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Phylogenetic, Structural and Functional Relationships between WD- and Kelch-Repeat Proteins

  • Andrew M. Hudson
  • Lynn CooleyEmail author
Part of the Subcellular Biochemistry book series (SCBI, volume 48)

Abstract

The β-propeller domain is a widespread protein organizational motif. Typically, β-propeller proteins are encoded by repeated sequences where each repeat unit corresponds to a twisted β-sheet structural motif; these β-sheets are arranged in a circle around a central axis to generate the β-propeller structure. Two superfamilies of β-propeller proteins, the WD-repeat and Kelch-repeat families, exhibit similarities not only in structure, but, remarkably, also in the types of molecular functions they perform. While it is unlikely that WD and Kelch repeats evolved from a common ancestor, their evolution into diverse families of similar function may reflect the evolutionary advantages of the stable core β-propeller fold. In this chapter, we examine the relationships between these two widespread protein families, emphasizing recently published work relating to the structure and fucntion of both Kelch and WD-repeat proteins.

Keywords

Horseshoe Crab Galactose Oxidase Substrate Adaptor Ring Domain Protein Coronin Protein 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Neer E, Schmidt C, Nambudripad R et al. The ancient regulatory-protein family of WD-repeat proteins. Nature 1994; 371(6495):297–300.PubMedCrossRefGoogle Scholar
  2. 2.
    Way M, Sanders M, Garcia C et al. Sequence and domain organization of scruin, an actin-cross-linking protein in the acrosomal process of Limulus sperm. J Cell Biol 1995; 128(1–2):51–60.PubMedCrossRefGoogle Scholar
  3. 3.
    Xue F, Cooley L. kelch encodes a component of intercellular bridges in Drosophila egg chambers. Cell 1993; 72(5):681–693.PubMedCrossRefGoogle Scholar
  4. 4.
    Li D, Roberts R. WD-repeat proteins: structure characteristics, biological function and their involvement in human diseases. Cell Mol Life Sci 2001; 58(14):2085–2097.PubMedCrossRefGoogle Scholar
  5. 5.
    Smith T, Gaitatzes C, Saxena K et al. The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 1999; 24(5):181–185.PubMedCrossRefGoogle Scholar
  6. 6.
    Yu L, Gaitatzes C, Neer E et al. Thirty-plus functional families from a single motif. Protein Sci 2000; 9(12):2470–2476.PubMedCrossRefGoogle Scholar
  7. 7.
    Adams J, Kelso R, Cooley L. The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol 2000; 10(1):17–24.PubMedCrossRefGoogle Scholar
  8. 8.
    Prag S, Adams J. Molecular phylogeny of the kelch-repeat superfamily reveals an expansion of BTB/kelch proteins in animals. BMC Bioinformatics 2003; 4:42.PubMedCrossRefGoogle Scholar
  9. 9.
    Madrona A, Wilson D. The structure of Ski8p, a protein regulating mRNA degradation: Implications for WD protein structure. Protein Sci 2004; 13(6):1557–1565.PubMedCrossRefGoogle Scholar
  10. 10.
    Ito N, Phillips SE, Stevens C et al. Novel thioether bond revealed by a 1.7 A crystal structure of galactose oxidase. Nature 1991; 350(6313):87–90.PubMedCrossRefGoogle Scholar
  11. 11.
    Lambright DG, Sondek J, Bohm A et al. The 2.0 A crystal structure of a heterotrimeric G protein. Nature 1996; 379(6563):311–319.PubMedCrossRefGoogle Scholar
  12. 12.
    Sondek J, Bohm A, Lambright DG et al. Crystal structure of a G-protein beta gamma dimer at 2.1A resolution. Nature 1996; 379(6563):369–374.PubMedCrossRefGoogle Scholar
  13. 13.
    Li X, Zhang D, Hannink M et al. Crystal structure of the Kelch domain of human Keap1. J Biol Chem 2004; 279(52):54750–54758.PubMedCrossRefGoogle Scholar
  14. 14.
