The DNA cytosine deaminase APOBEC3H haplotype i likely contributes to breast and lung cancer mutagenesis

Nature Communications

Volumn 7, Issue , 2016, Pages

  Starrett, Gabriel J ^a,b,c,d   Luengas, Elizabeth M ^a,b,c,d   McCann, Jennifer L ^a,b,c,d   Ebrahimi, Diako ^a,b,c,d   Temiz, Nuri A ^a,b   Love, Robin P ^e   Feng, Yuqing ^e   Adolph, Madison B ^e   Chelico, Linda ^e   Law, Emily K ^a,b,c,d   Carpenter, Michael A ^a,b,c,d   Harris, Reuben S ^a,b,c,d  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE DEAMINASE; DNA CYTOSINE DEAMINASE APOBEC3H; GENOMIC DNA; UNCLASSIFIED DRUG; APOBEC3H PROTEIN, HUMAN; DNA; HYDROLASE;

CANCER; DNA; ENZYME ACTIVITY; GENE EXPRESSION; GENOMICS; MUTATION; PROTEIN; RESPIRATORY DISEASE; TUMOR; WOMENS HEALTH;

ARTICLE; BREAST CANCER; CELLULAR DISTRIBUTION; CHROMOSOME 22; CONTROLLED STUDY; DEAMINATION; FEMALE; GENE DELETION; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENETIC LINKAGE; HAPLOTYPE; HUMAN; HUMAN CELL; LINKAGE ANALYSIS; LUNG ADENOCARCINOMA; LUNG CANCER; MOLECULAR MECHANICS; MUTAGENESIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION; SINGLE NUCLEOTIDE POLYMORPHISM; SOMATIC MUTATION; STEADY STATE; UPREGULATION; ADENOCARCINOMA; BREAST TUMOR; GENETIC PREDISPOSITION; GENETICS; LUNG TUMOR; METABOLISM; MUTATION;

ADENOCARCINOMA; AMINOHYDROLASES; BREAST NEOPLASMS; DNA; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HAPLOTYPES; HUMANS; LUNG NEOPLASMS; MUTATION;

EID: 84988869897     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12918     Document Type: Article

References (78)

