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Annual Review of Biochemistry

Volume 90, 2021

From Bioorganic Models to Cells

Abstract

I endeavor to share how various choices—some deliberate, some unconscious—and the unmistakable influence of many others shaped my scientific pursuits. I am fascinated by how two long-term, major streams of my research, DNA replication and purine biosynthesis, have merged with unexpected interconnections. If I have imparted to many of the talented individuals who have passed through my lab a degree of my passion for uncloaking the mysteries hidden in scientific research and an understanding of the honesty and rigor it demands and its impact on the world community, then my mentorship has been successful.

Keyword(s): autobiography, DNA replication, enzymatic catalysis, purine biosynthesis
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2021-06-20
2024-04-16
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Literature Cited

  1. 1. 
    Fruton JS, Simmonds S. 1958. General Biochemistry New York: Wiley. , 2nd ed..
  2. 2. 
    Sumner JB. 1926. The isolation and crystallization of the enzyme urease. J. Biol. Chem. 69:435–41
     [Google Scholar]
  3. 3. 
    Neurath H, Hartley BS. 1959. The hydrolysis of peptide and ester bonds by proteolytic enzymes. J. Cell. Comp. Physiol. 54:179–202
     [Google Scholar]
  4. 4. 
    Bruice TC, Benkovic SJ, French TC. 1965. Stopped-flow apparatus for a Zeiss PMQ II spectrophotometer. Rev. Sci. Inst. 36:860–61
     [Google Scholar]
  5. 5. 
    Bruice TC, Benkovic SJ. 1963. A Comparison of the bimolecular and intramolecular nucleophilic catalysis of the hydrolysis of substituted phenyl acetates by the dimethylamino group. J. Am. Chem. Soc. 85:1–8
     [Google Scholar]
  6. 6. 
    Bruice TC, Benkovic SJ. 1966. Bioorganic Mechanisms, Vol. I New York: Benjamin
  7. 7. 
    Bruice TC, Benkovic SJ. 1966. Bioorganic Mechanisms, Vol. II New York: Benjamin
  8. 8. 
    Benkovic SJ, Schray KJ. 1968. The kinetics and mechanisms of phosphoenolpyruvate hydrolysis. Biochemistry 7:4090–96
     [Google Scholar]
  9. 9. 
    Schray KJ, Benkovic SJ. 1971. Mechanisms of hydrolysis of phosphate ester derivatives of phosphoenolpyruvic acid. J. Am. Chem. Soc. 93:2522–29
     [Google Scholar]
  10. 10. 
    Benkovic SJ, Benkovic PA, Chrzanowski R. 1970. Studies on models for tetrahydrofolic acid. II. The mechanism for condensation of formaldehyde with tetrahydroquinoxaline analogs. J. Am. Chem. Soc. 92:523–28
     [Google Scholar]
  11. 11. 
    Benkovic SJ, Bullard WP, Benkovic PA. 1972. Studies on models for tetrahydrofolic acid. III. Hydrolytic interconversions of the tetrahydroquinoxaline analogs at the formate level of oxidation. J. Am. Chem. Soc. 94:7542–49
     [Google Scholar]
  12. 12. 
    Benkovic SJ. 1966. Studies on sulfate esters. II. Carboxyl group catalysis in the hydrolysis of salicyl sulfate. J. Am. Chem. Soc. 88:5511–15
     [Google Scholar]
  13. 13. 
    Benkovic SJ, Benkovic PA. 1968. Studies on sulfate esters. III. A comparison of the solvolyses of salicyl sulfate and sulfur trioxide. J. Am. Chem. Soc. 90:2646–50
     [Google Scholar]
  14. 14. 
    Benkovic SJ, Kleinschuster JJ, deMaine MM, Siewers IJ. 1971. On the mechanism of action of fructose 1,6-diphosphatase. Inhibition by structural analogs of fructose 1,6-diphosphate. Biochemistry 10:4881–87
     [Google Scholar]
  15. 15. 
    Libby CB, Frey WA, Villafranca JJ, Benkovic SJ. 1975. Kinetic and binding studies of Mn (II) and fructose 1,6-bisphosphate with rabbit liver hexosebisphosphatase. J. Biol. Chem. 250:7564–73
     [Google Scholar]
  16. 16. 
    Schray KJ, Benkovic SJ, Benkovic PA, Rose IA. 1973. Catalytic reactions of phosphoglucose isomerase with cyclic forms of glucose 6-phosphate and fructose 6-phosphate. J. Biol. Chem. 248:2219–24
     [Google Scholar]
  17. 17. 
    Fishbein R, Benkovic PA, Schray KJ, Siewers IJ, Steffens JJ, Benkovic SJ. 1974. Anomeric specificity of phosphofructokinase from rabbit muscle. J. Biol. Chem. 249:6047–51
     [Google Scholar]
  18. 18. 
    Schray KJ, Fishbein R, Bullard WP, Benkovic SJ. 1975. The anomeric form of D-fructose 1,6-bisphosphate used as substrate in the muscle and yeast aldolase reactions. J. Biol. Chem. 250:4883–87
     [Google Scholar]
  19. 19. 
    Frey WA, Fishbein R, deMaine MM, Benkovic SJ. 1977. Substrate form of D-fructose 1,6-bisphosphate utilized by fructose 1,6-bisphosphatase. Biochemistry 16:2479–84
     [Google Scholar]
  20. 20. 
