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Biographical Memoirs: Volume 64
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Biographical Memoirs: Volume 64 FELIX HAUROWITZ March 1, 1896-December 2, 1987 BY FRANK W. PUTNAM FELIX HAUROWITZ was born in Prague, then the capital of Bohemia and one of the provinces of the Austro-Hungarian empire. In his long life he saw many changes in the world, including the collapse of that empire at the end of World War I, in which he served, and the invasion of Prague by Hitler's army at the beginning of World War II. His flight with his family to Turkey was followed by a decade there before he moved to Indiana University at Bloomington, where he lived and worked the rest of his life. He survived successive political revolutions, and he participated in revolutions in science and medicine that have affected the condition of humankind. Felix and his wife, Gina, and family were displaced from the country and culture he cherished, but he never forgot either. In his last days he often talked about his early experiences in Prague. Yet he was fated to spend more than half his life in other countries, Turkey and America, which he also came to love. He was of a generation that will not be seen again. The product of centuries of European intellectual tradition-learned scholars, dedicated scientists, enlightened human beings—they were driven by barbaric intolerance to a new land to which they contributed so much. Their impact will be enduring, and Felix Haurowitz was one of the great ones among them.
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Biographical Memoirs: Volume 64 Felix came from a family engaged in the textile trade but interested in literature, music, and foreign languages. German was his native language, but because Prague was predominantly Czech, he also spoke fluent Czech since his early childhood. His early education was at home with private teachers, then in a Catholic school run by a German order, and finally in a gymnasium. There for eight years he had Latin lessons daily and also studied Greek. No doubt this contributed to his linguistic fluency, for he later mastered Turkish well enough to lecture and write books in that language. Although the gymnasium taught a variety of subjects, including mathematics in which he excelled, it offered very little chemistry. He detested the required sports and gymnastic lessons but later became an enthusiastic mountaineer and skier. During the gymnasium years he also took private lessons in English, French, and Italian and also piano lessons. In later life he played the piano daily. He said he never practiced or played perfectly but that he played for personal satisfaction and relaxation. On completing the gymnasium he enrolled in a textile school to please his father, although his mother wanted him to become a doctor. He enjoyed the textile school and said he learned much there of use for his later work in the laboratory. However, in November 1915 he was drafted for military service. He was assigned to an Austrian artillery battalion and sent to officers' school in Hungary. He made the highest grade in his class and was promoted to Fähnrich (ensign). He was made commander of the artillery battalion and assigned to the Austrian front in the southern Tirol. However, because they occupied an inaccessible ridge, there was little activity, so he began to prepare for medical school by reading textbooks of inorganic and organic chemistry by Holleman. These he found fascinating. In April 1918 he was given leave to enroll in the medical school of the Ger-
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Biographical Memoirs: Volume 64 man University in Prague. The war ended in October 1918 with the disintegration of the Austro-Hungarian empire, and Czechoslovakia became an independent republic. In his first year in medical school Haurowitz worked as a volunteer assistant in the Department of Physiological Chemistry for Professor Richard von Zeynek, a hemoglobin chemist, and thereby began a life interest in this critical respiratory protein. His initial assignment was to work with Dr. Hedwig Langecker from whom he received his first introduction to the techniques of the biochemistry laboratory. Haurowitz analyzed the lipid-rich gonads of the jellyfish Rhizostoma cuvieri, which von Zeynek had collected. The latter was so pleased with the young student's report that he edited it and sent it off to the Hoppe-Seyler's Zeitschrift für physiologische Chemie with Haurowitz as the sole author. This was the latter's first publication. Von Zeynek gave him a half-time paid assistantship, which he held until he received his M.D. in 1922, when it was converted to a full-time position. He was asked to prepare crystalline horse hemoglobin and study it spectrophotometrically, and this led to his main research interest in the period from 1922 to 1936. Haurowitz did well in all his courses in medical school; as was the custom, he spent a semester elsewhere, at the University of Würzburg in Bavaria. There he met the famous protein chemist Franz Hofmeister. After receiving his M.D. in 1922, Haurowitz was awarded the Dr. rer. nat. (D.Sc.) in 1923 for several papers published between 1920 and 1923. Already engaged in hemoglobin research, he visited the laboratory of Leonor Michaelis in Berlin to learn physicochemical methods from P. Rona, especially pH measurement, which was then new. A paper on ion measurements in blood serum resulted from this period. In the summer of 1924 he worked in the laboratory of the Nobelist F. Willstaetter in Munich on the purification of gastric lipase.
