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Structure of human Ki67 FHA domain and its binding to a phosphoprotein fragment from hNIFK reveal unique recognition sites and new views to the structural basis of FHA domain functions.

Li H, Byeon IJ, Ju Y, Tsai MD
J Mol Biol 335 371-81 (2004)
Cited: 33 times
EuropePMC logo PMID: 14659764

Abstract

Recent studies by use of short phosphopeptides showed that forkhead-associated (FHA) domains recognize pTXX(D/I/L) motifs. Solution structures and crystal structures of several different FHA domains and their complexes with short phosphopeptides have been reported by several groups. We now report the solution structure of the FHA domain of human Ki67, a large nuclear protein associated with the cell-cycle. Using fragments of its binding partner hNIFK, we show that Ki67-hNIFK binding involves ca 44 residues without a pTXX(D/I/L) motif. The pThr site of hNIFK recognized by Ki67 FHA is pThr234-Pro235, a motif also recognized by the proline isomerase Pin1. Heteronuclear single quantum coherence (HSQC) NMR was then used to map out the binding surface, and structural analyses were used to identify key binding residues of Ki67 FHA. The results represent the first structural characterization of the complex of an FHA domain with a biologically relevant target protein fragment. Detailed analyses of the results led us to propose that three major factors control the interaction of FHA with its target protein: the pT residue, +1 to +3 residues, and an extended binding surface, and that variation in the three factors is the likely cause of the great diversity in the function and specificity of FHA domains from different sources.

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  2. Diphosphothreonine-specific interaction between an SQ/TQ cluster and an FHA domain in the Rad53-Dun1 kinase cascade. Lee H, Yuan C, Hammet A, Mahajan A, Chen ES, Wu MR, Su MI, Heierhorst J, Tsai MD. Mol Cell 30 767-778 (2008)
  3. Dynamic and structural characterization of a bacterial FHA protein reveals a new autoinhibition mechanism. Barthe P, Roumestand C, Canova MJ, Kremer L, Hurard C, Molle V, Cohen-Gonsaud M. Structure 17 568-578 (2009)
  4. Sequential phosphorylation and multisite interactions characterize specific target recognition by the FHA domain of Ki67. Byeon IJ, Li H, Song H, Gronenborn AM, Tsai MD. Nat Struct Mol Biol 12 987-993 (2005)
  5. Overcoming the solubility limit with solubility-enhancement tags: successful applications in biomolecular NMR studies. Zhou P, Wagner G. J Biomol NMR 46 23-31 (2010)
  6. EDD mediates DNA damage-induced activation of CHK2. Henderson MJ, Munoz MA, Saunders DN, Clancy JL, Russell AJ, Williams B, Pappin D, Khanna KK, Jackson SP, Sutherland RL, Watts CK. J Biol Chem 281 39990-40000 (2006)
  7. Forkhead-associated domain-containing protein Rv0019c and polyketide-associated protein PapA5, from substrates of serine/threonine protein kinase PknB to interacting proteins of Mycobacterium tuberculosis. Gupta M, Sajid A, Arora G, Tandon V, Singh Y. J Biol Chem 284 34723-34734 (2009)
  8. DAWDLE, a forkhead-associated domain gene, regulates multiple aspects of plant development. Morris ER, Chevalier D, Walker JC. Plant Physiol 141 932-941 (2006)
  9. The nucleolar protein NIFK promotes cancer progression via CK1α/β-catenin in metastasis and Ki-67-dependent cell proliferation. Lin TC, Su CY, Wu PY, Lai TC, Pan WA, Jan YH, Chang YC, Yeh CT, Chen CL, Ger LP, Chang HT, Yang CJ, Huang MS, Liu YP, Lin YF, Shyy JY, Tsai MD, Hsiao M. Elife 5 (2016)
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  11. PhosphoThr peptide binding globally rigidifies much of the FHA domain from Arabidopsis receptor kinase-associated protein phosphatase. Ding Z, Lee GI, Liang X, Gallazzi F, Arunima A, Van Doren SR. Biochemistry 44 10119-10134 (2005)
  12. Crystal structure analysis reveals a novel forkhead-associated domain of ESAT-6 secretion system C protein in Staphylococcus aureus. Tanaka Y, Kuroda M, Yasutake Y, Yao M, Tsumoto K, Watanabe N, Ohta T, Tanaka I. Proteins 69 659-664 (2007)
  13. Directed evolution of the forkhead-associated domain to generate anti-phosphospecific reagents by phage display. Pershad K, Wypisniak K, Kay BK. J Mol Biol 424 88-103 (2012)
  14. alpha-Helical burst on the folding pathway of FHA domains from Rad53 and Ki67. Matsumura Y, Shinjo M, Mahajan A, Tsai MD, Kihara H. Biochimie 92 1031-1039 (2010)
  15. Expression of Pin1 and Ki67 in cervical cancer and their significance. Li H, Shen H, Xu Q, Deng D, Wang S, Lu Y, Ma D. J Huazhong Univ Sci Technolog Med Sci 26 120-122 (2006)
  16. Prognostic molecular biomarkers in endometrial cancer: A review. Hernández JE, González-Montiel A, Allos-Villalva JCC, Cantú D, Barquet S, Olivares-Mundo A, Herrera LA, Prada D. J Cancer Res Ther (Manch) 7 17-28 (2019)
  17. Structural insights into the recognition of phosphorylated Hop1 by Mek1. Xie C, He C, Jiang Y, Yu H, Cheng L, Nshogoza G, Ala MS, Tian C, Wu J, Shi Y, Li F. Acta Crystallogr D Struct Biol 74 1027-1038 (2018)
  18. Comparative genomics and interactomics of polyadenylation factors for the prediction of new parasite targets: Entamoeba histolytica as a working model. Avila-Bonilla RG, Velazquez-Guzman JA, Reyes-Zepeda EI, Gutierrez-Avila JL, Reyes-López CA, Cisneros-Sarabia A, Saavedra E, Lopéz-Sandoval A, Ramírez-Moreno E, López-Camarillo C, Marchat LA. Biosci Rep 43 BSR20221911 (2023)


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