Home LiteratureArticle Details
PMID: 18435556 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Prevalence of intrinsic disorder in the intracellular region of human single-pass type I proteins: the case of the notch ligand Delta-4.

Journal of proteome research ·Vol. 7 ·No. 6 ·2008-06-00 ·Pages 2496-506

De Biasio A, Guarnaccia C, Popovic M, Uversky VN, Pintar A, Pongor S

Abstract

Intrinsic disorder (ID) is a widespread phenomenon found especially in signaling and regulation-related eukaryotic proteins. The functional importance of flexible disordered regions often resides in their ability to allow proteins to bind different partners. The incidence and location of intrinsic disorder in 369 human single-pass transmembrane receptors with the type I topology was assessed based on both disorder predictions and amino acid physico-chemical properties. We provide evidence that ID concentrates in the receptors' cytoplasmic region. As a benchmark for this analysis, we present a structural study on the previously uncharacterized intracellular region of human Delta-4 (DLL4_IC), a single-pass transmembrane protein and a ligand of Notch receptors. DLL4_IC is required for receptor/ligand endocytosis; it undergoes regulated intramembrane proteolysis, and mediates protein-protein interactions through its C-terminal PDZ binding motif. Using a recombinant purified protein, we demonstrate using various biophysical methods that DLL4_IC is mainly disordered in solution but can form interconvertible local secondary structures in response to variations in the physico-chemical milieu. Most of these conformational changes occur in the highly conserved C-terminal segment that includes the PDZ-binding motif. On the basis of our results, we propose that global disorder, in concert with local preorganization, may play a role in Notch signaling mediated by Delta-4.

