2aff Citations

Sequential phosphorylation and multisite interactions characterize specific target recognition by the FHA domain of Ki67.

Nat Struct Mol Biol 12 987-93 (2005)
Cited: 51 times
EuropePMC logo PMID: 16244663

Abstract

The forkhead-associated (FHA) domain of human Ki67 interacts with the human nucleolar protein hNIFK, recognizing a 44-residue fragment, hNIFK226-269, phosphorylated at Thr234. Here we show that high-affinity binding requires sequential phosphorylation by two kinases, CDK1 and GSK3, yielding pThr238, pThr234 and pSer230. We have determined the solution structure of Ki67FHA in complex with the triply phosphorylated peptide hNIFK226-269(3P), revealing not only local recognition of pThr234 but also the extension of the beta-sheet of the FHA domain by the addition of a beta-strand of hNIFK. The structure of an FHA domain in complex with a biologically relevant binding partner provides insights into ligand specificity and potentially links the cancer marker protein Ki67 to a signaling pathway associated with cell fate specification.

Reviews - 2aff mentioned but not cited (1)

  1. Mechanistic insights into phosphoprotein-binding FHA domains. Liang X, Van Doren SR. Acc Chem Res 41 991-999 (2008)

Articles - 2aff mentioned but not cited (11)

  1. Charge environments around phosphorylation sites in proteins. Kitchen J, Saunders RE, Warwicker J. BMC Struct Biol 8 19 (2008)
  2. EssC: domain structures inform on the elusive translocation channel in the Type VII secretion system. Zoltner M, Ng WM, Money JJ, Fyfe PK, Kneuper H, Palmer T, Hunter WN. Biochem J 473 1941-1952 (2016)
  3. Structural and functional studies on the N-terminal domain of the Shigella type III secretion protein MxiG. McDowell MA, Johnson S, Deane JE, Cheung M, Roehrich AD, Blocker AJ, McDonnell JM, Lea SM. J Biol Chem 286 30606-30614 (2011)
  4. Structure and interactions of the cytoplasmic domain of the Yersinia type III secretion protein YscD. Gamez A, Mukerjea R, Alayyoubi M, Ghassemian M, Ghosh P. J Bacteriol 194 5949-5958 (2012)
  5. Dl-3-n-butylphthalide inhibits neuroinflammation by stimulating foxp3 and Ki-67 in an ischemic stroke model. Liu X, Liu R, Fu D, Wu H, Zhao X, Sun Y, Wang M, Pu X. Aging (Albany NY) 13 3763-3778 (2021)
  6. Mechanism of PhosphoThreonine/Serine Recognition and Specificity for Modular Domains from All-atom Molecular Dynamics. Huang YM, Chang CE. BMC Biophys 4 12 (2011)
  7. Dimerization Mediated by a Divergent Forkhead-associated Domain Is Essential for the DNA Damage and Spindle Functions of Fission Yeast Mdb1. Luo S, Xin X, Du LL, Ye K, Wei Y. J Biol Chem 290 21054-21066 (2015)
  8. Structural insights into the recognition of phosphopeptide by the FHA domain of kanadaptin. Xu Q, Deller MC, Nielsen TK, Grant JC, Lesley SA, Elsliger MA, Deacon AM, Wilson IA. PLoS One 9 e107309 (2014)
  9. Achieving peptide binding specificity and promiscuity by loops: case of the forkhead-associated domain. Huang YM, Chang CE. PLoS One 9 e98291 (2014)
  10. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)
  11. Design, Synthesis, and Anticancer Screening for Repurposed Pyrazolo[3,4-d]pyrimidine Derivatives on Four Mammalian Cancer Cell Lines. Othman EM, Bekhit AA, Anany MA, Dandekar T, Ragab HM, Wahid A. Molecules 26 (2021)


Reviews citing this publication (7)