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Biographical Memoirs: Volume 64 This also led to a publication. The young Haurowitz was fast developing a reputation. The same year the colloid chemist R. E. Liesegang visited him in Prague and invited him to write a book on the advances in biochemistry and pharmacology since the advent of World War I in 1914. Haurowitz declined to write on pharmacology but wrote his first book, Biochemie des Menschen und der Tiere seit 1914. This began a series of ''progress'' books with new ones appearing in German in 1932, 1938, and 1948 and then in English in 1950 and 1959 after he moved to America. These books gave him international recognition, and he later felt that the series in German did much to develop interest in and enhance the status of physiological chemistry and biochemistry in the German-speaking countries at a time when there were very few such departments in Germany. However, the immediate result of his first book and the concurrent research was his appointment as a docent. This rank was similar to that of an assistant professor, but it also entitled the recipient to announce any course he wanted to teach provided it did not duplicate another. He introduced courses in Prague on biophysical chemistry and advances in biochemistry. In 1930 he was appointed a tenured associate professor in the same department and finally achieved independence as a research scientist. On becoming a docent, Felix Haurowitz married Gina Perutz in June 1925. She was a student of art history to whom he had been engaged for some time. She became his lifelong companion, supportive of him in everything he did. A few months after the wedding, they moved to Heidelberg for a research semester in the new Protein Research Institute of Albrecht Kossel, known for his fundamental work on protamines and histones for which he had received a Nobel prize in 1910. On their return to Prague he devoted the next five years almost entirely to research on hemoglo-
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Biographical Memoirs: Volume 64 bin. During this period he attended a series of international congresses where he gave papers on his studies of hemoglobin. He always recalled with pride the memories of the great biochemists he met at these early meetings, their gracious comments on his work, and the correspondence and personal contacts that ensued. During the period of research on hemoglobin in Prague from 1925 through 1936, Haurowitz made a number of fundamental discoveries. Through spectroscopic studies of the combination of various oxidizing agents and other ligands with hemoglobin, he determined the absorption spectra of methemoglobin and other physical properties, and he crystallized several derivatives for the first time. He was the first to isolate fetal hemoglobin (Hb F) from fetal blood, and he crystallized it and determined its affinity for oxygen. He later pointed out that this was the first step in the search for further hemoglobins. However, his attempts to isolate abnormal hemoglobins from the blood of patients with anemias failed because there were no cases of thalassemia or sickle cell anemia in Prague. He also discovered the drastic change in the crystalline shape of deoxyhemoglobin from hexagonal plates to elongated prisms when oxygen was allowed to diffuse into the crystals. He showed this phenomenon to Max Perutz when the latter was in Prague visiting his cousin Gina while en route to Sir William Bragg's laboratory at Cambridge. Max later acknowledged that this surprising change gave him the idea to study the crystallographic structure of hemoglobin. Felix loved to tell of this meeting. He also claimed that this was the first observation of an allosteric reaction, and, in fact, it is sometimes cited as such. While at Prague he also published studies on other proteins and on methods of protein chemistry, but up to 1930 he was most noted for his work on hemoglobin. A new and lifelong research interest began in 1930 and
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Biographical Memoirs: Volume 64 was stimulated by a phone call from a colleague, Fritz Breinl, who had just returned from a year at the Rockefeller Institute in New York. Breinl, a virologist, was excited by the experiments of Karl Landsteiner with synthetic haptens. He asked Haurowitz to read the papers and discuss with him what could be done to solve the mystery of antibody production. Thus began an exciting but short-lived collaboration that led to what was later called the template theory of antibody formation. Equally important, it committed Haurowitz to an experimental study of the role of antigen in antibody production for the rest of his research career. As might be expected, they used horse hemoglobin as an antigen in the work for their first paper. Unlike Landsteiner, who used only qualitative indices for the amount of antigen-antibody precipitate (- or +, ++, +++), Haurowitz and Breinl used quantitative methods to determine the amount of hemoglobin in the precipitate, and they also indirectly determined the amino acid content of the nonhemoglobin portion of the precipitate. In his autobiography for the National Academy, Haurowitz underlined the following statement for emphasis: "I concluded that the antibody must be serum globulin and suggested therefore that the antigen interferes with the process of globulin biosynthesis in such a way that globulins complementarily adjusted to the antigen are formed." Thus began the template theory, as it was later called, to which he adhered with some modifications for the rest of his life. Shortly after this startling theory was announced, Haurowitz began experiments to determine the distribution of the antigen in the organism. Because radioactive isotopes were not yet known, he employed protein antigens to which various colored dyes were attached covalently, for example, arsenic-containing azoproteins. The chemical groups used to derivatize and label the proteins were known as haptens.
