1932

Abstract

This first serious attempt at an autobiographical accounting has forced me to sit still long enough to compile my thoughts about a long personal and scientific journey. I especially hope that my trajectory will be of interest and perhaps beneficial to much younger women who are just getting started in their careers. To paraphrase from Virginia Woolf's writings in at the beginning of the 20th century, “for most of history Anonymous was a Woman.” However, Ms. Woolf is also quoted as saying “nothing has really happened until it has been described,” a harbinger of the enormous historical changes that were about to be enacted and recorded by women in the sciences and other disciplines. The progress in my chosen field of study—the chemical basis of enzyme action—has also been remarkable, from the first description of an enzyme's 3D structure to a growing and deep understanding of the origins of enzyme catalysis.

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2019-06-20
2024-06-18
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Literature Cited

  1. 1. 
    Klinman NR. 1969. Antibody with homogeneous antigen binding produced by splenic foci in organ culture. Immunochemistry 6:757–59
    [Google Scholar]
  2. 2. 
    Klinman JP, Rose IA. 1971. Mechanism of the aconitate isomerase reaction. Biochemistry 10:2259–66
    [Google Scholar]
  3. 3. 
    Klinman JP, Rose IA. 1971. Stereochemistry of the interconversions of citrate and acetate catalyzed by citrate synthase, adenosine triphosphate citrate lyase, and citrate lyase. Biochemistry 10:2267–72
    [Google Scholar]
  4. 4. 
    Klinman JP. 1972. The mechanism of enzyme-catalyzed reduced nicotinamide adenine dinucleotide-dependent reductions. Substituent and isotope effects in the yeast alcohol dehydrogenase reaction. J. Biol. Chem. 247:7977–87
    [Google Scholar]
  5. 5. 
    Klinman JP. 1976. Isotope effects and structure-reactivity correlations in the yeast alcohol dehydrogenase reaction. A study of the enzyme-catalyzed oxidation of aromatic alcohols. Biochemistry 15:2018–26
    [Google Scholar]
  6. 6. 
    Klinman JP, Humphries H, Voet JG 1980. Deduction of kinetic mechanism in multisubstrate enzyme reactions from tritium isotope effects. J. Biol. Chem. 255:11648–51
    [Google Scholar]
  7. 7. 
    Summers MC, Markovic R, Klinman JP 1979. Stereochemistry and kinetic isotope effects in the bovine plasma amine oxidase catalyzed oxidation of dopamine. Biochemistry 18:1969–79
    [Google Scholar]
  8. 8. 
    Miller SM, Klinman JP. 1985. Secondary isotope effects and structure-reactivity correlations in the dopamine β-monooxygenase reaction: evidence for a chemical mechanism. Biochemistry 24:2114–27
    [Google Scholar]
  9. 9. 
    Ahn N, Klinman JP. 1983. Mechanism of modulation of dopamine β-monooxygenase by pH and fumarate as deduced from initial rate and primary isotope effect studies. Biochemistry 22:3096–106
    [Google Scholar]
  10. 10. 
    Ahn NG, Klinman JP. 1987. Activation of dopamine β-monooxygenase by external and internal electron donors in resealed chromaffin granule ghosts. J. Biol. Chem. 262:1485–92
    [Google Scholar]
  11. 11. 
    Palcic MM, Klinman JP. 1983. Isotopic probes yield microscopic constants: separation of binding energy from catalytic efficiency in the bovine plasma amine oxidase reaction. Biochemistry 22:5957–66
    [Google Scholar]
  12. 12. 
    Klinman JP, Krueger M, Brenner M, Edmondson DE 1984. Evidence for two copper atoms/subunit in dopamine β-monooxygenase catalysis. J. Biol. Chem. 259:3399–402
    [Google Scholar]
  13. 13. 
    Brenner MC, Murray CJ, Klinman JP 1989. Rapid-freeze and chemical-quench studies of dopamine β-monooxygenase: comparison of pre-steady-state and steady-state parameters. Biochemistry 28:4656–64
    [Google Scholar]
  14. 14. 
