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Chemical Mutagens David M. DeMarini, Ph.D. US Environmental Protection Agency Research Triangle Park, North Carolina Disclaimer This Presentation Does Not Necessarily Reflect the Policy of the U.S. EPA The Mutagenesis Moonshot: The Propitious Beginnings of the Environmental Mutagen Society David M. DeMarini U.S. Environmental Protection Agency Outline • Mutagen 1 (X-rays): mutating genes experimentally • Mutagen 2 (UV): genetic material & genetic repair • Mutagen 3 (mustard gas): chemical mutagens • Fallout from fallout: mutagenesis at Oak Ridge • Pollution, politics and persuasion: influence of the environment on our germ cells • Emergence of the environmental movement • EMS takes off in 1969 • Early successes • Legacy of action without activism Before the Mutagens Gregor Mendel In 1866 this Czech priest deduced that particulate units explain hereditary traits in peas. Hugo de Vries (The Netherlands) 1. In 1900 he coined the term “mutation.” 2. In 1901 he noted that the artificial induction of mutations will permit production of better plants and animals. 3. In 1904 he suggested in a lecture to U.S. scientists that X-rays might be able to alter the hereditary particles in the germ cells. Mutagen 1: X-Rays Early Studies in Germany in 1905- 1912 on the Mutagenicity of X-rays First studies of X-ray-induced mutagenicity were done for morphological changes in Bacillus and Aspergillus Erwin Baur Elizabeth Schiemann X-Rays Are Mutagenic • Hermann Muller at U of Texas (Science 64:84, 1927) reported on the first mutagenicity assay (SLRL in Drosophila) and first mutagen (X-rays), but he did not show any data. He reported the data in PNAS 14:714, 1928. • Lewis Stadler at U of Missouri showed the mutagenicity of X- rays in maize (PNAS 14:69, 1928) and barley (Science 68:186, 1928). X-Rays and Cancer? • In his 1927 paper, Muller suggested that mutations might cause cancer. • In a 1934 paper Muller (Proc Int Radiol Congr 4th, 2:100) noted “…producing mutations in somatic cells by radiation … in which mitosis occurs, may result in cancer, leukemia, etc.” Mutagen 2: UV Light UV Light is Mutagenic • Edgar Altenburg at Rice University in Houston, Texas showed UV was mutagenic in Drosophila (Science 78:587, 1933). • Lewis Stadler at U of Missouri showed UV was mutagenic in maize (PNAS 22:584, 1936). UV Light Suggests Nucleic Acid as the Genetic Material Frederick Gates at the Rockefeller Institute in New York showed that the maximum bactericidal effect of UV was the absorption spectrum of nucleic acids (265 nm) and suggested that UV damage to nucleic acid caused the cells to die (FL Gates, J Gen Physiol 13:231, 1929). Alexander Hollaender • Published in 1929 on UV bactericidal effects while at the Univ of Wisconsin. • At NIH, he showed UV induced maximal mutagenesis in fungal spores at 265 nm and suggested that UV acted on nucleic acid to produce mutations. (Emmons & Hollaender, Am J Bot 26:467, 1939; Hollaender, Proc 7th Int Cong Genet 153, 1941; J Bacteriol 46:531, 1943). Hollaender Gave First Suggestion That Cells Can Repair UV Damage Based on studies showing higher survival of UV-irradiated fungal spores after being held in liquid medium prior to plating, Hollaender suggested “the possibility of recovery of the irradiated bacteria is not entirely excluded.” Hollaender & Curtis (Proc Soc Exp Biol Med 33:61, 1935), and Hollaender & Claus (J Gen Physiol 19:753, 1936). First UV-Sensitive Mutant in 1946 Evelyn Witkin at Rutgers Univ in New Jersey isolated the first UV-sensitive mutants of E. coli. (PNAS 32:59, 1946; Genetics 32:221, 1947). DNA Repair Emerges from UV Work • Repair replication in the gap generated by excision of UV- induced DNA damage was discovered by Pettijohn & Hanawalt at Stanford (J Mol Biol 9:395, 1964) and Setlow & Carrier at Oak Ridge Richard Setlow Phil Hanawalt (PNAS 81:7397, 1964). • XP cells were deficient in repair replication after UV James Cleaver discovered by Cleaver at UC- San Francisco (Nature 218:652, 1968). Mutagen 3: Chemicals Allyl isothiocyanate Auerbach and Robson • Mustard gas induced SLRL in Drosophila (reported to UK Ministry of Supply 1942). • Allyl isothiocyanate induced SLRL (Auerbach & Robson, Nature 154:81, 1944). • Mustard gas data published (Auerbach & Robson, Nature 157:302, 1946). More Chemical Mutagens (1946-1948) • Iosif Rapoport (USSR) reported that epichlorohydrin, ethylene oxide, and glycidol induced SLRL (Rapoport, C R Dokl Acad Sci USSR 54:65, 1946; 60:469, 1948). • Milislav Demerec at Cold Spring Harbor, New York confirmed Auerbach’s work and was the first to show a rodent carcinogen, 1,2,5,6-dibenzanthracene, was a germ-cell mutagen in Drosophila (Demerec, Nature 159:604, 1947). Fallout from Fallout: Mutagenesis Comes to Oak Ridge Ionizing Radiation Causes Heritable Chromosomal Mutations in Mice • Snell (1937) in the U.S. and Hertwig and Brenneke (1937) in Germany had provided the foundation for the establishment of the rodent dominant-lethal and heritable- translocation tests to detect heritable chromosomal effects of