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Herbert Tabor, 1918–2020: Polyamines, NIH, and the JBC Downloaded by Guest on October 2, 2021 7 H RETROSPECTIVE Herbert Tabor, 1918–2020: Polyamines, NIH, and the JBC RETROSPECTIVE Reed B. Wicknera,1 On August 20, 2020, at the age of 101, Herbert Tabor died peacefully at his home on the National Institutes of Health campus in Bethesda, Maryland. Herb was best known for his elucidation of the biochemical pathways for polyamines, including characterization of the biosynthetic enzymes, their genes and regulation, and the functions of the polyamines, chiefly using Escherichia coli and Saccharomyces cerevisiae.He was Editor-in-Chief of The Journal of Biological Chem- istry (JBC) for nearly 40 years, overseeing its dramatic expansion and modernization, leading conversion from the traditional means of distribution of scientific information to the present web-based system. Herbert Tabor was born November 28, 1918, in New York City, and was graduated from Townsend Harris High School in 1933 at the age of 14. At Harvard College he entered the Biochemical Sciences pro- gram headed by John Edsall. Graduating in 1937, Herb attended Harvard Medical School, where his work with A. Baird Hastings on the ionization constant Herbert Tabor in his laboratory in 1974. Image credit: of MgHPO4 was the subject of his first paper, fittingly Tabor family photo collection. in the JBC (1). As an intern at Yale-New Haven Hospi- tal in 1942, Herb gave a patient with streptococcal donated to the government for this purpose. Herb was septicemia an injection of penicillin, the first dose in assigned to work with Sanford Rosenthal, and they the first major clinical trial of the drug in the United showed that saline infusions were an adequate sub- States (it worked!). Unbeknownst to Herb at the time stitute for the usual plasma in the treatment of burns or (until 25 years later), that dose was prepared at Merck shock (3). Because plasma was in short supply during by Gilbert Ashwell, later to be a distinguished col- the war years, this was an important advance. league and close friend of Herb at the NIH. The atmosphere at NIH was very collegial (as I think In January 1943, Herb joined the US Public Health Service and was assigned as the Medical Officer to the it is now), and Herb soon became friends with Arthur Coast Guard cutter USCGC Duane, escorting convoys Kornberg, Leon Heppel, and Bernard Horecker, each between the United States and Britain. The events of whom had only recently arrived at NIH. In 1946, challenged his limited surgical training [recounted in they formed a daily lunchtime seminar group, critically the article, “It all started on a streetcar in Boston” (2)], evaluating new papers (mostly in biochemistry) and but he managed without untoward sequellae. their own work. This institution continued for many decades with a dazzling array of participants, including NIH Days Maxine Singer, Gil Ashwell, Jerry Hurwitz, Vic Gins- In September 1943, Herb was transferred to the NIH in burg, Jesse Rabinowitz, Osamu Hayaishi, Jay Seeg- Bethesda, Maryland, at that time relocated from miller, Alan Mehler, Paul Marks, Howard Hiatt, downtown Washington, DC, to six small buildings on Herman Kalckar, Bruce Ames, Jack Strominger, Hans land that Helen and Luke Wilson had only recently Klenow, and Chris Raetz. This seminar series was very aLaboratory of Biochemistry and Genetics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892 Author contributions: R.B.W. wrote the paper. The author declares no competing interest. Published under the PNAS license. 1Email: [email protected]. Published January 25, 2021. PNAS 2021 Vol. 118 No. 5 e2023986118 https://doi.org/10.1073/pnas.2023986118 | 1of3 Downloaded by guest on October 2, 2021 central to the intellectual life of the early participants mutation producing streptomycin-resistance. Polyamine- and evolved in later years into a joint seminar of Herb’s deficient yeast mutants were oxygen-sensitive and department (“Laboratory” in NIH terms), the Labora- polyamine-deficient E. coli were sensitive to the tory of Biochemical Pharmacology, and the Laboratory oxygen-generating compound paraquat, showing of Biochemistry and Metabolism led by Gil Ashwell. that polyamines have an important role in protec- The vigorous give-and-take and careful examination tion from oxidation. Following their early discovery of the paper of the day was very educational for me as of glutationylspermidine in E. coli, trypanosomes a young postdoc in Herb’s group. were found by others to have a diglutathionylspermidine From the mid-1940s to the mid-1950s, Herb stud- that was important in protection of trypanosomes from ied the effects of folate in hemoglobin regeneration, oxidation, leading to the use of the ornithine decarbox- the mechanism of histidine degradation (via for- ylase inhibitor difluoroornithine as an effective treatment miminoglutamate and folate intermediates), and the for some cases of trypanosomiasis. use of urinary formiminoglutamate to assess the ef- Recently, with Manas