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Lane et al. 239 (9): 2865
Gregolin et al. 243 (16): 4236
Guchhait et al. 249 (20): 6646
Polakis et al. 249 (20): 6657
J. Biol. Chem., Vol. 281, Issue 49, 40, December 8, 2006
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Classics
Acetyl-CoA Carboxylase and Other Biotin-dependent Enzymes: the Work of M. Daniel Lane
The Enzymatic Synthesis of Holotranscarboxylase from Apotranscarboxylase and (+)-Biotin. II. Investigation of the Reaction Mechanism
(Lane, M. D., Rominger, K. L., Young, D. L., and Lynen, F. (1964) J. Biol. Chem. 239, 2865–2871)
Liver Acetyl-CoA Carboxylase. II. Further Molecular Characterization
(Gregolin, C., Ryder, E., Warner, R. C., Kleinschimdt, A. K., Chang, H.-C., and Lane, M. D. (1968) J. Biol. Chem. 243, 4236–4245)
Acetyl Coenzyme A Carboxylase System of Escherichia coli. Site of Carboxylation of Biotin and Enzymatic Reactivity of 1'-N-(Ureido)-Carboxybiotin Derivatives
(Guchhait, R. B., Polakis, S. E., Hollis, D., Fenselau, C., and Lane, M. D. (1974) J. Biol. Chem. 249, 6646–6656)
Acetyl Coenzyme A Carboxylase System of Escherichia coli. Studies on the Mechanisms of the Biotin Carboxylase- and Carboxyltransferase-catalyzed Reactions
(Polakis, S. E., Guchhait, R. B., Zwergel, E. E., Lane, M. D., and Cooper, T. G. (1974) J. Biol. Chem. 249, 6657–6667)
Malcolm Daniel Lane was born in Chicago in 1930. He received both his B.S. and M.S. from Iowa State University in 1951 and 1953, respectively. Lane then went to the University of Illinois for graduate school and was awarded his Ph.D. in 1956. He joined the faculty of the Virginia Polytechnic Institute and State University in Blacksburg, Virginia in 1956 as Associate Professor and was promoted to Professor of Biochemistry in 1963.
Upon joining the faculty at Virginia Polytechnic Institute, Lane decided to try to determine how propionate was metabolized in the bovine liver. About this time, Journal of Biological Chemistry (JBC) Classics author Severo Ochoa (1, 2) reported that propionyl-CoA was carboxylated to form methylmalonyl-CoA, which was then was converted to succinyl-CoA. Lane was able to purify propionyl-CoA carboxylase from bovine liver mitochondria.
Then in 1959 a paper by Lynen and Knappe appeared in Angewandte Chemie (3) indicating that 
-methylcrotonyl-CoA carboxylase, a biotin-dependent carboxylase, catalyzed the ATP-dependent carboxylation of "free" biotin in the absence of its acyl-CoA substrate. Lynen proposed that the free biotin had accessed the active site of the carboxylase and by mimicking the biotinyl prosthetic group it had been carboxylated. Lane determined that propionyl-CoA carboxylase was also a biotin-dependent enzyme and determined that the biotin prosthetic group was linked to propionyl-CoA carboxylase through an amide linkage to a lysyl 
-amino group.
In 1962 Lane decided to take a sabbatical leave in Munich with Feodor Lynen at the Max-Planck Institüt Für Zellchemie where he continued to work on the enzymatic mechanism by which biotin became attached to propionyl-CoA carboxylase. Before leaving for Munich, Lane developed an apoenzyme system with which to investigate the "biotin loading" reaction. This system made use of Propionibacterium shermanii, which expressed huge amounts of methylmalonyl-CoA:pyruvate transcarboxylase, another biotin-dependent enzyme. The organism also had an absolute requirement for biotin in its growth medium and produced large amounts of the apotranscarboxylase when grown at very low levels of biotin.
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In Munich, Lane was able to resolve and purify both the apotranscarboxylase and the synthetase that catalyzed biotin loading onto the apoenzyme (4). Dave Young, a postdoctoral fellow who had recently completed his medical training at Duke University, and Karl Rominger, a Ph.D. candidate under Lynen's direction, collaborated with him on these studies. In a second paper, which is the first JBC Classic reprinted here, Lane and his colleagues showed that the synthetase catalyzed a two-step reaction. The first step involved the ATP-dependent formation of biotinyl-5'-AMP and pyrophosphate after which the biotinyl group was transferred from the AMP derivative to the appropriate lysyl
-amino group of the apotranscarboxylase. Lane and Lynen also showed that the covalently bound biotinyl prosthetic group, like free biotin, was carboxylated on the 1'-N position (5). Shortly after he returned from Munich, Lane left Virginia Polytechnic Institute to become Associate Professor of Biochemistry at the New York University School of Medicine. He was later promoted to Professor of Biochemistry in 1969. In New York, Lane and his colleagues isolated acetyl coenzyme A carboxylase from chicken liver (6). The biotin-containing enzyme catalyzes the carboxylation of acetyl-CoA to malonyl-CoA in a 2-step process involving a carboxybiotin intermediate. In an accompanying paper, Lane described the molecular characteristics of the enzyme, including its reversible inter-conversion between protomeric and polymeric forms. The paper is reprinted here as the second JBC Classic by Lane. He determined that the carboxylase has a binding site for citrate and another for acetyl-CoA and that citrate binding might be involved in regulating the enzyme.
