Crystal structure of Plasmodium vivax FK506-binding protein 25 reveals conformational changes responsible for its noncanonical activity

Proteins: Structure, Function and Bioinformatics

Volumn 82, Issue 7, 2014, Pages 1235-1244

  Rajan, Sreekanth ^a   Austin, David ^a   Harikishore, Amaravadhi ^a   Nguyen, Quoc Toan ^a   Baek, Kwanghee ^b   Yoon, Ho Sup ^a,b  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b Kyung Hee University   (South Korea)

Author keywords

FK506; FKBP; FKBP25; Malaria; Plasmodium vivax; PPIase

Indexed keywords

CALMODULIN BINDING PROTEIN; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 25; PEPTIDYLPROLYL ISOMERASE; UNCLASSIFIED DRUG; PROTOZOAL PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ASSAY; NONHUMAN; PLASMODIUM VIVAX; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; CATALYTIC DOMAIN; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLASMODIUM VIVAX; PROTEIN CONFORMATION; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; TACROLIMUS BINDING PROTEINS;

EID: 84902094702     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24487     Document Type: Article

References (60)

1. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002;419:498-511.
2. Monaghan P, Fardis M, Revill WP, Bell A. Antimalarial effects of macrolactones related to FK520 (ascomycin) are independent of the immunosuppressive properties of the compounds. J Infect Dis 2005;191:1342-1349.
3. Birkholtz LM, Bastien O, Wells G, Grando D, Joubert F, Kasam V, Zimmermann M, Ortet P, Jacq N, Saidani N, Roy S, Hofmann-Apitius M, Breton V, Louw AI, Marechal E. Integration and mining of malaria molecular, functional and pharmacological data: how far are we from a chemogenomic knowledge space? Malar J 2006;5:110.
4. Magarinos MP, Carmona SJ, Crowther GJ, Ralph SA, Roos DS, Shanmugam D, Van Voorhis WC, Aguero F. TDR targets: a chemogenomics resource for neglected diseases. Nucleic Acids Res 2011;40(Database issue):D1118-D1127.
5. LaCount DJ. Interactome mapping in malaria parasites: challenges and opportunities. Methods Mol Biol 2012;812:121-145.
6. Florens L, Washburn MP, Raine JD, Anthony RM, Grainger M, Haynes JD, Moch JK, Muster N, Sacci JB, Tabb DL, Witney AA, Wolters D, Wu Y, Gardner MJ, Holder AA, Sinden RE, Yates JR, Carucci DJ. A proteomic view of the Plasmodium falciparum life cycle. Nature 2002;419:520-526.
7. Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Innamorato F, Iodice J, Kissinger JC, Kraemer E, Li W, Miller JA, Nayak V, Pennington C, Pinney DF, Roos DS, Ross C, Stoeckert CJ, Jr, Treatman C, Wang H. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 2009;37(Database issue):D539-D543.
8. Modis Y. Exploiting structural biology in the fight against parasitic diseases. Trends Parasitol 2012;28:124-130.
9. Alag R, Bharatham N, Dong A, Hills T, Harikishore A, Widjaja AA, Shochat SG, Hui R, Yoon HS. Crystallographic structure of the tetratricopeptide repeat domain of Plasmodium falciparum FKBP35 and its molecular interaction with Hsp90 C-terminal pentapeptide. Protein Sci 2009;18:2115-2124.
10. Alag R, Qureshi IA, Bharatham N, Shin J, Lescar J, Yoon HS. NMR and crystallographic structures of the FK506 binding domain of human malarial parasite Plasmodium vivax FKBP35. Protein Sci 2010;19:1577-1586.
11. Alag R, Shin J, Yoon HS. NMR assignments of the FK506-binding domain of FK506-binding protein 35 from Plasmodium vivax. Biomol NMR Assign 2009;3:243-245.
12. Bharatham N, Chang MW, Yoon HS. Targeting FK506 binding proteins to fight malarial and bacterial infections: current advances and future perspectives. Curr Med Chem 2011;18:1874-1889.
13. Kang CB, Ye H, Yoon HR, Yoon HS. Solution structure of FK506 binding domain (FKBD) of Plasmodium falciparum FK506 binding protein 35 (PfFKBP35). Proteins 2008;70:300-302.
14. Kotaka M, Ye H, Alag R, Hu G, Bozdech Z, Preiser PR, Yoon HS, Lescar J. Crystal structure of the FK506 binding domain of Plasmodium falciparum FKBP35 in complex with FK506. Biochemistry 2008;47:5951-5961.
