Endogenous Formaldehyde Is a Hematopoietic Stem Cell Genotoxin and Metabolic Carcinogen

Molecular Cell

Volumn 60, Issue 1, 2015, Pages 177-188

  Pontel, Lucas B ^a   Rosado, Ivan V ^a,b   Burgos Barragan, Guillermo ^a   Garaycoechea, Juan I ^a   Yu, Rui ^c   Arends, Mark J ^d   Chandrasekaran, Gayathri ^e   Broecker, Verena ^f   Wei, Wei ^g   Liu, Limin ^g   Swenberg, James A ^c   Crossan, Gerry P ^a   Patel, Ketan J ^a,h  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b Instituto de Biomedicina de Sevilla   (Spain)

^c University of North Carolina at Chapel Hill   (United States)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

^f ADDENBROOKE S HOSPITAL   (United Kingdom)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; ALCOHOL DEHYDROGENASE 5; CARCINOGEN; CATALASE; DRINKING WATER; FANCONI ANEMIA GROUP D2 PROTEIN; FORMALDEHYDE; GENOTOXIN; METHANOL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; S NITROSOGLUTATHIONE; TOXIN; UNCLASSIFIED DRUG; ADH5 PROTEIN, MOUSE; DNA ADDUCT; FANCD2 PROTEIN, MOUSE; MUTAGENIC AGENT;

ARTICLE; BONE MARROW DEPRESSION; BONE MARROW TRANSPLANTATION; CONTROLLED STUDY; DNA ADDUCT; DNA DAMAGE; EMBRYO; FEMALE; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL; KIDNEY DISEASE; LIVER CELL; LIVER DISEASE; MALE; MOUSE; NONHUMAN; TANDEM MASS SPECTROMETRY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ANIMAL; CELL CULTURE; CYTOLOGY; GENE INACTIVATION; GENETICS; KIDNEY; LIVER; METABOLISM; PATHOLOGY;

ALCOHOL DEHYDROGENASE; ANIMALS; CARCINOGENS; CELLS, CULTURED; DNA ADDUCTS; FANCONI ANEMIA COMPLEMENTATION GROUP D2 PROTEIN; FORMALDEHYDE; GENE KNOCKOUT TECHNIQUES; HEMATOPOIETIC STEM CELLS; KIDNEY; LIVER; MICE; MUTAGENS;

EID: 84945301259     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.08.020     Document Type: Article

References (43)