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Biographical Memoirs: Volume 64 Haptens can convey antigenic specificity to a protein carrier to which they are linked but by themselves are not antigenic. The antibodies specific for the protein carrier can be removed by a process called absorption so that the remaining antibodies are specific for the chemical hapten. This ingenious procedure pioneered by Landsteiner was further developed by Felix Haurowitz who employed many different haptens and used it for quantitative determination of the composition of the antigen-antibody precipitate, calculation of dissociation constants, and other parameters of the antibody-antigen interaction. It became the primary experimental basis for his further immunochemical research until the introduction of radioactive isotopes. Although he never met Landsteiner, Haurowitz exchanged many reprints with him, and at the Landsteiner Centennial he said that he considered himself "as a kind of student or pupil of Landsteiner." In the mid-1930s immunochemistry was developing rapidly as an exciting new field. In the United States Michael Heidelberger and his co-workers, notably Elvin Kabat, introduced a parallel quantitative approach by using the Kjeldahl method to determine the antibody nitrogen in precipitates of antigenic polysaccharides. The template theory was widely discussed and generally accepted, although Linus Pauling proposed a different concept. However, little was yet known about protein structure, and nothing was even surmised about the role of RNA and DNA in protein biosynthesis. Moreover, the end of the Prague era was at hand, for in Europe war clouds were on the horizon. Breinl returned to his first love, virology, and later died a tragic death from rickettsial fever. In the summer of 1938 when Haurowitz was working at the Carlsberg Laboratory in Copenhagen at the invitation of Albert Fischer, his stay was abruptly terminated by the
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Biographical Memoirs: Volume 64 Munich agreement. Because of Hitler's threat of a Nazi invasion of Czechoslovakia, he decided to return to Prague as quickly as possible to be with his wife and their two children, who had been born in 1929 and 1931. Not daring to cross Germany with a Czechoslovakian passport, he traveled by boat to Poland and continued by train to Prague. He was soon mobilized as an M.D. by the Czech army, but returned to civilian life when Czechoslovakia abandoned the Sudeten area of the country to Germany. The German University became an independent university of the German Reich, and Haurowitz was deprived of his right to teach. Just at that time he received an offer of the chair of biochemistry at the University of Istanbul. Though reluctant to leave Prague, he visited Istanbul, found the conditions favorable, and accepted the offer. Soon after, Hitler's troops invaded Prague. Two weeks later the Haurowitz family left for Istanbul to begin a new life. Most of their property except their furniture and library was seized by the Gestapo. They arrived in Istanbul with only 2,000 koruny (about $70). Toward the end of World War II, severe inflation forced them to sell some of their furniture to supplement his salary. The Haurowitz family loved their life in Istanbul and considered it the most beautiful city in the world both for its natural beauty and for the Roman, Byzantine, and Islamic monuments. Felix and Gina often spoke with pleasure of their life there. They adapted well. Since lectures needed to be given in Turkish, his lectures were at first translated during class, but by the end of the second year he lectured and examined in Turkish. In fact, he was put on a committee to help modernize the Turkish language and rid it of Arabic terms. He published papers in Turkish and also a textbook on biochemistry that went through several editions. He developed a group of hard-working Turkish co-
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Biographical Memoirs: Volume 64 workers, some of whom later became professors in Istanbul and other Turkish universities. He maintained contact with them long after leaving Turkey, and in 1973 the University of Istanbul honored him by conferring the honorary degree of doctor of medicine. At Istanbul Haurowitz's research was almost exclusively on problems of immunochemistry. Much of his time was spent in teaching large lecture and laboratory courses, and the budget was very low, especially during World War II. Yet in this period he published a number of papers in international journals, as well as in Turkish journals. He showed that the antibodies produced by the injection of a uniform antigen, such as an azoprotein, were always heterogeneous and could