Skip to main content
SpringerLink
Log in

The Catalytic Mechanisms of the Molybdenum and Tungsten Enzymes

  • Chapter
  • First Online:
Book cover Metallocofactors that Activate Small Molecules

Part of the book series: Structure and Bonding ((STRUCTURE,volume 179))

Abstract

Molybdenum and tungsten are, respectively, the only second and third transition metal ions with well-defined functions in living organisms and with a single exception are found in association with a novel pyranopterin dithiolene cofactor called molybdopterin. This review focusses on the catalytic mechanisms of the molybdenum and tungsten enzymes, with an emphasis on the molybdenum and tungsten sites. Most, but not all, of the enzymes catalyze oxygen atom transferase redox chemistry, with the metal cycling between M(VI) and M(IV) formal oxidation states during the catalytic cycle. We discuss the range of reactions and what is known of mechanism for both oxo-transferase and non-oxo-transferase molybdenum and tungsten enzymes.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Pushie MJ, Cotelesage JJH, George GN (2014) Metallomics 6:15–24

    Article  CAS  PubMed  Google Scholar 

  2. Lane T, Saito MA, George GN, Pickering IJ, Prince RC, Morel FFM (2005) Nature 435:42

    Article  CAS  PubMed  Google Scholar 

  3. Hiller CJ, Rettberg LA, Lee CC, Stiebritz MT, Hu Y (2019) Current understanding of the biosynthesis of the unique nitrogenase cofactor core. Struct Bond. https://link.springer.com/chapter/10.1007/430_2018_29

  4. Wenke BB, Spatzal T (2019) Looking at nitrogenase: insights from modern structural approaches. Struct Bond. https://link.springer.com/chapter/10.1007/430_2018_28

  5. Hille R, Halt J, Basu P (2014) Chem Rev 114:3963–4038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Jormakka M, Richardson D, Byrne B, Iwata S (2004) Structure 12:95–104

    Article  CAS  PubMed  Google Scholar 

  7. Bertero MG, Rothery RA, Palak M, Hou C, Lim D, Blasco F, Weiner JH, Strynadka NCJ (2003) Nat Struct Biol 10:681–687

    Article  CAS  PubMed  Google Scholar 

  8. Kloer DP, Hagel C, Heider J, Schulz GE (2006) Structure 14:1377–1388

    Article  CAS  PubMed  Google Scholar 

  9. Gisewhite DR, Yang J, Williams BR, Esmail A, Stein BW, Kirk ML, Burgmayer SJN (2018) J Am Chem Soc 140:12808–12818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Cotelesage JJH, Crawford AM, Prince RC, George GN (unpublished)

    Google Scholar 

  11. Bray RC, Swann JC (1972) Struct Bond 11:107–144

    Article  CAS  Google Scholar 

  12. Ljundahl LG, Andreesen JR (1975) FEBS Lett 54:279–282

    Google Scholar 

  13. George GN, Prince RC, Mukund S, Adams MWW (1992) J Am Chem Soc 114:3521–3523

    Article  CAS  Google Scholar 

  14. Olson JS, Ballou DP, Palmer G, Massey V (1974) J Biol Chem 249:4363–4382

    Google Scholar 

  15. Rothery RA, Stein B, Solomonson M, Kirk ML, Weiner JH (2012) Proc Natl Acad Sci U S A 109:14773–14778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Stetter KO (2006) Philos Trans R Soc B 361:1837–1843

    Article  CAS  Google Scholar 

  17. Pushie MJ, George GN (2011) Coord Chem Rev 255(9–10):1055–1084

    Article  CAS  Google Scholar 

  18. Kisker C, Schindelin H, Pacheco A, Wehbi WA, Garrett RM, Rajagopalan KV, Enemark JH, Rees DC (1997) Cell 91:973–983

    Article  CAS  PubMed  Google Scholar 

  19. Schrader N, Fischer K, Theis K, Mendel RR, Schwarz G, Kisker C (2003) Structure 11:1251–1263

    Article  CAS  PubMed  Google Scholar 

  20. Fischer K, Barbier G, Hecht H-J, Mendel RR, Campbell WH, Schwarz G (2005) Plant Cell 17:1167–1179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kappler U, Bailey S (2005) J Biol Chem 280:24999–25007