1. Anderson M.M., Hazen S.L., Hsu F.F., Heinecke J.W. Human neutrophils employ the myeloperoxidase-hydrogen peroxide-chloride system to convert hydroxy-amino acids into glycolaldehyde, 2-hydroxypropanal, and acrolein. A mechanism for the generation of highly reactive alpha-hydroxy and alpha,beta-unsaturated aldehydes by phagocytes at sites of inflammation. J. Clin. Invest. 1997, 99:424-432.
2. Andrew P.J., Mayer B. Enzymatic function of nitric oxide synthases. Cardiovasc. Res. 1999, 43:521-531.
3. Auerbach C. The Mutagenic Mode of Action of Formalin. Science 1949, 110:419-420.
4. Blonder J.P., Mutka S.C., Sun X., Qiu J., Green L.H., Mehra N.K., Boyanapalli R., Suniga M., Look K., Delany C., et al. Pharmacologic inhibition of S-nitrosoglutathione reductase protects against experimental asthma in BALB/c mice through attenuation of both bronchoconstriction and inflammation. BMC Pulm. Med. 2014, 14:3.
5. Bogliolo M., Schuster B., Stoepker C., Derkunt B., Su Y., Raams A., Trujillo J.P., Minguillón J., Ramírez M.J., Pujol R., et al. Mutations in ERCC4, encoding the DNA-repair endonuclease XPF, cause Fanconi anemia. Am. J. Hum. Genet. 2013, 92:800-806.
6. Dorokhov Y.L., Shindyapina A.V., Sheshukova E.V., Komarova T.V. Metabolic methanol: molecular pathways and physiological roles. Physiol. Rev. 2015, 95:603-644.
7. Garaycoechea J.I., Crossan G.P., Langevin F., Daly M., Arends M.J., Patel K.J. Genotoxic consequences of endogenous aldehydes on mouse haematopoietic stem cell function. Nature 2012, 489:571-575.
8. Herskowitz I.H. The differential induction of lethal mutations by formalin in the two sexes of Drosophila. Science 1950, 112:302-303.
9. Hira A., Yabe H., Yoshida K., Okuno Y., Shiraishi Y., Chiba K., Tanaka H., Miyano S., Nakamura J., Kojima S., et al. Variant ALDH2 is associated with accelerated progression of bone marrow failure in Japanese Fanconi anemia patients. Blood 2013, 122:3206-3209.
10. Houghtaling S., Timmers C., Noll M., Finegold M.J., Jones S.N., Meyn M.S., Grompe M. Epithelial cancer in Fanconi anemia complementation group D2 (Fancd2) knockout mice. Genes Dev. 2003, 17:2021-2035.
11. Jensen R.P., Luo W., Pankow J.F., Strongin R.M., Peyton D.H. Hidden formaldehyde in e-cigarette aerosols. N. Engl. J. Med. 2015, 372:392-394.
12. Kashiyama K., Nakazawa Y., Pilz D.T., Guo C., Shimada M., Sasaki K., Fawcett H., Wing J.F., Lewin S.O., Carr L., 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, 92:807-819.
13. Kiel M.J., Yilmaz O.H., Iwashita T., Yilmaz O.H., Terhorst C., Morrison S.J. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005, 121:1109-1121.
14. Knipscheer P., Räschle M., Smogorzewska A., Enoiu M., Ho T.V., Schärer O.D., Elledge S.J., Walter J.C. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 2009, 326:1698-1701.
15. Langevin F., Crossan G.P., Rosado I.V., Arends M.J., Patel K.J. Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice. Nature 2011, 475:53-58.
16. Libbrecht L., Desmet V., Roskams T. Preneoplastic lesions in human hepatocarcinogenesis. Liver Int. 2005, 25:16-27.
17. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993, 362:709-715.
18. Lindahl T., Nyberg B. Rate of depurination of native deoxyribonucleic acid. Biochemistry 1972, 11:3610-3618.
19. Liu L., Yan Y., Zeng M., Zhang J., Hanes M.A., Ahearn G., McMahon T.J., Dickfeld T., Marshall H.E., Que L.G., Stamler J.S. Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 2004, 116:617-628.
20. Loenarz C., Schofield C.J. Expanding chemical biology of 2-oxoglutarate oxygenases. Nat. Chem. Biol. 2008, 4:152-156.
21. Luo W., Li H., Zhang Y., Ang C.Y. Determination of formaldehyde in blood plasma by high-performance liquid chromatography with fluorescence detection. J. Chromatogr. B Biomed. Sci. Appl. 2001, 753:253-257.
22. Mattila J.T., Thomas A.C. Nitric oxide synthase: non-canonical expression patterns. Front. Immunol. 2014, 5:478.