    Benkovic SJ. 1979. Anomeric specificity of carbohydrate-utilizing enzymes. Methods Enzymol 63:370–79
     [Google Scholar]
  21. 21. 
    Smith GK, Mueller WT, Wasserman GF, Taylor WD, Benkovic SJ. 1980. Characterization of the enzyme complex involving the folate-requiring enzymes of de novo purine biosynthesis. Biochemistry 19:4313–21
     [Google Scholar]
  22. 22. 
    Caperelli CA, Benkovic PA, Chettur G, Benkovic SJ. 1980. Purification of a complex catalyzing folate cofactor synthesis and transformylation in de novo purine biosynthesis. J. Biol. Chem. 255:1885–90
     [Google Scholar]
  23. 23. 
    Smith GK, Mueller WT, Benkovic PA, Benkovic SJ. 1981. On the cofactor specificity of glycinamide ribonucleotide and 5-aminoimidazole-4-carboxamide ribonucleotide transformylase from chicken liver. Biochemistry 20:1241–45
     [Google Scholar]
  24. 24. 
    Inglese J, Smith JM, Benkovic SJ. 1990. Active-site mapping and site-specific mutagenesis of glycinamide ribonucleotide transformylase from Escherichia coli. Biochemistry 29:6678–87
     [Google Scholar]
  25. 25. 
    Inglese J, Benkovic SJ. 1991. Multisubstrate adduct inhibitors of glycinamide ribonucleotide transformylase: synthetic and enzyme-assembled. Tetrahedron Lett 47:2351–64
     [Google Scholar]
  26. 26. 
    Moad G, Luthy CL, Benkovic SJ. 1978. The mechanism of oxidation of 6-methyl-5-carba-5-deazatetrahydropterin. Evidence for the involvement of a 4a-adduct in the oxidation of tetrahydropterins. Tetrahedron Lett. 19:2271–74
     [Google Scholar]
  27. 27. 
    Lazarus RA, Dietrich RF, Wallick DE, Benkovic SJ. 1981. On the mechanism of action of phenylalanine hydroxylase. Biochemistry 20:6834–41
     [Google Scholar]
  28. 28. 
    Lazarus RA, DeBrosse CW, Benkovic SJ. 1982. Phenylalanine hydroxylase: structural determination of the tetrahydropterin intermediates by 13C NMR spectroscopy. J. Am. Chem. Soc. 104:6869–71
     [Google Scholar]
  29. 29. 
    Gottschall DW, Dietrich RF, Benkovic SJ, Shiman R. 1982. Phenylalanine hydroxylase. Correlation of the iron content with activity and the preparation and reconstitution of the apoenzyme. J. Biol. Chem. 257:845–49
     [Google Scholar]
  30. 30. 
    Benkovic SJ, Sammons D, Armarego WLF, Waring P, Inners R 1985. Tautomeric nature of quinonoid 6,7-dimethyl-7,8-dihydro-6H-pterin in aqueous solution: a 15N NMR study. J. Am. Chem. Soc. 107:3706–12
     [Google Scholar]
  31. 31. 
    Carr RT, Balasubramanian S, Hawkins PC, Benkovic SJ. 1995. Mechanism of metal-independent hydroxylation by Chromobacterium violaceum phenylalanine hydroxylase. Biochemistry 34:7525–32
     [Google Scholar]
  32. 32. 
    Shim JH, Benkovic SJ. 1998. Evaluation of the kinetic mechanism of Escherichia coli glycinamide ribonucleotide transformylase. Biochemistry 37:8776–82
     [Google Scholar]
  33. 33. 
    Smith GK, Benkovic PA, Benkovic SJ. 1981. l(−)-10-Formyltetrahydrofolate is the cofactor for glycinamide ribonucleotide transformylase from chicken liver. Biochemistry 20:4034–36
     [Google Scholar]
  34. 34. 
    Smith GK, Mueller WT, Slieker LJ, DeBrosse CW, Benkovic SJ. 1982. Direct transfer of one-carbon units in the transformylations of de novo purine biosynthesis. Biochemistry 21:2870–74
     [Google Scholar]
  35. 35. 
    Daubner SC, Schrimsher JL, Schendel FJ, Young M, Henikoff S et al. 1985. A multifunctional protein possessing glycinamide ribonucleotide synthetase, glycinamide ribonucleotide transformylase, and aminoimidazole ribonucleotide synthetase activities in de novo purine biosynthesis. Biochemistry 24:7059–62
     [Google Scholar]
  36. 36. 
    Lazarus RA, Benkovic SJ, Kaufman S. 1983. Phenylalanine hydroxylase stimulator protein is a 4a-carbinolamine dehydratase. J. Biol. Chem. 258:10960–62
     [Google Scholar]
  37. 37. 
    Pember SO, Villafranca JJ, Benkovic SJ. 1986. Phenylalanine hydroxylase from Chromobacterium violaceum is a copper-containing monooxygenase. Kinetics of the reductive activation of the enzyme. Biochemistry 25:6611–19
     [Google Scholar]
  38. 38. 
    Marlier JF, Bryant FR, Benkovic SJ. 1981. Stereochemical and kinetic investigation of 32P-labeled inorganic phosphate exchange reaction catalyzed by primer-independent and primer-dependent polynucleotide phosphorylase from Micrococcus luteus. Biochemistry 20:2212–19
     [Google Scholar]
  39. 39. 
