The rate of spontaneous mutations in human myeloid cells

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 749, Issue 1-2, 2013, Pages 49-57

  Araten, David J ^a,b   Krejci, Ondrej ^c   DiTata, Kimberly ^b   Wunderlich, Mark ^c   Sanders, Katie J ^b   Zamechek, Leah ^b   Mulloy, James C ^c  

^a DEPARTMENT OF VETERANS AFFAIRS   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

GPI linked proteins; Human myeloid cultures; Mutation rate; Myeloid leukemia.; PIG A gene; Spontaneous somatic mutations

Indexed keywords

PROTEIN P53;

ACUTE GRANULOCYTIC LEUKEMIA; ALLELE; AML ETO GENE; ARTICLE; BONE MARROW CELL; CD34 SELECTION; CELL DIVISION; CONTROLLED STUDY; FLOW CYTOMETRY; FLT3 GENE; FUSION GENE; GENE; GRANULOCYTE; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMOGENESIS; MLL AF9 GENE; NRAS GENE; PHENOTYPE; PIG A GENE; PRIORITY JOURNAL; SOMATIC MUTATION;

ACUTE MYELOGENOUS LEUKEMIA; AML; B-LYMPHOBLASTOID CELL LINES; BLCLS; GLYCOSYLPHOSPHATIDYLINOSITOL; GPI; GPI-LINKED PROTEINS; HUMAN MYELOID CULTURES; MUTATION RATE; MYELOID LEUKEMIA.; PAROXYSMAL NOCTURNAL HEMOGLOBINURIA; PIG-A GENE; PNH; SPONTANEOUS SOMATIC MUTATIONS;

CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 2 SUBUNIT; FETAL BLOOD; FLOW CYTOMETRY; GENE KNOCKDOWN TECHNIQUES; GENES, P53; GLYCOSYLPHOSPHATIDYLINOSITOLS; HUMANS; MEMBRANE PROTEINS; MUTATION; MUTATION RATE; MYELOID CELLS; MYELOID-LYMPHOID LEUKEMIA PROTEIN; ONCOGENE PROTEINS, FUSION;

EID: 84884594161     PISSN: 00275107     EISSN: 09218262     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2013.05.004     Document Type: Article

References (75)

