with a targeted disruption of the Fanconi anemia C gene. Blood. 1996;88:49-58.
9. Joenje H, Levitus M, Waisfisz Q, et al. Complementation analysis in Fanconi anemia: assignment of the reference FA-H patient to group A. Am J Hum Genet. 2000;67:759-762.
10. Timmers C, Taniguchi T, Hejna J, et al. Positional cloning of a novel Fanconi anemia gene, FANCD2. Mol Cell. 2001;7:241-248.
11. Lo Ten Foe JR, Rooimans MA, Bosnoyan-Collins L, et al. Expression cloning of a cDNA for the major Fanconi anemia gene, FAA. Nat Genet. 1996;14:320-323.
12. The Fanconi Anemia/Breast Cancer Consortium. Positional cloning of the Fanconi anaemia group A gene. Nat Genet. 1996;14:324-328.
13. Strathdee CA, Gavish H, Shannon WR, Buchwald M. Cloning of cDNAs for Fanconi's anaemia by functional complementation. Nature. 1992;356:763-767.
14. Hejna JA, Timmers CD, Reifsteck C, et al. Localization of the Fanconi anemia complementation group D gene to a 200-kb region on chromosome 3p25.3. Am J Hum Genet. 2000;66:1540-1551.
15. Garcia-Higuera I, Taniguchi T, Ganesan S, et al. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell. 2001;7:249-262.
16. de Winter JP, Leveille F, van Berkel CGM, et al. Isolation of a cDNA representing the Fanconi anemia complementation group E gene. Am J Hum Genet. 2000;67:1306-1308.
17. de Winter JP, Rooimans MA, van der Weel L, et al. The Fanconi anemia complementation gene FANCF encodes a novel protein with homology to ROM. Nat Genet. 2000;24:15-16.
18. de Winter JP, Waisfisz Q, Rooimans MA, et al. The Fanconi anaemia group G gene is identical with human XRCC9. Nat Genet. 1998;20:281-283.
19. Liu N, Lamerdin JE, Tucker JD, et al. The human XRCC9 gene corrects chromosomal instability and mutagen sensitivities in CHO UV40 cells. Proc Natl Acad Sci U S A. 1997;94:9232-9237.
20. Kupfer GM, Naf D, Suliman A, Pulsipher M, D'Andrea AD. The Fanconi anemia proteins, FAA and FAC, interact to form a nuclear complex. Nat Genet. 1997;17:487-490.
21. Garcia-Higuera I, Kuang Y, Naf D, Wasik J, D'Andrea AD. Fanconi anemia proteins FANCA, FANCC, and FANCG/XRCC9 interact in a functional nuclear complex. Mol Cell Biol. 1999;19:4866-4873.
22. de Winter JP, van Der Weel L, de Groot J, et al. The Fanconi anemia protein FANCF forms a nuclear complex with FANCA, FANCC and FANCG. Hum Mol Genet. 2000;9:2665-2674.
23. Medhurst AL, Huber PAJ, Waisfisz Q, de Winter JP, Mathew CG. Direct interactions of the five known Fanconi anaemia proteins suggest a common functional pathway. Hum Mol Genet. 2001;10:423-429.
24. Yamashita T, Kupfer GM, Naf D, et al. The Fanconi anemia pathway requires FAA phosphorylation and FAA/FAC nuclear accumulation. Proc Natl Acad Sci U S A. 1998;95:13085-13090.
25. Qiao F, Moss A, Kupfer GM. Fanconi anemia proteins localize to chromatin and the nuclear matrix in a DNA damage- and cell cycle-regulated manner. J Biol Chem. 2001;276:23391-23396.
26. Futaki M, Watanabe S, Kajigaya S, Liu JM. Fanconi anemia protein, FANCG, is a phosphoprotein and is upregulated with FANCA after TNF-alpha treatment. Biochem Biophys Res Commun. 2001;281:347-351.
27. Moynahan ME, Cui TY, Jasin M. Homology-directed DNA repair, mitomycin-c resistance, and chromosome stability is restored with correction of a Brca1 mutation. Cancer Res. 2001;61:4842-4850.
28. Weissman AM. Themes and variations on ubiquitylation. Nat Rev Mol Cell Biol. 2001;2:169-178.
29. Hicke L. Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol. 2001;2:195-201.
30. Miki Y, Swensen J, Shattuck-Eidens D, et al. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science. 1994;266:66-71.
31. Scully R, Livingston DM. In search of the tumour-suppressor functions of BRCA1 and BRCA2. Nature. 2000;408:429-432.
32. Scully R, Chen J, Plug A, et al. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell. 1997;88:265-275.
33. Chen J, Silver DP, Walpita D, et al. Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol Cell. 1998;2:317-328.
34. Zhong Q, Chen C-F, Li S, et al. Association of BRCA1 with the hRad50-hMre11-p95 complex and the DNA damage response. Science. 1999;285:747-750.