be fractionated by absorption with more or less modified azoproteins. He reported a method for purification of antibodies based on the dissociation of the antigen-antibody precipitate at low pH. Despite the progress in research, the good life in Istanbul, and the satisfaction gained from the contribution he made to the development of medical education and extension of health care in Turkey, there was concern about the future of the children, who were reaching college age. In 1946 Gina and the two children, Martin and Alice, moved to the United States. However, Felix decided to stay in Turkey for two more years to fulfill his contract. Alice registered as a student at Indiana University in Bloomington and lived at the home of Harry G. Day, a professor of biochemistry in the Department of Chemistry. When Haurowitz visited the family in 1947 he gave a lecture at Dr. Day's invitation. This was followed by a reception where he met H.J. Muller, the geneticist and Nobel laureate whose wife was the daughter of a colleague in Istanbul. The next day Haurowitz was asked whether he would accept an appointment as professor of chemistry to teach biochemistry at Indiana Univer-
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Biographical Memoirs: Volume 64 sity. He said he would be glad to do so but he had to return to Istanbul for one more year and also had been offered the chair of biochemistry in the Medical School at the University of Basel in Switzerland. While en route to Basel, he received the formal offer from Indiana University in London and accepted it. He moved to Bloomington in 1948 and spent the rest of his life there. In 1948 Indiana University was expanding rapidly and was strong in chemistry and biology, particularly in genetics where it had a famous group: H.J. Muller, Tracy Sonneborn, and Ralph Cleland. Irwin Gunsalus and Salvador Luria were also there as assistant professors of microbiology. They asked Haurowitz to teach graduate courses in proteins and nucleic acids, which he gladly did. Among his students was Jim Watson, then a graduate student of Luria. Harry Day became a close friend and helped Haurowitz in many ways, as did his other colleagues in the Chemistry Department, particularly Frank Gucker, the chairman, who later became dean of arts and sciences. In 1950 while I was an assistant professor at the University of Chicago, Haurowitz invited me to give a seminar in the Department of Chemistry, my first such invitation. I was then a member of the Phage Group. I well remember the ferment and excitement in Bloomington at that time. In Bloomington Haurowitz's research was almost entirely devoted to immunochemistry, but in addition to teaching courses in biochemistry and protein chemistry, he found time to write several books. Although he completed another book on the progress of biochemistry (from 1949 to 1959), he felt that the field had expanded too greatly to be covered any more by a single author, and he declined the publisher's request to become editor of a series of such volumes. In 1950 he published a book that had wide influence and the one of which he was most proud, Chemistry
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Biographical Memoirs: Volume 64 Bestimmung bei entmilzten Hunden. Z. Physiol. Chem. 198:191-95. 1932 With F. Breinl. Quantitative Untersuchung der Verteilung eines arsenhaltigen Antigens im Organismus . Z. Physiol. Chem. 205:259-70. With W. Nonnenbruch. Fermente und Autolyse der Leber von normalen und entnierten Meerschweinchen. Z. Exp. Med. 81:752-57. With H. Raudnitz, and F. Petru. Dehydrierung des Cholesterins und der Cholsaeure. Z. Physiol. Chem. 209:103-9. With F. Breinl. Aenderungen der Spezifitaet von Immunserum nach chemischer Vorbehandlung. Z. Immunitaetsforsch. 77:176-86. Biochemie 1924-1931. Dresden and Leipzig: Theodor Steinkopff. 1933 With F. Breinl. Chemische Untersuchung der spezifischen Bindung von Arsanil-Eiweiss und Arsanilsaeure an Immunserum. Z. Physiol. Chem. 214:111-20. With E. Clar. Konstitution der Porphyrine. Ber. Dtsch. Chem. Ges. 66:331-34. With H. Kittel. Magnetisches Verhalten einiger Haemoglobin-Derivate. Ber. Dtsch. Chem. Ges. 66:1046-49. With M. Reiss and J. Balint. Ueber das Hypophysen-Vorderlappen-Sexualhormon aus Schwangerenharn. Z. Physiol. Chem. 222:44-49. Chemische Untersuchungen und neuere Anschauungen ueber Immunitaet. Med. Klin. 29:1-9. Chromatoproteide. Handb. Biochem. Erg. Bd. I:364-83. 1934 Sexualhormone. Med. Welt 8:73-86. Die chemische Zusammensetzung des Haematoprosthetins von Herzog. Z. Physiol. Chem. 223:74-75. Konstitution und biologische Eigenschaften des Blutfarbstoffes und seiner Derivate. Klin. Wochenschr. 13:321-23. 1935 Die Haemoglobine des Menschen. Z. Physiol. Chem. 232:125-45.