    Article  CAS  PubMed  Google Scholar 

  22. McGrath AP, Laming EL, Casas Garcia GP, Kvansakul M, Guss JM, Trewhella J, Calmes B, Bernhardt PV, Hanson GR, Kappler U, Maher MJ (2015) Elife 4:e09066–e09066

    Article  PubMed  PubMed Central  Google Scholar 

  23. Plitzko B, Havemeyer A, Kunze T, Clement B (2015) J Biol Chem 290:10126–10135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Enroth C, Eger BT, Okamoto K, Nishino T, Nishino T, Pai EF (2000) Proc Natl Acad Sci U S A 97:10723–10728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Doonan CJ, Stockert A, Hille R, George GN (2005) J Am Chem Soc 127:4518–4522

    Article  CAS  PubMed  Google Scholar 

  26. Coelho C, Foti A, Hartmann T, Santos-Silva T, Leimkuhler S, Romao MJ (2015) Nat Chem Biol 11:779–783

    Article  CAS  PubMed  Google Scholar 

  27. Dobbek H, Gremer L, Kiefersauer R, Huber R, Meyer O (2002) Proc Natl Acad Sci U S A 99:15971–15976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Gnida M, Ferner R, Gremer L, Meyer O, Meyer-Klaucke W (2003) Biochemistry 42:222–230

    Article  CAS  PubMed  Google Scholar 

  29. Gladyshev VN, Khangulov SV, Stadtman TC (1994) Proc Natl Acad Sci U S A 91:232–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Wagener N, Pierik AJ, Ibdah A, Hille R, Dobbek H (2009) Proc Natl Acad Sci U S A 106:1055–11060

    Article  Google Scholar 

  31. George GN, Hilton J, Temple C, Prince RC, Rajagopalan RC (1999) J Am Chem Soc 121:1256–1266

    Article  CAS  Google Scholar 

  32. Li HK, Temple C, Rajagopalan KV, Schindelin H (2000) J Am Chem Soc 122:7673–7680

    Article  CAS  Google Scholar 

  33. Chan MK, Mukund S, Kletzin A, Adams MWW, Rees DC (1995) Science 267:1463–1469

    Article  CAS  PubMed  Google Scholar 

  34. Rappé AK, Goddard WA (1982) J Am Chem Soc 104:448–456

    Article  Google Scholar 

  35. Groom CR, Bruno IJ, Lightfoot MP, Ward SC (2016) Acta Cryst B72:171–179

    Google Scholar 

  36. Qiu JA, Wilson HL, Pushie MJ, Kisker C, George GN, Rajagopalan KV (2010) Biochemistry 49:3989–4000

    Article  CAS  PubMed  Google Scholar 

  37. George GN, Garrett RM, Prince RC, Rajagopalan KV (1996) J Am Chem Soc 118:8588–8592

    Article  CAS  Google Scholar 

  38. George GN, Garrett RM, Prince RC, Rajagopalan KV (2004) Inorg Chem 43:8456–8460

    Article  CAS  PubMed  Google Scholar 

  39. Johnson JL, Rajagopalan KV (1982) Proc Natl Acad Sci U S A 79:6856–6860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Rajagopalan KV (1991) In: Meister A (ed) Advances in enzymology and related areas of molecular biology. Wiley, New York, pp 215–290

