Two cutinase-like proteins secreted by Mycobacterium tuberculosis show very different lipolytic activities reflecting their physiological function

FASEB J. 2010 Jun;24(6):1893-903. doi: 10.1096/fj.09-144766. Epub 2010 Jan 26.

Abstract

Cutinases are extracellular enzymes that are able to degrade cutin, a polyester protecting plant leaves and many kinds of lipids. Although cutinases are mainly found in phytopathogenic fungi or bacteria, 7 genes related to the cutinase family have been predicted in the genome of Mycobacterium tuberculosis. These genes may encode proteins that are involved in the complex lipid metabolism of the bacterium. Here, we report on the biochemical characterization of two secreted proteins of M. tuberculosis, Rv1984c and Rv3452, belonging to the cutinase family. Although their amino acid sequence shows 50% identity with that of the well-characterized cutinase from Fusarium solani pisi, and a high level of homology has been found to exist between these two enzymes, they show distinct substrate specificities. Rv1984c preferentially hydrolyzes medium-chain carboxylic esters and monoacylglycerols, whereas Rv3452 behaves like a phospholipase A(2), and it is able to induce macrophage lysis. The tetrahydrolipstatin inhibitor, a specific lipase inhibitor, abolishes the activity of both enzymes. Site-directed mutagenesis was performed to identify the catalytic triad of Rv1984c. Structural models for Rv1984c and Rv3452 were built, based on the crystal structure of F. solani cutinase, with a view to investigating the contribution of specific residues to the substrate specificity. Our findings open new prospects for investigating the physiological roles of cutinase-like proteins in the lipid metabolism and virulence of M. tuberculosis.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Carboxylic Ester Hydrolases / genetics
  • Carboxylic Ester Hydrolases / metabolism*
  • Catalysis
  • Enzyme Inhibitors / pharmacology
  • Esters / metabolism*
  • Lactones / pharmacology
  • Lipase / antagonists & inhibitors
  • Lipolysis / drug effects
  • Lipolysis / physiology*
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Mice
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Mycobacterium tuberculosis / enzymology*
  • Orlistat
  • Phospholipases A2 / genetics
  • Phospholipases A2 / metabolism*
  • Protein Conformation
  • Sequence Homology, Amino Acid
  • Substrate Specificity

Substances

  • Enzyme Inhibitors
  • Esters
  • Lactones
  • Orlistat
  • Carboxylic Ester Hydrolases
  • cutinase
  • Lipase
  • Phospholipases A2