ionizing radiation. • No methods were available to detect heritable gene mutations in mammals. Ionizing Radiation and Concern for Germ-Cell Mutation • The detonation of the atomic bombs in 1945 caused the U.S. government to establish the Biology Divison at the Oak Ridge National Laboratory in Tennessee in 1947 with Alexander Hollaender as the Director. • Hollaender hired William (Bill) Russell to determine if ionizing radiation caused germ-cell mutations in mice because the government was unwilling to make public policy based on data from an insect. Ionizing Radiation Induces Germ-Cell Gene Mutations in Mice in 1951 • Bill Russell (CSHSQB 16:327, 1951) developed the mouse 7-locus specific locus assay and showed that ionizing radiation was a germ-cell mutagen in mice. • With Liane Russell, Bill showed that fractionated doses and different dose rates gave first evidence of DNA repair in mammals (Russell et al., Science 128:1546, 1958). Radiation Risk Assessment • Risk for germ-cell mutations by ionizing radiation in mice was extrapolated to humans in the 1950s (Neel & Lewis, Annu Rev Genet 24:327, 1990) and extended to chemicals and cancer risk assessment in the 1970s (Calabrese, James Neel Chemico-Biol Interact 308:110, 2019). • Work by Mary Lyon (1966) at Harwell, UK with a 5-locus assay and Udo Ehling (1983) in Berlin added to these assessments. Mary Lyon Oak Ridge Scientists & Founders of EMS Fred de Serres Fred de Serres designed a forward- mutation assay at the ad-3 locus in Neurospora to mimic Russell’s mouse specific-locus assay. It was the first microbial assay that detected both gene & chromosomal (multi-locus) mutations and permitted one to infer the nature of Fred de Serres the mutation (base substitution, frameshift, or deletion) (de Serres & Kolmark, Nature 182:1249, 1958). Ernest H.Y. Chu With Heinrich Malling, Ernie Chu developed one of the first gene-mutation assays in mammalian cells, the assay in V79 cells that detected BrdU- resistant mutants (Chu and Malling, PNAS 61:1306, 1968). Abraham W. Hsie Abe Hsie developed the quantitative CHO/Hprt assay, which became a standard mammalian cell mutagenesis assay (Hsie et al., Somatic Cell Genet 1:383, 1975) Heinrich V. Malling • Improved the Neurospora assay • Co-invented the V79/BrdU assay. • Invented first tester set (Malling & de Serres (Mutat Res 6:181, 1968). • Invented enzymatic in vitro (S30) metabolic activation (Malling, Mutat Res 13:425, 1971). • Invented biochemical specific-locus assay (Malling & Valcovic,1977). • Invented transgenic mouse assay (Malling & Burkhart, Mutat Res 212:11, 1989). More Chemical Mutagens Discovered, Producing Increasing Concern for Environmental Germ-Cell Mutagens More Chemical Mutagens Discovered • Horowitz (1946) at Stanford found Edward mustard gas mutagenic in Tatum Neurospora. • Tatum (1947) at Yale found derivative of mustard gas was Milislav mutagenic in E. coli. Demerec • Demerec (1951) at Cold Spring Harbor found formaldehyde mutagenic in E. coli. Waclav • Szybalski (1958) at Rutgers found Szybalski 22/431 chemicals mutagenic in E. coli. • Freese (1968) at NIH found base Ernst analogues, alkylating agents, drugs Freese were mutagenic. Scientific Concern About Environmental Germ-Cell Mutagens • Many untested chemicals being introduced into the environment after World War II. • Muller expressed concern for chemical germ- cell mutagens along with radiation. • Joshua Lederberg at U of Wisconsin wrote to Muller in 1950 to bring this concern to the National Academies of Science (NAS). • Lederberg raised this concern directly to the NAS in 1955. More Concern • Lederberg stressed concern at 1962 genetics conference. Joshua • Matthew Meselson at Lederberg Harvard asked James Crow at U of Wisconsin to organize an NIH genetics conference Matthew in 1966 to address this issue. Messelson • Crow published influential summary of the NIH conference (Crow, Scientist James Citizen, June-July 113, 1968). Crow Even More Concern • K. Luning (1966) in Stockholm screened 6 derivatives of phenobarbital for mutagenicity in Drosophila. • S. Epstein (1968) at Harvard screened 39 chemicals in mouse Sam Epstein dominant-lethal assay (aflatoxin, extracts of air and drinking water, food additives, pesticides and drugs). • M. Legator and S. Epstein (1969) proposed in the Mrak Report that pesticides should be tested for mutagenicity prior to approval. Marvin Legator The Environmental Movement Oil Spill off coast of Santa Barbara 1969 Cuyahoga River on fire in Cleveland, Ohio 1969 Some Environmental Events of the 1960s • Thalidomide removed from U.S. market due to teratogenic effects in 1961. • London smog kills 750 in 1962. • Berne Accord to Protect Rhine River 1963. • Nuclear Test Ban Treaty (US/USSR) 1963. • Weather inversion in NYC kills 80 in 1964. • U.S. Senate hearings on leaded gasoline in 1966. • France begins nuclear testing in the Pacific 1966. • Oil spill of coast of Santa Barbara 1969. • U.S. Dept of Health Education & Welfare recommends genetic toxicity testing of pesticides in 1969.
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