    Padmanabhan B, Tong K, Ohta T et al. Structural basis for defects of Keap1 activity provoked by its point mutations in lung cancer. Mol Cell 2006; 21(5):689–700.PubMedCrossRefGoogle Scholar
  15. 15.
    Wall M, Coleman D, Lee E et al. The structure of the G protein heterotrimer Gi alpha 1 beta 1 gamma 2. Cell 1995; 83(6):1047–1058.PubMedCrossRefGoogle Scholar
  16. 16.
    Beamer L, Li X, Bottoms C et al. Conserved solvent and side-chain interactions in the 1.35 Angstrom structure of the Kelch domain of Keap1. Acta Crystallogr D Biol Crystallogr 2005; 61(Pt 10):1335–1342.PubMedCrossRefGoogle Scholar
  17. 17.
    Bork P, Doolittle R. Drosophila kelch motif is derived from a common enzyme fold. J Mol Biol 1994; 236(5):1277–1282.PubMedCrossRefGoogle Scholar
  18. 18.
    Paoli M. Protein folds propelled by diversity. Prog Biophys Mol Biol 2001; 76(1–2):103–130.PubMedCrossRefGoogle Scholar
  19. 19.
    Jawad-Alami Z, Paoli M. Novel sequences propel familiar folds. Structure 2002; 10(4):447–454.CrossRefGoogle Scholar
  20. 20.
    Murzin A. Structural principles for the propeller assembly of beta-sheets: the preference for seven-fold symmetry. Proteins 1992; 14(2):191–201.PubMedCrossRefGoogle Scholar
  21. 21.
    Beisel H, Kawabata S, Iwanaga S et al. Tachylectin-2: crystal structure of a specific GlcNAc/GalNAc-binding lectin involved in the innate immunity host defense of the Japanese horseshoe crab Tachypleus tridentatus. EMBO J 1999; 18(9):2313–2322.PubMedCrossRefGoogle Scholar
  22. 22.
    Kiyosue T, Wada M. LKP1 (LOV kelch protein 1): a factor involved in the regulation of flowering time in arabidopsis. Plant J 2000; 23(6):807–815.PubMedCrossRefGoogle Scholar
  23. 23.
    Nelson D, Lasswell J, Rogg L et al. FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 2000; 101(3):331–340.PubMedCrossRefGoogle Scholar
  24. 24.
    Somers DE, Schultz TF, Milnamow M et al. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 2000; 101(3):319–329.PubMedCrossRefGoogle Scholar
  25. 25.
    Finn RD, Mistry J, Schuster-Bockler B et al. Pfam: clans, web tools and services. Nucleic Acids Res 2006; 34(Database issue):D247–251.PubMedCrossRefGoogle Scholar
  26. 26.
    Larsen N, Harrison S. Crystal structure of the spindle assembly checkpoint protein Bub3. J Mol Biol 2004; 344(4):885–892.PubMedCrossRefGoogle Scholar
  27. 27.
    Voegtli W, Madrona A, Wilson D. The structure of Aip1p, a WD repeat protein that regulates Cofilin-mediated actin depolymerization. J Biol Chem 2003; 278(36):34373–34379.PubMedCrossRefGoogle Scholar
  28. 28.
    Wilson D, Cerna D, Chew E. The 1.1-angstrom structure of the spindle checkpoint protein Bub3p reveals functional regions. J Biol Chem 2005; 280(14):13944–13951.PubMedCrossRefGoogle Scholar
  29. 29.
    Orlicky S, Tang X, Willems A et al. Structural basis for phosphodependent substrate selection and orientation by the SCFCdc4 ubiquitin ligase. Cell 2003; 112(2):243–256.PubMedCrossRefGoogle Scholar
  30. 30.
    Garcia-Higuera I, Gaitatzes C, Smith T et al. Folding a WD repeat propeller. Role of highly conserved aspartic acid residues in the G protein beta subunit and Sec13. J Biol Chem 1998; 273(15):9041–9049.PubMedCrossRefGoogle Scholar
  31. 31.
    Owen C, DeRosier D. A 13-A map of the actin-scruin filament from the limulus acrosomal process. J Cell Biol 1993; 123(2):337–344.PubMedCrossRefGoogle Scholar
  32. 32.
    Andrade M, González-Guzmán M, Serrano R et al. A combination of the F-box motif and kelch repeats defines a large Arabidopsis family of F-box proteins. Plant Mol Biol 2001; 46(5):603–614.PubMedCrossRefGoogle Scholar
  33. 33.
    Kuroda H, Takahashi N, Shimada H et al. Classification and expression analysis of Arabidopsis F-box-containing protein genes. Plant Cell Physiol 2002; 43(10):1073–1085.PubMedCrossRefGoogle Scholar