1. Kuong, K. J. & Loeb, L. A. APOBEC3B mutagenesis in cancer. Nat. Genet. 45, 964-965 (2013).
2. Helleday, T., Eshtad, S. & Nik-Zainal, S. Mechanisms underlying mutational signatures in human cancers. Nat. Rev. Genet. 15, 585-598 (2014).
3. McGranahan, N. & Swanton, C. Biological and therapeutic impact of intratumor heterogeneity in cancer evolution. Cancer Cell 27, 15-26 (2015).
4. Roberts, S. A. & Gordenin, D. A. Hypermutation in human cancer genomes: footprints and mechanisms. Nat. Rev. Cancer 14, 786-800 (2014).
5. Nik-Zainal, S. et al. Mutational processes molding the genomes of 21 breast cancers. Cell 149, 979-993 (2012).
6. Alexandrov, L. B. et al. Signatures of mutational processes in human cancer. Nature 500, 415-421 (2013).
7. Burns, M. B. et al. APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494, 366-370 (2013).
8. Burns, M. B., Temiz, N. A. & Harris, R. S. Evidence for APOBEC3B mutagenesis in multiple human cancers. Nat. Genet. 45, 977-983 (2013).
9. Roberts, S. A. et al. An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat. Genet. 45, 970-976 (2013).
10. de Bruin, E. C. et al. Spatial and temporal diversity in genomic instability processes defines lung cancer evolution. Science 346, 251-256 (2014).
11. Nik-Zainal, S. et al. Landscape of somatic mutations in 560 breast cancer whole-genome sequences. Nature 534, 47-54 (2016).
12. Morganella, S. et al. The topography of mutational processes in breast cancer genomes. Nat. Commun. 7, 11383 (2016).
13. Conticello, S. G. The AID/APOBEC family of nucleic acid mutators. Genome Biol. 9, 229 (2008).
14. Harris, R. S. & Dudley, J. P. APOBECs and virus restriction. Virology 479-480C, 131-145 (2015).
15. Simon, V., Bloch, N. & Landau, N. R. Intrinsic host restrictions to HIV-1 and mechanisms of viral escape. Nat. Immunol. 16, 546-553 (2015).
16. Landry, S., Narvaiza, I., Linfesty, D. C. & Weitzman, M. D. APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep. 12, 444-450 (2011).
17. Suspene, R. et al. Somatic hypermutation of human mitochondrial and nuclear DNA by APOBEC3 cytidine deaminases, a pathway for DNA catabolism. Proc. Natl Acad. Sci. USA 108, 4858-4863 (2011).
18. Shee, C. et al. Engineered proteins detect spontaneous DNA breakage in human and bacterial cells. Elife 2, e01222 (2013).
19. Caval, V., Suspene, R., Shapira, M., Vartanian, J. P. & Wain-Hobson, S. A prevalent cancer susceptibility APOBEC3A hybrid allele bearing APOBEC3B 3UTR enhances chromosomal DNA damage. Nat. Commun. 5, 5129 (2014).
20. Chan, K. et al. An APOBEC3A hypermutation signature is distinguishable from the signature of background mutagenesis by APOBEC3B in human cancers. Nat. Genet. 47, 1067-1072 (2015).
21. Caval, V. et al. Molecular basis of the attenuated phenotype of human APOBEC3B DNA mutator enzyme. Nucleic Acids Res. 43, 9340-9349 (2015).
22. Stenglein, M. D., Burns, M. B., Li, M., Lengyel, J. & Harris, R. S. APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat. Struct. Mol. Biol. 17, 222-229 (2010).
23. Land, A. M. et al. Endogenous APOBEC3A DNA cytosine deaminase is cytoplasmic and nongenotoxic. J. Biol. Chem. 288, 17253-17260 (2013).
24. Thielen, B. K. et al. Innate immune signaling induces high levels of TC-specific deaminase activity in primary monocyte-derived cells through expression of APOBEC3A isoforms. J. Biol. Chem. 285, 27753-27766 (2010).
25. Koning, F. A., Goujon, C., Bauby, H. & Malim, M. H. Target cell-mediated editing of HIV-1 cDNA by APOBEC3 proteins in human macrophages. J. Virol. 85, 13448-13452 (2011).
26. Leonard, B. et al. The PKC/NF-kappaB signaling pathway induces APOBEC3B expression in multiple human cancers. Cancer Res. 75, 4538-4547 (2015).
27. Vieira, V. C. et al. Human papillomavirus E6 triggers upregulation of the antiviral and cancer genomic DNA deaminase APOBEC3B. mBio 5, e02234-14 (2014).
28. Verhalen, B., Starrett, G. J., Harris, R. S. & Jiang, M. Functional upregulation of the DNA cytosine deaminase APOBEC3B by polyomaviruses. J. Virol. 90, 6379-6386 (2016).
29. Bogerd, H. P. et al. Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc. Natl Acad. Sci. USA 103, 8780-8785 (2006).