    Prigge ST, Kolhekar AS, Eipper BA, Mains RE, Amzel LM 1997. Amidation of bioactive peptides: the structure of peptidylglycine α-hydroxylating monooxygenase. Science 278:1300–5
    [Google Scholar]
  15. 15. 
    Klinman JP. 2006. The copper-enzyme family of dopamine β-monooxygenase and peptidylglycine α-hydroxylating monooxygenase: resolving the chemical pathway for substrate hydroxylation. J. Biol. Chem. 281:3013–16
    [Google Scholar]
  16. 16. 
    Zhu H, Sommerhalter M, Nguy AKL, Klinman JP 2015. Solvent and temperature probes of the long-range electron-transfer step in tyramine β-monooxygenase: demonstration of a long-range proton-coupled electron-transfer mechanism. J. Am. Chem. Soc. 137:5720–29
    [Google Scholar]
  17. 17. 
    Evans JP, Ahn K, Klinman JP 2003. Evidence that dioxygen and substrate activation are tightly coupled in dopamine β-monooxygenase: implications for the reactive oxygen species. J. Biol. Chem. 278:49691–98
    [Google Scholar]
  18. 18. 
    Duine JA, Jongejan JA. 1989. Pyrroloquinoline quinone: a novel cofactor. Vitam. Horm. 45:223–62
    [Google Scholar]
  19. 19. 
    Blaschko H, Buffoni F. 1965. Pyridoxal phosphate as a constituent of histaminase (benzylamine oxidase) of pig plasma. Proc. R. Soc. B 163:45–60
    [Google Scholar]
  20. 20. 
    Janes SM, Mu D, Wemmer D, Smith AJ, Kaur S et al. 1990. A new redox cofactor in eukaryotic enzymes: 6-hydroxydopa at the active site of bovine serum amine oxidase. Science 248:981–87
    [Google Scholar]
  21. 21. 
    Wang SX, Mure M, Medzihradszky KF, Burlingame AL, Brown DE et al. 1996. A crosslinked cofactor in lysyl oxidase: redox function for amino acid side chains. Science 273:1078–84
    [Google Scholar]
  22. 22. 
    Klinman JP, Bonnot F. 2014. Intrigues and intricacies of the biosynthetic pathways for the enzymatic quinocofactors: PQQ, TTQ, CTQ, TPQ, and LTQ. Chem. Rev. 114:4343–65
    [Google Scholar]
  23. 23. 
    Cai D, Klinman JP. 1994. Evidence for a self-catalytic mechanism of 2,4,5-trihydroxyphenylalanine quinone biogenesis in yeast copper amine oxidase. J. Biol. Chem. 269:32039–42
    [Google Scholar]
  24. 24. 
    Tang C, Klinman JP. 2001. The catalytic function of bovine lysyl oxidase in the absence of copper. J. Biol. Chem. 276:30575–78
    [Google Scholar]
  25. 25. 
    DuBois JL, Klinman JP. 2005. Mechanism of post-translational quinone formation in copper amine oxidases and its relationship to the catalytic turnover. Arch. Biochem. Biophys. 433:255–65
    [Google Scholar]
  26. 26. 
    Davidson VL, Wilmot CM. 2013. Posttranslational biosynthesis of the protein-derived cofactor tryptophan tryptophylquinone. Annu. Rev. Biochem. 82:531–50
    [Google Scholar]
  27. 27. 
    Datta S, Mori Y, Takagi K, Kawaguchi K, Chen ZW et al. 2001. Structure of a quinohemoprotein amine dehydrogenase with an uncommon redox cofactor and highly unusual crosslinking. PNAS 98:14268–73
    [Google Scholar]
  28. 28. 
    Jalkanen S, Salmi M. 2001. Cell surface monoamine oxidases: enzymes in search of a function. EMBO J 20:3893–901
    [Google Scholar]
  29. 29. 
    Shen SH, Wertz DL, Klinman JP 2012. Implication for functions of the ectopic adipocyte copper amine oxidase (AOC3) from purified enzyme and cell-based kinetic studies. PLOS ONE 7:e29270
    [Google Scholar]
  30. 30. 