    Bryant FR, Benkovic SJ, Sammons D, Frey PA. 1981. The stereochemical course of thiophosphoryl group transfer catalyzed by T4 polynucleotide kinase. J. Biol. Chem. 256:5965–66
     [Google Scholar]
  40. 40. 
    Rahil JF, deMaine MM, Benkovic SJ. 1982. Rapid-quench and isotope-trapping studies on fructose-1,6-bisphosphatase. Biochemistry 21:3358–63
     [Google Scholar]
  41. 41. 
    Bryant FR, Johnson KA, Benkovic SJ. 1983. Elementary steps in the DNA polymerase I reaction pathway. Biochemistry 22:3537–46
     [Google Scholar]
  42. 42. 
    Gupta AP, Benkovic SJ. 1984. Stereochemical course of the 3′–5′-exonuclease activity of DNA polymerase I. Biochemistry 23:5874–81
     [Google Scholar]
  43. 43. 
    Slieker LJ, Benkovic SJ. 1984. Synthesis of (6R,11S)- and (6R,11R)-5,10-methylene[11–1H,2H]tetrahydrofolate. Stereochemical paths of serine hydroxymethyltransferase, 5,10-methylenetetrahydrofolate dehydrogenase, and thymidylate synthetase catalysis. J. Am. Chem. Soc. 106:1833–38
     [Google Scholar]
  44. 44. 
    Domanico PL, Rahil JF, Benkovic SJ. 1985. Unambiguous stereochemical course of rabbit liver fructose bisphosphatase hydrolysis. Biochemistry 24:1623–28
     [Google Scholar]
  45. 45. 
    Mizrahi V, Benkovic P, Benkovic SJ 1986. Mechanism of DNA polymerase I: exonuclease/polymerase activity switch and DNA sequence dependence of pyrophosphorolysis and misincorporation reactions. PNAS 83:5769–73
     [Google Scholar]
  46. 46. 
    Mizrahi V, Benkovic PA, Benkovic SJ 1986. Mechanism of the idling-turnover reaction of the large (Klenow) fragment of Escherichia coli DNA polymerase I. PNAS 83:231–35
     [Google Scholar]
  47. 47. 
    Kuchta RD, Mizrahi V, Benkovic PA, Johnson KA, Benkovic SJ. 1987. Kinetic mechanism of DNA polymerase I (Klenow). Biochemistry 26:8410–17
     [Google Scholar]
  48. 48. 
    Kuchta RD, Benkovic P, Benkovic SJ. 1988. Kinetic mechanism whereby DNA polymerase I (Klenow) replicates DNA with high fidelity. Biochemistry 27:6716–25
     [Google Scholar]
  49. 49. 
    Allen DJ, Benkovic SJ. 1989. Resonance energy transfer measurements between substrate binding sites within the large (Klenow) fragment of Escherichia coli DNA polymerase I. Biochemistry 28:9586–93
     [Google Scholar]
  50. 50. 
    Guest CR, Hochstrasser RA, Dupuy CG, Allen DJ, Benkovic SJ, Millar DP. 1991. Interaction of DNA with the Klenow fragment of DNA polymerase I studied by time-resolved fluorescence spectroscopy. Biochemistry 30:8759–70
     [Google Scholar]
  51. 51. 
    Dahlberg ME, Benkovic SJ. 1991. Kinetic mechanism of DNA polymerase I (Klenow fragment): identification of a second conformational change and evaluation of the internal equilibrium constant. Biochemistry 30:4835–43
     [Google Scholar]
  52. 52. 
    Alberts BM, Barry J, Bedinger P, Formosa T, Jongeneel CV, Kreuzer KN. 1983. Studies on DNA replication in the bacteriophage T4 in vitro system. Cold Spring Harb. Symp. Quant. Biol. 47:Part 2655–68
     [Google Scholar]
  53. 53. 
    Alberts BM. 1985. Protein machines mediate the basic genetic processes. Trends Genet. 1:26–30
     [Google Scholar]
  54. 54. 
    Nossal NG. 1992. Protein-protein interactions at a DNA replication fork: bacteriophage T4 as a model. FASEB J. 6:3871–78
     [Google Scholar]
  55. 55. 
    Capson TL, Benkovic SJ, Nossal NG. 1991. Protein-DNA cross-linking demonstrates stepwise ATP-dependent assembly of T4 DNA polymerase and its accessory proteins on the primer-template. Cell 65:249–58
     [Google Scholar]
  56. 56. 
    Capson TL, Peliska JA, Kaboord BF, Frey MW, Lively C et al. 1992. Kinetic characterization of the polymerase and exonuclease activities of the gene 43 protein of bacteriophage T4. Biochemistry 31:10984–94
     [Google Scholar]
  57. 57. 
    Kaboord BF, Benkovic SJ 1993. Rapid assembly of the bacteriophage T4 core replication complex on a linear primer/template construct. PNAS 90:10881–85
     [Google Scholar]
  58. 58. 
    Kaboord BF, Benkovic SJ. 1995. Accessory proteins function as matchmakers in the assembly of the T4 DNA polymerase holoenzyme. Curr. Biol. 5:149–57
     [Google Scholar]
  59. 59. 
    Kaboord BF, Benkovic SJ. 1996. Dual role of the 44/62 protein as a matchmaker protein and DNA polymerase chaperone during assembly of the bacteriophage T4 holoenzyme complex. Biochemistry 35:1084–92
     [Google Scholar]
  60. 60. 