30. Lackey, L. et al. APOBEC3B and AID have similar nuclear import mechanisms. J. Mol. Biol. 419, 301-314 (2012).
31. Lackey, L., Law, E. K., Brown, W. L. & Harris, R. S. Subcellular localization of the APOBEC3 proteins during mitosis and implications for genomic DNA deamination. Cell Cycle 12, 762-772 (2013).
32. Leonard, B. et al. APOBEC3B upregulation and genomic mutation patterns in serous ovarian carcinoma. Cancer Res. 73, 7222-7231 (2013).
33. Henderson, S., Chakravarthy, A., Su, X., Boshoff, C. & Fenton, T. R. APOBEC-mediated cytosine deamination links PIK3CA helical domain mutations to human papillomavirus-driven tumor development. Cell Rep. 7, 1833-1841 (2014).
34. Cescon, D. W., Haibe-Kains, B. & Mak, T. W. APOBEC3B expression in breast cancer reflects cellular proliferation, while a deletion polymorphism is associated with immune activation. Proc. Natl Acad. Sci. USA 112, 2841-2846 (2015).
35. Sieuwerts, A. M. et al. Elevated APOBEC3B correlates with poor outcomes for estrogen-receptor-positive breast cancers. Horm. Cancer 5, 405-413 (2014).
36. Tsuboi, M. et al. APOBEC3B high expression status is associated with aggressive phenotype in Japanese breast cancers. Breast Cancer 23, 780-788 (2015).
37. Periyasamy, M. et al. APOBEC3B-mediated cytidine deamination is required for estrogen receptor action in breast cancer. Cell Rep. 13, 108-121 (2015).
38. Yan, S. et al. Increased APOBEC3B predicts worse outcomes in lung cancer: a comprehensive retrospective study. J. Cancer 7, 618-625 (2016).
39. Walker, B. A. et al. APOBEC family mutational signatures are associated with poor prognosis translocations in multiple myeloma. Nat. Commun. 6, 6997 (2015).
40. Xu, L. et al. High APOBEC3B expression is a predictor of recurrence in patients with low-risk clear cell renal cell carcinoma. Urol. Oncol. 33, 340 e341-340 e348 (2015).
41. Burns, M. B., Leonard, B. & Harris, R. S. APOBEC3B: pathological consequences of an innate immune DNA mutator. Biomed. J. 38, 102-110 (2015).
42. Harris, R. S. Molecular mechanism and clinical impact of APOBEC3Bcatalyzed mutagenesis in breast cancer. Breast Cancer Res. 17, 8 (2015).
43. Swanton, C., McGranahan, N., Starrett, G. J. & Harris, R. S. APOBEC enzymes: mutagenic fuel for cancer evolution and heterogeneity. Cancer Discov. 5, 704-712 (2015).
44. Nik-Zainal, S. et al. Association of a germline copy number polymorphism of APOBEC3A and APOBEC3B with burden of putative APOBEC-dependent mutations in breast cancer. Nat. Genet. 46, 487-491 (2014).
45. Kidd, J. M., Newman, T. L., Tuzun, E., Kaul, R. & Eichler, E. E. Population stratification of a common APOBEC gene deletion polymorphism. PLoS Genet. 3, e63 (2007).
46. OhAinle, M., Kerns, J. A., Li, M. M., Malik, H. S. & Emerman, M. Antiretroelement activity of APOBEC3H was lost twice in recent human evolution. Cell Host Microbe 4, 249-259 (2008).
47. Wang, X. et al. Analysis of human APOBEC3H haplotypes and anti-human immunodeficiency virus type 1 activity. J. Virol. 85, 3142-3152 (2011).
48. Refsland, E. W. et al. Natural polymorphisms in human APOBEC3H and HIV-1 Vif combine in primary T lymphocytes to affect viral G-to-A mutation levels and infectivity. PLoS Genet. 10, e1004761 (2014).
49. Li, M. M. & Emerman, M. Polymorphism in human APOBEC3H affects a phenotype dominant for subcellular localization and antiviral activity. J. Virol. 85, 8197-8207 (2011).
50. Ooms, M., Krikoni, A., Kress, A. K., Simon, V. & Munk, C. APOBEC3A, APOBEC3B, and APOBEC3H haplotype 2 restrict human T-lymphotropic virus type 1. J. Virol. 86, 6097-6108 (2012).
51. Ooms, M., Majdak, S., Seibert, C. W., Harari, A. & Simon, V. The localization of APOBEC3H variants in HIV-1 virions determines their antiviral activity. J. Virol. 84, 7961-7969 (2010).
52. Genomes Project, C. et al. A global reference for human genetic variation. Nature 526, 68-74 (2015).
53. Harris, R. S. et al. DNA deamination mediates innate immunity to retroviral infection. Cell 113, 803-809 (2003).
54. Yu, Q. et al. Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat. Struct. Mol. Biol. 11, 435-442 (2004).