    Rucker R, Chowanadisai W, Nakano M 2009. Potential physiological importance of pyrroloquinoline quinone. Altern. Med. Rev. 14:268–77
    [Google Scholar]
  31. 31. 
    Akagawa M, Minematsu K, Shibata T, Kondo T, Ishii T, Uchida K 2016. Identification of lactate dehydrogenase as a mammalian pyrroloquinoline quinone (PQQ)-binding protein. Sci. Rep. 6:26723
    [Google Scholar]
  32. 32. 
    Bigeleisen JM, Goeppert-Mayer M. 1947. Calculation of equilibrium constants for isotopic exchange reactions. J. Chem. Phys. 15:261–67
    [Google Scholar]
  33. 33. 
    Truhlar DG, Garrett BC, Hipes PG, Kuppermann A 1984. Test of variational transition-state theory against accurate quantal results for a reaction with very large reaction-path curvature and a low barrier. J. Chem. Phys. 81:3542–45
    [Google Scholar]
  34. 34. 
    Thiemens MH. 1999. Mass-independent isotope effects in planetary atmospheres and the early solar system. Science 283:341–45
    [Google Scholar]
  35. 35. 
    Hermes JD, Cleland WW. 1984. Evidence from multiple isotope effect determinations for coupled hydrogen motion and tunneling in the reaction catalyzed by glucose-6-phosphate-dehydrogenase. J. Am. Chem. Soc. 106:7263–64
    [Google Scholar]
  36. 36. 
    Welsh KM, Creighton DJ, Klinman JP 1980. Transition-state structure in the yeast alcohol dehydrogenase reaction: the magnitude of solvent and α-secondary hydrogen isotope effects. Biochemistry 19:2005–16
    [Google Scholar]
  37. 37. 
    Douzou P. 1982. Developments in low-temperature biochemistry and biology. Proc. R. Soc. B 217:1–28
    [Google Scholar]
  38. 38. 
    Cha Y, Murray CJ, Klinman JP 1989. Hydrogen tunneling in enzyme reactions. Science 243:1325–30
    [Google Scholar]
  39. 39. 
    Grant KL, Klinman JP. 1989. Evidence that both protium and deuterium undergo significant tunneling in the reaction catalyzed by bovine serum amine oxidase. Biochemistry 28:6597–605
    [Google Scholar]
  40. 40. 
    Jonsson T, Edmondson DE, Klinman JP 1994. Hydrogen tunneling in the flavoenzyme monoamine oxidase B. Biochemistry 33:14871–78
    [Google Scholar]
  41. 41. 
    Jonsson T, Glickman MH, Sun SJ, Klinman JP 1996. Experimental evidence for extensive tunneling of hydrogen in the lipoxygenase reaction: implications for enzyme catalysis. J. Am. Chem. Soc. 118:10319–20
    [Google Scholar]
  42. 42. 
    Bahnson BJ, Colby TD, Chin JK, Goldstein BM, Klinman JP 1997. A link between protein structure and enzyme catalyzed hydrogen tunneling. PNAS 94:12797–802
    [Google Scholar]
  43. 43. 
    Saunders WHJ. 1985. Calculations of isotope effects in elimination reactions. New experimental criteria for tunneling in slow proton transfers. J. Am. Chem. Soc. 107:164–69
    [Google Scholar]
  44. 44. 
    Glickman MH, Wiseman JS, Klinman JP 1994. Extremely large isotope effects in the soybean lipoxygenase-linoleic acid reaction. J. Am. Chem. Soc. 116:793–94
    [Google Scholar]
  45. 45. 
    Glickman M, Klinman JP. 1995. Nature of rate-limiting steps in the soybean lipoxygenase-1 reaction. Biochemistry 34:14077–92
    [Google Scholar]
  46. 46. 
    Dogonadze RR, Kuznetsov AM, Levich VG 1968. Theory of hydrogen-ion discharge on metals: case of high overvoltages. Electrochim. Acta 13:1025–44
    [Google Scholar]
  47. 47. 