1. DePinho R. The age of cancer. Nature 2000, 408:248-254.
2. Edwards B., Howe H., Ries L., Thun M., Rosenberg H., Yancik R., Wingo P., Jemal A., Feigal E. Annual report to the nation on the status of cancer 1973-1999, featuring implications of age and aging on US cancer burden. Cancer 2002, 94:2766-2792.
3. Moorman A., Roman E., Cartwright R., Morgan G. Age-specific incidence rates for cytogenetically-defined subtypes of acute myeloid leukaemia. Brit. J. Cancer 2002, 86:1061-1063.
4. Albertini R., Nicklas J., O'Neill J., Robison S. In vivo somatic mutations in humans: measurement and analysis. Annu. Rev. Genet. 1990, 24:305-326.
5. Albertini R., Castle K., Borcherding W. T cell cloning to detect the mutant 6-thioguanine-resistant lymphocytes present in human peripheral blood. PNAS 1982, 79:6617-6621.
6. Morley A., Trainor K., Seshadri R., Ryall R. Measurement of in vivo mutations in human lymphocytes. Nature 1983, 302:155-156.
7. Seshadri R., Kutlaca R., Trainor K., Matthews C., Morley A. Mutation rate of normal and malignant human lymphocytes. Cancer Res. 1987, 47:407-409.
8. Kendal W., Frost P. Pitfalls and practice of Luria-Delbruck fluctuation analysis: a review. Cancer Res. 1988, 48:1060-1065.
9. Rossman T., Goncharova E., Nadas A. Modeling and measurement of the spontaneous mutation rate in mammalian cells. Mutat. Res. 1995, 328:21-30.
10. Nicolas J., Jakob H., Jacob F. Metabolic cooperation between normal mouse embryonal carcinoma cells and therif differentiated derivatives. PNAS 1978, 75:3292-3296.
11. Green M.H.L., O'Neill J.P., Cole J. Suggestions concerning the relationship between mutant frequency and mutation rate at the hprt locus in human peripheral T-lymphocytes. Mutat. Res. 1995, 334:323-339.
12. Miyata T., Takeda J., Iida Y., Yamada N., Inoue N., Takahashi M., Maeda K., Kitani T., Kinoshita T. The cloning of PIG-A, a component in the early step of GPI-anchor biosynthesis. Science 1993, 259:1318-1320.
13. Araten D., Nafa K., Pakdeesuwan K., Luzzatto L. Clonal populations of hematopoietic cells with paroxysmal nocturnal hemoglobinuria genotype and phenotype are present in normal individuals. Proc. Natl. Acad. Sci. USA 1999, 96:5209-5214.
14. Araten D.J., Golde D.W., Zhang R.H., Thaler H.T., Gargiulo L., Notaro R., Luzzatto L. A quantitative measurement of the human somatic mutation rate. Cancer Res. 2005, 65:8111-8117.
15. Araten D.J., Luzzatto L. The mutation rate in PIG-A is normal in patients with paroxysmal nocturnal hemoglobinuria (PNH). Blood 2006, 108:734-736.
16. Araten D.J., Bessler M., McKenzie S., Castro-Malaspina H., Childs B.H., Boulad F., Karadimitris A., Notaro R., Luzzatto L. Dynamics of hematopoiesis in paroxysmal nocturnal hemoglobinuria (PNH): no evidence for intrinsic growth advantage of PNH clones. Leukemia 2002, 16:2243-2248.
17. Keller P., Payne J.L., Tremml G., Greer P.A., Gaboli M., Pandolfi P.P., Bessler M. FES-Cre targets phosphatidylinositol glycan class A (PIGA) inactivation to hematopoietic stem cells in the bone marrow. J. Exp. Med. 2001, 194:581-590.
18. Rosti V., Tremml G., Soares V., Pandolfi P., Luzzatto L. Murine embryonic stem cells without pig-a gene activity are competent for hematopoiesis with the PNH phenotype but not for clonal expansion. J. Clin. Investig. 1997, 100:1028-1036.
19. Hu R., Mukhina G.L., Piantadosi S., Barber J.P., Jones R.J., Brodsky R.A. PIG-A mutations in normal hematopoiesis. Blood 2005, 105:3848-3854.
20. Araten D., Martinez-Climent J., Holm E., DiTata K., Sanders K. A quantitative analysis of genomic instability in lymphoid and plasma cell neoplasms based on the PIG-A gene. Mutat. Res. 2010, 686:1-8.
21. Araten D., Sanders K., Anscher D., Zamechek L., Hunger S., IbrahimF S. Leukemic blasts with the paroxysmal nocturnal hemoglobinuria phenotype in children with acute lymphoblastic leukemia. Am. J. Pathol. 2012, 181:1862-1869.
