Threonine 98, the pivotal residue of tissue inhibitor of metalloproteinases (TIMP)-1 in metalloproteinase recognition

J Biol Chem. 2004 Apr 23;279(17):17562-9. doi: 10.1074/jbc.M312589200. Epub 2004 Jan 20.

Abstract

Tissue inhibitors of metalloproteinases (TIMPs) are the endogenous modulators of the zinc-dependent mammalian matrix metalloproteinases (MMPs) and their close associates, proteinases of the ADAM (a disintegrin and metalloproteinase) and ADAM with thrombospondin repeats families. There are four variants of TIMPs, and each has its defined set of metalloproteinase (MP) targets. TIMP-1, in particular, is inactive against several of the membrane-type MMPs (MT-MMPs), MMP-19, and the ADAM proteinase TACE (tumor necrosis factor-alpha-converting enzyme, ADAM-17). The molecular basis for such inactivity is unknown. Previously, we showed that TIMP-1 could be transformed into an active inhibitor against MT1-MMP by the replacement of threonine 98 residue with leucine (T98L). Here, we reveal that the T98L mutation has in fact transformed TIMP-1 into a versatile inhibitor against an array of MPs otherwise insensitive to wild-type TIMP-1; examples include TACE, MMP-19, and MT5-MMP. Using T98L as the scaffold, we created a TIMP-1 variant that is fully active against TACE. The binding affinity of the mutant (V4S/TIMP-3-AB-loop/V69L/T98L) (K (app)(i) 0.14 nm) surpassed that of TIMP-3 (K (app)(i) 0.22 nm), the only natural TIMP inhibitor of the enzyme. The requirement for leucine is absolute for the transformation in inhibitory pattern. On the other hand, the mutation has minimal impact on the MPs already well inhibited by wild-type TIMP-1, such as gelatinase-A and stromelysin-1. Not only have we unlocked the molecular basis for the inactivity of TIMP-1 against several of the MPs, but also our findings fundamentally modify the current beliefs on the molecular mechanism of TIMP-MP recognition and selectivity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Amino Acid Sequence
  • Collagenases / metabolism
  • Crystallography, X-Ray
  • Escherichia coli / metabolism
  • Humans
  • Kinetics
  • Leucine / chemistry
  • Matrix Metalloproteinase 13
  • Matrix Metalloproteinase 2 / metabolism
  • Matrix Metalloproteinase 3 / metabolism
  • Matrix Metalloproteinase 7 / metabolism
  • Matrix Metalloproteinases / metabolism
  • Matrix Metalloproteinases, Secreted
  • Models, Molecular
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Mutation
  • Protein Binding
  • Protein Folding
  • Protein Structure, Tertiary
  • Sequence Homology, Amino Acid
  • Threonine / chemistry*
  • Thrombospondins / chemistry
  • Time Factors
  • Tissue Inhibitor of Metalloproteinase-1 / chemistry*
  • Tissue Inhibitor of Metalloproteinase-1 / metabolism*

Substances

  • Thrombospondins
  • Tissue Inhibitor of Metalloproteinase-1
  • Threonine
  • Collagenases
  • MMP13 protein, human
  • MMP26 protein, human
  • Matrix Metalloproteinase 13
  • Matrix Metalloproteinases
  • Matrix Metalloproteinases, Secreted
  • Matrix Metalloproteinase 3
  • Matrix Metalloproteinase 7
  • Matrix Metalloproteinase 2
  • Leucine