  34. 34.
    Jennings B, Pickles L, Wainwright S et al. Molecular recognition of transcriptional repressor motifs by the WD domain of the Groucho/TLE corepressor. Mol Cell 2006; 22(5):645–655.PubMedCrossRefGoogle Scholar
  35. 35.
    Tarricone C, Perrina F, Monzani S et al. Coupling PAF signaling to dynein regulation: structure of LIS1 in complex with PAF-acetylhydrolase. Neuron 2004; 44(5):809–821.PubMedGoogle Scholar
  36. 36.
    Robinson R, Turbedsky K, Kaiser D et al. Crystal structure of Arp2/3 complex. Science 2001; 294(5547):1679–1684.PubMedCrossRefGoogle Scholar
  37. 37.
    Beltzner C, Pollard T. Identification of functionally important residues of Arp2/3 complex by analysis of homology models from diverse species. J Mol Biol 2004; 336(2):551–565.PubMedCrossRefGoogle Scholar
  38. 38.
    Lo S, Li X, Henzl M et al. Structure of the Keap1: Nrf2 interface provides mechanistic insight into Nrf2 signaling. EMBO J 2006; 25(15):3605–3617.PubMedCrossRefGoogle Scholar
  39. 39.
    Cullinan SB, Gordan JD, Jin J et al. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol Cell Biol 2004; 24(19):8477–8486.PubMedCrossRefGoogle Scholar
  40. 40.
    Kobayashi A, Kang MI, Okawa H et al. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol 2004; 24(16):7130–7139.PubMedCrossRefGoogle Scholar
  41. 41.
    Zhang DD, Lo SC, Cross JV et al. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol Cell Biol 2004; 24(24):10941–10953.PubMedCrossRefGoogle Scholar
  42. 42.
    Petroski M, Deshaies R. Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 2005; 6(1):9–20.PubMedCrossRefGoogle Scholar
  43. 43.
    Patton E, Willems A, Tyers M. Combinatorial control in ubiquitin-dependent proteolysis: don’t Skp the F-box hypothesis. Trends Genet 1998; 14(6):236–243.PubMedCrossRefGoogle Scholar
  44. 44.
    Han L, Mason M, Risseeuw E et al. Formation of an SCF(ZTL) complex is required for proper regulation of circadian timing. Plant J 2004; 40(2):291–301.PubMedCrossRefGoogle Scholar
  45. 45.
    Imaizumi T, Schultz T, Harmon F et al. FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 2005; 309(5732):293–297.PubMedCrossRefGoogle Scholar
  46. 46.
    Sawa M, Nusinow D, Kay S et al. FKF1 and GIGANTEA Complex Formation is Required for Day-Length Measurement in Arabidopsis. Science 2007; 318(5848):261–265.PubMedCrossRefGoogle Scholar
  47. 47.
    Stogios P, Downs G, Jauhal J et al. Sequence and structural analysis of BTB domain proteins. Genome Biol 2005; 6(10):R82.PubMedCrossRefGoogle Scholar
  48. 48.
    Xu L, Wei Y, Reboul J et al. BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 2003; 425(6955):316–321.PubMedCrossRefGoogle Scholar
  49. 49.
    Rybakin V, Clemen C. Coronin proteins as multifunctional regulators of the cytoskeleton and membrane trafficking. Bioessays 2005; 27(6):625–632.PubMedCrossRefGoogle Scholar
  50. 50.
    Uetrecht A, Bear J. Coronins: the return of the crown. Trends Cell Biol 2006; 16(8):421–426.PubMedCrossRefGoogle Scholar
  51. 51.
    Ono S. Regulation of actin filament dynamics by actin depolymerizing factor/cofilin and actin-interacting protein 1: new blades for twisted filaments. Biochemistry 2003; 42(46):13363–13370.PubMedCrossRefGoogle Scholar
  52. 52.
    Xiang X. LIS1 at the microtubule plus end and its role in dynein-mediated nuclear migration. J Cell Biol 2003; 160(3):289–290.PubMedCrossRefGoogle Scholar
  53. 53.
    McNally KP, Bazirgan OA, McNally FJ. Two domains of p80 katanin regulate microtubule severing and spindle pole targeting by p60 katanin. J Cell Sci 2000; 113(Pt 9):1623–1633.PubMedGoogle Scholar
  54. 54.