    Berdis AJ, Benkovic SJ. 1996. Role of adenosine 5′-triphosphate hydrolysis in the assembly of the bacteriophage T4 DNA replication holoenzyme complex. Biochemistry 35:9253–65
     [Google Scholar]
  61. 61. 
    Sexton DJ, Berdis AJ, Benkovic SJ. 1997. Assembly and disassembly of DNA polymerase holoenzyme. Curr. Opin. Chem. Biol. 1:316–22
     [Google Scholar]
  62. 62. 
    Carver TE Jr., Sexton DJ, Benkovic SJ. 1997. Dissociation of bacteriophage T4 DNA polymerase and its processivity clamp after completion of Okazaki fragment synthesis. Biochemistry 36:14409–17
     [Google Scholar]
  63. 63. 
    Berdis AJ, Benkovic SJ. 1997. Mechanism of bacteriophage T4 DNA holoenzyme assembly: the 44/62 protein acts as a molecular motor. Biochemistry 36:2733–43
     [Google Scholar]
  64. 64. 
    Soumillion P, Sexton DJ, Benkovic SJ. 1998. Clamp subunit dissociation dictates bacteriophage T4 DNA polymerase holoenzyme disassembly. Biochemistry 37:1819–27
     [Google Scholar]
  65. 65. 
    Sexton DJ, Kaboord BF, Berdis AJ, Carver TE, Benkovic SJ. 1998. Dissecting the order of bacteriophage T4 DNA polymerase holoenzyme assembly. Biochemistry 37:7749–56
     [Google Scholar]
  66. 66. 
    Kroutil LC, Frey MW, Kaboord BF, Kunkel TA, Benkovic SJ. 1998. Effect of accessory proteins on T4 DNA polymerase replication fidelity. J. Mol. Biol. 278:135–46
     [Google Scholar]
  67. 67. 
    Berdis AJ, Benkovic SJ 1998. Simultaneous formation of functional leading and lagging strand holoenzyme complexes on a small, defined DNA substrate. PNAS 95:11128–33
     [Google Scholar]
  68. 68. 
    Alley SC, Ishmael FT, Jones AD, Benkovic SJ. 2000. Mapping protein−protein interactions in the bacteriophage T4 DNA polymerase holoenzyme using a novel trifunctional photo-cross-linking and affinity reagent. J. Am. Chem. Soc. 122:6126–27
     [Google Scholar]
  69. 69. 
    Alley SC, Abel-Santos E, Benkovic SJ 2000. Tracking sliding clamp opening and closing during bacteriophage T4 DNA polymerase holoenzyme assembly. Biochemistry 39:3076–90
     [Google Scholar]
  70. 70. 
    Valentine AM, Ishmael FT, Shier VK, Benkovic SJ. 2001. A zinc ribbon protein in DNA replication: primer synthesis and macromolecular interactions by the bacteriophage T4 primase. Biochemistry 40:15074–85
     [Google Scholar]
  71. 71. 
    Alley SC, Trakselis MA, Mayer MU, Ishmael FT, Jones AD, Benkovic SJ. 2001. Building a replisome solution structure by elucidation of protein-protein interactions in the bacteriophage T4 DNA polymerase holoenzyme. J. Biol. Chem. 276:39340–49
     [Google Scholar]
  72. 72. 
    Trakselis MA, Alley SC, Abel-Santos E, Benkovic SJ 2001. Creating a dynamic picture of the sliding clamp during T4 DNA polymerase holoenzyme assembly by using fluorescence resonance energy transfer. PNAS 98:8368–75
     [Google Scholar]
  73. 73. 
    Trakselis MA, Mayer MU, Ishmael FT, Roccasecca RM, Benkovic SJ. 2001. Dynamic protein interactions in the bacteriophage T4 replisome. Trends Biochem. Sci. 26:566–72
     [Google Scholar]
  74. 74. 
    Trakselis MA, Berdis AJ, Benkovic SJ. 2003. Examination of the role of the clamp-loader and ATP hydrolysis in the formation of the bacteriophage T4 polymerase holoenzyme. J. Mol. Biol. 326:435–51
     [Google Scholar]
  75. 75. 
    Millar D, Trakselis MA, Benkovic SJ. 2004. On the solution structure of the T4 sliding clamp (gp45). Biochemistry 43:12723–27
     [Google Scholar]
  76. 76. 
    Yang J, Zhuang Z, Roccasecca RM, Trakselis MA, Benkovic SJ 2004. The dynamic processivity of the T4 DNA polymerase during replication. PNAS 101:8289–94
     [Google Scholar]
  77. 77. 
    Zhang Z, Spiering MM, Trakselis MA, Ishmael FT, Xi J et al. 2005. Assembly of the bacteriophage T4 primosome: single-molecule and ensemble studies. PNAS 102:3254–59
     [Google Scholar]
  78. 78. 
    Wong KF, Selzer T, Benkovic SJ, Hammes-Schiffer S 2005. Impact of distal mutations on the network of coupled motions correlated to hydride transfer in dihydrofolate reductase. PNAS 102:6807–12
     [Google Scholar]
  79. 79. 
    Xi J, Zhang Z, Zhuang Z, Yang J, Spiering MM et al. 2005. Interaction between the T4 helicase loading protein (gp59) and the DNA polymerase (gp43): unlocking of the gp59-gp43-DNA complex to initiate assembly of a fully functional replisome. Biochemistry 44:7747–56
     [Google Scholar]
  80. 80. 