23. McGhee J.D., von Hippel P.H. Formaldehyde as a probe of DNA structure. r. Mechanism of the initial reaction of Formaldehyde with DNA. Biochemistry 1977, 16:3276-3293.
24. Miller M.R., Megson I.L. Recent developments in nitric oxide donor drugs. Br. J. Pharmacol. 2007, 151:305-321.
25. Nguyen T., Brunson D., Crespi C.L., Penman B.W., Wishnok J.S., Tannenbaum S.R. DNA damage and mutation in human cells exposed to nitric oxide in vitro. Proc. Natl. Acad. Sci. USA 1992, 89:3030-3034.
26. Niedernhofer L.J., Garinis G.A., Raams A., Lalai A.S., Robinson A.R., Appeldoorn E., Odijk H., Oostendorp R., Ahmad A., van Leeuwen W., et al. A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis. Nature 2006, 444:1038-1043.
27. Oberbeck N., Langevin F., King G., de Wind N., Crossan G.P., Patel K.J. Maternal aldehyde elimination during pregnancy preserves the fetal genome. Mol. Cell 2014, 55:807-817.
28. Ridpath J.R., Nakamura A., Tano K., Luke A.M., Sonoda E., Arakawa H., Buerstedde J.M., Gillespie D.A., Sale J.E., Yamazoe M., et al. Cells deficient in the FANC/BRCA pathway are hypersensitive to plasma levels of formaldehyde. Cancer Res. 2007, 67:11117-11122.
29. Rogers J.M., Brannen K.C., Barbee B.D., Zucker R.M., Degitz S.J. Methanol exposure during gastrulation causes holoprosencephaly, facial dysgenesis, and cervical vertebral malformations in C57BL/6J mice. Birth Defects Res. B Dev. Reprod. Toxicol. 2004, 71:80-88.
30. Rosado I.V., Langevin F., Crossan G.P., Takata M., Patel K.J. Formaldehyde catabolism is essential in cells deficient for the Fanconi anemia DNA-repair pathway. Nat. Struct. Mol. Biol. 2011, 18:1432-1434.
31. Sanghani P.C., Stone C.L., Ray B.D., Pindel E.V., Hurley T.D., Bosron W.F. Kinetic mechanism of human glutathione-dependent formaldehyde dehydrogenase. Biochemistry 2000, 39:10720-10729.
32. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., Casero R.A., Shi Y. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119:941-953.
33. Staab C.A., Alander J., Morgenstern R., Grafström R.C., Höög J.-O. The Janus face of alcohol dehydrogenase 3. Chem. Biol. Interact. 2009, 178:29-35.
34. Stingele J., Schwarz M.S., Bloemeke N., Wolf P.G., Jentsch S. A DNA-dependent protease involved in DNA-protein crosslink repair. Cell 2014, 158:327-338.
35. Swenberg J.A., Moeller B.C., Lu K., Rager J.E., Fry R.C., Starr T.B. Formaldehyde carcinogenicity research: 30 years and counting for mode of action, epidemiology, and cancer risk assessment. Toxicol. Pathol. 2013, 41:181-189.
36. Till J.E., McCulloch E.A. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat. Res. 1961, 14:213-222.
37. Trocho C., Pardo R., Rafecas I., Virgili J., Remesar X., Fernández-López J.A., Alemany M. Formaldehyde derived from dietary aspartame binds to tissue components in vivo. Life Sci. 1998, 63:337-349.
38. Walport L.J., Hopkinson R.J., Schofield C.J. Mechanisms of human histone and nucleic acid demethylases. Curr. Opin. Chem. Biol. 2012, 16:525-534.
39. Walter D., Lier A., Geiselhart A., Thalheimer F.B., Huntscha S., Sobotta M.C., Moehrle B., Brocks D., Bayindir I., Kaschutnig P., et al. Exit from dormancy provokes DNA-damage-induced attrition in haematopoietic stem cells. Nature 2015, 520:549-552.
40. Wei W., Li B., Hanes M.A., Kakar S., Chen X., Liu L. S-nitrosylation from GSNOR deficiency impairs DNA repair and promotes hepatocarcinogenesis. Sci. Transl. Med. 2010, 2:19ra13.
41. Yu B.P. Cellular defenses against damage from reactive oxygen species. Physiol. Rev. 1994, 74:139-162.
42. Yu R., Lai Y., Hartwell H.J., Moeller B.C., Doyle-Eisele M., Kracko D., Bodnar W.M., Starr T.B., Swenberg J.A. Formation, accumulation and hydrolysis of endogenous and exogenous formaldehyde induced DNA damage. Toxicol. Sci. 2015, 146:170-182.
43. Zhou W., Otto E.A., Cluckey A., Airik R., Hurd T.W., Chaki M., Diaz K., Lach F.P., Bennett G.R., Gee H.Y., et al. FAN1 mutations cause karyomegalic interstitial nephritis, linking chronic kidney failure to defective DNA damage repair. Nat. Genet. 2012, 44:910-915.