Escherichia coli LipA is a lipoyl synthase: in vitro biosynthesis of lipoylated pyruvate dehydrogenase complex from octanoyl-acyl carrier protein

Biochemistry. 2000 Dec 12;39(49):15166-78. doi: 10.1021/bi002060n.

Abstract

The Escherichia coli lipA gene product has been genetically linked to carbon-sulfur bond formation in lipoic acid biosynthesis [Vanden Boom, T. J., Reed, K. E., and Cronan, J. E., Jr. (1991) J. Bacteriol. 173, 6411-6420], although in vitro lipoate biosynthesis with LipA has never been observed. In this study, the lipA gene and a hexahistidine tagged lipA construct (LipA-His) were overexpressed in E. coli as soluble proteins. The proteins were purified as a mixture of monomeric and dimeric species that contain approximately four iron atoms per LipA polypeptide and a similar amount of acid-labile sulfide. Electron paramagnetic resonance and electronic absorbance spectroscopy indicate that the proteins contain a mixture of [3Fe-4S] and [4Fe-4S] cluster states. Reduction with sodium dithionite results in small quantities of an S = 1/2 [4Fe-4S](1+) cluster with the majority of the protein containing a species consistent with an S = 0 [4Fe-4S](2+) cluster. LipA was assayed for lipoate or lipoyl-ACP formation using E. coli lipoate-protein ligase A (LplA) or lipoyl-[acyl-carrier-protein]-protein-N-lipoyltransferase (LipB), respectively, to lipoylate apo-pyruvate dehydrogenase complex (apo-PDC) [Jordan, S. W., and Cronan, J. E. (1997) Methods Enzymol. 279, 176-183]. When sodium dithionite-reduced LipA was incubated with octanoyl-ACP, LipB, apo-PDC, and S-adenosyl methionine (AdoMet), lipoylated PDC was formed. As shown by this assay, octanoic acid is not a substrate for LipA. Confirmation that LipA catalyzes formation of lipoyl groups from octanoyl-ACP was obtained by MALDI mass spectrometry of a recombinant PDC lipoyl-binding domain that had been lipoylated in a LipA reaction. These results provide information about the mechanism of LipA catalysis and place LipA within the family of iron-sulfur proteins that utilize AdoMet for radical-based chemistry.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Acyl Carrier Protein / metabolism*
  • Acylation
  • Bacterial Proteins / metabolism*
  • Cloning, Molecular
  • Dithionite
  • Escherichia coli / enzymology
  • Iron / analysis
  • Iron-Sulfur Proteins / metabolism*
  • Models, Chemical
  • Oxidation-Reduction
  • Protein Processing, Post-Translational
  • Pyruvate Dehydrogenase Complex / metabolism*
  • S-Adenosylmethionine / metabolism
  • Sulfur / analysis
  • Thioctic Acid / biosynthesis*

Substances

  • Acyl Carrier Protein
  • Bacterial Proteins
  • Iron-Sulfur Proteins
  • LipA protein, Bacteria
  • Pyruvate Dehydrogenase Complex
  • lipase activator protein, Bacteria
  • Dithionite
  • Sulfur
  • Thioctic Acid
  • S-Adenosylmethionine
  • Iron