  1. Multisite protein phosphorylation--from molecular mechanisms to kinetic models. Salazar C, Höfer T. FEBS J 276 3177-3198 (2009)
  2. Survey of the year 2005 commercial optical biosensor literature. Rich RL, Myszka DG. J Mol Recognit 19 478-534 (2006)
  3. BRCT domains: A little more than kin, and less than kind. Gerloff DL, Woods NT, Farago AA, Monteiro AN. FEBS Lett 586 2711-2716 (2012)
  4. Modular peptide binding: from a comparison of natural binders to designed armadillo repeat proteins. Reichen C, Hansen S, Plückthun A. J Struct Biol 185 147-162 (2014)
  5. FHA domains: Phosphopeptide binding and beyond. Almawi AW, Matthews LA, Guarné A. Prog Biophys Mol Biol 127 105-110 (2017)
  6. Quo Vadis Biomolecular NMR Spectroscopy? Selenko P. Int J Mol Sci 20 (2019)
  7. Short Linear Motifs in Colorectal Cancer Interactome and Tumorigenesis. Fasano C, Grossi V, Forte G, Simone C. Cells 11 3739 (2022)

Articles citing this publication (32)

  1. Cell signaling, post-translational protein modifications and NMR spectroscopy. Theillet FX, Smet-Nocca C, Liokatis S, Thongwichian R, Kosten J, Yoon MK, Kriwacki RW, Landrieu I, Lippens G, Selenko P. J Biomol NMR 54 217-236 (2012)
  2. Contextual specificity in peptide-mediated protein interactions. Stein A, Aloy P. PLoS One 3 e2524 (2008)
  3. Versatile regulation of multisite protein phosphorylation by the order of phosphate processing and protein-protein interactions. Salazar C, Höfer T. FEBS J 274 1046-1061 (2007)
  4. 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)
  5. 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)
  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. Pellino proteins contain a cryptic FHA domain that mediates interaction with phosphorylated IRAK1. Lin CC, Huoh YS, Schmitz KR, Jensen LE, Ferguson KM. Structure 16 1806-1816 (2008)
  8. Structural and functional analysis of phosphothreonine-dependent FHA domain interactions. Pennell S, Westcott S, Ortiz-Lombardía M, Patel D, Li J, Nott TJ, Mohammed D, Buxton RS, Yaffe MB, Verma C, Smerdon SJ. Structure 18 1587-1595 (2010)
  9. Phosphorylation-induced conformational switching of CPI-17 produces a potent myosin phosphatase inhibitor. Eto M, Kitazawa T, Matsuzawa F, Aikawa S, Kirkbride JA, Isozumi N, Nishimura Y, Brautigan DL, Ohki SY. Structure 15 1591-1602 (2007)
  10. Structure of the yeast Pml1 splicing factor and its integration into the RES complex. Brooks MA, Dziembowski A, Quevillon-Cheruel S, Henriot V, Faux C, van Tilbeurgh H, Séraphin B. Nucleic Acids Res 37 129-143 (2009)
  11. NIPP1 maintains EZH2 phosphorylation and promoter occupancy at proliferation-related target genes. Minnebo N, Görnemann J, O'Connell N, Van Dessel N, Derua R, Vermunt MW, Page R, Beullens M, Peti W, Van Eynde A, Bollen M. Nucleic Acids Res 41 842-854 (2013)
  12. Intermolecular binding between TIFA-FHA and TIFA-pT mediates tumor necrosis factor alpha stimulation and NF-κB activation. Huang CC, Weng JH, Wei TY, Wu PY, Hsu PH, Chen YH, Wang SC, Qin D, Hung CC, Chen ST, Wang AH, Shyy JY, Tsai MD. Mol Cell Biol 32 2664-2673 (2012)
  13. 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)
  14. Protein Arginine Methyltransferase 8: Tetrameric Structure and Protein Substrate Specificity. Lee WC, Lin WL, Matsui T, Chen ES, Wei TY, Lin WH, Hu H, Zheng YG, Tsai MD, Ho MC. Biochemistry 54 7514-7523 (2015)
