Advertisement

Divergent mechanisms of iron-containing enzymes for hydrocarbon biosynthesis

  • Courtney E. Wise
  • Job L. Grant
  • Jose A. Amaya
  • Steven C. Ratigan
  • Chun H. Hsieh
  • Olivia M. Manley
  • Thomas M. MakrisEmail author
Minireview
Part of the following topical collections:
  1. 60 Years of Oxygen Activation

Abstract

Increasing levels of energy consumption, dwindling resources, and environmental considerations have served as compelling motivations to explore renewable alternatives to petroleum-based fuels, including enzymatic routes for hydrocarbon synthesis. Phylogenetically diverse species have long been recognized to produce hydrocarbons, but many of the enzymes responsible have been identified within the past decade. The enzymatic conversion of Cn chain length fatty aldehydes (or acids) to Cn-1 hydrocarbons, alkanes or alkenes, involves a C–C scission reaction. Surprisingly, the enzymes involved in hydrocarbon synthesis utilize non-heme mononuclear iron, dinuclear iron, and thiolate-ligated heme cofactors that are most often associated with monooxygenation reactions. In this review, we examine the mechanisms of several enzymes involved in hydrocarbon biosynthesis, with specific emphasis on the structural and electronic changes that enable this functional switch.

Graphical abstract

Keywords

Biosynthesis Cofactor Cytochrome Mossbauer spectroscopy Electron paramagnetic resonance 

Notes

Acknowledgements

Financial support was provided by an ASPIRE grant from the USC Vice President of Research and a National Science Foundation CAREER Grant 1555066 (to T.M.M.).