    Google Scholar 

  41. Romão MJ, Archer M, Moura I, Moura JJG, LeGall J, Engh R, Schneider M, Hof P, Huber R (1995) Science 270:1170–1176

    Article  PubMed  Google Scholar 

  42. Garton SD, Hilton J, Hiroyuki O, Crouse BR, Rajagopalan KV, Johnson MK (1997) J Am Chem Soc 119:12906–12916

    Article  CAS  Google Scholar 

  43. McNaughton RL, Helton ME, Rubie ND, Kirk ML (2000) Inorg Chem 39:4386–4387

    Article  CAS  Google Scholar 

  44. Cotelesage JJH, Pushie MJ, Grochulski P, Pickering IJ, George GN (2012) J Inorg Biochem 115:127–137

    Article  CAS  PubMed  Google Scholar 

  45. Pushie MJ, Cotelesage JJH, Lyashenko G, Hille R, George GN (2013) Inorg Chem 52:2830–2837

    Article  CAS  PubMed  Google Scholar 

  46. Warelow TP, Pushie MJ, Cotelesage JJH, Santini JM, George GN (2017) Sci Rep 7:1757/1–1757/7

    Article  CAS  Google Scholar 

  47. Rây P, Dutt NK (1943) J Indian Chem Soc 20:81–92

    Google Scholar 

  48. Rzepa HS, Cass ME (2007) Inorg Chem 46:8024–8031

    Article  CAS  PubMed  Google Scholar 

  49. Dobbek H, Gremer L, Meyer O, Huber R (1999) Proc Natl Acad Sci U S A 96:8884–8889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. George GN, Pickering IJ, Kisker C (1999) Inorg Chem 38:2539–2540

    Article  CAS  Google Scholar 

  51. George GN, Pickering IJ, Pushie MJ, Nienaber K, Hackett MJ, Ascone I, Hedman B, Hodgson KO, Aitken JB, Levina A, Glover C, Lay PA (2012) J Synchrotron Radiat 19:875–886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Nienaber KH, Pushie MJ, Cotelesage JJH, Pickering IJ, George GN (2018) J Phys Chem Lett 9:540–544

    Article  CAS  PubMed  Google Scholar 

  53. George GN (2016) X-ray absorption spectroscopy of molybdenum and tungsten enzymes. In: Kirk ML, Hille R, Schulzke C (eds) Molybdenum and tungsten enzymes: spectroscopic and theoretical investigations. Royal Society of Chemistry, Series on Meta, pp 121–167, ISBN 978-1-78262-878-1

    Google Scholar 

  54. Harris HH, George GN, Rajagopalan KV (2006) Inorg Chem 45:493–495

    Article  CAS  PubMed  Google Scholar 

  55. Shih VE, Abroms IF, Johnson JL, Carney M, Mandell R, Robb RM, Cloherty JP, Rajagopalan KV (1977) N Engl J Med 297:1022–1028

    Article  CAS  PubMed  Google Scholar 

  56. Johnson JL, Coyne KE, Garrett RM, Zabot M-T, Dorche C, Kisker C, Rajagopalan KV (2002) Hum Mutat 20:74

    Article  PubMed  CAS  Google Scholar 

  57. Karakas E, Wilson HL, Graf TN, Xiang S, Jaramillo-Busquets S, Rajagopalan KV, Kisker C (2005) J Biol Chem 280:33506–33515

    Article  CAS  PubMed  Google Scholar 

  58. Peariso K, McNaughton RL, Kirk ML (2002) J Am Chem Soc 124:9006–9007

    Article  CAS  PubMed  Google Scholar 

  59. Izumi Y, Glaser T, Rose K, McMaster J, Basu P, Enemark JH, Hedman B, Hodgson KO, Solomon EI (1999) J Am Chem Soc 121:10035–10046

    Article  CAS  Google Scholar 

  60. Fischer K, Barbier G, Hecht H-J, Mendel RR, Campbell WH, Schwarz G (2005) Plant Cell 17:1167–1179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. George GN, Mertens JA, Campbell WA (1999) J Am Chem Soc 121:9730–9731

    Article  CAS  Google Scholar 

  62. Cambell WH, Kinghorn KR (1990) Trends Biochem Sci 15:315–319

    Article  Google Scholar 

  63. Qiu JA, Wilson HL, Rajagopalan KV (2012) Biochemistry 51:1134–1147

    Article  CAS  PubMed  Google Scholar 

  64. Havemeyer A, Bittner F, Wollers S, Mendel R, Kunze T, Clement B (2006) J Biol Chem 281:34796–34802

    Article  CAS  PubMed  Google Scholar 

  65. Schneider J, Girreser U, Havemeyer A, Bittner F, Clement B (2018) Chem Res Toxicol 31:447–453

    Article  CAS  PubMed  Google Scholar 

  66. Llamas A, Chamizo-Ampudia A, Tejada-Jimenez M, Galvan A, Fernandez E (2017) Biofactors 43:486–494

    Article  CAS  PubMed  Google Scholar 

  67. Rajapakshe A, Astashkin AV, Klein EL, Reichmann D, Mendel RR, Bittner F, Enemark JH (2011) Biochemistry 50:8813–8822

    Article  CAS  PubMed  Google Scholar 

  68. Giles LJ, Ruppelt C, Yang J, Mendel RR, Bittner F, Kirk ML (2014) Inorg Chem 53:9460–9462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Yang J, Giles LJ, Ruppelt C, Mendel RR, Bittner F, Kirk ML (2015) J Am Chem Soc 137:5276–5279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Kubitza C, Ginsel C, Bittner F, Havemeyer A, Clement B, Scheidiga AJ (2018) Acta Cryst F74:337–344

    Google Scholar 

  71. Pacheco A, Hazzard JT, Tollin G, Enemark JH (1999) J Biol Inorg Chem 4:390–401

    Article  CAS  PubMed  Google Scholar 

  72. Pushie MJ, George GN (2010) J Phys Chem B 114:3266–3275

    Article  CAS  PubMed  Google Scholar 

  73. Utesch T, Mroginski MA (2010) J Phys Chem Lett 1:2159–2164

    Article  CAS  Google Scholar 

  74. Atashkin AV, Rajapakshe A, Cornelison MJ, Johnson-Winters K, Enemark JH (2012) J Phys Chem B 116:1942–1950

    Google Scholar 

  75. Feng C, Wilson HL, Hurley JK, Hazzard JT, Tollin G, Rajagopalan KV, Enemark JH (2003) Biochemistry 42:12235–12242

    Article  CAS  PubMed  Google Scholar 

  76. Emesh S, Rapson TD, Rajapakshe SA, Kappler U, Bernhardt PV, Tollin G, Enemark JH (2009) Biochemistry 48:2156–2163

    Article  CAS  PubMed  Google Scholar 

  77. McGrath AP, Laming EL, Casus Garcia GPM, Guss JM, Trewella J, Calmes B, Bernhardt PV, Hanson GR, Kappler U, Maher MJ (2015) eLife 4:e09066/1–26

    Google Scholar 

  78. Hsiao J-C, McGrath AP, Kielmann L, Kalimuthu P, Darain F, Bernhardt PV, Harmer J, Lee M, Meyers K, Maher MJ, Kappler U (2018) BBA-Bioenergetics 1859:19–27

    Article  CAS  PubMed  Google Scholar 

  79. Enroth C, Eger BT, Okamoto K, Nishino T, Nishino T, Pai EF (2000) Proc Natl Acad Sci U S A 97:10723–10728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Burt HM, Dutt YC (1989) J Cryst Growth 94:15–22

    Article  CAS  Google Scholar 

  81. Pascual E, Addadi L, Andrés M, Sivera F (2015) Nat Rev Rheumatol 11:725–730

    Article  CAS  PubMed  Google Scholar 

  82. Williams JW, Bray RC (1981) Biochem J 195:753–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Hawkes TR, George GN, Bray RC (1984) Biochem J 218:961–968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Dent CE, Philpot GR (1954) Lancet 266:182–185

    Article  CAS  PubMed  Google Scholar 

  85. Ichida K, Amaya Y, Nishino T, Hosoya T, Sakai O (1997) J Clin Invest 99:2391–2397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Bray RC (1975) In: Boyer PD (ed) The enzymes. Academic Press, New York, pp 299–419