15. Alag R, Balakrishna AM, Rajan S, Qureshi IA, Shin J, Lescar J, Gruber G, Yoon HS. Structural insights into substrate binding by PvFKBP35, a peptidylprolyl cis-trans isomerase from the human malarial parasite Plasmodium vivax. Eukaryot Cell 2013;12:627-634.
16. Harikishore A, Niang M, Rajan S, Preiser PR, Yoon HS. Small molecule Plasmodium FKBP35 inhibitor as a potential antimalaria agent. Sci Rep 2013;3:2501.
17. Barth S, Nesper J, Hasgall PA, Wirthner R, Nytko KJ, Edlich F, Katschinski DM, Stiehl DP, Wenger RH, Camenisch G. The peptidyl prolyl cis/trans isomerase FKBP38 determines hypoxia-inducible transcription factor prolyl-4-hydroxylase PHD2 protein stability. Mol Cell Biol 2007;27:3758-3768.
18. Choi BH, Feng L, Yoon HS. FKBP38 protects Bcl-2 from caspase-dependent degradation. J Biol Chem 2010;285:9770-9779.
19. Jinwal UK, Koren J, III, Borysov SI, Schmid AB, Abisambra JF, Blair LJ, Johnson AG, Jones JR, Shults CL, O'Leary JC, III, Jin Y, Buchner J, Cox MB, Dickey CA. The Hsp90 cochaperone, FKBP51, increases Tau stability and polymerizes microtubules. J Neurosci 2010;30:591-599.
20. Wang T, Li BY, Danielson PD, Shah PC, Rockwell S, Lechleider RJ, Martin J, Manganaro T, Donahoe PK. The immunophilin FKBP12 functions as a common inhibitor of the TGF beta family type I receptors. Cell 1996;86:435-444.
21. Riggs DL, Roberts PJ, Chirillo SC, Cheung-Flynn J, Prapapanich V, Ratajczak T, Gaber R, Picard D, Smith DF. The Hsp90-binding peptidylprolyl isomerase FKBP52 potentiates glucocorticoid signaling in vivo. EMBO J 2003;22:1158-1167.
22. Cameron AM, Steiner JP, Sabatini DM, Kaplin AI, Walensky LD, Snyder SH. Immunophilin FK506 binding protein associated with inositol 1, 4, 5-trisphosphate receptor modulates calcium flux. Proc Natl Acad Sci USA 1995;92:1784-1788.
23. Kuzuhara T, Horikoshi M. A nuclear FK506-binding protein is a histone chaperone regulating rDNA silencing. Nat Struct Mol Biol 2004;11:275-283.
24. Nelson CJ, Santos-Rosa H, Kouzarides T. Proline isomerization of histone H3 regulates lysine methylation and gene expression. Cell 2006;126:905-916.
25. Edlich F, Weiwad M, Wildemann D, Jarczowski F, Kilka S, Moutty MC, Jahreis G, Lucke C, Schmidt W, Striggow F, Fischer G. The specific FKBP38 inhibitor N-(N', N'-dimethylcarboxamidomethyl)cycloheximide has potent neuroprotective and neurotrophic properties in brain ischemia. J Biol Chem 2006;281:14961-14970.
26. Chattopadhaya S, Harikishore A, Yoon HS. Role of FK506 binding proteins in neurodegenerative disorders. Curr Med Chem 2011;18:5380-5397.
27. Yang WM, Inouye CJ, Seto E. Cyclophilin A and FKBP12 interact with YY1 and alter its transcriptional activity. J Biol Chem 1995;270:15187-15193.
28. Ochocka AM, Kampanis P, Nicol S, Allende-Vega N, Cox M, Marcar L, Milne D, Fuller-Pace F, Meek D. FKBP25, a novel regulator of the p53 pathway, induces the degradation of MDM2 and activation of p53. FEBS Lett 2009;583:621-626.
29. Jayaraman T, Brillantes AM, Timerman AP, Fleischer S, Erdjument-Bromage H, Tempst P, Marks AR. FK506 binding protein associated with the calcium release channel (ryanodine receptor). J Biol Chem 1992;267:9474-9477.
30. Crackower MA, Kolas NK, Noguchi J, Sarao R, Kikuchi K, Kaneko H, Kobayashi E, Kawai Y, Kozieradzki I, Landers R, Mo R, Hui CC, Nieves E, Cohen PE, Osborne LR, Wada T, Kunieda T, Moens PB, Penninger JM. Essential role of Fkbp6 in male fertility and homologous chromosome pairing in meiosis. Science 2003;300:1291-1295.
31. Shirane M, Nakayama KI. Inherent calcineurin inhibitor FKBP38 targets Bcl-2 to mitochondria and inhibits apoptosis. Nat Cell Biol 2003;5:28-37.
32. Ahearn IM, Tsai FD, Court H, Zhou M, Jennings BC, Ahmed M, Fehrenbacher N, Linder ME, Philips MR. FKBP12 binds to acylated H-ras and promotes depalmitoylation. Mol Cell 2011;41:173-185.
33. Yang WM, Yao YL, Seto E. The FK506-binding protein 25 functionally associates with histone deacetylases and with transcription factor YY1. EMBO J 2001;20:4814-4825.