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Biographical Memoirs: Volume 64 Ueber Globin und seine haemaffine Gruppe. Z. Physiol. Chem. 232:146-58. Ueber Methaemoglobin und seine Verbindungen mit Wasserstoffperoxyd, mit Cyaniden, Fluoriden und Sulfiden. Z. Physiol. Chem. 232:159-64. Dilatometrische Untersuchung der Hitzedenaturierung von Eiweissloesungen. Kolloid-Z. 71:198-204. Eigenschaften der Porphyrin-Metallkomplexs und ihre Abhaengigkeit von der Wertigkeit und Susceptibilitaet ihrer Metallatome. Ber. Dtsch. Chem. Ges. 68:1795-1806. 1936 Ionenstruktur, Loeslichkeit und Flockung der Proteine. Kolloid-Z. 74:208-18. With F. Kraus. Die Verteilung chemische markierter Antigene im Organismus normaler und sensibilisierter Tiere. Z. Physiol. Chem. 239:76-82. With F. Marx. Loeslichkeit und Flockung der Proteine und anderer lyophiler Kolloide. Kolloid-Z. 77:65-74. Ueber die Bindung zwischen Antigen und praezipitierendem Antikoerper. Z. Physiol. Chem. 245:23-40. 1937 Antigene, Antikoerper und Immunitaet. Klin. Wochenschr. 16:257-61. With W. R. Brdicka and F. Kraus. Die katalatische und peroxidatische Wirkung der Haemine. Enzymologia 2:9-16. Die Reaktion zwischen Haemin und Wasserstoffperoxyd. Enzymologia 4:139-44. 1938 Die Anordnung der Peptidketten in Sphaeroproteinmolekuelen. Z. Physiol. Chem. 256:28-32. With F. K. Munzberg. Einwirkung von schwerem Wasser auf Eiweiss und Aminosaeuren bei Koerpertemperatur. Z. Physiol. Chem. 256:271-72. Absorption und Fluoreszenz der Porphyrine in verschiedenen Loesungsmitteln und Feinbau des Porphinringes. Ber. Dtsch. Chem. Ges. 71:1404-12.
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Biographical Memoirs: Volume 64 Neue Ergebnisse der Immunochemie. Med. Klin. 34:873-77. Das Gleichgewicht zwischen Haemoglobin und Sauerstoff. Z. Physiol. Chem. 254:266-74. Fortschritte der Biochemie 1931-1938. Dresden and Leipzig: Theodor Steinkopff. 1939 With G. Appel. Chemische Analyse der Komplementbindung. Z. Immunitaetsforsch. 95:200-203. With G. Appel. Praezipitation von Jodproteinen verschiedenen Jodgehaltes durch Antijodsera. Z. Immunitaetsforsch. 95:478-86. Chemie der Antigene und der Antikoerper. In Fortschr. Allergielehre, ed. P. Kallos, vol. 1, pp. 19-72. 1940 With K. Sarafyan, M. M. Yenson, S. Berkol, and P. Schwerin. Tabii ve ikame edilmis proteinlerin determinant gruplari hakkinda imunokimyevi totkikler (Immunochemical investigations on the determinant groups of native and substituted proteins). Rev. Fac. Sci. Univ. Istanboul 5:91-98. With P. Schwerin. Haeminkatalysen im Grenzflaechenfilm zwischen Wasser und Oelphase. Enzymologia 9:193-97. Hayati ve Tibbi Kimya (Physiological and Medical Chemistry). University of Istanbul. (2nd ed. 1943, 3rd ed. 1945, 4th ed. 1946.) 1941 With P. Schwerin and K. Sarafyan. Antigenic properties of substituted serum globulin. J. Immunol. 40:391-97. With P. Schwerin and M. M. Yenson. Destruction of hemin and hemoglobin by the action of unsaturated fatty acids and oxygen. J. Biol. Chem. 140:353-59. Katalytische Oxydation von Sulfiden durch Haemin oder Haemoglobin. Enzymologia 10:141-45. The prosthetic group of sulfhemoglobin. J. Biol. Chem. 137:771-81. 1942 With M. Vardar and P. Schwerin. The specific groups of antibodies. J. Immunol. 43:327-30.