References

  1. 1.
    Hill J, Nelson E, Tilman D, Polasky S, Tiffany D (2006) Proc Natl Acad Sci USA 103:11206–11210PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Brennan L, Owende P (2010) Renew Sustain Energy Rev 14:557–577CrossRefGoogle Scholar
  3. 3.
    Carroll A, Somerville C (2009) Annu Rev Plant Biol 60:165–182PubMedCrossRefGoogle Scholar
  4. 4.
    Van Dyk JS, Pletschke BI (2012) Biotechnol Adv 30:1458–1480PubMedCrossRefGoogle Scholar
  5. 5.
    Liao JC, Mi L, Pontrelli S, Luo SS (2016) Nat Rev Microbiol 14:288–304PubMedCrossRefGoogle Scholar
  6. 6.
    Liu TG, Khosla C (2010) Annu Rev Genet 44:53–69PubMedCrossRefGoogle Scholar
  7. 7.
    Peralta-Yahya PP, Keasling JD (2010) Biotechnol J 5:147–162PubMedCrossRefGoogle Scholar
  8. 8.
    Rabinovitch-Deere CA, Oliver JWK, Rodriguez GM, Atsumi S (2013) Chem Rev 113:4611–4632PubMedCrossRefGoogle Scholar
  9. 9.
    Lu XF, Vora H, Khosla C (2008) Metab Eng 10:333–339PubMedCrossRefGoogle Scholar
  10. 10.
    Xu P, Gu Q, Wang WY, Wong L, Bower AGW, Collins CH, Koffas MAG (2013) Nat Commun 4:1409–1416PubMedCrossRefGoogle Scholar
  11. 11.
    Zhou YJJ, Buijs NA, Zhu ZW, Qin JF, Siewers V, Nielsen J (2016) Nat Commun 7:11709–11717PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Qiu Y, Tittiger C, Wicker-Thomas C, Le Goff G, Young S, Wajnberg E, Fricaux T, Taquet N, Blomquist GJ, Feyereisen R (2012) Proc Natl Acad Sci USA 109:14858–14863PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Lea-Smith DJ, Ortiz-Suarez ML, Lenn T, Nurnberg DJ, Baers LL, Davey MP, Parolini L, Huber RG, Cotton CA, Mastroianni G, Bombelli P, Ungerer P, Stevens TJ, Smith AG, Bond PJ, Mullineaux CW, Howe CJ (2016) Plant Physiol 172:1928–1940PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Krebs C, Fujimori DG, Walsh CT, Bollinger JM (2007) Acc Chem Res 40:484–492PubMedCrossRefGoogle Scholar
  15. 15.
    Krest CM, Onderko EL, Yosca TH, Calixto JC, Karp RF, Livada J, Rittle J, Green MT (2013) J Biol Chem 288:17074–17081PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Que L (2007) Acc Chem Res 40:493–500PubMedCrossRefGoogle Scholar
  17. 17.
    Groves JT, McClusky GA (1976) J Am Chem Soc 98:859–861CrossRefGoogle Scholar
  18. 18.
    Groves JT, McClusky GA, White RE, Coon MJ (1978) Biochem Biophys Res Commun 81:154–160PubMedCrossRefGoogle Scholar
  19. 19.
    Han J, Chan HWS, Calvin M (1969) J Am Chem Soc 91:5156–5159PubMedCrossRefGoogle Scholar
  20. 20.
    Winters K, Parker PL, Van Baalen C (1969) Science 163:467–468PubMedCrossRefGoogle Scholar
  21. 21.
    Schirmer A, Rude MA, Li X, Popova E, del Cardayre SB (2010) Science 329:559–562PubMedCrossRefGoogle Scholar
  22. 22.
    Cheesbrough TM, Kolattukudy PE (1984) Proc Natl Acad Sci USA 81:6613–6617PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Cheesbrough TM, Kolattukudy PE (1988) J Biol Chem 263:2738–2743PubMedGoogle Scholar
  24. 24.
    Dennis M, Kolattukudy PE (1992) Proc Natl Acad Sci USA 89:5306–5310PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Lawson DM, Artymiuk PJ, Yewdall SJ, Smith JMA, Livingstone JC, Treffry A, Luzzago A, Levi S, Arosio P, Cesareni G, Thomas CD, Shaw WV, Harrison PM (1991) Nature 349:541–544PubMedCrossRefGoogle Scholar
  26. 26.
    Nordlund P, Sjoberg BM, Eklund H (1990) Nature 345:593–598PubMedCrossRefGoogle Scholar
  27. 27.
    Stubbe J, Riggs-Gelasco P (1998) Trends Biochem Sci 23:438–443PubMedCrossRefGoogle Scholar
  28. 28.
    Elango N, Radhakrishnan R, Froland WA, Wallar BJ, Earhart CA, Lipscomb JD, Ohlendorf DH (1997) Protein Sci 6:556–568PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Rosenzweig AC, Frederick CA, Lippard SJ, Nordlund P (1993) Nature 366:537–543PubMedCrossRefGoogle Scholar
