Structure of puromycin-sensitive aminopeptidase and polyglutamine binding

Madabushi, Sowmya; Chow, K. Martin; Song, Eun Suk; Goswami, Anwesha; Hersh, Louis B.; Rodgers, David W.

doi:10.1371/journal.pone.0287086

Structure of puromycin-sensitive aminopeptidase and polyglutamine binding

Journal Article · Thu Jul 13 00:00:00 EDT 2023 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0287086· OSTI ID:2423659

Madabushi, Sowmya ^[1]; Chow, K. Martin ^[1]; Song, Eun Suk ^[1]; Goswami, Anwesha ^[1]; Hersh, Louis B. ^[1]; ^[1]

Univ. of Kentucky, Lexington, KY (United States)

Puromycin-sensitive aminopeptidase (E.C. 3.4.11.14, UniProt P55786), a zinc metallopeptidase belonging to the M1 family, degrades a number of bioactive peptides as well as peptides released from the proteasome, including polyglutamine. We report the crystal structure of PSA at 2.3 Å. Overall, the enzyme adopts a V-shaped architecture with four domains characteristic of the M1 family aminopeptidases, but it is in a less compact conformation compared to most M1 enzymes of known structure. A microtubule binding sequence is present in a C-terminal HEAT repeat domain of the enzyme in a position where it might serve to mediate interaction with tubulin. In the catalytic metallopeptidase domain, an elongated active site groove lined with aromatic and hydrophobic residues and a large S1 subsite may play a role in broad substrate recognition. The structure with bound polyglutamine shows a possible interacting mode of this peptide, which is supported by mutation.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2423659

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 7 Vol. 18; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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A TOG: -tubulin Complex Structure Reveals Conformation-Based Mechanisms for a Microtubule Polymerase Ayaz, P.; Ye, X.; Huddleston, P. Science, Vol. 337, Issue 6096 https://doi.org/10.1126/science.1221698	journal	August 2012
Inactivation and Metabolism of Neuropeptides McKelvy, J. F.; Blumberg, S. Annual Review of Neuroscience, Vol. 9, Issue 1 https://doi.org/10.1146/annurev.ne.09.030186.002215	journal	March 1986
Glutamine Repeats and Neurodegeneration Zoghbi, Huda Y.; Orr, Harry T. Annual Review of Neuroscience, Vol. 23, Issue 1 https://doi.org/10.1146/annurev.neuro.23.1.217	journal	March 2000
Aminopeptidases do not directly degrade tau protein Chow, K.; Guan, Hanjun; Hersh, Louis B. Molecular Neurodegeneration, Vol. 5, Issue 1 https://doi.org/10.1186/1750-1326-5-48	journal	January 2010
Cu, Zn-superoxide dismutase 1 (SOD1) is a novel target of Puromycin-sensitive aminopeptidase (PSA/NPEPPS): PSA/NPEPPS is a possible modifier of amyotrophic lateral sclerosis Ren, Guijie; Ma, Zhongcai; Hui, Maria Molecular Neurodegeneration, Vol. 6, Issue 1 https://doi.org/10.1186/1750-1326-6-29	journal	May 2011
The MAP2/Tau family of microtubule-associated proteins Dehmelt, Leif; Halpain, Shelley Genome Biology, Vol. 6, Issue 1, p. 204 https://doi.org/10.1186/gb-2004-6-1-204	journal	December 2004
Phase I/II Clinical Study of Tosedostat, an Inhibitor of Aminopeptidases, in Patients With Acute Myeloid Leukemia and Myelodysplasia Löwenberg, Bob; Morgan, Gareth; Ossenkoppele, Gert J. Journal of Clinical Oncology, Vol. 28, Issue 28 https://doi.org/10.1200/JCO.2009.27.6295	journal	October 2010
Male Reproductive Defects Caused by Puromycin-Sensitive Aminopeptidase Deficiency in Mice Osada, Tomoharu; Watanabe, Gen; Kondo, Shunzo Molecular Endocrinology, Vol. 15, Issue 6 https://doi.org/10.1210/mend.15.6.0643	journal	June 2001
Puromycin-Sensitive Aminopeptidase Is Essential for the Maternal Recognition of Pregnancy in Mice Osada, Tomoharu; Watanabe, Gen; Sakaki, Yoshiyuki Molecular Endocrinology, Vol. 15, Issue 6 https://doi.org/10.1210/mend.15.6.0644	journal	June 2001
The puromycin-sensitive aminopeptidase PAM-1 is required for meiotic exit and anteroposterior polarity in the one-cellCaenorhabditis elegansembryo Lyczak, Rebecca; Zweier, Lynnsey; Group, Thomas Development, Vol. 133, Issue 21 https://doi.org/10.1242/dev.02615	journal	November 2006
Serverification of Molecular Modeling Applications: The Rosetta Online Server That Includes Everyone (ROSIE) Lyskov, Sergey; Chou, Fang-Chieh; Conchúir, Shane Ó. PLoS ONE, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pone.0063906	journal	May 2013
Fully Flexible Docking of Medium Sized Ligand Libraries with RosettaLigand DeLuca, Samuel; Khar, Karen; Meiler, Jens PLOS ONE, Vol. 10, Issue 7 https://doi.org/10.1371/journal.pone.0132508	journal	July 2015
Structural Bases of Coronavirus Attachment to Host Aminopeptidase N and Its Inhibition by Neutralizing Antibodies Reguera, Juan; Santiago, César; Mudgal, Gaurav PLoS Pathogens, Vol. 8, Issue 8 https://doi.org/10.1371/journal.ppat.1002859	journal	August 2012
Increased Anxiety and Impaired Pain Response in Puromycin-Sensitive Aminopeptidase Gene-Deficient Mice Obtained by a Mouse Gene-Trap Method Osada, Tomoharu; Ikegami, Shiro; Takiguchi-Hayashi, Keiko The Journal of Neuroscience, Vol. 19, Issue 14 https://doi.org/10.1523/JNEUROSCI.19-14-06068.1999	journal	July 1999
Membrane Bound Members of the M1 Family: More Than Aminopeptidases Albiston, Anthony; Ye, Siying; Chai, Siew Protein & Peptide Letters, Vol. 11, Issue 5 https://doi.org/10.2174/0929866043406643	journal	October 2004
Crystal Structure of Insulin-Regulated Aminopeptidase with Bound Substrate Analogue Provides Insight on Antigenic Epitope Precursor Recognition and Processing Mpakali, Anastasia; Saridakis, Emmanuel; Harlos, Karl The Journal of Immunology, Vol. 195, Issue 6 https://doi.org/10.4049/jimmunol.1501103	journal	August 2015

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59 BASIC BIOLOGICAL SCIENCES
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Structure of puromycin-sensitive aminopeptidase and polyglutamine binding

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