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Biographical Memoirs: Volume 64 Separation and determination of multiple antibodies. J. Immunol. 43:331-40. With P. Schwerin. The valence of antibodies and the structure of the antigen-antibody precipitate. Br. J. Exp. Pathol. 23:146-50. 1943 With M. Tunca and P. Schwerin. On the failure of azogelatin as an antigen. Biochem. J. 37:249-50. With P. Schwerin. The specificity of antibodies to antigens containing two different determinant groups. J. Immunol. 47:111-19. With M. M. Yenson. Quantitative determination of antigen, antibody and complement in precipitates. J. Immunol. 47:309-13. Quantitative Untersuchungen ueber Antigen, Antikoerper und Komplement. Schweiz. Med. Wochenschr. 73:264-66. 1944 With M. Vardar. Die Struktur der Proteins. C. R. Soc. Sci. Phys. Nat. 11:2-11. Studies in the field of immunochemistry. Bull. Fac. Med. Univ. Istanbul 7:3789-98. 1945 With M. Tunca. The linkage of glutamine in proteins. Biochem. J. 38:443-45. With M. Tunca, P. Schwerin, and V. Goksu. The action of trypsin on native and denatured proteins. J. Biol. Chem. 157:621-25. 1946 With S. Tekman. Preparation of purified azoprotein antibodies. Nature 157:335. With P. Schwerin and S. Tunc. The mutual precipitation of proteins and azoproteins. Arch. Biochem. 11:515-20. 1947 Antibodies. Their nature and formation. Lancet 152(I):149-51. With S. Tekman, M. Bilen, and P. Schwerin. The purification of azoprotein antibodies by the dissociation of specific precipitates. Biochem. J. 41:304-8.
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Biographical Memoirs: Volume 64 1948 Fortschritte der Biochemie 1938-1947. Basel: S. Karger. 1949 The bond between haem and globin. (Barcroft Memorial Conference on Hemoglobin.) Butterworths Scientific Publ., pp. 53-56. With F. Bursa. The linkage of glutamic acid in protein molecules. Biochem. J. 44:509-12. Biological problems and immunochemistry. Q. Rev. Biol. 24:93-101. With A. Tumer. The proteolytic cleavage of irradiated proteins. Enzymologia 13:229-31. The internal structure of protein molecules. Experientia 5:347-54. 1950 Progress in Biochemistry Since 1939. New York: Interscience. (Also translated into Japanese.) With S. G. Lisie. Quantitative determination of thiourea. Anal. Chem. Acta 4:43-49. With C. F. Crampton. The intracellular distribution in rabbit liver of injected antigens labeled with I-131. Science 112:300-302. Chemistry and Biology of Proteins. New York: Academic Press. (Also translated into Japanese and Russian.) Die innere Struktur der Eiweissmolekuele. Naturwiss. Rundsch. 3:447-53. 1951 Hemoglobin, anhydrohemoglobin and oxyhemoglobin. J. Biol. Chem. 193:443-52. 1952 With C. F. Crampton. The fate in rabbits of intravenously injected I-131-ovalbumin. J. Immunol. 68:73-85. With F. DiMoia and S. Tekman. The reaction of native and denatured ovalbumin with Congo red. J. Am. Chem. Soc. 74:2265-71. With C. F. Crampton and H. H. Reller. Persistence of C-14-anthranilazo-ovalbumin in injected rabbits. Proc. Soc. Exp. Biol. Med. 80:448-51.
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Biographical Memoirs: Volume 64 With C. F. Crampton. Deposition of small doses of injected antigen in rabbits. J. Immunol. 69:457-59. The mechanism of the immunological response. Biol. Rev. 27:247-80. 1953 Theories of antibody formation. In Nature and Significance of the Antibody Response, ed. A. M. Pappenheimer, Jr., pp. 1-10. New York: Columbia University Press. Protein synthesis and immunochemistry. In Information Theory in Biology, ed. Henry Quastler, pp. 125-146. Urbana, University of Illinois Press. The immunological response. Ann. Rev. Microbiol. 7:389-414. With C. F. Crampton and H. H. Reller. Deposition of beef serum gamma-globulin in rabbit organs and subcellular fractions. J. Immunol. 71:319-24. 1954 With R. L. Hardin. Respiratory proteins. In Proteins, eds. H. Neurath and K. Bailey, pp. 279-344. New York: Academic Press. Proteins as antigens and antibodies. In Serological Approaches to Studies of Protein Structure and Metabolism, ed. W. H. Cole, pp. 2-9. New Brunswick, N.J.: Rutgers University Press. 1955 With W. Friedberg and H. Walter. The fate in rats of heterologous proteins labelled ''internally'' by S-35 and "externally" by I-131. Science 121:871. With P. Boucher, M. Dicks, and D. Therriault. Interfacial pressure of proteins. Arch. Biochem. Biophys. 59:52-60. The biosynthesis of plasma proteins and antibodies. Scientia 49:335-41. Immunochemistry, the chemistry of antigens and antibodies. J. Chem. Education 32:615-21. With H. H. Reller and H. Walter. The metabolic fate of isotopically labelled proteins, azoproteins and azohaptens. J. Immunol. 75:417-22. Biochemistry, An Introductory Textbook. New York: J. Wiley & Sons, Inc. (Also translated into Spanish.)
