Home LiteratureArticle Details
PMID: 18287282 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Structural constraints on autoprocessing of the human nucleoporin Nup98.

Protein science : a publication of the Protein Society ·Vol. 17 ·No. 3 ·2008-03-00 ·Pages 494-505

Sun Y, Guo HC

Abstract

Nucleoporin Nup98, a 98-kDa protein component of the nuclear pore complex, plays an important role in both protein and RNA transport. During its maturation process, Nup98 undergoes post-translational autoproteolysis, which is critical for targeting to the NPC. Here we present high-resolution crystal structures of the C-terminal autoproteolytic domains of Nup98 (2.3 A for the wild type and 1.9 A for the S864A precursor), and propose a detailed autoproteolysis mechanism through an N-O acyl shift. Structural constraints are found at the autocleavage site, and could thus provide a driving force for autocleavage at the scissile peptide bond. Such structural constraints appear to be generated, at least in part, by anchoring a conserved phenylalanine side chain into a highly conserved hydrophobic pocket at the catalytic site. Our high-resolution crystal structures also reveal that three highly conserved residues, Tyr866, Gly867, and Leu868, provide most of the interactions between the autoproteolytic domain and the C-terminal tail. These results suggest that Nup98 may represent a new subtype of protein that utilizes autoprocessing to control biogenesis pathways and intracellular translocation.