MeSH Terms
Adaptor Proteins, Signal Transducing Amino Acid Sequence Calcium-Binding Proteins Chromatography, Gel Circular Dichroism Humans Hydrophobic and Hydrophilic Interactions Intercellular Signaling Peptides and Proteins/biosynthesis,chemistry,genetics Membrane Proteins/chemistry Molecular Sequence Data Nuclear Magnetic Resonance, Biomolecular Receptors, Cell Surface/chemistry Recombinant Proteins/biosynthesis,chemistry,isolation & purification Sequence Alignment Static Electricity
Chemicals
Adaptor Proteins, Signal Transducing Calcium-Binding Proteins DLL4 protein, human Intercellular Signaling Peptides and Proteins Membrane Proteins Receptors, Cell Surface Recombinant Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
De Biasio Alfredo
Protein Structure and Bioinformatics Group, International Centre for Genetic Engineering and Biotechnology (ICGEB), AREA Science Park, Padriciano 99, I-34012 Trieste, Italy.
Guarnaccia Corrado
Popovic Matija
Uversky Vladimir N
Pintar Alessandro
Pongor Sándor
References (51)
51 references, click to expand
  1. Protein disorder prediction: implications for structural proteomics.
    Structure. 2003 Nov;11(11):1453-9 PMID: 14604535
  2. The intracellular region of the Notch ligand Jagged-1 gains partial structure upon binding to synthetic membranes.
    FEBS J. 2007 Oct;274(20):5325-36 PMID: 17892488
  3. The C-terminal PDZ-ligand of JAGGED1 is essential for cellular transformation.
    J Biol Chem. 2003 Mar 7;278(10):8771-9 PMID: 12496248
  4. The Notch ligands, Delta1 and Jagged2, are substrates for presenilin-dependent "gamma-secretase" cleavage.
    J Biol Chem. 2003 Mar 7;278(10):7751-4 PMID: 12551931
  5. The roles of receptor and ligand endocytosis in regulating Notch signaling.
    Development. 2005 Apr;132(8):1751-62 PMID: 15790962
  6. Intrinsically unstructured proteins and their functions.
    Nat Rev Mol Cell Biol. 2005 Mar;6(3):197-208 PMID: 15738986
  7. Intracellular pH topography: determination by a fluorescent probe.
    FEBS Lett. 1983 Jun 13;156(2):227-30 PMID: 6852257
  8. The Protein Data Bank.
    Nucleic Acids Res. 2000 Jan 1;28(1):235-42 PMID: 10592235
  9. Human transcription factors contain a high fraction of intrinsically disordered regions essential for transcriptional regulation.
    J Mol Biol. 2006 Jun 16;359(4):1137-49 PMID: 16697407
  10. Intrinsic disorder in cell-signaling and cancer-associated proteins.
    J Mol Biol. 2002 Oct 25;323(3):573-84 PMID: 12381310
  11. Sequence complexity of disordered protein.
    Proteins. 2001 Jan 1;42(1):38-48 PMID: 11093259
  12. Crossing paths with Notch in the hyper-network.
    Curr Opin Cell Biol. 2007 Apr;19(2):166-75 PMID: 17317139
  13. Data growth and its impact on the SCOP database: new developments.
    Nucleic Acids Res. 2008 Jan;36(Database issue):D419-25 PMID: 18000004
  14. Lipid-binding activity of intrinsically unstructured cytoplasmic domains of multichain immune recognition receptor signaling subunits.
    Biochemistry. 2006 Dec 26;45(51):15731-9 PMID: 17176095
  15. Why are "natively unfolded" proteins unstructured under physiologic conditions?
    Proteins. 2000 Nov 15;41(3):415-27 PMID: 11025552
  16. Intrinsically disordered regions of human plasma membrane proteins preferentially occur in the cytoplasmic segment.
    J Mol Biol. 2007 May 4;368(3):902-13 PMID: 17368479
  17. Accuracy of protein flexibility predictions.
    Proteins. 1994 Jun;19(2):141-9 PMID: 8090708
  18. Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues.
    Nature. 1989 Oct 5;341(6241):456-8 PMID: 2677744
  19. Protein secondary structure prediction based on position-specific scoring matrices.
    J Mol Biol. 1999 Sep 17;292(2):195-202 PMID: 10493868
  20. PDZ domains - common players in the cell signaling.
    Acta Biochim Pol. 2003;50(4):985-1017 PMID: 14739991
  21. Prediction and functional analysis of native disorder in proteins from the three kingdoms of life.
    J Mol Biol. 2004 Mar 26;337(3):635-45 PMID: 15019783
  22. DNAWorks: an automated method for designing oligonucleotides for PCR-based gene synthesis.
    Nucleic Acids Res. 2002 May 15;30(10):e43 PMID: 12000848
  23. Predicting intrinsic disorder from amino acid sequence.
    Proteins. 2003;53 Suppl 6:566-72 PMID: 14579347
  24. Evaluation and improvement of multiple sequence methods for protein secondary structure prediction.
    Proteins. 1999 Mar 1;34(4):508-19 PMID: 10081963
  25. What does it mean to be natively unfolded?
