Structural basis of substrate recognition by a bacterial deubiquitinase important for dynamics of phagosome ubiquitination

Sheedlo, Michael J.; Qiu, Jiazhang; Tan, Yunhao; Paul, Lake N.; Luo, Zhao-Qing; Das, Chittaranjan

doi:10.1073/pnas.1514568112

Title: Structural basis of substrate recognition by a bacterial deubiquitinase important for dynamics of phagosome ubiquitination

Journal Article · Mon Nov 23 00:00:00 EST 2015 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1514568112· OSTI ID:1237752

Sheedlo, Michael J. ^[1]; Qiu, Jiazhang ^[1]; Tan, Yunhao ^[2]; Paul, Lake N. ^[1]; Luo, Zhao-Qing ^[1]; Das, Chittaranjan ^[1]

Purdue Univ., West Lafayette, IN (United States)
Purdue Univ., West Lafayette, IN (United States); Boston Children’s Hospital and Harvard Medical School, Boston, MA (United States)

Manipulation of the host’s ubiquitin network is emerging as an important strategy for counteracting and repurposing the posttranslational modification machineries of the host by pathogens. Ubiquitin E3 ligases encoded by infectious agents are well known, as are a variety of viral deubiquitinases (DUBs). Bacterial DUBs have been discovered, but little is known about the structure and mechanism underlying their ubiquitin recognition. In this report, we found that members of the Legionella pneumophila SidE effector family harbor a DUB module important for ubiquitin dynamics on the bacterial phagosome. Structural analysis of this domain alone and in complex with ubiquitin vinyl methyl ester (Ub-VME) reveals unique molecular contacts used in ubiquitin recognition. Instead of relying on the Ile44 patch of ubiquitin, as commonly used in eukaryotic counterparts, the SdeA_Dub module engages Gln40 of ubiquitin. The architecture of the active-site cleft presents an open arrangement with conformational plasticity, permitting deubiquitination of three of the most abundant polyubiquitin chains, with a distinct preference for Lys63 linkages. We have shown that this preference enables efficient removal of Lys63 linkages from the phagosomal surface. Remarkably, the structure reveals by far the most parsimonious use of molecular contacts to achieve deubiquitination, with less than 1,000 Å² of accessible surface area buried upon complex formation with ubiquitin. In conclusion, this type of molecular recognition appears to enable dual specificity toward ubiquitin and the ubiquitin-like modifier NEDD8.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; National Institutes of Health (NIH)

Grant/Contract Number:: AC02-06CH11357; 2R01GM103401; R56AI103168; K02AI085403; R21AI105714

OSTI ID:: 1237752

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 112, Issue 49; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 67 works

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59 BASIC BIOLOGICAL SCIENCES
type IV secretion
ubiquitination
Legionella
phagosome
deubiquitinase

Title: Structural basis of substrate recognition by a bacterial deubiquitinase important for dynamics of phagosome ubiquitination

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