  30. 30.
    Fox BG, Froland WA, Dege JE, Lipscomb JD (1989) J Biol Chem 264:10023–10033PubMedGoogle Scholar
  31. 31.
    Bollinger JM, Edmondson DE, Huynh BH, Filley J, Norton JR, Stubbe J (1991) Science 253:292–298PubMedCrossRefGoogle Scholar
  32. 32.
    Stirling DI, Colby J, Dalton H (1979) Biochem J 177:361–364PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Tinberg CE, Lippard SJ (2010) Biochemistry 49:7902–7912PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Das D, Eser BE, Han J, Sciore A, Marsh EN (2011) Angew Chem Int Ed Engl 50:7148–7152PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Eser BE, Das D, Han J, Jones PR, Marsh EN (2011) Biochemistry 50:10743–10750PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Aukema KG, Makris TM, Stoian SA, Richman JE, Munck E, Lipscomb JD, Wackett LP (2013) ACS Catal 3:2228–2238PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Eser BE, Das D, Han J, Jones PR, Marsh EN (2012) Biochemistry 51:5703PubMedCrossRefGoogle Scholar
  38. 38.
    Li N, Chang WC, Warui DM, Booker SJ, Krebs C, Bollinger JM Jr (2012) Biochemistry 51:7908–7916PubMedCrossRefGoogle Scholar
  39. 39.
    Warui DM, Li N, Norgaard H, Krebs C, Bollinger JM Jr, Booker SJ (2011) J Am Chem Soc 133:3316–3319PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Li N, Norgaard H, Warui DM, Booker SJ, Krebs C, Bollinger JM Jr (2011) J Am Chem Soc 133:6158–6161PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Warui DM, Li N, Norgaard H, Krebs C, Bollinger JM, Booker SJ (2011) J Am Chem Soc 133:3316–3319PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Roberts ES, Vaz ADN, Coon MJ (1991) Proc Natl Acad Sci USA 88:8963–8966PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Vaz ADN, Roberts ES, Coon MJ (1991) J Am Chem Soc 113:5886–5887CrossRefGoogle Scholar
  44. 44.
    Denisov IG, Makris TM, Sligar SG, Schlichting I (2005) Chem Rev 105:2253–2277PubMedCrossRefGoogle Scholar
  45. 45.
    Raner GM, Chiang EW, Vaz ADN, Coon MJ (1997) Biochemistry 36:4895–4902PubMedCrossRefGoogle Scholar
  46. 46.
    Atkins WM, Sligar SG (1988) Biochemistry 27:1610–1616PubMedCrossRefGoogle Scholar
  47. 47.
    Grinkova YV, Denisov IG, McLean MA, Sligar SG (2013) Biochem Biophys Res Commun 430:1223–1227PubMedCrossRefGoogle Scholar
  48. 48.
    Nakajin S, Hall PF (1981) J Biol Chem 256:3871–3876PubMedGoogle Scholar
  49. 49.
    Mak PJ, Gregory MC, Denisov IG, Sligar SG, Kincaid JR (2015) Proc Natl Acad Sci USA 112:15856–15861PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Banerjee R, Proshlyakov Y, Lipscomb JD, Proshlyakov DA (2015) Nature 518:431–434PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Shu LJ, Nesheim JC, Kauffmann K, Munck E, Lipscomb JD, Que L (1997) Science 275:515–518PubMedCrossRefGoogle Scholar
  52. 52.
    Jiang W, Yun D, Saleh L, Barr EW, Xing G, Hoffart LM, Maslak MA, Krebs C, Bollinger JM Jr (2007) Science 316:1188–1191PubMedCrossRefGoogle Scholar
  53. 53.
    Jiang W, Yun D, Saleh L, Bollinger JM, Krebs C (2008) Biochemistry 47:13736–13744PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Boal AK, Cotruvo JA, Stubbe J, Rosenzweig AC (2010) Science 329:1526–1530PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Cotruvo JA, Stubbe J (2010) Biochemistry 49:1297–1309PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Fox BG, Surerus KK, Munck E, Lipscomb JD (1988) J Biol Chem 263:10553–10556PubMedGoogle Scholar
  57. 57.
    Hendrich MP, Munck E, Fox BG, Lipscomb JD (1990) J Am Chem Soc 112:5861–5865CrossRefGoogle Scholar