    Hu S, Sharma SC, Scouras AD, Soudackov AV, Carr CA et al. 2014. Extremely elevated room-temperature kinetic isotope effects quantify the critical role of barrier width in enzymatic C–H activation. J. Am. Chem. Soc. 136:8157–60
    [Google Scholar]
  48. 48. 
    Hu S, Soudackov AV, Hammes-Schiffer S, Klinman JP 2017. Enhanced rigidification within a double mutant of soybean lipoxygenase provides experimental support for vibronically nonadiabatic proton-coupled electron transfer models. ACS Catal 7:3569–74
    [Google Scholar]
  49. 49. 
    Horitani M, Offenbacher AR, Carr CA, Yu T, Hoeke V et al. 2017. 13C ENDOR spectroscopy of lipoxygenase–substrate complexes reveals the structural basis for C–H activation by tunneling. J. Am. Chem. Soc. 139:1984–97
    [Google Scholar]
  50. 50. 
    Westheimer FH. 1961. The magnitude of the primary kinetic isotope effect for components of hydrogen and deuterium. Chem. Rev. 61:265–73
    [Google Scholar]
  51. 51. 
    Knapp MJ, Rickert K, Klinman JP 2002. Temperature-dependent isotope effects in soybean lipoxygenase-1: Correlating hydrogen tunneling with protein dynamics. J. Am. Chem. Soc. 124:3865–74
    [Google Scholar]
  52. 52. 
    Klinman JP, Offenbacher AR, Hu S 2017. Origins of enzyme catalysis: experimental findings for C–H activation, new models, and their relevance to prevailing theoretical constructs. J. Am. Chem. Soc. 139:18409–27
    [Google Scholar]
  53. 53. 
    Offenbacher AR, Hu S, Poss EM, Carr CAM, Scouras AD et al. 2017. Hydrogen–deuterium exchange of lipoxygenase uncovers a relationship between distal, solvent exposed protein motions and the thermal activation barrier for catalytic proton-coupled electron tunneling. ACS Cent. Sci. 3:570–79
    [Google Scholar]
  54. 54. 
    Guagliardi A, Martino M, Iaccarino I, DeRosa M, Rossi M, Bartolucci S 1996. Purification and characterization of the alcohol dehydrogenase from a novel strain of Bacillus stearothermophilus growing at 70°C. Int. J. Biochem. Cell Biol. 28:239–46
    [Google Scholar]
  55. 55. 
    Kohen A, Cannio R, Bartolucci S, Klinman JP 1999. Enzyme dynamics and hydrogen tunnelling in a thermophilic alcohol dehydrogenase. Nature 399:496–99
    [Google Scholar]
  56. 55a. 
    Klinman JP, Offenbacher AR 2018. Understanding biological hydrogen transfer through the lens of temperature dependent kinetic isotope effects. Acc. Chem. Res 51:1966–74
    [Google Scholar]
  57. 56. 
    Klinman JP. 2009. An integrated model for enzyme catalysis emerges from studies of hydrogen tunneling. Chem. Phys. Lett. 471:179–93
    [Google Scholar]
  58. 57. 
    Nagel ZD, Klinman JP. 2009. A 21st century revisionist's view at a turning point in enzymology. Nat. Chem. Biol. 5:543–50
    [Google Scholar]
  59. 58. 
    Klinman JP, Kohen A. 2013. Hydrogen tunneling links protein dynamics to enzyme catalysis. Annu. Rev. Biochem. 82:471–96
    [Google Scholar]
  60. 59. 
    Liang Z-X, Lee T, Resing KA, Ahn NG, Klinman JP 2004. Thermal-activated protein mobility and its correlation with catalysis in thermophilic alcohol dehydrogenase. PNAS 101:9556–61
    [Google Scholar]
  61. 60. 
    Liang Z-X, Tsigos I, Bouriotis V, Klinman JP 2004. Impact of protein flexibility on hydride-transfer parameters in thermophilic and psychrophilic alcohol dehydrogenases. J. Am. Chem. Soc. 126:9500–1
    [Google Scholar]
  62. 61. 
    Nagel ZD, Dong M, Bahnson BJ, Klinman JP 2011. Impaired protein conformational landscapes as revealed in anomalous Arrhenius prefactors. PNAS 108:10520–25
    [Google Scholar]
  63. 62. 