34. Yao YL, Yang WM. The metastasis-associated proteins 1 and 2 form distinct protein complexes with histone deacetylase activity. J Biol Chem 2003;278:42560-42568.
35. Liang J, Deborah TH, Schreiber SL, Clardy J. Structure of the human 25 kDa FK506 binding protein complexed with rapamycin. J Am Chem Soc 1996;118:1231-1232.
36. Harrison RK, Stein RL. Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK-506 binding protein: evidence for the existence of a family of distinct enzymes. Biochemistry 1990;29:3813-3816.
37. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 2011;67 (Part 4):271-281.
38. Evans P. Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 2006;62 (Part 1):72-82.
39. Long F, Vagin AA, Young P, Murshudov GN. BALBES: a molecular-replacement pipeline. Acta Crystallogr D Biol Crystallogr 2008;64 (Part 1):125-132.
40. Langer G, Cohen SX, Lamzin VS, Perrakis A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat Protoc 2008;3:1171-1179.
41. Murshudov GN, Skubak P, Lebedev AA, Pannu NS, Steiner RA, Nicholls RA, Winn MD, Long F, Vagin AA. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr 2011;67 (Part 4):355-367.
42. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 2011;67 (Part 4):235-242.
43. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 2010;66 (Part 1):12-21.
44. Ramachandran GN, Ramakrishnan C, Sasisekharan V. Stereochemistry of polypeptide chain configurations. J Mol Biol 1963;7:95-99.
45. Edlich F, Weiwad M, Erdmann F, Fanghanel J, Jarczowski F, Rahfeld JU, Fischer G. Bcl-2 regulator FKBP38 is activated by Ca2+/calmodulin. EMBO J 2005;24:2688-2699.
46. Gibrat JF, Madej T, Bryant SH. Surprising similarities in structure comparison. Curr Opin Struct Biol 1996;6:377-385.
47. Monneau YR, Soufari H, Nelson CJ, Mackereth CD. Structure and activity of the peptidyl-prolyl isomerase domain from the histone chaperone Fpr4 toward histone H3 proline isomerization. J Biol Chem 2013;288:25826-25837.
48. Maestre-Martinez M, Haupt K, Edlich F, Neumann P, Parthier C, Stubbs MT, Fischer G, Lucke C. A charge-sensitive loop in the FKBP38 catalytic domain modulates Bcl-2 binding. J Mol Recognit 2011;24:23-34.
49. Sinars CR, Cheung-Flynn J, Rimerman RA, Scammell JG, Smith DF, Clardy J. Structure of the large FK506-binding protein FKBP51, an Hsp90-binding protein and a component of steroid receptor complexes. Proc Natl Acad Sci USA 2003;100:868-873.
50. Li P, Ding Y, Wu B, Shu C, Shen B, Rao Z. Structure of the N-terminal domain of human FKBP52. Acta Crystallogr D Biol Crystallogr 2003;59 (Part 1):16-22.
51. Linnert M, Lin YJ, Manns A, Haupt K, Paschke AK, Fischer G, Weiwad M, Lucke C. The FKBP-type domain of the human aryl hydrocarbon receptor-interacting protein reveals an unusual Hsp90 interaction. Biochemistry 2013;52:2097-2107.
52. Rhoads AR, Friedberg F. Sequence motifs for calmodulin recognition. FASEB J 1997;11:331-340.
53. Yamniuk AP, Vogel HJ. Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides. Mol Biotechnol 2004;27:33-57.
54. Erickson-Viitanen S, DeGrado WF. Recognition and characterization of calmodulin-binding sequences in peptides and proteins. Methods Enzymol 1987;139:455-478.
55. Lucke C, Weiwad M. Insights into immunophilin structure and function. Curr Med Chem 2011;18:5333-5354.
56. Vaid A, Sharma P. PfPKB, a protein kinase B-like enzyme from Plasmodium falciparum. II. Identification of calcium/calmodulin as its upstream activator and dissection of a novel signaling pathway. J Biol Chem 2006;281:27126-27133.
57. Vaid A, Thomas DC, Sharma P. Role of Ca2+/calmodulin-PfPKB signaling pathway in erythrocyte invasion by Plasmodium falciparum. J Biol Chem 2008;283:5589-5597.
58. Gouet P, Robert X, Courcelle E. ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res 2003;31:3320-3323.
59. DeLano WL. The PyMOL molecular graphics system. Palo Alto, CA: DeLano Scientific; 2002.
60. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF chimera-a visualization system for exploratory research and analysis. J Comput Chem 2004;25:1605-1612.