  58. 58.
    Pandelia ME, Li N, Norgaard H, Warui DM, Rajakovich LJ, Chang WC, Booker SJ, Krebs C, Bollinger JM Jr (2013) J Am Chem Soc 135:15801–15812PubMedCrossRefGoogle Scholar
  59. 59.
    Rajakovich LJ, Norgaard H, Warui DM, Chang WC, Li N, Booker SJ, Krebs C, Bollinger JM Jr, Pandelia ME (2015) J Am Chem Soc 137:11695–11709PubMedCrossRefGoogle Scholar
  60. 60.
    Broadwater JA, Achim C, Munck E, Fox BG (1999) Biochemistry 38:12197–12204PubMedCrossRefGoogle Scholar
  61. 61.
    Broadwater JA, Ai J, Loehr TM, Sanders-Loehr J, Fox BG (1998) Biochemistry 37:14664–14671PubMedCrossRefGoogle Scholar
  62. 62.
    Bollinger JM, Krebs C, Vicol A, Chen SX, Ley BA, Edmondson DE, Huynh BH (1998) J Am Chem Soc 120:1094–1095CrossRefGoogle Scholar
  63. 63.
    Moenne-Loccoz P, Baldwin J, Ley BA, Loehr TM, Bollinger JM Jr (1998) Biochemistry 37:14659–14663PubMedCrossRefGoogle Scholar
  64. 64.
    Skulan AJ, Brunold TC, Baldwin J, Saleh L, Bollinger JM, Solomon EI (2004) J Am Chem Soc 126:8842–8855PubMedCrossRefGoogle Scholar
  65. 65.
    Vu VV, Emerson JP, Martinho M, Kim YS, Munck E, Park MH, Que L Jr (2009) Proc Natl Acad Sci USA 106:14814–14819PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Valentine AM, Stahl SS, Lippard SJ (1999) J Am Chem Soc 121:3876–3887CrossRefGoogle Scholar
  67. 67.
    Lee SK, Nesheim JC, Lipscomb JD (1993) J Biol Chem 268:21569–21577PubMedGoogle Scholar
  68. 68.
    Tong WH, Chen S, Lloyd SG, Edmondson DE, Huynh BH, Stubbe J (1996) J Am Chem Soc 118:2107–2108CrossRefGoogle Scholar
  69. 69.
    Buer BC, Paul B, Das D, Stuckey JA, Marsh EN (2014) ACS Chem Biol 9:2584–2593PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Korboukh VK, Li N, Barr EW, Bollinger JM, Krebs C (2009) J Am Chem Soc 131:13608–13609PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Li N, Korboukh VK, Krebs C, Bollinger JM (2010) Proc Natl Acad Sci USA 107:15722–15727PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Komor AJ, Rivard BS, Fan RX, Guo YS, Que L, Lipscomb JD (2016) J Am Chem Soc 138:7411–7421PubMedCrossRefGoogle Scholar
  73. 73.
    Makris TM, Vu VV, Meier KK, Komor AJ, Rivard BS, Munck E, Que L Jr, Lipscomb JD (2015) J Am Chem Soc 137:1608–1617PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Choi YS, Zhang HJ, Brunzelle JS, Nair SK, Zhao HM (2008) Proc Natl Acad Sci USA 105:6858–6863PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Knoot CJ, Kovaleva EG, Lipscomb JD (2016) J Biol Inorg Chem 21:589–603PubMedCrossRefGoogle Scholar
  76. 76.
    Platter E, Lawson M, Marsh C, Sazinsky MH (2011) Arch Biochem Biophys 508:39–45PubMedCrossRefGoogle Scholar
  77. 77.
    Brunold TC, Solomon EI (1999) J Am Chem Soc 121:8277–8287CrossRefGoogle Scholar
  78. 78.
    Brunold TC, Solomon EI (1999) J Am Chem Soc 121:8288–8295CrossRefGoogle Scholar
  79. 79.
    Murray LJ, Naik SG, Ortillo DO, Garcia-Serres R, Lee JK, Huynh BH, Lippard SJ (2007) J Am Chem Soc 129:14500–14510PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Paul B, Das D, Ellington B, Marsh EN (2013) J Am Chem Soc 135:5234–5237PubMedCrossRefGoogle Scholar
  81. 81.
    Das D, Ellington B, Paul B, Marsh EN (2014) ACS Chem Biol 9:570–577PubMedCrossRefGoogle Scholar
  82. 82.
    Waugh MW, Marsh EN (2014) Biochemistry 53:5537–5543PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Shokri A, Que L (2015) J Am Chem Soc 137:7686–7691PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Reed JR, Vanderwel D, Choi SW, Pomonis JG, Reitz RC, Blomquist GJ (1994) Proc Natl Acad Sci USA 91:10000–10004PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Balabanidou V, Kampouraki A, MacLean M, Blomquist GJ, Tittiger C, Juárez MP, Mijailovsky SJ, Chalepakis G, Anthousi A, Lynd A, Antoine S, Hemingway J, Ranson H, Lycett GJ, Vontas J (2016) Proc Natl Acad Sci USA 113:9268–9273PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Chen N, Fan YL, Bai Y, Li XD, Zhang ZF, Liu TX (2016) Insect Biochem Mol Biol 76:84–94PubMedCrossRefGoogle Scholar