    Nagel ZD, Meadows CW, Dong M, Bahnson BJ, Klinman JP 2012. Active site hydrophobic residues impact hydrogen tunneling differently in a thermophilic alcohol dehydrogenase at optimal versus nonoptimal temperatures. Biochemistry 51:4147–56
    [Google Scholar]
  64. 63. 
    Nagel ZD, Cun S, Klinman JP 2013. Identification of a long-range protein network that modulates active site dynamics in extremophilic alcohol dehydrogenases. J. Biol. Chem. 288:14087–97
    [Google Scholar]
  65. 64. 
    Meadows CW, Ou R, Klinman JP 2014. Picosecond-resolved fluorescent probes at functionally distinct tryptophans within a thermophilic alcohol dehydrogenase: relationship of temperature-dependent changes in fluorescence to catalysis. J. Phys. Chem. B 118:6049–61
    [Google Scholar]
  66. 65. 
    Meadows CW, Balakrishnan G, Kier BL, Spiro TG, Klinman JP 2015. Temperature-jump fluorescence provides evidence for fully reversible microsecond dynamics in a thermophilic alcohol dehydrogenase. J. Am. Chem. Soc. 137:10060–63
    [Google Scholar]
  67. 66. 
    Vaughn MB, Zhang J, Spiro TG, Dyer RB, Klinman JP 2018. Activity-related microsecond dynamics revealed by temperature-jump Förster resonance energy transfer measurements on thermophilic alcohol dehydrogenase. J. Am. Chem. Soc. 140:900–3
    [Google Scholar]
  68. 67. 
    Zhang J, Klinman JP. 2011. Enzymatic methyl transfer: role of an active site residue in generating active site compaction that correlates with catalytic efficiency. J. Am. Chem. Soc. 133:17134–37
    [Google Scholar]
  69. 68. 
    Zhang J, Kulik HJ, Martinez TJ, Klinman JP 2015. Mediation of donor-acceptor distance in an enzymatic methyl transfer reaction. PNAS 112:7954–59
    [Google Scholar]
  70. 69. 
    Zhang J, Klinman JP. 2016. Convergent mechanistic features between the structurally diverse N- and O-methyltransferases, glycine N-methyltransferase and catechol O-methyltransferase. J. Am. Chem. Soc. 138:9158–65
    [Google Scholar]
  71. 70. 
    Goto Y, Klinman JP. 2002. Binding of dioxygen to non-metal sites in proteins: exploration of the importance of binding site size versus hydrophobicity in the copper amine oxidase from Hansenula polymorpha. . Biochemistry 41:13637–43
    [Google Scholar]
  72. 71. 
    Mure M, Mills SA, Klinman JP 2002. Catalytic mechanism of the topa quinone containing copper amine oxidases. Biochemistry 41:9269–78
    [Google Scholar]
  73. 72. 
    Knapp MJ, Klinman JP. 2003. Kinetic studies of oxygen reactivity in soybean lipoxygenase-1. Biochemistry 42:11466–75
    [Google Scholar]
  74. 73. 
    Johnson BJ, Cohen J, Welford RW, Pearson AR, Schulten K et al. 2007. Exploring molecular oxygen pathways in Hansenula polymorpha copper-containing amine oxidase. J. Biol. Chem. 282:17767–76
    [Google Scholar]
  75. 74. 
    Collazo L, Klinman JP. 2016. Control of the position of oxygen delivery in soybean lipoxygenase-1 by amino acid side chains within a gas migration channel. J. Biol. Chem. 291:9052–59
    [Google Scholar]
  76. 75. 
    Kalms J, Schmidt A, Frielingsdorf S, Utesch T, Gotthard G et al. 2018. Tracking the route of molecular oxygen in O2-tolerant membrane-bound [NiFe] hydrogenase. PNAS 115:E2229–37
    [Google Scholar]
  77. 76. 
    Hwang CC, Grissom CB. 1994. Unusually large deuterium isotope effects in soybean lipoxygenase are not caused by a magnetic isotope effect. J. Am. Chem. Soc. 116:795–96
    [Google Scholar]
  78. 77. 
