title: Nickel-dependent metalloenzymes.
abstract: This review describes the functions, structures, and mechanisms of nine nickel-containing enzymes: glyoxalase I, acireductone dioxygenase, urease, superoxide dismutase, [NiFe]-hydrogenase, carbon monoxide dehydrogenase, acetyl-coenzyme A synthase/decarbonylase, methyl-coenzyme M reductase, and lactate racemase. These enzymes catalyze their various chemistries by using metallocenters of diverse structures, including mononuclear nickel, dinuclear nickel, nickel-iron heterodinuclear sites, more complex nickel-containing clusters, and nickel-tetrapyrroles. Selected other enzymes are active with nickel, but the physiological relevance of this metal specificity is unclear. Additional nickel-containing proteins of undefined function have been identified.
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824, USA.
authors.forename: Jodi L
authors.initials: JL
authors.lastname: Boer
authors.affiliation: Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824, USA.
authors.forename: Scott B
authors.initials: SB
authors.lastname: Mulrooney
authors.affiliation: Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824, USA; Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI 48824, USA. Electronic address: hausinge@msu.edu.
authors.forename: Robert P
authors.initials: RP
authors.lastname: Hausinger
mesh_terms: D000445:Aldehyde Oxidoreductases / Q000737:chemistry / Q000378:metabolism; D000818:Animals; D001419:Bacteria / Q000737:chemistry / Q000201:enzymology; D049308:Dioxygenases / Q000737:chemistry / Q000378:metabolism; D004798:Enzymes / Q000737:chemistry / Q000378:metabolism*; D006801:Humans; D006864:Hydrogenase / Q000737:chemistry / Q000378:metabolism; D007791:Lactoylglutathione Lyase / Q000737:chemistry / Q000378:metabolism; D008958:Models, Molecular; D009097:Multienzyme Complexes / Q000737:chemistry / Q000378:metabolism; D009532:Nickel / Q000737:chemistry / Q000378:metabolism*; D010088:Oxidoreductases / Q000737:chemistry / Q000378:metabolism; D011487:Protein Conformation; D019998:Racemases and Epimerases / Q000737:chemistry / Q000378:metabolism; D013482:Superoxide Dismutase / Q000737:chemistry / Q000378:metabolism; D014510:Urease / Q000737:chemistry / Q000378:metabolism
chemical_list: D004798:Enzymes; D009097:Multienzyme Complexes; D009532:Nickel; D010088:Oxidoreductases; C043296:nickel-iron hydrogenase; D006864:Hydrogenase; D049308:Dioxygenases; C083734:aci-reductone oxidase (CO-forming); D013482:Superoxide Dismutase; D000445:Aldehyde Oxidoreductases; C019823:carbon monoxide dehydrogenase; C021572:methyl coenzyme M reductase; D014510:Urease; D007791:Lactoylglutathione Lyase; D019998:Racemases and Epimerases; C021498:lactate racemase
keywords: Catalytic mechanism; Enzyme; Metallocenter; Nickel; Protein structure
references.citation: Biochemistry. 2008 Feb 26;47(8):2428-38
references.pmid: 18237192
references.citation: Biochemistry. 2008 Jul 15;47(28):7376-84
references.pmid: 18558723
references.citation: Science. 1997 Nov 21;278(5342):1457-62
references.pmid: 9367957
references.citation: Metallomics. 2009;1(3):207-21
references.pmid: 20046957
references.citation: Microbiol Rev. 1989 Mar;53(1):85-108
references.pmid: 2651866
references.citation: J Biol Chem. 1960 Feb;235:390-5
references.pmid: 13811155
references.citation: Biochemistry. 1998 Jun 16;37(24):8754-63
references.pmid: 9628737
references.citation: Curr Opin Chem Biol. 2011 Apr;15(2):276-83