  87. 87.
    Martinez-Paz P, Morales M, Martinez-Guitarte JL, Morcillo G (2012) Comp Biochem Physiol C-Toxicol Pharmacol 155:333–343PubMedCrossRefGoogle Scholar
  88. 88.
    Rettie AE, Sheffels PR, Korzekwa KR, Gonzalez FJ, Philpot RM, Baillie TA (1995) Biochemistry 34:7889–7895PubMedCrossRefGoogle Scholar
  89. 89.
    Ghosh D, Griswold J, Erman M, Pangborn W (2009) Nature 457:219–223PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Monk BC, Tomasiak TM, Keniya MV, Huschmann FU, Tyndall JDA, O’Connell JD, Cannon RD, McDonald JG, Rodriguez A, Finer-Moore JS, Stroud RM (2014) Proc Natl Acad Sci USA 111:3865–3870PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Rittle J, Green MT (2010) Science 330:933–937PubMedCrossRefGoogle Scholar
  92. 92.
    Reed JR, Quilici DR, Blomquist GJ, Reitz RC (1995) Biochemistry 34:16221–16227PubMedCrossRefGoogle Scholar
  93. 93.
    Ortiz de Montellano PR, de Voss JJ (2005) Substrate oxidation by p450 enzymes. Kluwer, New YorkGoogle Scholar
  94. 94.
    Cheesbrough TM, Kolattukudy PE (1988) J Biol Chem 263:2738–2743PubMedGoogle Scholar
  95. 95.
    Cheesbrough TM, Kolattukudy PE (1984) Proc Natl Acad Sci USA 81:6613–6617PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Dennis MW, Kolattukudy PE (1991) Arch Biochem Biophys 287:268–275PubMedCrossRefGoogle Scholar
  97. 97.
    Banerjee A, Sharma R, Chisti Y, Banerjee UC (2002) Crit Rev Biotechnol 22:245–279PubMedCrossRefGoogle Scholar
  98. 98.
    Sorigue D, Legeret B, Cuine S, Morales P, Mirabella B, Guedeney G, Li-Beisson Y, Jetter R, Peltier G, Beisson F (2016) Plant Physiol 171:2393–2405PubMedPubMedCentralGoogle Scholar
  99. 99.
    Aarts MG, Keijzer CJ, Stiekema WJ, Pereira A (1995) Plant Cell 7:2115–2127PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Shanklin J, Achim C, Schmidt H, Fox BG, Munck E (1997) Proc Natl Acad Sci USA 94:2981–2986PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Bai YH, McCoy JG, Levin EJ, Sobrado P, Rajashankar KR, Fox BG, Zhou M (2015) Nature 524:252–256PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Rude MA, Baron TS, Brubaker S, Alibhai M, Del Cardayre SB, Schirmer A (2011) Appl Environ Microbiol 77:1718–1727PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Lee DS, Yamada A, Sugimoto H, Matsunaga I, Ogura H, Ichihara K, Adachi SI, Park SY, Shiro Y (2003) J Biol Chem 278:9761–9767PubMedCrossRefGoogle Scholar
  104. 104.
    Piontek K, Strittmatter E, Ullrich R, Grobe G, Pecyna MJ, Kluge M, Scheibner K, Hofrichter M, Plattner DA (2013) J Biol Chem 288:34767–34776PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Belcher J, McLean KJ, Matthews S, Woodward LS, Fisher K, Rigby SEJ, Nelson DR, Potts D, Baynham MT, Parker DA, Leys D, Munro AW (2014) J Biol Chem 289:6535–6550PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Fujishiro T, Shoji O, Nagano S, Sugimoto H, Shiro Y, Watanabe Y (2011) J Biol Chem 286:29941–29950PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Fukuda H, Fujii T, Sukita E, Tazaki M, Nagahama S, Ogawa T (1994) Biochem Biophys Res Commun 201:516–522PubMedCrossRefGoogle Scholar
  108. 108.
    Fukuda H, Nakamura K, Sukita E, Ogawa T, Fujii T (1996) J Biochem 119:314–318PubMedCrossRefGoogle Scholar
  109. 109.