Chattopadhyay, Herb fectiveness of antifolate drugs used in the treatment of showed that polyamines are critical for the glutamate- leukemia. He purified diamine oxidase (histaminase) dependent acid resistance of E. coli, mediated by the and showed that it converted putrescine (1,4-amino- alternative σ factor (rpoS), the transcription factor butane) to Δ1-pyrroline, one of his first forays into the GadE, and the two glutamate decarboxylases (8). polyamines. Their 2015 paper reporting these results in JBC was In 1946, Herb married Celia White (M.D. from 72 years after Herb’s first JBC paper. Columbia University and the first woman intern in Medicine at the Massachusetts General Hospital) who The Journal of Biological Chemistry was to become his lifelong collaborator. Their four The JBC was founded in 1905 (PNAS is a newcomer, wonderful children (Edward, born 1947; Richard and starting only in 1915). Herb became a member of the Marilyn, born 1949; Stanley, born 1954) have all made Editorial Board in 1961, an Associate Editor in 1968, their mark in bioscience and computers. In 1952, Celia and became the Editor-in-Chief in 1971, a post he joined NIH where she collaborated with Herb as they held for 39 years. Herb oversaw the more than 10-fold focused on polyamines. expansion in the size of the journal, along with a broadening of its scope from strictly biochemistry to Polyamines include genetics, cell biology, and other related areas. Herb and Celia together devoted the bulk of their Under Herb’s leadership, the JBC advanced the careers to the study of the polyamines, putrescine, technology of journal publishing, with the first CD spermidine, and spermine. They described their bio- versions of the JBC in 1992, and in 1995 was the first synthetic pathways in bacteria and yeast, the enzymes biomedical journal to publish a completely online and their regulation, and the functions of polyamines version (9). (4, 5). Putrescine is made mainly from ornithine by As Editor-in-Chief, Herb handled many problem decarboxylation by an enzyme regulated by feedback papers, such as complaints about the quality of the degradation. Spermidine and spermine are made by reviews, authorship issues, and referencing problems. transfer of aminopropyl groups from decarboxylated I learned from Herb that, “There are only two kinds of adenosylmethionine. The adenosylmethionine decar- scientists: Those who don’t refer to you, and those boxylase has an unusual pyruvoyl prosthetic group. who don’t refer to you enough.” Modification of polyamines by acetylation and gluta- Herb was a modest, soft-spoken man, totally de- thionylation were found and related to growth at low voted to science, did laboratory work himself, and temperature and stationary phase, respectively (6, 7). worked very hard until the end. He never had a large The Tabors isolated mutants in the biosynthetic group, and gave some of his postdoctorates a great enzymes in E. coli and S. cerevisiae, and constructed deal of independence. For example, Chris Raetz be- polyamine-free strains whose growth was suboptimal gan his work on mutants in enzymes of membrane (E. coli) or arrested (yeast) without added amines. lipid metabolism as a postdoc with Herb (10). Herb They showed that translation, as measured by non- was a truly fine person, very serious, but not without a sense codon read-through or ribosomal frameshift sense of humor. His exposition on some subject might efficiency was critically affected by polyamine deficiency. end with, “I’ve told you all I know, maybe more.” Herb Moreover, the slow growth of E. coli mutants became no Tabor is already missed, but the lessons he taught us growth if cells also had an rpsL (ribosomal protein S12) live on. 1 H. Tabor, A. B. Hastings, The ionization constant of secondary magnesium phosphate. J. Biol. Chem. 148, 627–632 (1943). 2 C. W. Tabor, H. Tabor, It all started on a streetcar in Boston. Annu. Rev. Biochem. 68,1–32 (1999). 3 S. M. Rosenthal, H. Tabor, Electrolyte changes and chemotherapy in experimental burn and traumatic shock and hemorrhage. Arch. Surg. 51, 244–252 (1945). 4 C. W. Tabor, H. Tabor, Polyamines. Annu. Rev. Biochem. 53, 749–790 (1984). 5 C. W. Tabor, H. Tabor, Polyamines in microorganisms. Microbiol. Rev. 49,81–99 (1985). 6 C. W. Tabor, L. G. Dobbs, Metabolism of 1,4-diaminobutane and spermidine in Escherichia coli: The effects of low temperature during storage and harvesting of cultures. J. Biol. Chem. 245, 2086–2091 (1970). 2of3 | PNAS Wickner https://doi.org/10.1073/pnas.2023986118 Herbert Tabor, 1918–2020: Polyamines, NIH, and the JBC Downloaded by guest on October 2, 2021 7 H. Tabor, C. W. Tabor, Isolation, characterization, and turnover of glutathionylspermidine from Escherichia coli. J. Biol. Chem. 250, 2648–2654 (1975). 8 M. K. Chattopadhyay, C. N. Keembiyehetty, W. Chen, H. Tabor, Polyamines stimulate the level of the σ38 subunit (RpoS) of Escherichia coli RNA polymerase, resulting in the induction of the glutamate decarboxylase-dependent acid response system via the gadE regulon.
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