MeSH Terms
Catalysis Crystallography, X-Ray Humans Hydrogen Bonding Models, Molecular Nuclear Pore Complex Proteins/chemistry,metabolism Protein Processing, Post-Translational Protein Structure, Tertiary
Chemicals
Nuclear Pore Complex Proteins Nup98 protein, human
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Sun Yixin
Department of Physiology and Biophysics, Boston University School of Medicine, Boston, Massachusetts 02118-2526, USA.
Guo Hwai-Chen
References (39)
39 references, click to expand
  1. Autocatalytic processing of gamma-glutamyltranspeptidase.
    J Biol Chem. 2002 Nov 8;277(45):43536-43 PMID: 12207027
  2. Activation and oligomerization of aspartylglucosaminidase.
    J Biol Chem. 1998 Sep 25;273(39):25320-8 PMID: 9737998
  3. Crystal structure of GyrA intein from Mycobacterium xenopi reveals structural basis of protein splicing.
    Nat Struct Biol. 1998 Jan;5(1):31-6 PMID: 9437427
  4. Taspase1: a threonine aspartase required for cleavage of MLL and proper HOX gene expression.
    Cell. 2003 Oct 31;115(3):293-303 PMID: 14636557
  5. Crystal structures of Flavobacterium glycosylasparaginase. An N-terminal nucleophile hydrolase activated by intramolecular proteolysis.
    J Biol Chem. 1998 Aug 7;273(32):20205-12 PMID: 9685368
  6. Structural insights into the mechanism of intramolecular proteolysis.
    Cell. 1999 Sep 3;98(5):651-61 PMID: 10490104
  7. Vesicular stomatitis virus matrix protein inhibits host cell gene expression by targeting the nucleoporin Nup98.
    Mol Cell. 2000 Nov;6(5):1243-52 PMID: 11106761
  8. Autocatalytic cleavage of Clostridium difficile toxin B.
    Nature. 2007 Mar 22;446(7134):415-9 PMID: 17334356
  9. Structural constraints on protein self-processing in L-aspartate-alpha-decarboxylase.
    EMBO J. 2003 Dec 1;22(23):6193-204 PMID: 14633979
  10. Investigation of the specificity of the herpes simplex virus type 1 protease by point mutagenesis of the autoproteolysis sites.
    J Virol. 1994 Jan;68(1):526-9 PMID: 8254766
  11. A conserved biogenesis pathway for nucleoporins: proteolytic processing of a 186-kilodalton precursor generates Nup98 and the novel nucleoporin, Nup96.
    J Cell Biol. 1999 Mar 22;144(6):1097-112 PMID: 10087256
  12. The three-dimensional structure of the autoproteolytic, nuclear pore-targeting domain of the human nucleoporin Nup98.
    Mol Cell. 2002 Aug;10(2):347-58 PMID: 12191480
  13. Single base deletion in exon 7 of the glycosylasparaginase gene causes a mild form of aspartylglycosaminuria in a patient of Mauritian origin.
    J Inherit Metab Dis. 1996;19(1):76-83 PMID: 8830180
  14. Complex formation among the RNA export proteins Nup98, Rae1/Gle2, and TAP.
    J Biol Chem. 2003 Jun 6;278(23):20979-88 PMID: 12637516
  15. Crystallographic snapshot of a productive glycosylasparaginase-substrate complex.
    J Mol Biol. 2007 Feb 9;366(1):82-92 PMID: 17157318
  16. Conformational constraints for protein self-cleavage in the proteasome.
    J Mol Biol. 1998 Jun 26;279(5):1187-91 PMID: 9642094
  17. Peering through the pore: nuclear pore complex structure, assembly, and function.
    Dev Cell. 2003 Jun;4(6):775-89 PMID: 12791264
  18. Crystallography & NMR system: A new software suite for macromolecular structure determination.
    Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):905-21 PMID: 9757107
  19. Processing of X-ray diffraction data collected in oscillation mode.
    Methods Enzymol. 1997;276:307-26 PMID: 27754618
  20. MOLMOL: a program for display and analysis of macromolecular structures.
    J Mol Graph. 1996 Feb;14(1):51-5, 29-32 PMID: 8744573
  21. NARC-1/PCSK9 and its natural mutants: zymogen cleavage and effects on the low density lipoprotein (LDL) receptor and LDL cholesterol.
    J Biol Chem. 2004 Nov 19;279(47):48865-75 PMID: 15358785
  22. Autoproteolysis of PIDD marks the bifurcation between pro-death caspase-2 and pro-survival NF-kappaB pathway.
    EMBO J. 2007 Jan 10;26(1):197-208 PMID: 17159900
  23. Modularity within the architecture of the nuclear pore complex.
    Curr Opin Struct Biol. 2005 Apr;15(2):221-6 PMID: 15837182
  24. The role of NUP98 gene fusions in hematologic malignancy.
    Leuk Lymphoma. 2004 Jul;45(7):1341-50 PMID: 15359631
  25. Influenza virus targets the mRNA export machinery and the nuclear pore complex.
    Proc Natl Acad Sci U S A. 2007 Feb 6;104(6):1853-8 PMID: 17267598
  26. Semisynthesis of a segmental isotopically labeled protein splicing precursor: NMR evidence for an unusual peptide bond at the N-extein-intein junction.
    Proc Natl Acad Sci U S A. 2004 Apr 27;101(17):6397-402 PMID: 15087498
  27. Structural comparison of Ntn-hydrolases.
    Protein Sci. 2000 Dec;9(12):2329-37 PMID: 11206054
  28. Autoproteolysis in nucleoporin biogenesis.
    Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11370-5 PMID: 10500183
  29. Structural insights into the protein splicing mechanism of PI-SceI.
    J Biol Chem. 2000 Jun 2;275(22):16408-13 PMID: 10828056
  30. Characterization and functional analysis of the cis-autoproteolysis active center of glycosylasparaginase.
    J Biol Chem. 1998 Apr 17;273(16):9695-702 PMID: 9545304
  31. Spectrum of mutations in aspartylglucosaminuria.
    Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11222-6 PMID: 1722323
  32. Structure of a slow processing precursor penicillin acylase from Escherichia coli reveals the linker peptide blocking the active-site cleft.
    J Mol Biol. 2000 Sep 29;302(4):887-98 PMID: 10993730
  33. Autocatalytic processing of the 20S proteasome.
    Nature. 1996 Aug 1;382(6590):468-71 PMID: 8684489
  34. Protein splicing and related forms of protein autoprocessing.
    Annu Rev Biochem. 2000;69:447-96 PMID: 10966466
  35. Capsid assembly in a family of animal viruses primes an autoproteolytic maturation that depends on a single aspartic acid residue.
    J Biol Chem. 1994 May 6;269(18):13680-4 PMID: 8175803
  36. Precursor structure of cephalosporin acylase. Insights into autoproteolytic activation in a new N-terminal hydrolase family.
    J Biol Chem. 2002 Jan 25;277(4):2823-9 PMID: 11706000
  37. Mechanism of autoproteolysis at the NS2-NS3 junction of the hepatitis C virus polyprotein.
    Trends Biochem Sci. 1998 Mar;23(3):92-4 PMID: 9581498
  38. A dual role for an aspartic acid in glycosylasparaginase autoproteolysis.
    Structure. 2003 Aug;11(8):997-1003 PMID: 12906830
  39. Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G protein-coupled receptor proteolytic site motif.
    J Biol Chem. 2004 Jul 23;279(30):31823-32 PMID: 15150276
Article Info
Journal
Protein science : a publication of the Protein Society
Abbr.
Protein Sci
ISSN
0961-8368
Published
2008-03-00
Pages
494-505
Language
English
Region
United States
NLM ID
9211750
PMCID
PMC2248301
Subset
IM
Grants
NIDDK NIH HHS · R01 DK053893 · United States
NIDDK NIH HHS · R01 DK075294 · United States
NIDDK NIH HHS · DK053893 · United States
NIDDK NIH HHS · DK075294 · United States
Databases
PDB
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com