    Xi J, Zhuang Z, Zhang Z, Selzer T, Spiering MM et al. 2005. Interaction between the T4 helicase-loading protein (gp59) and the DNA polymerase (gp43): a locking mechanism to delay replication during replisome assembly. Biochemistry 44:2305–18
     [Google Scholar]
  81. 81. 
    Smiley RD, Zhuang Z, Benkovic SJ, Hammes GG. 2006. Single-molecule investigation of the T4 bacteriophage DNA polymerase holoenzyme: multiple pathways of holoenzyme formation. Biochemistry 45:7990–97
     [Google Scholar]
  82. 82. 
    Nelson SW, Yang J, Benkovic SJ. 2006. Site-directed mutations of T4 helicase loading protein (gp59) reveal multiple modes of DNA polymerase inhibition and the mechanism of unlocking by gp41 helicase. J. Biol. Chem. 281:8697–706
     [Google Scholar]
  83. 83. 
    Yang J, Nelson SW, Benkovic SJ. 2006. The control mechanism for lagging strand polymerase recycling during bacteriophage T4 DNA replication. Mol. Cell 21:153–64
     [Google Scholar]
  84. 84. 
    Lionnet T, Spiering MM, Benkovic SJ, Bensimon D, Croquette V 2007. Real-time observation of bacteriophage T4 gp41 helicase reveals an unwinding mechanism. PNAS 104:19790–95
     [Google Scholar]
  85. 85. 
    Nelson SW, Kumar R, Benkovic SJ. 2008. RNA primer handoff in bacteriophage T4 DNA replication: the role of single-stranded DNA-binding protein and polymerase accessory proteins. J. Biol. Chem. 283:22838–46
     [Google Scholar]
  86. 86. 
    Arumugam SR, Lee TH, Benkovic SJ. 2009. Investigation of stoichiometry of T4 bacteriophage helicase loader protein (gp59). J. Biol. Chem. 284:29283–89
     [Google Scholar]
  87. 87. 
    Manosas M, Spiering MM, Zhuang Z, Benkovic SJ, Croquette V. 2009. Coupling DNA unwinding activity with primer synthesis in the bacteriophage T4 primosome. Nat. Chem. Biol. 5:904–12
     [Google Scholar]
  88. 88. 
    Manosas M, Perumal SK, Croquette V, Benkovic SJ. 2012. Direct observation of stalled fork restart via fork regression in the T4 replication system. Science 338:1217–20
     [Google Scholar]
  89. 89. 
    Manosas M, Spiering MM, Ding F, Bensimon D, Allemand JF et al. 2012. Mechanism of strand displacement synthesis by DNA replicative polymerases. Nucleic Acids Res 40:6174–86
     [Google Scholar]
  90. 90. 
    Hedglin M, Perumal SK, Hu Z, Benkovic S. 2013. Stepwise assembly of the human replicative polymerase holoenzyme. eLife 2:e00278
     [Google Scholar]
  91. 91. 
    Spiering MM, Hanoian P, Gannavaram S, Benkovic SJ 2017. RNA primer-primase complexes serve as the signal for polymerase recycling and Okazaki fragment initiation in T4 phage DNA replication. PNAS 114:5635–40
     [Google Scholar]
  92. 92. 
    Benkovic SJ, Spiering MM. 2017. Understanding DNA replication by the bacteriophage T4 replisome. J. Biol. Chem. 292:18434–42
     [Google Scholar]
  93. 93. 
    Matthews DA, Bolin JT, Burridge JM, Filman DJ, Volz KW et al. 1985. Refined crystal structures of Escherichia coli and chicken liver dihydrofolate reductase containing bound trimethoprim. J. Biol. Chem. 260:381–91
     [Google Scholar]
  94. 94. 
    Iyengar R, Rose IA. 1981. Liberation of the triosephosphate isomerase reaction intermediate and its trapping by isomerase, yeast aldolase, and methylglyoxal synthase. Biochemistry 20:1229–35
     [Google Scholar]
  95. 95. 
    Pompliano DL, Peyman A, Knowles JR. 1990. Stabilization of a reaction intermediate as a catalytic device: definition of the functional role of the flexible loop in triosephosphate isomerase. Biochemistry 29:3186–94
     [Google Scholar]
  96. 96. 
    Fierke CA, Johnson KA, Benkovic SJ. 1987. Construction and evaluation of the kinetic scheme associated with dihydrofolate reductase from Escherichia coli. Biochemistry 26:4085–92
     [Google Scholar]
  97. 97. 
    Parvez M, Napper AD, Benkovic SJ. 1988. Structure of 6-(iodomethyl)-2-oxo-2-phenoxy-1,2-oxaphosphorinane. Acta Crystallogr. C 44:Part 81414–16
     [Google Scholar]
  98. 98. 
    Adams J, Johnson K, Matthews R, Benkovic SJ. 1989. Effects of distal point-site mutations on the binding and catalysis of dihydrofolate reductase from Escherichia coli. Biochemistry 28:6611–18
     [Google Scholar]
  99. 99. 
    Fierke CA, Benkovic SJ. 1989. Probing the functional role of threonine-113 of Escherichia coli dihydrofolate reductase for its effect on turnover efficiency, catalysis, and binding. Biochemistry 28:478–86
     [Google Scholar]
  100. 100. 