35. Wang Y, Cortez D, Yazdi P, Neff N, Elledge SJ, Qin J. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 2000;14:927-939.
36. Lorick KL, Jensen JP, Fang S, Ong AM, Hatakeyama S, Weissman AM. RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc Natl Acad Sci U S A. 1999;96:11364-11369.
37. Ruffner H, Joazeiro CA, Hemmati D, Hunter T, Verma IM. Cancer-predisposing mutations within the RING domain of BRCA1: loss of ubiquitin protein ligase activity and protection from radiation hypersensitivity. Proc Natl Acad Sci U S A. 2001;98:5134-5139.
38. Hashizume R, Fukuda M, Maeda I, et al. The ring heterodimer Brca1-Bard1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J Biol Chem. 2001;276:14537-14540.
39. Joazeiro CAP, Weissman AM. RING finger proteins: mediators of ubiquitin ligase activity. Cell. 2000;102:549-552.
40. Siddique MA, Nakanishi K, Taniguchi T, Grompe M, D'Andrea AD. Function of the Fanconi anemia pathway in FA complementation group F and D1 cells. Exp Hematol. 2001:29:1448-1455.
41. Chen M, Tomkins DJ, Auerbach W, et al. Inactivation of Fac in mice produces inducible chromosomal instability and reduced fertility reminiscent of Fanconi anaemia. Nat Genet. 1996;12:448-451.
42. Carreau M, Gan OI, Liu L, et al. Bone marrow failure in the Fanconi anemia group C mouse model after DNA damage. Blood. 1998;91:2737-2744.
43. Cheng NC, van de Vrugt HJ, van der Valk MA, et al. Mice with a targeted disruption of the Fanconi anemia homolog Fanca. Hum Mol Genet. 2000;9:1805-1811.
44. Yang Y, Kuang Y, Montes de Oca R, et al. Targeted disruption of the murine Fanconi anemia gene, Fancg/Xrcc9. Blood. 2001;98:3435-3440.
45. Gush KA, Fu K-L, Grompe M, Walsh CE. Phenotypic correction of Fanconi anemia group C knockout mice. Blood. 2000;95:700-704.
46. Heinrich MC, Hoatlin ME, Zigler AJ, et al. DNA cross-linker-induced G2/M arrest in group C Fanconi anemia lymphoblasts reflects normal checkpoint function. Blood. 1998;91:275-287.
47. Sala-Trepat M, Rouillard D, Escarceller M, Laquerbe A, Moustacchi E, Papadopoulo D. Arrest of S-phase progression is impaired in Fanconi anemia cells. Exp Cell Res. 2000;260:208-215.
48. Centurion SA, Kuo H-R, Lambert WC. Damage-resistant DNA synthesis in Fanconi anemia cells treated with a DNA cross-linking agent. Exp Cell Res. 2000;260:216-221.
49. Painter RB. Radioresistant DNA synthesis: an intrinsic feature of ataxia telangiectasia. Mutat Res. 1981;84:183-190.
50. Lin D-S, Kim S-T, Xu B, et al. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature. 2000;404:613-617.
51. Xu B, Kim S-T, Kastan MB. Involvement of BRCA1 in S-phase and G2-phase checkpoints after ionizing radiation. Mol Cell Biol. 2001;21:3445-3450.
52. Zhao S, Weng Y-C, Yuan S-SF, et al. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature. 2000;405:473-477.
53. Gatei M, Young D, Cerosaletti KM, et al. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat Genet. 2000;25:115-119.
54. Wu X, Ranganathan V, Weisman DS, et al. ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature. 2000;405:477-482.
55. Chen J. Ataxia telangiectasia-related protein is involved in the phosphorylation of BRCA1 following deoxyribonucleic acid damage. Cancer Res. 2000;60:5037-5039.
56. Cortez WJ, Wangt Y, Qin J, Elledge SJ. Requirement of ATM-dependent phosphorylation of BRCA1 in the DNA damage response to double-strand breaks. Science. 1999;286:1162-1166.
57. Matsuoka S, Rotman G, Ogawa A, Shiloh Y, Tamai K, Elledge SJ. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci U S A. 2000;97:10389-10394.
58. Buscemi G, Savio C, Zannini L, et al. Chk2 activation dependence on Nbs1 after DNA damage. Mol Cell Biol. 2001;21:5214-5222.
59. Lee JS, Collins KM, Brown AL, Lee CH, Chung JH. hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature. 2000;404:201-204.