Lane left New York in 1970 to become Professor of Biological Chemistry at the Johns Hopkins University School of Medicine. Right around the time Lane took up his new post at Johns Hopkins, Thomas C. Bruice and A. F. Hegarty published a paper (7) that called into question Lane's conclusion that biotin was carboxylated on the 1'-N position. They pointed out that carboxylation could occur at the ureido-O and result in the same derivative. In the third JBC Classic, Lane uses the acetyl coenzyme A carboxylase system from Escherichia coli to provide definitive evidence that the ureido-N of biotin is the site of carboxylation.
In the final JBC Classic reprinted here, Lane presents a thorough analysis of the acetyl coenzyme A carboxylase system from Escherichia coli. He defines the requirements and properties of isotopic exchange and stoichiometric reactions representative of the two half-reactions in acetyl-CoA carboxylation and also describes studies using prosthetic group and intermediate model derivatives as substrates to elucidate the mechanisms of the partial reactions.
Lane was eventually promoted to Director and DeLamar Professor in 1978. He is currently Distinguished Service Professor in the Department of Biological Chemistry at Johns Hopkins. More information about Lane's early work on biotin can be found in his JBC Reflections (8).
Lane's honors and awards include the American Institute of Nutrition's Mead-Johnson award in 1966, the American Society of Biological Chemists' William C. Rose award in 1981, and the Johns Hopkins University School of Medicine Professor's Award for Distinction in Teaching in 1986. He was elected to the American Academy of Arts and Sciences in 1982, the American Society for Nutritional Sciences in 1996, and the National Academy of Sciences in 1987. In addition to serving as president of the American Society for Biochemistry and Molecular Biology in 1990, Lane served on the Society's Program Committee, Membership Committee, and Public Affairs Committee. He has served on the Editorial Boards of several journals, including those of the Journal of Biological Chemistry, Biochemistry et Biophysica Acta, the Archives Biochemistry and Biophysics, and Annual Reviews of Biochemistry. He also served on the editorial board and was Executive Editor of Biochemical and Biophysical Research Communications in 1986.
REFERENCES
- JBC Classics: Stern, J. R., and Ochoa, S. (1951) J. Biol. Chem. 191, 161–172; Korkes, S., del Campillo, A., Gunsalus, I. C., and Ochoa, S. (1951) J. Biol. Chem. 193, 721–735 (http://www.jbc.org/cgi/content/full/280/11/e8)
- JBC Classics: Salas, M., Smith, M. A., Stanley, W. M., Jr., Wahba, A. J., and Ochoa, S. (1965) J. Biol. Chem. 240, 3988–3995 (http://www.jbc.org/cgi/content/full/281/21/e16)
- Lynen, F., Knappe, J., Lorch, E., Jutting, G., and Ringelmann, E. (1959) Die biochemische Funktion des Biotins. Angew. Chem. 71, 481–486
- Lane, M. D., Young, D. L., and Lynen, F. (1964) The enzymatic synthesis of holotranscarboxylase from apotranscarboxylase and (+)-biotin. I. Purification of the apoenzyme and synthetase; characteristics of the reaction. J. Biol. Chem. 239, 2858–2864
[Free Full Text] - Lane, M. D., and Lynen, F. (1963) The biochemical function of biotin. VI. Chemical structure of the carboxylated active site of propionyl carboxylase. Proc. Natl. Acad. Sci. U. S. A. 49, 379–385
[Free Full Text] - Gregolin, C., Ryder, E., and Lane, M. D. (1968) Liver acetyl coenzyme A carboxylase. I. Isolation and catalytic properties. J. Biol. Chem. 243, 4227–4235
[Abstract/Free Full Text] - Bruice, T. C., and Hegarty, A. F. (1970) Biotin-bound CO2 and the mechanism of enzymatic carboxylation reactions. Proc. Natl. Acad. Sci. U. S. A. 65, 805–809
[Abstract/Free Full Text] - Lane, M. D. (2004) The biotin connection: Severo Ochoa, Harland Wood, and Feodor Lynen. J. Biol. Chem. 279, 39187–39194
[Free Full Text]
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