    Eur J Biochem. 2002 Jan;269(1):2-12 PMID: 11784292
  26. The intracellular region of Notch ligands: does the tail make the difference?
    Biol Direct. 2007 Jul 10;2:19 PMID: 17623096
  27. Determination of the helix and beta form of proteins in aqueous solution by circular dichroism.
    Biochemistry. 1974 Jul 30;13(16):3350-9 PMID: 4366945
  28. Intrinsic disorder in transcription factors.
    Biochemistry. 2006 Jun 6;45(22):6873-88 PMID: 16734424
  29. The Delta intracellular domain mediates TGF-beta/Activin signaling through binding to Smads and has an important bi-directional function in the Notch-Delta signaling pathway.
    Nucleic Acids Res. 2007;35(3):912-22 PMID: 17251195
  30. SMART 5: domains in the context of genomes and networks.
    Nucleic Acids Res. 2006 Jan 1;34(Database issue):D257-60 PMID: 16381859
  31. The Notch ligand Delta1 is sequentially cleaved by an ADAM protease and gamma-secretase.
    Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7638-43 PMID: 12794186
  32. Use of fast protein size-exclusion liquid chromatography to study the unfolding of proteins which denature through the molten globule.
    Biochemistry. 1993 Dec 7;32(48):13288-98 PMID: 8241185
  33. Structural disorder throws new light on moonlighting.
    Trends Biochem Sci. 2005 Sep;30(9):484-9 PMID: 16054818
  34. Probability-based protein secondary structure identification using combined NMR chemical-shift data.
    Protein Sci. 2002 Apr;11(4):852-61 PMID: 11910028
  35. The notch ligand Delta1 recruits Dlg1 at cell-cell contacts and regulates cell migration.
    J Biol Chem. 2004 Dec 31;279(53):55818-26 PMID: 15485825
  36. Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis.
    Nature. 2006 Dec 21;444(7122):1083-7 PMID: 17183323
  37. Evidence for horizontal gene transfer in Escherichia coli speciation.
    J Mol Biol. 1991 Dec 20;222(4):851-6 PMID: 1762151
  38. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure.
    J Mol Biol. 1991 Nov 20;222(2):311-33 PMID: 1960729
  39. DICHROWEB: an interactive website for the analysis of protein secondary structure from circular dichroism spectra.
    Bioinformatics. 2002 Jan;18(1):211-2 PMID: 11836237
  40. The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins.
    J Mol Biol. 2005 Apr 8;347(4):827-39 PMID: 15769473
  41. DisProt: the Database of Disordered Proteins.
    Nucleic Acids Res. 2007 Jan;35(Database issue):D786-93 PMID: 17145717
  42. Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis.
    Nature. 2006 Dec 21;444(7122):1032-7 PMID: 17183313
  43. The Notch ligands, Jagged and Delta, are sequentially processed by alpha-secretase and presenilin/gamma-secretase and release signaling fragments.
    J Biol Chem. 2003 Sep 5;278(36):34427-37 PMID: 12826675
  44. Notch signaling: cell fate control and signal integration in development.
    Science. 1999 Apr 30;284(5415):770-6 PMID: 10221902
  45. Mechanism by which 2,2,2-trifluoroethanol/water mixtures stabilize secondary-structure formation in peptides: a molecular dynamics study.
    Proc Natl Acad Sci U S A. 2002 Sep 17;99(19):12179-84 PMID: 12196631
  46. Electric fields at the plasma membrane level: a neglected element in the mechanisms of cell signalling.
    Bioessays. 1996 Jun;18(6):495-504 PMID: 8787537
  47. Improving the prediction of protein secondary structure in three and eight classes using recurrent neural networks and profiles.
    Proteins. 2002 May 1;47(2):228-35 PMID: 11933069
  48. Analysis of molecular recognition features (MoRFs).
    J Mol Biol. 2006 Oct 6;362(5):1043-59 PMID: 16935303
  49. Intrinsically disordered protein.
    J Mol Graph Model. 2001;19(1):26-59 PMID: 11381529
  50. Notch signalling: a simple pathway becomes complex.
    Nat Rev Mol Cell Biol. 2006 Sep;7(9):678-89 PMID: 16921404
  51. Composition Profiler: a tool for discovery and visualization of amino acid composition differences.
    BMC Bioinformatics. 2007 Jun 19;8:211 PMID: 17578581
Article Info
Journal
Journal of proteome research
Abbr.
J Proteome Res
ISSN
1535-3893
Published
2008-06-00
Epub
2008-00-25
Pages
2496-506
Language
English
Region
United States
NLM ID
101128775
PMCID
PMC2743940
Subset
IM
Grants
NIGMS NIH HHS · R01 GM071714 · United States
NIGMS NIH HHS · R01 GM071714-03 · United States
NLM NIH HHS · R01 LM007688 · United States
NLM NIH HHS · R01 LM007688-01A1S1 · United States
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