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Biographical Memoirs: Volume 64 1956 The nature of the protein molecule. Problems of protein structure. J. Cell. Comp. Physiol. 47:1-16. With J. Horowitz. Condensation of gamma-glutamyl peptides with thiocyanate. Biochem. Biophys. Acta 20:574-75. 1957 With H. Walter, S. Fleischer, A. Lietze, H. F. Cheng, J. E. Turner, and W. Friedberg. The metabolic fate of injected homologous serum proteins in rabbits. J. Biol. Chem. 224:107-19. With M. Zimmerman, R. L. Hardin, S. G. Lisie, J. Horowitz, A. Lietze, and F. Bursa. Condensation of proteins with thiocyanate. J. Biol. Chem. 224:827-39. With R. Sowinski and H. F. Cheng. The dissociation of antigen-antibody precipitates. J. Am. Chem. Soc. 79:1882-88. Isolation, purification and properties of proteolytic enzymes from animal sources. Ann. N.Y. Acad. Sci. 68:3-10. With N. Penn and N. Yenson. Interaction between internally labeled complement and specific precipitates. J. Immunol. 78:409-12. With M. Dicks and D. G. Therriault. Reaction of globin with haemin in interfacial films. Nature 180:437-38. Nature and formation of antibodies. In Molecular Structure and Biological Specificity, ed. L. Pauling and H. A. Itano, pp. 18-27. Washington, D.C.: Am. Inst. Biol. Sci. 1958 Protein symplexes (conjugated proteins). Encycl. Plant Physiol. 8:333-42. With M. Sela. Serological properties of poly-L-tyrosine derivatives. Experientia 14:91. With J. D. Hawkins. Effect of histamine and an anti-histaminic drug on the haemolytic action of guinea pig complement. Nature 181:1666-67. With J. E. Turner and R. T. Bottle. Dependence of the optical rotatory power of proteins on disulfide bonds. J. Am. Chem. Soc. 80:4117.
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Biographical Memoirs: Volume 64 1959 The role of the antigen in antibody formation. In Immunity and Virus Infection, ed. V. A. Najjar, pp. 18-25. New York: J. Wiley & Sons. Biosynthese der Proteine und ihre Beeinflussung durch Antigene. Naturwiss. 46:60-63. With J. E. Turner and M. B. Kennedy. Disulfide bonds in proteins. In Sulfur in Proteins, ed. R. Benesch, pp. 25-31. New York and London: Academic Press. With J. Horowitz. Mechanism of plastein formation. Biochem. Biophys. Acta 33:231-37. With S. Fleischer and G. Vidaver. The rate of incorporation of S35 -amino acids into hair protein. J. Biol. Chem. 234:2717-18. With Fleischer, A. Lietze, and H. Walter. Conversion of serum proteins into tissue proteins. Proc. Soc. Exp. Biol. Med. 101:860-63. Progress in Biochemistry Since 1949. Basel: S. Karger; New York: Interscience. 1960 With M. Richter. Incorporation of amino acids into antibody during the secondary response. J. Immunol. 84:123-27. With M. Richter. Continuous synthesis of antibody after primary immunization with protein antigens. J. Immunol. 84:420-25. Immunochemistry. Ann. Rev. Biochem. 29:609-34. 1961 With H. Wurz. Changes in the optical rotation of proteins after cleavage of the disulfide bonds. J. Am. Chem. Soc. 83:280-83. Use of radioisotopes in immunochemical research. Ergeb. Mikrobiol. 34:1-26. Untersuchungen ueber die Natur der Antikoerper. Angew. Chemie 73:153-60. With H. F. Cheng, M. Dicks, R. H. Shellhamer, E. S. Brown, and A. N. Roberts. Localization of antigens by autoradiography. Proc. Soc. Exp. Biol. Med. 106:93-97. With M. Richter and B. Patras. Antibody formation in primary and secondary response. In Immunochemical Approaches to Problems in Microbiology, ed. M. Heidelberger and O. J. Plescia, pp. 359-67. New Brunswick, N.J.: Rutgers University Press.