references.pmid: 21130022
references.citation: J Biol Inorg Chem. 2004 Jul;9(5):516-24
references.pmid: 15221478
references.citation: J Biol Chem. 2013 May 10;288(19):13178-85
references.pmid: 23539618
references.citation: Biochemistry. 2010 Dec 28;49(51):10902-11
references.pmid: 21090696
references.citation: J Biol Inorg Chem. 2002 Jan;7(1-2):101-12
references.pmid: 11862546
references.citation: J Biol Inorg Chem. 1999 Aug;4(4):468-77
references.pmid: 10555581
references.citation: Chem Rev. 2007 Oct;107(10):4273-303
references.pmid: 17850165
references.citation: Annu Rev Pathol. 2006;1:63-96
references.pmid: 18039108
references.citation: Bioorg Med Chem Lett. 1998 Apr 7;8(7):705-10
references.pmid: 9871526
references.citation: J Biol Inorg Chem. 2010 Jun;15(5):795-807
references.pmid: 20333421
references.citation: Science. 2002 Oct 18;298(5593):567-72
references.pmid: 12386327
references.citation: Proc Natl Acad Sci U S A. 2004 Jun 8;101(23):8569-74
references.pmid: 15173586
references.citation: J Biol Chem. 1993 Oct 25;268(30):22369-76
references.pmid: 8226748
references.citation: Proc Natl Acad Sci U S A. 2001 Oct 9;98(21):11973-8
references.pmid: 11593006
references.citation: Arch Microbiol. 2008 Sep;190(3):257-69
references.pmid: 18575848
references.citation: Nat Struct Biol. 2000 Oct;7(10):903-9
references.pmid: 11017201
references.citation: Biochim Biophys Acta. 2010 Feb;1804(2):263-74
references.pmid: 19914406
references.citation: Biochemistry. 2001 Oct 30;40(43):12875-85
references.pmid: 11669624
references.citation: West J Med. 1985 Jan;142(1):88-90
references.pmid: 3976224
references.citation: Adv Microb Physiol. 2006;51:1-71
references.pmid: 17091562
references.citation: Plant Physiol. 1995 Apr;107(4):1097-103
references.pmid: 7770520
references.citation: J Biol Chem. 1999 Jan 15;274(3):1193-5
references.pmid: 9880484
references.citation: Nat Struct Biol. 2003 Apr;10(4):271-9
references.pmid: 12627225
references.citation: Nat Struct Biol. 2001 Jun;8(6):505-9
references.pmid: 11373617
references.citation: Plant Sci. 2011 Mar;180(3):431-8
references.pmid: 21421389
references.citation: Nature. 2000 Oct 5;407(6804):623-6
references.pmid: 11034209
references.citation: Chem Rev. 2007 Oct;107(10):4206-72
references.pmid: 17927159
references.citation: J Biol Inorg Chem. 2004 Jul;9(5):511-5
references.pmid: 15221484
references.citation: Science. 2007 Nov 30;318(5855):1461-4
references.pmid: 18048691
references.citation: J Am Chem Soc. 2005 Apr 20;127(15):5449-62
references.pmid: 15826182
references.citation: Microbiology (Reading). 1998 Sep;144 ( Pt 9):2377-2406
references.pmid: 9782487
references.citation: Biometals. 2005 Aug;18(4):399-405
references.pmid: 16158232
references.citation: Nat Rev Microbiol. 2007 Feb;5(2):107-18
references.pmid: 17224920
references.citation: J Bacteriol. 2004 Nov;186(22):7821-5
references.pmid: 15516600
references.citation: Acc Chem Res. 2011 Jul 19;44(7):520-30
references.pmid: 21542631
references.citation: Biochemistry. 2002 Feb 12;41(6):1807-19
references.pmid: 11827525
references.citation: J Biol Chem. 2009 Jul 10;284(28):18571-5
references.pmid: 19363030
references.citation: Nature. 1995 Aug 24;376(6542):643
references.pmid: 7651512
references.citation: BMC Genomics. 2009 Feb 10;10:78
references.pmid: 19208259
references.citation: FEBS Lett. 1999 Jun 18;453(1-2):90-4
references.pmid: 10403382
references.citation: Nature. 2010 Aug 5;466(7307):779-82
references.pmid: 20639861