    Google Scholar 

  87. Enroth C, Eger BT, Okamoto K, Nishino T, Nishino T, Pai EF (2000) Proc Natl Acad Sci U S A 97:10723–10728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Hille R (1996) Chem Rev 96:2757–2816

    Article  CAS  PubMed  Google Scholar 

  89. Kitamura S, Sugihara K, Ohta S (2006) Drug Metab Pharmacokinet 21:83–98

    Article  CAS  PubMed  Google Scholar 

  90. Self WT, Stadtman TC (2000) Proc Natl Acad Sci U S A 97:7208–7213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Wagener N, Pierik AJ, Ibdah A, Hille R, Dobbek H (2009) Proc Natl Acad Sci U S A 106:1055–11060

    Article  Google Scholar 

  92. Cleere WF, Coughlan MP (1974) Biochem J 143:331–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Kim JH, Ryan MG, Knaut H, Hille R (1996) J Biol Chem 271:6771–6780

    Article  CAS  PubMed  Google Scholar 

  94. Dobbek H, Gremer L, Kiefersauer R, Huber R, Meyer O (2002) Proc Natl Acad Sci U S A 99:15971–15976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Gnida M, Ferner R, Gremer L, Meyer O, Meyer-Klaucke W (2003) Biochemistry 42:222–230

    Article  CAS  PubMed  Google Scholar 

  96. Zhang B, Hemann CF, Hille R (2010) J Biol Chem 285:12571–12578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Gourlay C, Nielsen DJ, White JM, Knottenbelt SZ, Kirk ML, Young CG (2006) J Am Chem Soc 128:2164–2165

    Article  CAS  PubMed  Google Scholar 

  98. Zhang L, Johnson Nelson K, Rajagopalan KV, George GN (2008) Inorg Chem 47:1074–1078

    Article  CAS  PubMed  Google Scholar 

  99. Creevey NL, McEwan AG, Hanson GR, Bernhardt PV (2008) Biochemistry 47:3770–3776

    Article  CAS  PubMed  Google Scholar 

  100. Temple CA, George GN, Hilton J, George MJ, Prince RC, Barber MJ, Rajagopalan KV (2000) Biochemistry 39:4046–4052

    Article  CAS  PubMed  Google Scholar 

  101. George GN, Hilton J, Rajagopalan KV (1996) J Am Chem Soc 118:1113–1117

    Article  CAS  Google Scholar 

  102. Schindelin H, Kisker C, Hilton J, Rajagppalan KV, Rees DC (1996) Science 272:1615–1621

    Article  CAS  PubMed  Google Scholar 

  103. Schneider F, Löwe J, Huber R, Schindelin H, Kisker C, Knäblein J (1996) J Mol Biol 263:53–69

    Article  CAS  PubMed  Google Scholar 

  104. McAlpine AS, McEwan AG, Shaw AL, Bailey S (1997) J Biol Inorg Chem 2:690–701

    Article  CAS  Google Scholar 

  105. McAlpine AS, McEwan AG, Bailey SJ (1998) J Mol Biol 275:613–623

    Article  CAS  PubMed  Google Scholar 

  106. Baugh PE, Garner CD, Charnock JM, Collison D, Davies ES, McAlpine AS, Bailey S, Lane I, Hanson GR, McEwan AG (1997) J Biol Inorg Chem 2:634–643

    Article  CAS  Google Scholar 

  107. George GN, Hilton J, Temple C, Prince RC, Rajagopalan KV (1999) J Am Chem Soc 121:1256–1266

    Article  CAS  Google Scholar 

  108. Li HK, Temple C, Rajagopalan KV, Schindelin H (2000) J Am Chem Soc 122:7673–7680

    Article  CAS  Google Scholar 

  109. Bray RC, Adams B, Smith AT, Bennett B, Bailey S (2000) Biochemistry 39:11258–11269

    Article  CAS  PubMed  Google Scholar 

  110. George GN, Nelson KJ, Harris HH, Doonan CJ, Rajagopalan KV (2007) Inorg Chem 46:3097–3104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Sparacino-Watkinsa C, Stolz JF, Basua P (2014) Chem Soc Rev 43:676–706