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Biographical Memoirs: Volume 64 Immunochemie, die Chemie der Antigene, Antikoerper und ihrer Reaktionen. Naturwiss. Rundsch. 14:219-26. With J. D. Hawkins. The recovery of injected antigens from rat spleens. Biochem. J. 80:200. The role of the blood plasma in bodily maintenance and repair. In Functions of the Blood, ed. R. G. Macfarlane and A. H. T. Robb-Smith, pp. 527-602. With H. Walter and S. Fleischer. Effect of different external labels on the metabolism of doubly labeled heterologous proteins. Arch. Biochem. Biophys. 95:290-95. 1962 Wesen und Bildung der Antikoerper. Zentralbl. Bakteriol. 184:318-23. With A. N. Roberts. Quantitative studies on the bis-diazotized benzidine method of hemagglutination. J. Immunol. 89:348-57. With A. N. Roberts. Intracellular localization and quantitation of tritiated antigens in RES tissues of mice during secondary and hyperimmune response. J. Exp. Med. 116:407-22. 1963 Chemistry and Function of Proteins. New York: Academic Press. (Also translated into Japanese and Russian.) 1964 The template theory of antibody formation. In Conceptual Advances in Immunology and Oncology, pp. 22-33. New York: University of Texas, Hoeber Medical Division. With J. L. Groff. Comparison of the peptide maps of antibodies against an acidic and basic determinant group. Immunochemistry 1:31-36. 1965 With E. F. Gold and K. L. Knight. Peptide maps of antibodies against an antigen containing two different determinant groups. Biochem. Biophys. Res. Comm. 18:76-80. Naturaleza y formacion de anticuerpos. Cien. Invest. 20:244-54. Antibody formation. Physiol. Rev. 45:1-47. Antibody formation and the coding problem. Nature 205:847-51.
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Biographical Memoirs: Volume 64 Immunological unresponsiveness and autoantibody formation. Ann. N. Y. Acad. Sci. 124:50-55. With M. Richter and S. Zimmerman. Relation of antibody titer to persistence of antigen. J. Immunol. 94:938-41. 1966 With K. L. Knight and M. A. Lopez. Comparison of two hapten-specific rabbit antibodies. J. Biol. Chem. 241:2286-92. With E. F. Gold, S. Cordes, M. A. Lopez, and K. L. Knight. Studies on chicken gamma-globulins and hapten-specific chicken antibodies. Immunochemistry 3:433. 1967 With K. L. Knight and M. J. Roelofs. Ratios of the Fab fragments I and II from rabbit antibodies and non-specific gamma-globulins. Biochem. Biophys. Acta 133:333-37. 1968 Immunochemistry and the Biosynthesis of Antibodies. New York: Interscience. (Also translated into Japanese and Russian.) The evolution of selective and instructive theories of antibody formation. Cold Spring Harbor Symp. Quant. Biol. 32:559-67. 1969 Struktur und Wirkungsweise der Antikoerper. Naturwissenschaften 56:189-94. Heterogeneity and biosynthesis of antibodies. FEBS Symp. 15:1-12. Studies on the structure and formation of antibodies. In Current Problems in Immunology, ed. O. Westphal, H. E. Bock, and E. Grundmann, pp. 63-68. New York: Springer Verlag. 1970 The molecular basis of immunity. Ann. N.Y. Acad. Sci. 169:11-22. The molecular basis of immunity. In Developmental Aspects of Antibody Formation and Structure, ed. J. Sterzl and I. Riha, pp. 909-18. 1971 Deviations from the central dogma of information transfer. Nova Acta Leopoldina 36:23-25.
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Biographical Memoirs: Volume 64 1972 With A. Sehon. Kinetics and thermodynamics of antigen-antibody interaction. In Progress in Immunology, ed. B. Amos, pp. 1287-89. New York: Academic Press. 1973 With M. Groh and G. Gansinger. Mechanism and kinetics of the hemin-catalyzed oxidation of linoleate in the oil-water interface. J. Biol. Chem. 248:3810-18. The role of RNA in antibody formation. Historical perspectives. Ann. N.Y. Acad. Sci. 207:8-16. The problem of antibody diversity; immunodifferentiation versus somatic mutation. Immunochemistry 10:775-83. 1974 Protein. Encyclopedia Britannica, 15th ed., pp. 81-98. With S. E. Zimmerman. Preferential allotypic expression of antihapten response in the first and second generation heterozygous rabbits of al, 3 allotype. Immunochemistry 11:403-7. 1979 Protein heterogeneity: Its history, its bases, and its limits, Ann. N. Acad. Sci. 325:37-50.
Representative terms from entire chapter: