Home LiteratureArticle Details
PMID: 15840729 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Scanning the human proteome for calmodulin-binding proteins.

Shen X, Valencia CA, Szostak JW, Szostak J, Dong B, Liu R

Abstract

The calcium ion (Ca(2+)) is a ubiquitous second messenger that is crucial for the regulation of a wide variety of cellular processes. The diverse transient signals transduced by Ca(2+) are mediated by intracellular Ca(2+)-binding proteins, also known as Ca(2+) sensors. A key obstacle to studying many Ca(2+)-sensing proteins is the difficulty in identifying the numerous downstream target interactions that respond to Ca(2+)-induced conformational changes. Among a number of Ca(2+) sensors in the eukaryotic cell, calmodulin (CaM) is the most widespread and the best studied. Employing the mRNA display technique, we have scanned the human proteome for CaM-binding proteins and have identified and characterized a large number of both known and previously uncharacterized proteins that interact with CaM in a Ca(2+)-dependent manner. The interactions of several identified proteins with Ca(2+)/CaM were confirmed by using pull-down assays and coimmunoprecipitation. Many of the CaM-binding proteins identified belong to protein families such as the DEAD/H box proteins, ribosomal proteins, proteasome 26S subunits, and deubiquitinating enzymes, suggesting the possible involvement of Ca(2+)/CaM in different signaling pathways. The selection method described herein could be used to identify the binding partners of other calcium sensors on the proteome-wide scale.

MeSH Terms
Binding Sites Calmodulin-Binding Proteins/analysis,genetics,metabolism Cloning, Molecular HeLa Cells Humans Proteome/genetics
Chemicals
Calmodulin-Binding Proteins Proteome
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Shen Xinchun
Division of Medicinal Chemistry and Natural Products, School of Pharmacy, and Carolina Center for Genome Sciences, University of North Carolina, Chapel Hill, NC 27599, USA.
Valencia C Alexander
Szostak Jack W
Szostak Jack
Dong Biao
Liu Rihe
References (49)
49 references, click to expand
  1. Rad23 promotes the targeting of proteolytic substrates to the proteasome.
    Mol Cell Biol. 2002 Jul;22(13):4902-13 PMID: 12052895
  2. Genes encoding calmodulin-binding proteins in the Arabidopsis genome.
    J Biol Chem. 2002 Mar 22;277(12):9840-52 PMID: 11782485
  3. CaMBOT: profiling and characterizing calmodulin-binding proteins.
    Cell Signal. 2003 Apr;15(4):347-54 PMID: 12618209
  4. mRNA display: ligand discovery, interaction analysis and beyond.
    Trends Biochem Sci. 2003 Mar;28(3):159-65 PMID: 12633996
  5. Calmodulin target database.
    J Struct Funct Genomics. 2000;1(1):8-14 PMID: 12836676
  6. Calcium signalling: dynamics, homeostasis and remodelling.
    Nat Rev Mol Cell Biol. 2003 Jul;4(7):517-29 PMID: 12838335
  7. Regulation of cell death: the calcium-apoptosis link.
    Nat Rev Mol Cell Biol. 2003 Jul;4(7):552-65 PMID: 12838338
  8. Calmodulin is a phospholipase C-beta interacting protein.
    J Biol Chem. 2003 Sep 5;278(36):33708-13 PMID: 12821674
  9. A protein interaction map of Drosophila melanogaster.
    Science. 2003 Dec 5;302(5651):1727-36 PMID: 14605208
  10. A map of the interactome network of the metazoan C. elegans.
    Science. 2004 Jan 23;303(5657):540-3 PMID: 14704431
  11. DEAD-box proteins: the driving forces behind RNA metabolism.
    Nat Rev Mol Cell Biol. 2004 Mar;5(3):232-41 PMID: 14991003
  12. Multiubiquitin chain receptors define a layer of substrate selectivity in the ubiquitin-proteasome system.
    Cell. 2004 Jul 9;118(1):99-110 PMID: 15242647
  13. Calmodulin and Munc13 form a Ca2+ sensor/effector complex that controls short-term synaptic plasticity.
    Cell. 2004 Aug 6;118(3):389-401 PMID: 15294163
  14. Calmodulin-mediated activation of Akt regulates survival of c-Myc-overexpressing mouse mammary carcinoma cells.
    J Biol Chem. 2004 Sep 10;279(37):38903-11 PMID: 15247222
  15. A complex between peptide:N-glycanase and two proteasome-linked proteins suggests a mechanism for the degradation of misfolded glycoproteins.
    Proc Natl Acad Sci U S A. 2004 Sep 21;101(38):13774-9 PMID: 15358861
  16. A network of control mediated by regulator of calcium/calmodulin-dependent signaling.
    Science. 2004 Oct 22;306(5696):698-701 PMID: 15499021
  17. Calmodulin binding domains: characterization of a phosphorylation and calmodulin binding site from myosin light chain kinase.
    Biochemistry. 1986 Mar 25;25(6):1458-64 PMID: 3754463
  18. Calmodulin binding by calcineurin. Ligand-induced renaturation of protein immobilized on nitrocellulose.
    J Biol Chem. 1987 Nov 5;262(31):15062-70 PMID: 2822712
  19. How calmodulin binds its targets: sequence independent recognition of amphiphilic alpha-helices.
    Trends Biochem Sci. 1990 Feb;15(2):59-64 PMID: 2186516
  20. A ribosomal calmodulin-binding protein from Dictyostelium.
    J Biol Chem. 1991 Dec 5;266(34):23091-6 PMID: 1744106
  21. D-E-A-D protein family of putative RNA helicases.
    Mol Microbiol. 1992 Feb;6(3):283-91 PMID: 1552844
  22. Selection of targeted biological modifiers from a bacteriophage library of random peptides. The identification of novel calmodulin regulatory peptides.
    J Biol Chem. 1993 Nov 5;268(31):23025-30 PMID: 8226817
  23. Calmodulin-binding domains: just two faced or multi-faceted?
    Trends Biochem Sci. 1995 Jan;20(1):38-42 PMID: 7878743
  24. Calcium signaling in neurons: molecular mechanisms and cellular consequences.
    Science. 1995 Apr 14;268(5208):239-47 PMID: 7716515
  25. Molecular and structural basis of target recognition by calmodulin.
    Annu Rev Biophys Biomol Struct. 1995;24:85-116 PMID: 7663132
  26. The elemental principles of calcium signaling.
    Cell. 1995 Dec 1;83(5):675-8 PMID: 8521483
  27. Calcium binding and conformational response in EF-hand proteins.
    Trends Biochem Sci. 1996 Jan;21(1):14-7 PMID: 8848832
  28. Sequence motifs for calmodulin recognition.
    FASEB J. 1997 Apr;11(5):331-40 PMID: 9141499
  29. RNA-peptide fusions for the in vitro selection of peptides and proteins.
    Proc Natl Acad Sci U S A. 1997 Nov 11;94(23):12297-302 PMID: 9356443
  30. Investigating the importance of proteasome-interaction for Rad23 function.
    Curr Genet. 2003 Jan;42(4):199-208 PMID: 12589471
  31. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae.
    Nature. 2000 Feb 10;403(6770):623-7 PMID: 10688190
  32. Rad23 links DNA repair to the ubiquitin/proteasome pathway.
    Nature. 1998 Feb 12;391(6668):715-8 PMID: 9490418
  33. New nuclear functions for calmodulin.
    Cell Calcium. 1998 Feb-Mar;23(2-3):115-21 PMID: 9601606
  34. Modulation of calmodulin function by ubiquitin-calmodulin ligase and identification of the responsible ubiquitylation site in vertebrate calmodulin.
    Eur J Biochem. 1998 Jul 15;255(2):422-31 PMID: 9716384
  35. Demonstration of heterodimer formation between S100B and S100A6 in the yeast two-hybrid system and human melanoma.
    Exp Cell Res. 1999 Feb 1;246(2):501-9 PMID: 9925766
  36. A mutant deubiquitinating enzyme (Ubp-M) associates with mitotic chromosomes and blocks cell division.
    Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):2828-33 PMID: 10077596
  37. Uch2/Uch37 is the major deubiquitinating enzyme associated with the 26S proteasome in fission yeast.
    J Mol Biol. 2004 Nov 26;344(3):697-706 PMID: 15533439
  38. Rad23 and Rpn10: perennial wallflowers join the melee.
    Trends Biochem Sci. 2004 Dec;29(12):637-40 PMID: 15544949
  39. Regulation of p68 RNA helicase by calmodulin and protein kinase C.
    J Biol Chem. 1994 Nov 25;269(47):29367-70 PMID: 7525583
  40. Calcium signaling.
    Cell. 1995 Jan 27;80(2):259-68 PMID: 7834745
  41. Constructing high complexity synthetic libraries of long ORFs using in vitro selection.
    J Mol Biol. 2000 Mar 24;297(2):309-19 PMID: 10715203
  42. Calmodulin: a prototypical calcium sensor.
    Trends Cell Biol. 2000 Aug;10(8):322-8 PMID: 10884684
  43. Ca2+-free calmodulin and calmodulin damaged by in vitro aging are selectively degraded by 26 S proteasomes without ubiquitination.
    J Biol Chem. 2000 Jul 7;275(27):20295-301 PMID: 10791958
  44. Optimized synthesis of RNA-protein fusions for in vitro protein selection.
    Methods Enzymol. 2000;318:268-93 PMID: 10889994
  45. Psoralen photo-crosslinked mRNA-puromycin conjugates: a novel template for the rapid and facile preparation of mRNA-protein fusions.
    Nucleic Acids Res. 2000 Sep 15;28(18):E83 PMID: 10982894
  46. S100A6 and S100A11 are specific targets of the calcium- and zinc-binding S100B protein in vivo.
    J Biol Chem. 2000 Nov 10;275(45):35302-10 PMID: 10913138
  47. Generation, control, and processing of cellular calcium signals.
    Crit Rev Biochem Mol Biol. 2001 Apr;36(2):107-260 PMID: 11370791
  48. In vitro selection and characterization of Bcl-X(L)-binding proteins from a mix of tissue-specific mRNA display libraries.
    J Biol Chem. 2001 Jun 15;276(24):20898-906 PMID: 11283018
  49. Global analysis of protein activities using proteome chips.
    Science. 2001 Sep 14;293(5537):2101-5 PMID: 11474067
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2005-04-26
Epub
2005-00-19
Pages
5969-74
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC1087907
Subset
IM
Grants
NIGMS NIH HHS · R01 GM053936 · United States
NIGMS NIH HHS · GM53936 · United States
Corrections
ErratumIn
-
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