    Article  Google Scholar 

  112. Coelho C, Romão MJ (2015) Protein Sci 24:1901–1911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Dias JM, Than ME, Humm A, Huber R, Bourenkov GP, Bartunik HD, Bursakov S, Calvete J, Calderia J, Carneiro C, Moura JJG, Moura I, Romão MJ (1999) Structure 7:65–79

    Article  CAS  PubMed  Google Scholar 

  114. Cerqueira NM, Pakhira B, Sarkar S (2015) J Biol Inorg Chem 30:323–335

    Article  CAS  Google Scholar 

  115. Rendon J, Biaso F, Ceccaldi P, Toci R, Seduk F, Magalon A, Guigliarelli B, Grimaldi S (2017) Inorg Chem 56:4422–4434

    Article  CAS  Google Scholar 

  116. Ceccaldi P, Rendon J, Léger C, Toci R, Guigliarelli B, Magalon A, Grimaldi S, Fourmond V (2015) Biochim Biophys Acta 1847:1055–1063

    Article  CAS  PubMed  Google Scholar 

  117. George GN, Bray RC, Morpeth FF, Boxer DH (1985) Biochem J 227:925–931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Maher MJ, Santini J, Pickering IJ, Prince RC, Macy JM, George GN (2004) Inorg Chem 43:402–404

    Article  CAS  PubMed  Google Scholar 

  119. Kloer DP, Hagel C, Heider J, Schulz GE (2006) Structure 14:1377–1388

    Article  CAS  PubMed  Google Scholar 

  120. Heider J, Szaleniec M, Sünwoldt K, Boll M (2016) J Mol Microbiol Biotechnol 26:45–62

    Article  CAS  PubMed  Google Scholar 

  121. Szaleniec M, Hagel C, Menke M, Nowak P, Witko M, Heider J (2007) Biochemistry 46:7637–7646

    Article  CAS  PubMed  Google Scholar 

  122. Szaleniec M, Borowski T, Schühle K, Nowak P, Witko M, Heider J (2010) J Am Chem Soc 132:6014–6024

    Article  CAS  PubMed  Google Scholar 

  123. Szaleniec M, Dudzik A, Kozik B, Borowski T, Heider J, Witko M (2014) J Inorg Biochem 139:9–20

    Article  CAS  PubMed  Google Scholar 

  124. Ellis PJ, Conrads T, Hille R, Kuhn P (2001) Structure 9:125–132

    Article  CAS  PubMed  Google Scholar 

  125. Warelow TP, Oke M, Schoepp-Cothenet B, Dahl JU, Bruselat N, Sivalingam GN, Leimkühler S, Thalassinos K, Kappler U, Naismith JH, Santini JM (2013) PLoS One 8:e72535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Conrads T, Hemann C, George GN, Pickering IJ, Prince RC, Hille R (2002) J Am Chem Soc 124:11276–11277

    Article  CAS  PubMed  Google Scholar 

  127. Hoke KR, Cobb N, Armstrong FA, Hille R (2004) Biochemistry 43:1667–1674

    Article  CAS  PubMed  Google Scholar 

  128. Mukhopadhyay R, Rosen BP (2002) Environ Health Perspect 110:745–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Radabaugh TR, Aposhian HV (2000) Chem Res Toxicol 13:26–30

    Article  CAS  PubMed  Google Scholar 

  130. Glasser NR, Oyala PH, Osborne TH, Santini JM, Newman DK (2018) Proc Natl Acad Sci U S A 115:E8614–E8623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Grimaldi S, Schoepp-Cothenet B, Ceccaldi P, Guigliarelli B, Magalon A (2013) Biochim Biophys Acta Bioenerg 1827:1048–1085