    Jeong YJ, Kang Y, Han AR, Lee YM, Kotani H, Fukuzumi S, Nam W (2008) Angewandte Chemie Int Edn 47:7321–7324CrossRefGoogle Scholar
  110. 110.
    Matsunaga I, Yamada A, Lee DS, Obayashi E, Fujiwara N, Kobayashi K, Ogura H, Shiro Y (2002) Biochemistry 41:1886–1892PubMedCrossRefGoogle Scholar
  111. 111.
    Grant JL, Hsieh CH, Makris TM (2015) J Am Chem Soc 137:4940–4943PubMedCrossRefGoogle Scholar
  112. 112.
    Ren XK, Yorke JA, Taylor E, Zhang T, Zhou WH, Wong LL (2015) Chem Eur J 21:15039–15047PubMedCrossRefGoogle Scholar
  113. 113.
    Cryle MJ, De Voss JJ (2004) Chem Commun (Camb). doi: 10.1039/b311652b:86-87 Google Scholar
  114. 114.
    Grant JL, Mitchell ME, Makris TM (2016) Proc Natl Acad Sci USA 113:10049–10054PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Kellner DG, Hung SC, Weiss KE, Sligar SG (2002) J Biol Chem 277:9641–9644PubMedCrossRefGoogle Scholar
  116. 116.
    Palcic MM, Rutter R, Araiso T, Hager LP, Dunford HB (1980) Biochem Biophys Res Commun 94:1123–1127PubMedCrossRefGoogle Scholar
  117. 117.
    Wang X, Peter S, Kinne M, Hofrichter M, Groves JT (2012) J Am Chem Soc 134:12897–12900PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Yosca TH, Rittle J, Krest CM, Onderko EL, Silakov A, Calixto JC, Behan RK, Green MT (2013) Science 342:825–829PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Wang XS, Ullrich R, Hofrichter M, Groves JT (2015) Proc Natl Acad Sci USA 112:3686–3691PubMedPubMedCentralGoogle Scholar
  120. 120.
    Lambeir AM, Dunford HB, Pickard MA (1987) Eur J Biochem 163:123–127PubMedCrossRefGoogle Scholar
  121. 121.
    Atkinson JK, Hollenberg PF, Ingold KU, Johnson CC, Le Tadic M-H, Newcomb M, Putt DA (1994) Biochemistry 33:10630–10637PubMedCrossRefGoogle Scholar
  122. 122.
    Atkinson JK, Ingold KU (1993) Biochemistry 32:9209–9214PubMedCrossRefGoogle Scholar
  123. 123.
    Auclair K, Hu Z, Little DM, Ortiz de Montellano PR, Groves JT (2002) J Am Chem Soc 124:6020–6027PubMedCrossRefGoogle Scholar
  124. 124.
    Cooper HLR, Groves JT (2011) Arch Biochem Biophys 507:111–118PubMedCrossRefGoogle Scholar
  125. 125.
    Newcomb M, Lansakara-P DSP, Kim HY, Chandrasena REP, Lippard SJ, Beauvais LG, Murray LJ, Izzo V, Hollenberg PF, Coon MJ (2007) J Org Chem 72:1128–1133PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    He X, de Montellano PRO (2004) J Biol Chem 279:39479–39484PubMedCrossRefGoogle Scholar
  127. 127.
    Rettie AE, Boberg M, Rettenmeier AW, Baillie TA (1988) J Biol Chem 263:13733–13738PubMedGoogle Scholar
  128. 128.
    Martinie RJ, Livada J, Chang WC, Green MT, Krebs C, Bollinger JM Jr, Silakov A (2015) J Am Chem Soc 137:6912–6919PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Matthews ML, Krest CM, Barr EW, Vaillancourt FH, Walsh CT, Green MT, Krebs C, Bollinger JM (2009) Biochemistry 48:4331–4343PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Matthews ML, Neumann CS, Miles LA, Grove TL, Booker SJ, Krebs C, Walsh CT, Bollinger JM (2009) Proc Natl Acad Sci USA 106:17723–17728PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Vaillancourt FH, Yin J, Walsh CT (2005) Proc Natl Acad Sci USA 102:10111–10116PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Mitchell AJ, Zhu Q, Maggiolo AO, Ananth NR, Hillwig ML, Liu XY, Boal AK (2016) Nat Chem Biol 12:636PubMedCrossRefGoogle Scholar
  133. 133.
    Price JC, Barr EW, Tirupati B, Bollinger JM Jr, Krebs C (2003) Biochemistry 42:7497–7508PubMedCrossRefGoogle Scholar
  134. 134.
    Chang WC, Guo YS, Wang C, Butch SE, Rosenzweig AC, Boal AK, Krebs C, Bollinger JM (2014) Science 343:1140–1144PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Liu W, Huang XY, Cheng MJ, Nielsen RJ, Goddard WA, Groves JT (2012) Science 337:1322–1325PubMedCrossRefGoogle Scholar