22. Krejci O., Wunderlich M., Geiger H., Chou F., Schleimer D., Jansen M., Andreassen P., Mulloy J. p53 signaling in response to increased DNA damage sensitizes AML1-ETO cells to stress-induced death 2008, 111:2190-2199.
23. Mulloy J., Cammeenga J., Berguido F., Wu K., Zhou P., Comenzo R., Jhanwar S., Moore M., Nimer S. Maintaining the self-renewal and differentiation potential of human CD34+ hematopoietic cells using a single genetic element. Blood 2003, 102:4369-4376.
24. Mulloy J., Wunderlich M., Zheng Y., Wei J. Transforming human blood stem and progenitor cells: a new way forward in leukemia modeling. Cell Cycle 2008, 7:3314-3319.
25. Nimer S., Moore M. Effects of the leukemia-associated AML1-ETO protein on hematopoietic stem and progenitor cells. Oncogene 2004, 23:4249-4254.
26. Wei J., Wunderlich M., Fox C., Alvarez S., Cigudosa J., Wilhelm J., Zheng Y., Cancelas J., Gu Y., Jansen M., DiMartino J., Mulloy J. Microenvironment determines lineage fate in a human model of MLL-AF9 leukemia. Cancer Cell 2008, 13:483-495.
27. Higuchi M., O'Brien D., Kumaravelu P., Lenny N., Yeoh E., Downing J. Expression of a conditional AML1-ETO oncogene bypasses embryonic lethality and establishes a murine model of human t(8;21) acute myeloid leukemia. Cancer Cell 2002, 1:63-74.
28. Yuan Y., Zhou L., Miyamoto T., Iwasaki H., Harakawa N., Hetherington C., Burel S., Lagasse E., Weissman I., Akashi K., Zhang D. AML1-ETO expression is directly involved in the development of acute myeloid leukemia in the presence of additional mutations. Proc. Natl. Acad. Sci. USA 2001, 98:10398-10403.
29. Frank R., Sun X., Berguido F., Jakubowiak A., Nimer S. The t(8;21) fusion protein, AML1/ETO, transforms NIH3T3 cells and activates AP-1. Oncogene 1999, 18:1701-1710.
30. Frank R., Zhang J., Uchida H., Meyers S., Hiebert S., Nimer S. The AML1/ETO fusion protein blocks transactivation of the GM-CSF promoter by AML1B. Oncogene 1995, 11:2667-2674.
31. Pabst T., Mueller B., Harakawa N., Schoch C., Haferlach T., Behr G., Hiddemann W., Zhang D., Tennen D. AML1-ETO downregulates the granulocytic differentiation factor C/EBPα in t(8;21) myeloid leukemia. Nat. Med. 2001, 4:444-451.
32. Vangala R., Heiss-Neumann M., Rangatia J., Singh S., Schoch C., Tenen D., Hiddemann W., Behre G. The myeloid master regulator transcription factor PU.1 is inactivated by AML1-ETO in t(8;21) myeloid leukemia. Blood 2003, 101:270-277.
33. Mao S., Franks R., Zhang J., Miyazaki Y., Nimer S. Functional and physical interactions betweenAML1proteins and ETS protein: MEF; implications for pathogenesis of t(8;21) positive leukemias. Mol. Cell. Biol. 1999, 19:3635-3644.
34. Mulloy J., Cammenga J., MacKenzie K., Berguido F., Moore M., Nimer S. The AML1-ETO fusion protein promotes the expansion of human hematopoietic stem cells. Blood 2002, 99:15-23.
35. Krivtsov A., Armstrong S. MLL translocations, histone modifications, and leukaemia stem-cell development. Nat. Rev. Cancer 2007, 7:823-833.
36. Corral J., Lavenir I., Imprey H., Warren A., Forster A., Larson T., Bell S., McKenzie A., King G., Rabbitts T. An MLL-AF9 fusion gene made by homologous recombination causes acute leukemia in chimeric mice: a method to create fusion oncogenes. Cell 1996, 85:853-861.
37. Thiel A., Blessington P., Zou T., Feather D., Wu X., Yan J., Zhang H., Liu Z., Ernst P., Koretzky G., Hua X. MLL-AF9-induced leukemogenesis requires coexpression of the wild-type MLL allele. Cancer Cell 2010, 17:148-159.
38. Wise-Draper T., Allen H., Thobe M., Jones E., Habash K., Munger K., Wells S. The human DEK proto-oncogene is a senescence inhibitor and an upregulated target of high-risk papillomavirus E7. J. Virol. 2005, 79:14309-14317.
39. Kendall S., Lindaric C., Adam S., Counter C. A network of genetic events sufficient to convert normal human cells to a tumorigenic state. Cancer Res. 2005, 65:9824-9828.