    Glickman MH, Cliff S, Thiemens M, Klinman JP 1997. Comparative study of 17O and 18O isotope effects as a probe for dioxygen activation: application to the soybean lipoxygenase reaction. J. Am. Chem. Soc. 119:11357–61
    [Google Scholar]
  79. 78. 
    Guy RD, Fogel ML, Berry JA 1993. Photosynthetic fractionation of the stable isotopes of oxygen and carbon. Plant Physiol 101:37–47
    [Google Scholar]
  80. 79. 
    Tian G, Klinman JP. 1993. Discrimination between 16O and 18O in oxygen binding to the reversible oxygen carriers hemoglobin, myoglobin, hemerythrin, and hemocyanin: a new probe for oxygen binding and reductive activation by proteins. J. Am. Chem. Soc. 115:8891–97
    [Google Scholar]
  81. 80. 
    Tian G, Berry JA, Klinman JP 1994. Oxygen-18 kinetic isotope effects in the dopamine β-monooxygenase reaction: evidence for a new chemical mechanism in non-heme metallomonooxygenases. Biochemistry 33:226–34
    [Google Scholar]
  82. 81. 
    Purdy MM, Koo LS, Ortiz de Montellano PR, Klinman JP 2006. Mechanism of O2 activation by cytochrome P450cam studied by isotope effects and transient state kinetics. Biochemistry 45:15793–806
    [Google Scholar]
  83. 82. 
    Stahl SS, Francisco WA, Merkx M, Klinman JP, Lippard SJ 2001. Oxygen kinetic isotope effects in soluble methane monooxygenase. J. Biol. Chem. 276:4549–53
    [Google Scholar]
  84. 83. 
    Mirica LM, McCusker KP, Munos JW, Liu HW, Klinman JP 2008. 18O kinetic isotope effects in non-heme iron enzymes: probing the nature of Fe/O2 intermediates. J. Am. Chem. Soc. 130:8122–23
    [Google Scholar]
  85. 84. 
    Zhu H, Peck SC, Bonnot F, van der Donk WA, Klinman JP 2015. Oxygen-18 kinetic isotope effects of nonheme iron enzymes HEPD and MPnS support iron(III) superoxide as the hydrogen abstraction species. J. Am. Chem. Soc. 137:10448–51
    [Google Scholar]
  86. 85. 
    Hermes JD, Roeske CA, O'Leary MH, Cleland WW 1982. Use of multiple isotope effects to determine enzyme mechanisms and intrinsic isotope effects. Malic enzyme and glucose 6-phosphate dehydrogenase. Biochemistry 21:5106–14
    [Google Scholar]
  87. 86. 
    Groves JT. 2006. High-valent iron in chemical and biological oxidations. J. Inorg. Biochem. 100:434–47
    [Google Scholar]
  88. 87. 
    Roth JP, Klinman JP. 2003. Catalysis of electron transfer during activation of O2 by the flavoprotein glucose oxidase. PNAS 100:62–67
    [Google Scholar]
  89. 88. 
    Roth JP, Wincek R, Nodet G, Edmondson DE, McIntire WS, Klinman JP 2004. Oxygen isotope effects on electron transfer to O2 probed using chemically modified flavins bound to glucose oxidase. J. Am. Chem. Soc. 126:15120–31
    [Google Scholar]
  90. 89. 
    Meyers MP, Klinman JP. 2011. Investigating inner-sphere reorganization via secondary kinetic isotope effects in the C-H cleavage reaction catalyzed by soybean lipoxygenase: tunneling in the substrate backbone as well as the transferred hydrogen. J. Am. Chem. Soc. 133:430–39
    [Google Scholar]
  91. 90. 
    Shen YQ, Bonnot F, Imsand EM, RoseFigura JM, Sjolander K, Klinman JP 2012. Distribution and properties of the genes encoding the biosynthesis of the bacterial cofactor, pyrroloquinoline quinone. Biochemistry 51:2265–75
    [Google Scholar]
  92. 91. 