    Li LY, Benkovic SJ. 1991. Impact on catalysis of secondary structural manipulation of the αC-helix of Escherichia coli dihydrofolate reductase. Biochemistry 30:1470–78
     [Google Scholar]
  101. 101. 
    Adams JA, Fierke CA, Benkovic SJ. 1991. The function of amino acid residues contacting the nicotinamide ring of NADPH in dihydrofolate reductase from Escherichia coli. Biochemistry 30:11046–54
     [Google Scholar]
  102. 102. 
    Wagner CR, Thillet J, Benkovic SJ. 1992. Complementary perturbation of the kinetic mechanism and catalytic effectiveness of dihydrofolate reductase by side-chain interchange. Biochemistry 31:7834–40
     [Google Scholar]
  103. 103. 
    Wagner CR, Huang Z, Singleton SF, Benkovic SJ. 1995. Molecular basis for nonadditive mutational effects in Escherichia coli dihydrofolate reductase. Biochemistry 34:15671–80
     [Google Scholar]
  104. 104. 
    Cameron CE, Benkovic SJ. 1997. Evidence for a functional role of the dynamics of glycine-121 of Escherichia coli dihydrofolate reductase obtained from kinetic analysis of a site-directed mutant. Biochemistry 36:15792–800
     [Google Scholar]
  105. 105. 
    Rajagopalan PT, Lutz S, Benkovic SJ. 2002. Coupling interactions of distal residues enhance dihydrofolate reductase catalysis: mutational effects on hydride transfer rates. Biochemistry 41:12618–28
     [Google Scholar]
  106. 106. 
    Antikainen NM, Smiley RD, Benkovic SJ, Hammes GG. 2005. Conformation coupled enzyme catalysis: single-molecule and transient kinetics investigation of dihydrofolate reductase. Biochemistry 44:16835–43
     [Google Scholar]
  107. 107. 
    Wang L, Tharp S, Selzer T, Benkovic SJ, Kohen A. 2006. Effects of a distal mutation on active site chemistry. Biochemistry 45:1383–92
     [Google Scholar]
  108. 108. 
    Janda KD, Schloeder D, Benkovic SJ, Lerner RA 1988. Induction of an antibody that catalyzes the hydrolysis of an amide bond. Science 241:1188–91
     [Google Scholar]
  109. 109. 
    Pollack SJ, Jacobs JW, Schultz PG. 1986. Selective chemical catalysis by an antibody. Science 234:1570–73
     [Google Scholar]
  110. 110. 
    Napper AD, Benkovic SJ, Tramontano A, Lerner RA. 1987. A stereospecific cyclization catalyzed by an antibody. Science 237:1041–43
     [Google Scholar]
  111. 111. 
    Lerner RA, Benkovic SJ. 1988. Principles of antibody catalysis. BioEssays 9:107–12
     [Google Scholar]
  112. 112. 
    Janda KD, Benkovic SJ, Lerner RA. 1989. Catalytic antibodies with lipase activity and R or S substrate selectivity. Science 244:437–40
     [Google Scholar]
  113. 113. 
    Janda KD, Weinhouse MI, Schloeder DM, Benkovic SJ, Lerner RA. 1990. Bait and switch strategy for obtaining catalytic antibodies with acyl-transfer capabilities. J. Am. Chem. Soc. 112:1274–75
     [Google Scholar]
  114. 114. 
    Iverson BL, Iverson SA, Roberts VA, Getzoff ED, Tainer JA et al. 1990. Metalloantibodies. Science 249:659–62
     [Google Scholar]
  115. 115. 
    Benkovic SJ, Adams JA, Borders CL Jr., Janda KD, Lerner RA. 1990. The enzymic nature of antibody catalysis: development of multistep kinetic processing. Science 250:1135–39
     [Google Scholar]
  116. 116. 
    Lerner RA, Benkovic SJ, Schultz PG. 1991. At the crossroads of chemistry and immunology: catalytic antibodies. Science 252:659–67
     [Google Scholar]
  117. 117. 
    Janda KD, Ashley JA, Jones TM, McLeod DA, Schloeder DM et al. 1991. Catalytic antibodies with acyl-transfer capabilities: mechanistic and kinetic investigations. J. Am. Chem. Soc. 113:291–97
     [Google Scholar]
  118. 118. 
    Gibbs RA, Posner BA, Filpula DR, Dodd SW, Finkelman MA et al. 1991. Construction and characterization of a single-chain catalytic antibody. PNAS 88:4001–4
     [Google Scholar]
  119. 119. 
    Benkovic SJ. 1992. Catalytic antibodies. Annu. Rev. Biochem. 61:29–54
     [Google Scholar]
  120. 120. 
    Huse WD, Sastry L, Iverson SA, Kang AS, Alting-Mees M et al. 1989. Generation of a large combinatorial library of the immunoglobulin repertoire in phage lambda. Science 246:1275–81
     [Google Scholar]
  121. 121. 
    Gibbs RA, Benkovic PA, Janda KD, Lerner RA, Benkovic SJ. 1992. Substituent effects of an antibody-catalyzed hydrolysis of phenyl esters: further evidence for an acyl-antibody intermediate. J. Am. Chem. Soc. 114:3528–34
     [Google Scholar]
  122. 122. 
    Stewart JD, Benkovic SJ. 1993. Catalytic antibodies: mechanistic and practical considerations. Chem. Soc. Rev. 22:213–19
     [Google Scholar]
  123. 123. 
