The energy landscape of adenylate kinase during catalysis

Kerns, S. Jordan; Agafonov, Roman V.; Cho, Young-Jin; Pontiggia, Francesco; Otten, Renee; Pachov, Dimitar V.; Kutter, Steffen; Phung, Lien A.; Murphy, Padraig N.; Thai, Vu; Alber, Tom; Hagan, Michael F.; Kern, Dorothee

doi:10.1038/nsmb.2941

Title: The energy landscape of adenylate kinase during catalysis

Journal Article · Mon Jan 12 00:00:00 EST 2015 · Nature Structural & Molecular Biology

DOI:https://doi.org/10.1038/nsmb.2941· OSTI ID:1182309

Kerns, S. Jordan ^[1]; Agafonov, Roman V. ^[1]; Cho, Young-Jin ^[1]; Pontiggia, Francesco ^[1]; Otten, Renee ^[1]; Pachov, Dimitar V. ^[1]; Kutter, Steffen ^[1]; Phung, Lien A. ^[1]; Murphy, Padraig N. ^[1]; Thai, Vu ^[1]; Alber, Tom ^[2]; Hagan, Michael F. ^[3]; Kern, Dorothee ^[1]

Brandeis Univ., Waltham, MA (United States). Dept. of Biochemistry. Howard Hughes Medical Inst.
Univ. of California, Berkeley, CA (United States)
Brandeis Univ., Waltham, MA (United States). Dept. of Physics

Kinases perform phosphoryl-transfer reactions in milliseconds; without enzymes, these reactions would take about 8,000 years under physiological conditions. Despite extensive studies, a comprehensive understanding of kinase energy landscapes, including both chemical and conformational steps, is lacking. In this paper, we scrutinize the microscopic steps in the catalytic cycle of adenylate kinase, through a combination of NMR measurements during catalysis, pre-steady-state kinetics, molecular-dynamics simulations and crystallography of active complexes. We find that the Mg²⁺ cofactor activates two distinct molecular events: phosphoryl transfer (>10⁵-fold) and lid opening (10³-fold). In contrast, mutation of an essential active site arginine decelerates phosphoryl transfer 10³-fold without substantially affecting lid opening. Finally, our results highlight the importance of the entire energy landscape in catalysis and suggest that adenylate kinases have evolved to activate key processes simultaneously by precise placement of a single, charged and very abundant cofactor in a preorganized active site.

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Research Organization:: Brandeis Univ., Waltham, MA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Inst. of Health (NIH) (United States); Damon Runyon Cancer Research Foundation (United States)

Contributing Organization:: Univ. of California, Berkeley, CA (United States)

Grant/Contract Number:: FG02-05ER15699; RO1-GM100966; DRG-2114-12

OSTI ID:: 1182309

Journal Information:: Nature Structural & Molecular Biology, Vol. 22, Issue 2; ISSN 1545-9993

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 110 works

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