    Wecksler SR, Stoll S, Iavarone AT, Imsand EM, Tran H et al. 2010. Interaction of PqqE and PqqD in the pyrroloquinoline quinone (PQQ) biosynthetic pathway links PqqD to the radical SAM superfamily. Chem. Commun. 46:7031–33
    [Google Scholar]
  93. 92. 
    Barr I, Latham JA, Iavarone AT, Chantarojsiri T, Hwang JD, Klinman JP 2016. Demonstration that the radical S-adenosylmethionine (SAM) enzyme PqqE catalyzes de novo carbon-carbon cross-linking within a peptide substrate PqqA in the presence of the peptide chaperone PqqD. J. Biol. Chem. 291:8877–84
    [Google Scholar]
  94. 93. 
    Latham JA, Barr I, Klinman JP 2017. At the confluence of ribosomally synthesized peptide modification and radical S-adenosylmethionine (SAM) enzymology. J. Biol. Chem. 292:16397–405
    [Google Scholar]
  95. 94. 
    Latham JA, Iavarone AT, Barr I, Juthani PV, Klinman JP 2015. PqqD is a novel peptide chaperone that forms a ternary complex with the radical S-adenosylmethionine protein PqqE in the pyrroloquinoline quinone biosynthetic pathway. J. Biol. Chem. 290:12908–18
    [Google Scholar]
  96. 95. 
    Evans RL, Latham JA, Xia YL, Klinman JP, Wilmot CM 2017. Nuclear magnetic resonance structure and binding studies of PqqD, a chaperone required in the biosynthesis of the bacterial dehydrogenase cofactor pyrroloquinoline quinone. Biochemistry 56:2735–46
    [Google Scholar]
  97. 96. 
    Magnusson OT, Toyama H, Saeki M, Schwarzenbacher R, Klinman JP 2004. The structure of a biosynthetic intermediate of pyrroloquinoline quinone (PQQ) and elucidation of the final step of PQQ biosynthesis. J. Am. Chem. Soc. 126:5342–43
    [Google Scholar]
  98. 97. 
    Magnusson OT, Toyama H, Saeki M, Rojas A, Reed JC et al. 2004. Quinone biogenesis: structure and mechanism of PqqC, the final catalyst in the production of pyrroloquinoline quinone. PNAS 101:7913–18
    [Google Scholar]
  99. 98. 
    Magnusson OT, RoseFigura JM, Toyama H, Schwarzenbacher R, Klinman JP 2007. Pyrroloquinoline quinone biogenesis: characterization of PqqC and its H84N and H84A active site variants. Biochemistry 46:7174–86
    [Google Scholar]
  100. 99. 
    RoseFigura JM, Puehringer S, Schwarzenbacher R, Toyama H, Klinman JP 2011. Characterization of a protein-generated O2 binding pocket in PqqC, a cofactorless oxidase catalyzing the final step in PQQ production. Biochemistry 50:1556–66
    [Google Scholar]
  101. 100. 
    Bonnot F, Iavarone AT, Klinman JP 2013. Multistep, eight-electron oxidation catalyzed by the cofactorless oxidase, PqqC: identification of chemical intermediates and their dependence on molecular oxygen. Biochemistry 52:4667–75
    [Google Scholar]
  102. 100a. 
    Koehn EM, Latham JA, Armand T, Evans RL III, Tu X 2019. Discovery of hydroxylase activity for PqqB provides a missing link in the pyrroloquinoline quinone biosynthetic pathway. J. Am. Chem. Soc 1414398–4405
    [Google Scholar]
  103. 101. 
    Daniell E. 2006. Every Other Thursday: Stories and Strategies from Successful Women Scientists New Haven, CT: Yale Univ. Press
    [Google Scholar]
  104. 102. 
    Mason MA, Wolfinger NH, Goulden M 2013. Do Babies Matter? Gender and Family in the Ivory Tower New Brunswick, NJ: Rutgers Univ. Press
    [Google Scholar]
  105. 103. 
    Wikipedia 2018. Judith Klinman. Wikipedi https://en.wikipedia.org/wiki/Judith_Klinman
    [Google Scholar]
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