    Kelso R, Hudson A, Cooley L. Drosophila Kelch regulates actin organization via Src64-dependent tyrosine phosphorylation. J Cell Biol 2002; 156(4):703–713.PubMedCrossRefGoogle Scholar
  55. 55.
    Sun S, Footer M, Matsudaira P. Modification of Cys-837 identifies an actin-binding site in the betapropeller protein scruin. Mol Biol Cell 1997; 8(3):421–430.PubMedGoogle Scholar
  56. 56.
    Soltysik-Espanola M, Rogers RA, Jiang S et al. Characterization of Mayven, a novel actin-binding protein predominantly expressed in brain. Mol Biol Cell 1999; 10(7):2361–2375.PubMedGoogle Scholar
  57. 57.
    Kim IF, Mohammadi E, Huang RC. Isolation and characterization of IPP, a novel human gene encoding an actin-binding, kelch-like protein. Gene 1999; 228(1–2):73–83.PubMedCrossRefGoogle Scholar
  58. 58.
    Hernandez MC, Andres-Barquin PJ, Martinez S et al. ENC-1: a novel mammalian kelch-related gene specifically expressed in the nervous system encodes an actin-binding protein. J Neurosci 1997; 17(9):3038–3051.PubMedGoogle Scholar
  59. 59.
    Eichinger L, Bomblies L, Vandekerckhove J et al. A novel type of protein kinase phosphorylates actin in the actin-fragmin complex. EMBO J 1996; 15(20):5547–5556.PubMedGoogle Scholar
  60. 60.
    Steinbacher S, Hof P, Eichinger L et al. The crystal structure of the Physarum polycephalum actinfragmin kinase: an atypical protein kinase with a specialized substrate-binding domain. EMBO J 1999; 18(11):2923–2929.PubMedCrossRefGoogle Scholar
  61. 61.
    Lecuyer C, Dacheux JL, Hermand E et al. Actin-binding properties and colocalization with actin during spermiogenesis of mammalian sperm calicin. Biol Reprod 2000; 63(6):1801–1810.PubMedCrossRefGoogle Scholar
  62. 62.
    Mata J, Nurse P. teal and the microtubular cytoskeleton are important for generating global spatial order within the fission yeast cell. Cell 1997; 89(6):939–949.PubMedCrossRefGoogle Scholar
  63. 63.
    The PyMOL Molecular Graphics System (http://www.pymol.org) [computer program]. Version 0.99: DeLano Scientific, Palo Alto, CA; 2002.Google Scholar
  64. 64.
    Nolen B, Pollard T. Insights into the influence of nucleotides on actin family proteins from seven structures of Arp2/3 complex. Mol Cell 2007; 26(3):449–457.PubMedCrossRefGoogle Scholar
  65. 65.
    Wu G, Xu G, Schulman B et al. Structure of a beta-TrCP1-Skp1-beta-catenin complex: destruction motif binding and lysine specificity of the SCF(beta-TrCP1) ubiquitin ligase. Mol Cell 2003; 11(6):1445–1456.PubMedCrossRefGoogle Scholar
  66. 66.
    Appleton B, Wu P, Wiesmann C. The crystal structure of murine coronin-1: a regulator of actin cytoskeletal dynamics inlymphocytes. Structure 2006; 14(1):87–96.PubMedCrossRefGoogle Scholar
  67. 67.
    Pickles L, Roe S, Hemingway E et al. Crystal structure of the C-terminal WD40 repeat domain of the human Groucho/TLE1 transcriptional corepressor. Structure 2002; 10(6):751–761.PubMedCrossRefGoogle Scholar
  68. 68.
    Cerna D, Wilson D. The structure of Sif2p, a WD repeat protein functioning in the SET3 corepressor complex. J Mol Biol 2005; 351(4):923–935.PubMedCrossRefGoogle Scholar
  69. 69.
    Cheng Z, Liu Y, Wang C et al. Crystal structure of Ski8p, a WD-repeat protein with dual roles in mRNA metabolism and meiotic recombination. Protein Sci 2004; 13(10):2673–2684.PubMedCrossRefGoogle Scholar
  70. 70.
    Sprague E, Redd M, Johnson A et al. Structure of the C-terminal domain of Tup1, a corepressor of transcription in yeast. EMBO J 2000; 19(12):3016–3027.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2008

Authors and Affiliations

  1. 1.Department of GeneticsYale University School of MedicineNew HavenUSA

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