40. Shaulian E., Zauberman A., Ginsberg D., Oren M. Identification of a minimal transforming domain of p53: negative dominance through abrogation of sequence-specific DNA binding. Mol. Cell. Biol. 1992, 12:5581-5592.
41. Hyun J., Choi J., Zeng H., Lee Y., Kim H., Yoon S., Chung M. Leukemic cell line, KG-1 has a functional loss of hOGG1 enzyme due to a point mutation and 8-hydroxydeoxyguanosine can kill KG. Oncogene 2000, 19:4476-4479.
42. Banker D., Radich J., Becker A., Kerkof K., Norwood T., William C., Appelbaum F. The t(8;21) translocation is not consistently associated with high Bcl-2 expression in de novo acute myeloid leukemias of adults. Clin. Cancer Res. 1998, 4:3051-3062.
43. Stubbs M., Kim Y., Krivtsov A., Wright R., Feng Z., Agarwal J., Kung A., Armstrong S. MLL-AF9 and FLT3 cooperation in acute myelogenous leukemia: development of a model for rapid therapeutic assessment. Leukemia 2008, 22:66-77.
44. Shih L., Huang C., Wang P., Wu J., Lin T., Dunn P., Kuo M. Acquisition of FLT3 on N-ras mutations in frequently associated with progression of myelodysplastic syndrome to acute myeloid leukemia. Leukemia 2004, 18:466-475.
45. Wunderlich M., Chou F., Link K., Mizukawa B., Perry R., Carroll M., Mulloy J. AML xenograft efficiency is significantly improved in NOD/SCID-IL2RG mice constitutively expressing human SCF, GM-CSF and IL-3. Leukemia 2010, 10:1785-1788.
46. Welch J., Ley T., Link D., Miller C., Larson D., Koboldt D., Wartman L., Lamprecht T., Liu F., Xia J., Kandoth C., Fulton R., McLellan M., Dooling D., Wallis J., Chen K., Harris C., Schmidt H., Kalicki-Veizer J., Lu C., Zhang Q., Lin L., O'Laughlin M., McMichael J., Delehaunty K., Fulton L., Magrini V., McGrath S., Demeter R., Vickery T., Hundal J., Cook L., Swift G., Reed J., Alldredge P., Wylie T., Walker J., Watson M., Heath S., Shannon W., Varghese N., Nagarajan R., Payton J., Baty J., Kulkarni S., Klco J., Tomasson M., Westervelt P., Walter M., Graubert T., DiPersio J., Ding L., Mardis E., Wilson R. The origin and evolution of mutations in acute myeloid leukemia. Cell 2012, 150:264-278.
47. Ley T., Mardis E., Ding L., Fulton B., McLellan M., Chen K., Dooling D., Dunford-Shore B., McGrath S., Hickenbotham M., Cook L., Larson D. DNA sequencing of a cytogenetically normal acute myeloid leukaemia genome. Nature 2008, 456:66-72.
48. Abkowitz J., Catlin S., McCallie M., Guttorp P. Evidence that the number of hematopoietic stem cells per animal is conserved in mammals. Blood 2002, 100:2665-2667.
49. Gordon M., Lewis J., Marley S. Of mice and men... and elephants. Blood 2002, 100:4679-4680.
50. Dingli D., Pacheco J. Allometric scaling of the active hematopoietic stem cell pool across mammals. PLoS ONE 2006, 2:1-4.
51. Luzzatto L., Nafa K. Genetics of PNH. PNH and the GPI-linked Proteins 2000, 21-47. Academic Press, San Diego. N. Young, J. Moss (Eds.).
52. O'Keefe C.L., Sugimori C., Afable M., Clemente M., Shain K., Araten D.J., List A., Epling-Burnette P.K., Maciejewski J.P. Deletions of Xp22.2 including PIG-A locus lead to paroxysmal nocturnal hemoglobinuria. Leukemia 2011, 25:379-382.
53. Laken S., Petersen G., Gruber S., Oddoux C., Ostrer H., Giardiello F., Hamilton S., Hampel H., Markowitz A., Klimstra D., Jhanwar S., Winawer S., Offit K., Luce M., Kinzler K., Vogelstein B. Familial colorectal cancer in Ashkenazim due to a hypermutable tract in APC. Nat. Genet. 1997, 17:79-83.
54. Kilpivaara O., Mukherjee S., Schram A., Wadleigh M., Mullally A., Ebert B., Bass A., Marubayashi S., Heguy A., Garcia-Manero G., Kantarjian H., Offit K., Stone R., Gilliland D., Klein R., Levine R. Nat. Genet. 2009, 41:455-459.
55. Chen J., Ferec C., Cooper D. Closely spaced multiple mutations as potential signatures of transient hypermutability in human genes. Hum. Mutat. 2009, 30:1435-1448.
56. Drake J. Mutations in clusters and showers. PNAS 2007, 104:8203-8204.
57. Kaufmann W. Mutational showers during carcinogenesis. Pig. Cell Melanoma Res. 2012, 25:566-568.