    Article  CAS  Google Scholar 

  132. Boyington JC, Gladyshev VN, Khangulov SV, Stadtman TC, Sun PD (1997) Science 275:1305–1308

    Article  CAS  PubMed  Google Scholar 

  133. Raaijmakers H, Macieira S, Dias JM, Teixeira S, Bursakov S, Huber R, Moura JJ, Moura I, Romão MJ (2002) Structure 10:1261–1273

    Article  CAS  PubMed  Google Scholar 

  134. Raaijmakers H, Romão MJ (2006) J Biol Inorg Chem 11:849–854

    Article  CAS  PubMed  Google Scholar 

  135. Mota CS, Rivas MG, Brondino CD, Moura I, Moura JJ, Gonzalez PJ, Cerqueira NM (2011) J Biol Inorg Chem 16:1255–1268

    Article  CAS  PubMed  Google Scholar 

  136. Robinson WE, Bassegoda A, Reisner E, Hirst J (2017) J Am Chem Soc 139:9927–9936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. George GN, Colangelo CM, Dong J, Scott RA, Khangulov SV, Gladyshev VN, Stadtman TC (1998) J Am Chem Soc 120:1267–1273

    Article  CAS  Google Scholar 

  138. George GN, Costa C, Moura JJG, Moura I (1999) J Am Chem Soc 121:2625–2626

    Article  CAS  Google Scholar 

  139. Khangulov SV, Gladyshev VN, Dismukes CG, Stadtman TC (1998) Biochemistry 37:3518–3528

    Article  CAS  PubMed  Google Scholar 

  140. Berg IA, Kockelkorn D, Ramos-Vera WH, Say RF, Zarzycki J, Hügler M, Alber BE, Fuchs G (2010) Nat Rev Microbiol 8:447–459

    Article  CAS  PubMed  Google Scholar 

  141. Pancost RD, Sinninghe Damsté JS, de Lint S, van der Maarel MJEC, Gottschal JC (2000) Appl Environ Microbiol 66:1126–1132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Schwörer B, Thauer RK (1991) Arch Microbiol 155:459–465

    Article  Google Scholar 

  143. Ponomarev DA, Shevchenko SM (2007) J Chem Educ 84:1725–1726

    Article  CAS  Google Scholar 

  144. Seiffert GB, Ullmann GM, Messerschmidt A, Schink B, Kroneck PMH, Einsle O (2007) Proc Natl Acad Sci U S A 104:3073–3077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Liao R-Z, Yu J-G, Himo F (2010) Proc Natl Acad Sci U S A 107:22523–22527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Messerschmidt A, Niessen H, Abt D, Einsle O, Schink B, Kroneck PMH (2004) Proc Natl Acad Sci U S A 101:11571–11576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Weinert T, Huwiler SG, Kung JW, Weidenweber S, Hellwig P, Stärk HJ, Biskup T, Weber S, Cotelesage JJ, George GN, Ermler U, Boll M (2015) Nat Chem Biol:586–591

    Article  CAS  PubMed  Google Scholar 

  148. Boll M, Fuchs G (1995) Eur J Biochem:921–933

    Google Scholar 

  149. Culka M, Huwiler SG, Boll M, Ullmann GM (2017) J Am Chem Soc 139:14488–14500

    Article  CAS  PubMed  Google Scholar 

  150. Holm RH, Solomon EI, Majumdar A, Tenderholt A (2011) Coord Chem Rev 255:993–1015

    Article  CAS  Google Scholar 

  151. Wagner T, Ermler U, Shima S (2016) Science 354:114–117

    Article  CAS  PubMed  Google Scholar 

  152. Niks D, Hille R (2018) Protein Sci. https://doi.org/10.1002/pro.3498

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  153. Johnson JL, Rajagopalan KV (1976) J Biol Chem 251:5505–5511