references.citation: Chem Rev. 2009 Oct;109(10):4617-43
references.pmid: 19711977
references.citation: Biochemistry. 2010 Sep 7;49(35):7516-23
references.pmid: 20669901
references.citation: Biochemistry. 2000 Jul 25;39(29):8575-84
references.pmid: 10913264
references.citation: Nature. 2010 Jun 3;465(7298):606-8
references.pmid: 20520712
references.citation: Dalton Trans. 2005 Nov 7;(21):3443-50
references.pmid: 16234923
references.citation: Microbes Infect. 2000 Apr;2(5):533-42
references.pmid: 10865198
references.citation: Can J Biochem. 1980 Dec;58(12):1335-44
references.pmid: 6788353
references.citation: J Am Chem Soc. 2002 Apr 17;124(15):4039-49
references.pmid: 11942842
references.citation: J Biol Inorg Chem. 2001 Jan;6(1):63-81
references.pmid: 11191224
references.citation: Biochemistry. 2008 Mar 18;47(11):3474-83
references.pmid: 18293927
references.citation: Biochemistry. 2004 Jun 29;43(25):8038-47
references.pmid: 15209499
references.citation: Biol Chem. 2012 Sep 08;393(10):1089-100
references.pmid: 23096350
references.citation: Curr Opin Microbiol. 2005 Apr;8(2):188-95
references.pmid: 15802251
references.citation: Dalton Trans. 2009 Oct 7;(37):7577-87
references.pmid: 19759926
references.citation: Chem Soc Rev. 2011 May;40(5):2279-92
references.pmid: 21365080
references.citation: Biochem J. 1996 Sep 15;318 ( Pt 3):889-96
references.pmid: 8836134
references.citation: Clin Microbiol Rev. 2006 Jul;19(3):449-90
references.pmid: 16847081
references.citation: Science. 2001 Aug 17;293(5533):1281-5
references.pmid: 11509720
references.citation: Anal Biochem. 1990 Aug 1;188(2):427-31
references.pmid: 2221393
references.citation: Biochemistry. 2009 Aug 11;48(31):7432-40
references.pmid: 19583207
references.citation: Chemphyschem. 2010 Apr 26;11(6):1127-40
references.pmid: 20301175
references.citation: J Mol Biol. 2000 Oct 20;303(2):329-44
references.pmid: 11023796
references.citation: Science. 1995 May 19;268(5213):998-1004
references.pmid: 7754395
references.citation: J Am Chem Soc. 2005 Mar 2;127(8):2776-84
references.pmid: 15725036
references.citation: J Am Chem Soc. 2005 Dec 14;127(49):17186-7
references.pmid: 16332057
references.citation: Dalton Trans. 2009 Jun 14;(22):4274-85
references.pmid: 19662302
references.citation: Eur J Biochem. 1997 Jan 15;243(1-2):110-4
references.pmid: 9030728
references.citation: J Biol Chem. 2001 Oct 19;276(42):38602-9
references.pmid: 11507093
references.citation: Arch Microbiol. 2000 Jan;173(1):1-9
references.pmid: 10648098
references.citation: J Bacteriol. 1997 Apr;179(7):2259-66
references.pmid: 9079911
references.citation: Int J Biol Macromol. 2013 Jul;58:301-9
references.pmid: 23624166
references.citation: Biochemistry. 2008 Nov 18;47(46):12185-96
references.pmid: 18950192
references.citation: Proc Natl Acad Sci U S A. 2004 Jan 13;101(2):446-51
references.pmid: 14699043
references.citation: Biochemistry. 2001 Apr 17;40(15):4569-82
references.pmid: 11294624
references.citation: J Am Chem Soc. 2013 Jan 16;135(2):659-68
references.pmid: 23214721
references.citation: IUBMB Life. 2009 Dec;61(12):1132-42
references.pmid: 19946895
references.citation: Biochemistry. 1999 Mar 23;38(12):3744-52
references.pmid: 10090763
references.citation: Structure. 1999 Feb 15;7(2):205-16
references.pmid: 10368287
references.citation: J Am Chem Soc. 1976 Nov 10;98(23):7460-1
references.pmid: 977876
references.citation: Metallomics. 2011 Nov;3(11):1153-62
references.pmid: 21799955