    Stewart JD, Krebs JF, Siuzdak G, Berdis AJ, Smithrud DB, Benkovic SJ 1994. Dissection of an antibody-catalyzed reaction. PNAS 91:7404–9
     [Google Scholar]
  124. 124. 
    Hirschmann R, Smith AB 3rd, Taylor CM, Benkovic PA, Taylor SD et al. 1994. Peptide synthesis catalyzed by an antibody containing a binding site for variable amino acids. Science 265:234–37
     [Google Scholar]
  125. 125. 
    Smiley JA, Benkovic SJ 1994. Selection of catalytic antibodies for a biosynthetic reaction from a combinatorial cDNA library by complementation of an auxotrophic Escherichia coli: antibodies for orotate decarboxylation. PNAS 91:8319–23
     [Google Scholar]
  126. 126. 
    Stewart JD, Benkovic SJ. 1995. Transition-state stabilization as a measure of the efficiency of antibody catalysis. Nature 375:388–91
     [Google Scholar]
  127. 127. 
    Smithrud DB, Benkovic PA, Benkovic SJ, Roberts V, Liu J et al. 2000. Cyclic peptide formation catalyzed by an antibody ligase. PNAS 97:1953–58
     [Google Scholar]
  128. 128. 
    Barbas CF 3rd, Kang AS, Lerner RA, Benkovic SJ 1991. Assembly of combinatorial antibody libraries on phage surfaces: the gene III site. PNAS 88:7978–82
     [Google Scholar]
  129. 129. 
    Kang AS, Barbas CF, Janda KD, Benkovic SJ, Lerner RA 1991. Linkage of recognition and replication functions by assembling combinatorial antibody Fab libraries along phage surfaces. PNAS 88:4363–66
     [Google Scholar]
  130. 130. 
    Stewart JD, Benkovic SJ. 1993. Reaction mechanisms displayed by catalytic antibodies. Acc. Chem. Res. 10:396–404
     [Google Scholar]
  131. 131. 
    Falzone CJ, Benkovic SJ, Wright PE. 1990. Partial 1H NMR assignments of the Escherichia coli dihydrofolate reductase complex with folate: evidence for a unique conformation of bound folate. Biochemistry 29:9667–77
     [Google Scholar]
  132. 132. 
    Falzone CJ, Cavanagh J, Cowart M, Palmer AG 3rd, Matthews CR et al. 1994. 1H, 15N and 13C resonance assignments, secondary structure, and the conformation of substrate in the binary folate complex of Escherichia coli dihydrofolate reductase. J. Biomol. NMR 4:349–66
     [Google Scholar]
  133. 133. 
    Epstein DM, Benkovic SJ, Wright PE. 1995. Dynamics of the dihydrofolate reductase-folate complex: Catalytic sites and regions known to undergo conformational change exhibit diverse dynamical features. Biochemistry 34:11037–48
     [Google Scholar]
  134. 134. 
    Bhabha G, Lee J, Ekiert DC, Gam J, Wilson IA et al. 2011. A dynamic knockout reveals that conformational fluctuations influence the chemical step of enzyme catalysis. Science 332:234–38
     [Google Scholar]
  135. 135. 
    Liu CT, Benkovic SJ. 2013. Capturing a sulfenic acid with arylboronic acids and benzoxaborole. J. Am. Chem. Soc. 135:14544–47
     [Google Scholar]
  136. 136. 
    Cannon WR, Singleton SF, Benkovic SJ. 1996. A perspective on biological catalysis. Nat. Struct. Biol. 3:821–33
     [Google Scholar]
  137. 137. 
    Cannon WR, Benkovic SJ. 1998. Solvation, reorganization energy, and biological catalysis. J. Biol. Chem. 273:26257–60
     [Google Scholar]
  138. 138. 
    Hammes-Schiffer S, Benkovic SJ. 2006. Relating protein motion to catalysis. Annu. Rev. Biochem. 75:519–41
     [Google Scholar]
  139. 139. 
    Benkovic SJ, Hammes-Schiffer S 2007. Dihydrofolate reductase: hydrogen tunneling and protein motion. Hydrogen-Transfer Reactions, Vol. 4 JT Hynes, RL Schowen, JP Klinman, H-H Limbach 1439–54 Weinheim, Ger: Wiley-VCH Verlag
     [Google Scholar]
  140. 140. 
    Agarwal PK, Billeter SR, Rajagopalan PT, Benkovic SJ, Hammes-Schiffer S 2002. Network of coupled promoting motions in enzyme catalysis. PNAS 99:2794–99
     [Google Scholar]
  141. 141. 
    Benkovic SJ, Hammes-Schiffer S. 2003. A perspective on enzyme catalysis. Science 301:1196–202
     [Google Scholar]
  142. 142. 
    Hammes-Schiffer S, Benkovic SJ. 2006. Relating protein motion to catalysis. Annu. Rev. Biochem. 75:519–41
     [Google Scholar]
  143. 143. 
    Nashine VC, Hammes-Schiffer S, Benkovic SJ. 2010. Coupled motions in enzyme catalysis. Curr. Opin. Chem. Biol. 14:644–51
     [Google Scholar]
  144. 144. 
    Hammes GG, Benkovic SJ, Hammes-Schiffer S. 2011. Flexibility, diversity, and cooperativity: pillars of enzyme catalysis. Biochemistry 50:10422–30
     [Google Scholar]
  145. 145. 