    Article  CAS  PubMed  Google Scholar 

  154. Stewart LJ, Bailey S, Bennett B, Charnock JM, Garner CD, McAlpine AS (2000) J Mol Biol 299:593–600

    Article  CAS  PubMed  Google Scholar 

  155. Garner CD, Stewart LJ (2002) Met Ions Biol Syst 39:699–726

    CAS  PubMed  Google Scholar 

  156. Schoepp-Cothenet B, van Lis R, Philippot P, Magalon A, Russell MJ, Nitschke W (2012) Sci Rep 2:263/1–263/5

    Google Scholar 

  157. Williams RJP, Fraústo da Silva JJR (2002) Biochem Biophys Res Commun 292:293–299

    Article  CAS  PubMed  Google Scholar 

  158. Stetter KO (2006) Philos Trans R Soc B 361:1837–1843

    Article  CAS  Google Scholar 

  159. Kletzin A, Adams MWW (1996) FEMS Microbiol Rev 18:5–63

    Article  CAS  PubMed  Google Scholar 

  160. Bruland KW, Lohan MC (2006) In: Elderfield H (ed) The oceans and marine geochemistry. Elsevier, North Holland, pp 23–47

    Google Scholar 

  161. Licht S (1988) J Electrochem Soc 135:2971–2975

    Article  CAS  Google Scholar 

  162. Romão MJ, Coelho C, Santos-Silva T, Foti A, Terao M, Garattini E, Leimkühler S (2017) Curr Opin Chem Biol 37:39–47

    Article  PubMed  CAS  Google Scholar 

  163. Bassegoda A, Madden C, Wakerley DW, Reisner E, Hirst J (2014) J Am Chem Soc 136:15473–15476

    Article  CAS  PubMed  Google Scholar 

  164. Wedepohl KH (1995) Geochim Cosmochim Acta 59:1217–1232

    Article  CAS  Google Scholar 

  165. Reich HJ, Hondal RJ (2016) ACS Chem Biol 11:821–841

    Article  CAS  PubMed  Google Scholar 

  166. Dolgova NV, Nehzati S, Choudhury S, Regnier N, Crawford AM, Ponomarenko O, George GN, Pickering IJ (2018) Biochim Biophys Acta 1862:2383–2392

    Article  CAS  Google Scholar 

  167. Zhang L, Johnson Nelson K, Rajagopalan KV, George GN (2008) Inorg Chem 47:1074–1078

    Article  CAS  PubMed  Google Scholar 

  168. Nitschke W, Russell MJ (2009) J Mol Evol 69:484–496

    Article  CAS  Google Scholar 

  169. Nitschke W, Russell MJ (2011) Bioessays 34:106–109

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Research in the authors’ laboratory is funded by the Natural Sciences and Engineering Research Council of Canada, the Saskatchewan Health Research Foundation (SHRF), the University of Saskatchewan, the Canada Foundation for Innovation, Chevron Energy Research Co., and a Canada Research Chair award (to G.N.G). R.C.P. acknowledges support from the Diane Gunson benevolence fund.

Author information

Authors and Affiliations

  1. Molecular and Environmental Sciences Group, Department of Geological Sciences, University of Saskatchewan, Saskatoon, SK, Canada

    Andrew M. Crawford, Julien J. H. Cotelesage & Graham N. George

  2. Stonybrook Apiary, Pittstown, NJ, USA

    Roger C. Prince

Authors
  1. Andrew M. Crawford
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Julien J. H. Cotelesage
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Roger C. Prince
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Graham N. George
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Graham N. George .

Editor information

Editors and Affiliations

  1. Departments of Molecular Biology & Biochemistry, and Chemistry, University of California, Irvine, CA, USA

    Markus W. Ribbe

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Crawford, A.M., Cotelesage, J.J.H., Prince, R.C., George, G.N. (2018). The Catalytic Mechanisms of the Molybdenum and Tungsten Enzymes. In: Ribbe, M. (eds) Metallocofactors that Activate Small Molecules. Structure and Bonding, vol 179. Springer, Cham. https://doi.org/10.1007/430_2018_30

Download citation

Publish with us

Policies and ethics

Search

Navigation