references.citation: J Mol Biol. 2010 Jul 16;400(3):274-83
references.pmid: 20471401
references.citation: Biochemistry. 2006 Aug 15;45(32):9706-16
references.pmid: 16893172
references.citation: Environ Microbiol. 2008 Jul;10(7):1831-43
references.pmid: 18412551
references.citation: Biochemistry. 2009 Apr 14;48(14):3146-56
references.pmid: 19243132
references.citation: Trends Microbiol. 2002 Feb;10(2):70-4
references.pmid: 11827807
references.citation: J Biol Chem. 1982 Sep 10;257(17):10023-9
references.pmid: 7107595
references.citation: J Am Chem Soc. 2004 May 5;126(17):5382-7
references.pmid: 15113209
references.citation: FEBS Lett. 1980 Sep 22;119(1):118-20
references.pmid: 7428919
references.citation: J Mol Biol. 2006 Nov 3;363(4):823-34
references.pmid: 16989860
references.citation: J Biol Chem. 1999 Feb 5;274(6):3331-7
references.pmid: 9920874
references.citation: Nat Prod Rep. 2010 May;27(5):681-94
references.pmid: 20442959
references.citation: Eur J Biochem. 1993 Feb 15;212(1):101-5
references.pmid: 8444148
references.citation: J Mol Biol. 2001 May 25;309(1):315-30
references.pmid: 11491299
references.citation: FEMS Microbiol Rev. 2003 Jun;27(2-3):239-61
references.pmid: 12829270
references.citation: Biochemistry. 2000 Feb 15;39(6):1274-7
references.pmid: 10684606
references.citation: Biochemistry. 2000 May 9;39(18):5389-96
references.pmid: 10820010
references.citation: Nat Struct Biol. 2002 Dec;9(12):966-72
references.pmid: 12402029
references.citation: J Biol Chem. 1998 Apr 17;273(16):10019-25
references.pmid: 9545348
references.citation: Biochemistry. 2013 Jan 8;52(1):4-18
references.pmid: 23240653
references.citation: J Biomol NMR. 2006 Feb;34(2):117-27
references.pmid: 16518698
references.citation: Biochemistry. 2002 May 28;41(21):6761-9
references.pmid: 12022880
references.citation: J Biol Chem. 2000 Jul 28;275(30):22657-62
references.pmid: 10801792
references.citation: Biochemistry. 2000 Aug 1;39(30):8719-27
references.pmid: 10913283
references.citation: Biochemistry. 1997 Jul 1;36(26):8164-72
references.pmid: 9201965
references.citation: J Am Chem Soc. 2001 Jun 27;123(25):5853-60
references.pmid: 11414817
references.citation: Nat Prod Rep. 2010 May;27(5):658-67
references.pmid: 20442957
references.citation: Inorg Chem. 2011 Feb 7;50(3):1047-57
references.pmid: 21222442
references.citation: Biochemistry. 2012 Oct 9;51(40):7816-32
references.pmid: 22970729
references.citation: J Inorg Biochem. 2007 Nov;101(11-12):1657-66
references.pmid: 17716738
references.citation: Inorg Chem. 2011 Mar 7;50(5):1868-78
references.pmid: 21247090
references.citation: Mol Microbiol. 1993 Sep;9(5):907-13
references.pmid: 7934918
references.citation: Proc Natl Acad Sci U S A. 2011 Aug 9;108(32):13095-9
references.pmid: 21788478
references.citation: J Biol Inorg Chem. 2005 May;10(3):239-49
references.pmid: 15803334
references.citation: J Phys Chem B. 2007 Aug 30;111(34):10263-74
references.pmid: 17676790
references.citation: Microbiol Rev. 1995 Sep;59(3):451-80
references.pmid: 7565414
references.citation: Science. 1995 Feb 24;267(5201):1156-8
references.pmid: 7855593
references.citation: J Am Chem Soc. 2004 Jan 21;126(2):460-1
references.pmid: 14719931
references.citation: EMBO J. 1997 Jun 16;16(12):3386-95
references.pmid: 9218781
references.citation: Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9558-63
references.pmid: 18621675
references.citation: Plant Sci. 2013 Feb;199-200:79-90
references.pmid: 23265321