60. Falck J, Mailand N, Syljuasen RG, Bartek J, Lukas J. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature. 2001;410:842-847.
61. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol. 2000;10:886-895.
62. Gatei M, Zhou BB, Hobson K, Scott S, Young D, Khanna KK. Ataxia telangiectasia mutated (ATM) kinase and ATM and Rad3 related kinase mediate phosphorylation of Brca1 at distinct and overlapping sites. In vivo assessment using phospho-specific antibodies. J Biol Chem. 2001;276:17276-17280.
63. Tibbetts RS, Cortez D, Brumbaugh KM, et al. Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev. 2000;14:2989-3002.
64. Scully R, Chen J, Ochs RL, et al. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell. 1997;90:425-435.
65. Moynahan ME, Pierce AJ, Jasin M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol Cell. 2001;7:263-272.
66. Thyagarajan B, Campbell C. Elevated homologous recombination activity in fanconi anemia fibroblasts. J Biol Chem. 1997;272:23328-23333.
67. Lundberg R, Mavinakere M, Campbell C. Deficient DNA end joining activity in extracts from fanconi anemia fibroblasts. J Biol Chem. 2001;276:9543-9549.
68. Escarceller M, Rousset S, Moustacchi E, Papadopoulo D. The fidelity of double strand breaks processing is impaired in complementation groups B and D of Fanconi anemia, a genetic instability syndrome. Somat Cell Mol Genet. 1997;23:401-411.
69. Escarceller M, Buchwald M, Singleton BK, et al. Fanconi anemia C gene product plays a role in the fidelity of blunt DNA end-joining. J Mol Biol. 1998;279:375-385.
70. McMahon LW, Walsh CE, Lambert MW. Human a spectrin II and the Fanconi anemia proteins FANCA and FANCC interact to form a nuclear complex. J Biol Chem. 1999;274:32904-32908.
71. Hoatlin ME, Zhi Y, Ball H, et al. A novel BTB/POZ transcriptional repressor protein interacts with the Fanconi anemia group C protein and PLZF. Blood. 1999;94:3737-3747.
72. Otsuki T, Kajigaya S, Ozawa K, Liu JM. SNX5, a new member of the sorting nexin family, binds to the Fanconi anemia complementation group A protein. Biochem Biophys Res Commun. 1999;265:630-5.
73. Kruyt FAE, Hoshino T, Liu JM, Joseph P, Jaiswal AK, Youssoufian H. Abnormal microsomal detoxification implicated in Fanconi anemia group C by interaction of the FAC protein with NADPH cytochrome P450 reductase. Blood. 1998;92:3050-3056.
74. Hoshino T, Wang J, Devetten MP, et al. Molecular chaperone GRP94 binds to the Fanconi anemia group C protein and regulates its intracellular expression. Blood. 1998;91:4379-4386.
75. Kupfer G, Yamashita T, Naf D, Suliman A, Asano S, D'Andrea AD. The Fanconi anemia protein, FAC, binds to the cyclin-dependent kinase, cdc2. Blood. 1997;90:1047-1054.
76. Cumming RC, Lightfoot J, Beard K, Youssoufian H, O'Brien PJ, Buchwald M. Fanconi anemia group C protein prevents apoptosis in hematopoietic cells through redox regulation of GSTP1. Nat Med. 2001;7:814-820.
77. Pang Q, Fagerlie S, Christianson TA, et al. The Fanconi anemia protein FANCC binds to and facilitates the activation of STAT1 by gamma interferon and hematopoietic growth factors. Mol Cell Biol. 2000;20:4724-4735.
78. Pang Q, Keeble W, Christianson TA, Faulkner GR, Bagby GC. FANCC interacts with Hsp70 to protect hematopoietic cells from IFN-gamma/TNF-alpha-mediated cytotoxicity. EMBO J. 2001;20:4478-4489.
79. Yamashita T, Barber DL, Zhu Y, Wu N, D'Andrea AD. The Fanconi anemia polypeptide FACC is localized to the cytoplasm. Proc Natl Acad Sci U S A. 1994;91:6712-6716.
80. Hoatlin ME, Christianson TA, Keeble WW, et al. The Fanconi anemia group C gene product is located in both the nucleus and cytoplasm of human cells. Blood. 1998;91:1418-1425.
81. Hadjur S, Ung K, Wadsworth L, et al. Defective hematopoiesis and hepatic steatosis in mice with combined deficiencies of the genes encoding Fancc and Cu/Zn superoxide dismutase. Blood. 2001;98:1003-1011.
82. Pang Q, Christianson TA, Keeble W, et al. The Fanconi anemia complementation group C gene product: structural evidence of multifunctionality. Blood. 2001;98:1392-1401.