    Liu CT, Layfield JP, Stewart RJ 3rd, French JB, Hanoian P et al. 2014. Probing the electrostatics of active site microenvironments along the catalytic cycle for Escherichia coli dihydrofolate reductase. J. Am. Chem. Soc. 136:10349–60
     [Google Scholar]
  146. 146. 
    Hanoian P, Liu CT, Hammes-Schiffer S, Benkovic S. 2015. Perspectives on electrostatics and conformational motions in enzyme catalysis. Acc. Chem. Res. 48:482–89
     [Google Scholar]
  147. 147. 
    Boger DL, Haynes NE, Warren MS, Ramcharan J, Kitos PA, Benkovic SJ. 1997. Multisubstrate analogue based on 5,8,10-trideazafolate. Bioorg. Med. Chem. 5:1853–57
     [Google Scholar]
  148. 148. 
    Su Y, Yamashita MM, Greasley SE, Mullen CA, Shim JH et al. 1998. A pH-dependent stabilization of an active site loop observed from low and high pH crystal structures of mutant monomeric glycinamide ribonucleotide transformylase at 1.8 to 1.9 Å. J. Mol. Biol. 281:485–99
     [Google Scholar]
  149. 149. 
    Boger DL, Kochanny MJ, Cai H, Wyatt D, Kitos PA et al. 1998. Design, synthesis, and evaluation of potential GAR and AICAR transformylase inhibitors. Bioorg. Med. Chem. 6:643–59
     [Google Scholar]
  150. 150. 
    Greasley SE, Yamashita MM, Cai H, Benkovic SJ, Boger DL, Wilson IA. 1999. New insights into inhibitor design from the crystal structure and NMR studies of Escherichia coli GAR transformylase in complex with β-GAR and 10-formyl-5,8,10-trideazafolic acid. Biochemistry 38:16783–93
     [Google Scholar]
  151. 151. 
    Marsilje TH, Hedrick MP, Desharnais J, Tavassoli A, Zhang Y et al. 2003. Design, synthesis, and biological evaluation of simplified α-keto heterocycle, trifluoromethyl ketone, and formyl substituted folate analogues as potential inhibitors of GAR transformylase and AICAR transformylase. Bioorg. Med. Chem. 11:4487–501
     [Google Scholar]
  152. 152. 
    Marsilje TH, Hedrick MP, Desharnais J, Capps K, Tavassoli A et al. 2003. 10-(2-benzoxazolcarbonyl)-5,10-dideaza-acyclic-5,6,7,8-tetrahydrofolic acid: a potential inhibitor of GAR transformylase and AICAR transformylase. Bioorg. Med. Chem. 11:4503–9
     [Google Scholar]
  153. 153. 
    Zhang Y, Desharnais J, Marsilje TH, Li C, Hedrick MP et al. 2003. Rational design, synthesis, evaluation, and crystal structure of a potent inhibitor of human GAR Tfase: 10-(trifluoroacetyl)-5,10-dideazaacyclic-5,6,7,8-tetrahydrofolic acid. Biochemistry 42:6043–56
     [Google Scholar]
  154. 154. 
    Wolan DW, Greasley SE, Wall MJ, Benkovic SJ, Wilson IA. 2003. Structure of avian AICAR transformylase with a multisubstrate adduct inhibitor β-DADF identifies the folate binding site. Biochemistry 42:10904–14
     [Google Scholar]
  155. 155. 
    An S, Kumar R, Sheets ED, Benkovic SJ. 2008. Reversible compartmentalization of de novo purine biosynthetic complexes in living cells. Science 320:103–6
     [Google Scholar]
  156. 156. 
    An S, Deng Y, Tomsho JW, Kyoung M, Benkovic SJ 2010. Microtubule-assisted mechanism for functional metabolic macromolecular complex formation. PNAS 107:12872–76
     [Google Scholar]
  157. 157. 
    French JB, Zhao H, An S, Niessen S, Deng Y et al. 2013. Hsp70/Hsp90 chaperone machinery is involved in the assembly of the purinosome. PNAS 110:2528–33
     [Google Scholar]
  158. 158. 
    French JB, Jones SA, Deng H, Pedley AM, Kim D et al. 2016. Spatial colocalization and functional link of purinosomes with mitochondria. Science 351:733–37
     [Google Scholar]
  159. 159. 
    Pedley AM, Benkovic SJ. 2017. A new view into the regulation of purine metabolism: the purinosome. Trends Biochem. Sci. 42:141–54
     [Google Scholar]
  160. 160. 
    Benkovic SJ, Pedley AM, Spiering MM. 2018. Intracellular enzyme organization. SciTech Eur. Q. 26:1–2
     [Google Scholar]
  161. 161. 
    Pareek V, Tian H, Winograd N, Benkovic SJ. 2020. Metabolomics and mass spectrometry imaging reveal channeled de novo purine synthesis in cells. Science 368:283–90
     [Google Scholar]
  162. 162. 
    Pedley AM, Benkovic SJ. 2018. Detecting purinosome metabolon formation with fluorescence microscopy. Methods Mol. Biol. 1764:279–89
     [Google Scholar]
/content/journals/10.1146/annurev-biochem-062320-062929
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From Bioorganic Models to Cells
Annual Review of Biochemistry 90, 57 (2021); https://doi.org/10.1146/annurev-biochem-062320-062929
/content/journals/10.1146/annurev-biochem-062320-062929
/content/journals/10.1146/annurev-biochem-062320-062929
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