Single-molecule spectroscopy reveals how calmodulin activates NO synthase by controlling its conformational fluctuation dynamics

Proc Natl Acad Sci U S A. 2015 Sep 22;112(38):11835-40. doi: 10.1073/pnas.1508829112. Epub 2015 Aug 26.

Abstract

Mechanisms that regulate the nitric oxide synthase enzymes (NOS) are of interest in biology and medicine. Although NOS catalysis relies on domain motions, and is activated by calmodulin binding, the relationships are unclear. We used single-molecule fluorescence resonance energy transfer (FRET) spectroscopy to elucidate the conformational states distribution and associated conformational fluctuation dynamics of the two electron transfer domains in a FRET dye-labeled neuronal NOS reductase domain, and to understand how calmodulin affects the dynamics to regulate catalysis. We found that calmodulin alters NOS conformational behaviors in several ways: It changes the distance distribution between the NOS domains, shortens the lifetimes of the individual conformational states, and instills conformational discipline by greatly narrowing the distributions of the conformational states and fluctuation rates. This information was specifically obtainable only by single-molecule spectroscopic measurements, and reveals how calmodulin promotes catalysis by shaping the physical and temporal conformational behaviors of NOS.

Keywords: FRET; conformational motion; domain–domain interaction; electron transfer; flavoprotein.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calmodulin / metabolism*
  • Carbocyanines / metabolism
  • Cattle
  • Fluorescence Resonance Energy Transfer / methods*
  • Nitric Oxide Synthase Type I / chemistry*
  • Nitric Oxide Synthase Type I / metabolism*
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Spectrophotometry, Ultraviolet
  • Time Factors

Substances

  • Calmodulin
  • Carbocyanines
  • cyanine dye 3
  • cyanine dye 5
  • Nitric Oxide Synthase Type I