  15. Augmented expression of Ki-67 is correlated with clinicopathological characteristics and prognosis for lung cancer patients: an up-dated systematic review and meta-analysis with 108 studies and 14,732 patients. Wei DM, Chen WJ, Meng RM, Zhao N, Zhang XY, Liao DY, Chen G. Respir Res 19 150 (2018)
  16. Crystal structure of the Pml1p subunit of the yeast precursor mRNA retention and splicing complex. Trowitzsch S, Weber G, Lührmann R, Wahl MC. J Mol Biol 385 531-541 (2009)
  17. Phosphorylation of mRNA decapping protein Dcp1a by the ERK signaling pathway during early differentiation of 3T3-L1 preadipocytes. Chiang PY, Shen YF, Su YL, Kao CH, Lin NY, Hsu PH, Tsai MD, Wang SC, Chang GD, Lee SC, Chang CJ. PLoS One 8 e61697 (2013)
  18. Robust Replication Control Is Generated by Temporal Gaps between Licensing and Firing Phases and Depends on Degradation of Firing Factor Sld2. Reusswig KU, Zimmermann F, Galanti L, Pfander B. Cell Rep 17 556-569 (2016)
  19. TRIB2 regulates normal and stress-induced thymocyte proliferation. Liang KL, O'Connor C, Veiga JP, McCarthy TV, Keeshan K. Cell Discov 2 15050 (2016)
  20. The RNA recognition motif of NIFK is required for rRNA maturation during cell cycle progression. Pan WA, Tsai HY, Wang SC, Hsiao M, Wu PY, Tsai MD. RNA Biol 12 255-267 (2015)
  21. Tyrosine phosphorylation within the intrinsically disordered cytosolic domains of the B-cell receptor: an NMR-based structural analysis. Rosenlöw J, Isaksson L, Mayzel M, Lengqvist J, Orekhov VY. PLoS One 9 e96199 (2014)
  22. A strategy for interaction site prediction between phospho-binding modules and their partners identified from proteomic data. Aucher W, Becker E, Ma E, Miron S, Martel A, Ochsenbein F, Marsolier-Kergoat MC, Guerois R. Mol Cell Proteomics 9 2745-2759 (2010)
  23. The FHA domain determines Drosophila Chk2/Mnk localization to key mitotic structures and is essential for early embryonic DNA damage responses. Takada S, Collins ER, Kurahashi K. Mol Biol Cell 26 1811-1828 (2015)
  24. The NMR structure of the NIPP1 FHA domain. Kumeta H, Ogura K, Adachi S, Fujioka Y, Tanuma N, Kikuchi K, Inagaki F. J Biomol NMR 40 219-224 (2008)
  25. Direct observations of shifts in the β-sheet register of a protein-peptide complex using explicit solvent simulations. Panteva MT, Salari R, Bhattacharjee M, Chong LT. Biophys J 100 L50-2 (2011)
  26. Nestin expression and in vivo proliferative potential of tanycytes and ependymal cells lining the walls of the third ventricle in the adult rat brain. Hendrickson ML, Zutshi I, Wield A, Kalil RE. Eur J Neurosci 47 284-293 (2018)
  27. Dimerization, but not phosphothreonine binding, is conserved between the forkhead-associated domains of Drosophila MU2 and human MDC1. Luo S, Ye K. FEBS Lett 586 344-349 (2012)
  28. The Greatwall kinase safeguards the genome integrity by affecting the kinome activity in mitosis. Bisteau X, Lee J, Srinivas V, Lee JHS, Niska-Blakie J, Tan G, Yap SYX, Hom KW, Wong CK, Chae J, Wang LC, Kim J, Rancati G, Sobota RM, Tan CSH, Kaldis P. Oncogene 39 6816-6840 (2020)
  29. Characterization of the iPSC-derived conditioned medium that promotes the growth of bovine corneal endothelial cells. Liu Q, Guo Y, Liu S, Wang P, Xue Y, Cui Z, Chen J. PeerJ 7 e6734 (2019)
  30. Kinetochore signalling: the KIss that MELTs Knl1. Bollen M. Curr Biol 24 R68-R70 (2014)
  31. News Pellino proteins splitting up the FHAmily! Pennell S, Smerdon SJ. Structure 16 1752-1754 (2008)
  32. The unique role of the hepatitis virus B X protein on HEK 293 cell morphology and cellular change. Zhang Y, Cheng J, Liu C. Arch Virol 161 1347-1352 (2016)


Related citations provided by authors (1)