55. Shi, K., Carpenter, M. A., Kurahashi, K., Harris, R. S. & Aihara, H. Crystal structure of the DNA deaminase APOBEC3B catalytic domain. J. Biol. Chem. 290, 28120-28130 (2015).
56. Carpenter, M. A. et al. Methylcytosine and normal cytosine deamination by the foreign DNA restriction enzyme APOBEC3A. J. Biol. Chem. 287, 34801-34808 (2012).
57. Zhen, A., Du, J., Zhou, X., Xiong, Y. & Yu, X. F. Reduced APOBEC3H variant anti-viral activities are associated with altered RNA binding activities. PLoS ONE 7, e38771 (2012).
58. zur Hausen, H. Papillomaviruses in the causation of human cancers-a brief historical account. Virology 384 260-265 (2009).
59. Lawrence, M. S. et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499, 214-218 (2013).
60. Rathore, A. et al. The local dinucleotide preference of APOBEC3G can be altered from 50-CC to 50-TC by a single amino acid substitution. J. Mol. Biol. 425, 4442-4454 (2013).
61. Kohli, R. M. et al. Local sequence targeting in the AID/APOBEC family differentially impacts retroviral restriction and antibody diversification. J. Biol. Chem. 285, 40956-40964 (2010).
62. Doseth, B., Ekre, C., Slupphaug, G., Krokan, H. E. & Kavli, B. Strikingly different properties of uracil-DNA glycosylases UNG2 and SMUG1 may explain divergent roles in processing of genomic uracil. DNA Repair (Amst) 11, 587-593 (2012).
63. Eftedal, I., Guddal, P. H., Slupphaug, G., Volden, G. & Krokan, H. E. Consensus sequences for good and poor removal of uracil from double stranded DNA by uracil-DNA glycosylase. Nucleic Acids Res. 21, 2095-2101 (1993).
64. Makridakis, N. M. & Reichardt, J. K. Translesion DNA polymerases and cancer. Front. Genet. 3, 174 (2012).
65. Kim, N., Mudrak, S. V. & Jinks-Robertson, S. The dCMP transferase activity of yeast Rev1 is biologically relevant during the bypass of endogenously generated AP sites. DNA Repair (Amst) 10, 1262-1271 (2011).
66. Chan, K., Resnick, M. A. & Gordenin, D. A. The choice of nucleotide inserted opposite abasic sites formed within chromosomal DNA reveals the polymerase activities participating in translesion DNA synthesis. DNA Repair (Amst) 12, 878-889 (2013).
67. Nabel, C. S. et al. AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat. Chem. Biol. 8, 751-758 (2012).
68. Siriwardena, S. U., Guruge, T. A. & Bhagwat, A. S. Characterization of the catalytic domain of human APOBEC3B and the critical structural role for a conserved methionine. J. Mol. Biol. 427, 3042-3055 (2015).
69. Ehrlich, M., Norris, K. F., Wang, R. Y., Kuo, K. C. & Gehrke, C. W. DNA cytosine methylation and heat-induced deamination. Biosci. Rep. 6, 387-393 (1986).
70. Leonard, B. et al. APOBEC3G expression correlates with T cell infiltration and improved clinical outcomes in high-grade serous ovarian carcinoma. Clin. Cancer Res. (2016).
71. Hultquist, J. F. et al. Human and rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1. J. Virol. 85, 11220-11234 (2011).
72. Zhu, M. et al. The eQTL-missense polymorphisms of APOBEC3H are associated with lung cancer risk in a Han Chinese population. Sci. Rep. 5, 14969 (2015).
73. McGranahan, N. et al. Clonal status of actionable driver events and the timing of mutational processes in cancer evolution. Sci. Transl. Med. 7, 283ra254 (2015).
74. Yoshihara, K. et al. Inferring tumour purity and stromal and immune cell admixture from expression data. Nat. Commun. 4, 2612 (2013).
75. LaRue, R. S., Lengyel, J., Jonsson, S. R., Andresdottir, V. & Harris, R. S. Lentiviral Vif degrades the APOBEC3Z3/APOBEC3H protein of its mammalian host and is capable of cross-species activity. J. Virol. 84, 8193-8201 (2010).
76. Chelico, L., Prochnow, C., Erie, D. A., Chen, X. S. & Goodman, M. F. Structural model for deoxycytidine deamination mechanisms of the HIV-1 inactivation enzyme APOBEC3G. J. Biol. Chem. 285, 16195-16205 (2010).
77. Chelico, L., Pham, P., Calabrese, P. & Goodman, M. F. APOBEC3G DNA deaminase acts processively 30 -4 50 on single-stranded DNA. Nat. Struct. Mol. Biol. 13, 392-399 (2006).
78. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).