58. Nik-Zainal S., Alexandrov L., Wedge D., VanLoo P., Greenman C., Raine K., Jones D., Hinton J., Marshall J., Stebbings L., Menzies A., Martin S., Leung K., Chen L., Leroy C., Ramakrishna M., Rance R., Lau K., Mudie L., Varela I., McBride D., Bignell G., Cooke S., Shlien A., Gamble J., Whitmore I., Maddison M., Tarpey P., Davies H., Papaemmanuil E., Stephens P., McLaren S., Butler A., Teague J., Jonsson G., Garber J., Silver D., Miron P., Fatima A., Boyault S., Langerod A., Tutt A., Martens J., Aparicio S., Borg A., Salomon A., Thomas G., Borrensen-Dale A., Richardson A., Neuberger M., Futreal P., Campbell P., Stratton M. Mutational processes molding the genomes of 21 breast cancers. Cell 2012, 149:979-993.
59. Shee C., Gibson J., Rosenberg S. Two mechanisms produce mutation hotspots at DNA breaks in Escherichia coli. Cell Rep. 2012, 2:714-721.
60. Wang J., Gonzalez K., Scaringe W., Tsai K., Liu N., Gu D., Li W., Hill K., Sommer S. Evidence for mutation showers. PNAS 2007, 104:8403-8408.
61. Grant B., Trombley L., Hunter T., Nicklas J., O'Neill J., Albertini R. HPRT mutations in vivo in human CD34+ hematopoietic stem cells. Mutat. Res. 1999, 8847:1-16.
62. Langlois R., Bigbee W., Jensen R. Flow cytometric characterization of normal and variant cells with monoclonal antibodies specific for glycophorin A. J. Immunol. 1985, 134:4009-4017.
63. Araten D., Sanders K., Pu J., Lee S. Spontaneously arising red cells with a McLeod-like phenotype in normal donors. Mutat. Res. 2009, 671:1-5.
64. Koptyra M., Falinski R., Nowicki M., Stoklosa T., Majsterek I., Nieborowska-Skorska M., Blasiak J., Skorski T. BCR/ABL kinase induces self-mutagenesis via reactive oxygen species to encode imatinib resistance. Blood 2006, 107:319-327.
65. Alcalay M., Meani N., Gelmetti V., Fantozzi A., Fagioli M., Orleth A., Riganelli D., Sebastiani C., Cappelli E., Casciari C., Sciurpi M., Mariano A., Minardi S., Luzi L., Muller H., DiFiore P., Frosina G., Pelicci P. Acute myeloid leukemia fusion proteins deregulate genes involved in stem cell maintenance and DNA repair. J. Clin. Invest. 2003, 112:1751-1761.
66. Mullighan C., Goorha S., Radtke I., Miller C., Coustan-Smith E., Dalton J., Girtman K., Mathew S.J.M.J., Pounds S., Su X., Pui C., Relling M., Evans W., Shurtleff S., Downing J. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature 2007, 446:758-764.
67. Adimoolam S., Ford J. p53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene. Proc. Natl. Acad. Sci. USA 2002, 99:12985-12990.
68. Chatterjee A., Mambo E., Osada M., Upadhyay S., Sidransky D. The effect of p53-RNAi and p53 knockout on human 8-oxoguanine DNA glycosylase (hOgg1) activity. FASEB J. 2006, 20:112-114.
69. Bielas J., Heddle J. Elevated mutagenesis and decreased DNA repair at a transgene are associated with proliferation but not apoptosis in p53-deficient cells. Proc. Natl. Acad. Sci. USA 2003, 100:12853-12858.
70. Sands A., Suraokar M., Sanchez A., Marth J., Donehower L., Bradley A. p53 deficiency does not affect the accumulation of point mutations in a transgene target. Proc. Natl. Acad. Sci. USA 1995, 92:8517-8521.
71. Liang L., Shao C., Deng L., Mendonca M., Stambrook P., Tischfield J. Radiation-induced genetic instability in vivo depends upon p53 status. Mutat. Res. 2002, 502:69-80.
72. Honma M., Momose M., Tanabe H., Sakamoto H., Yu Y., Little J., Sofuni T., Hayashi M., Carcinogenesis M. Requirement of wild-type p53 protein for maintenance of chromosomal integrity. Mol. Carcinogen. 2000, 28:203-214.
73. Christophorou M., Ringshausen I., Finch A., Swigart L., Evan G. The pathological response to DNA damage does not contribute to p53-mediated tumour suppression. Nature 2006, 443:214-217.
74. Loeb L.A. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res. 1991, 51:3075-3079.
75. Armitage P., Doll R. The age distribution of cancer and a multistage theory of carcinogenesis. Brit. J. Cancer 1954, 8:1-12.