  136. 136.
    Bigi MA, Reed SA, White MC (2011) Nature Chemistry 3:216–222PubMedCrossRefGoogle Scholar
  137. 137.
    Dennig A, Kuhn M, Tassoti S, Thiessenhusen A, Gilch S, Bulter T, Haas T, Hall M, Faber K (2015) Angew Chem 54:8819–8822CrossRefGoogle Scholar
  138. 138.
    Zachos I, Gassmeyer SK, Bauer D, Sieber V, Hollmann F, Kourist R (2015) Chem Commun 51:1918–1921CrossRefGoogle Scholar
  139. 139.
    Amaya JA, Rutland CD, Makris TM (2016) J Inorg Biochem 158:11–16PubMedCrossRefGoogle Scholar
  140. 140.
    Hsieh CH, Makris TM (2016) Biochem Biophys Res Commun 476:462–466PubMedCrossRefGoogle Scholar
  141. 141.
    Krest CM, Silakov A, Rittle J, Yosca TH, Onderko EL, Calixto JC, Green MT (2015) Nat Chem 7:696–702PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Faponle AS, Quesne MG, de Visser SP (2016) Chem Eur J 22:5478–5483PubMedCrossRefGoogle Scholar
  143. 143.
    Rui Z, Li X, Zhu XJ, Liu J, Domigan B, Barr I, Cate JHD, Zhang WJ (2014) Proc Natl Acad Sci USA 111:18237–18242PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Zechman JM, Labows JN Jr (1985) Can J Microbiol 31:232–237PubMedCrossRefGoogle Scholar
  145. 145.
    Koehntop KD, Emerson JP, Que L Jr (2005) J Biol Inorg Chem 10:87–93PubMedCrossRefGoogle Scholar
  146. 146.
    Ryle MJ, Liu A, Muthukumaran RB, Ho RY, Koehntop KD, McCracken J, Que L Jr, Hausinger RP (2003) Biochemistry 42:1854–1862PubMedCrossRefGoogle Scholar
  147. 147.
    Kovaleva EG, Lipscomb JD (2008) Nat Chem Biol 4:186–193PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    Xing G, Diao YH, Hoffart LM, Barr EW, Prabhu KS, Arner RJ, Reddy CC, Krebs C, Bollinger JM (2006) Proc Natl Acad Sci USA 103:6130–6135PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Tamanaha E, Zhang B, Guo Y, Chang WC, Barr EW, Xing G, St Clair J, Ye S, Neese F, Bollinger JM Jr, Krebs C (2016) J Am Chem Soc 138:8862–8874PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Pojer F, Kahlich R, Kammerer B, Li SM, Heide L (2003) J Biol Chem 278:30661–30668PubMedCrossRefGoogle Scholar
  151. 151.
    Rui Z, Harris NC, Zhu XJ, Huang W, Zhang WJ (2015) Acs Catalysis 5:7091–7094CrossRefGoogle Scholar
  152. 152.
    Shanklin J, Whittle E, Fox BG (1994) Biochemistry 33:12787–12794PubMedCrossRefGoogle Scholar
  153. 153.
    Behrouzian B, Buist PH (2003) Prostaglandins Leukot Essent Fatty Acids 68:107–112PubMedCrossRefGoogle Scholar
  154. 154.
    Shanklin J, Guy JE, Mishra G, Lindqvist Y (2009) J Biol Chem 284:18559–18563PubMedPubMedCentralCrossRefGoogle Scholar
  155. 155.
    Buist PH, Behrouzian B (1996) J Am Chem Soc 118:6295–6296CrossRefGoogle Scholar
  156. 156.
    Cooper HLR, Mishra G, Huang XY, Pender-Cudlip M, Austin RN, Shanklin J, Groves JT (2012) J Am Chem Soc 134:20365–20375PubMedPubMedCentralCrossRefGoogle Scholar
  157. 157.
    Jin Y, Lipscomb JD (2001) J Biol Inorg Chem 6:717–725PubMedCrossRefGoogle Scholar
  158. 158.
    Broadwater JA, Whittle E, Shanklin J (2002) J Biol Chem 277:15613–15620PubMedCrossRefGoogle Scholar
  159. 159.
    Broun P, Shanklin J, Whittle E, Somerville C (1998) Science 282:1315–1317PubMedCrossRefGoogle Scholar

Copyright information

© SBIC 2016

Authors and Affiliations

  • Courtney E. Wise
    • 1
  • Job L. Grant
    • 1
  • Jose A. Amaya
    • 1
  • Steven C. Ratigan
    • 1
  • Chun H. Hsieh
    • 1
  • Olivia M. Manley
    • 1
  • Thomas M. Makris
    • 1
    Email author
  1. 1.Department of Chemistry and BiochemistryUniversity of South CarolinaColumbiaUSA

Personalised recommendations