Structure of the TPR Domain of AIP: Lack of Client Protein Interaction with the C-Terminal α-7 Helix of the TPR Domain of AIP Is Sufficient for Pituitary Adenoma Predisposition

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Morgan, Rhodri M L ^a   Hernández Ramírez, Laura C ^b   Trivellin, Giampaolo ^b   Zhou, Lihong ^a   Roe, S Mark ^c   Korbonits, Márta ^b   Prodromou, Chrisostomos ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ARGININE; AROMATIC HYDROCARBON RECEPTOR; AROMATIC HYDROCARBON RECEPTOR INTERACTING PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; TETRACOPEPTIDE REPEAT; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; CANCER SUSCEPTIBILITY; CARBOXY TERMINAL SEQUENCE; CELL CYCLE ARREST; CONTROLLED STUDY; DIMERIZATION; ENZYME ACTIVITY; ENZYME ASSAY; GENE MUTATION; HUMAN; HYDROGEN BOND; HYPOPHYSIS ADENOMA; IMMUNOPRECIPITATION; ISOTHERMAL TITRATION CALORIMETRY; MISSENSE MUTATION; NONSENSE MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE; TRANSCRIPTION INITIATION;

ADENOMA; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTATION; PITUITARY NEOPLASMS; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84871730813     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053339     Document Type: Article

References (58)

1. Kuzhandaivelu N, Cong YS, Inouye C, Yang WM, Seto E, (1996) XAP2, a novel hepatitis B virus X-associated protein that inhibits X transactivation. Nucleic Acids Res 24: 4741-4750.
2. Carver LA, Bradfield CA, (1997) Ligand-dependent interaction of the aryl hydrocarbon receptor with a novel immunophilin homolog in vivo. J Biol Chem 272: 11452-11456.
3. Daly AF, Vanbellinghen JF, Khoo SK, Jaffrain-Rea ML, Naves LA, et al. (2007) Aryl hydrocarbon receptor-interacting protein gene mutations in familial isolated pituitary adenomas: analysis in 73 families. J Clin Endocrinol Metab 92: 1891-1896.
4. Vierimaa O, Georgitsi M, Lehtonen R, Vahteristo P, Kokko A, et al. (2006) Pituitary adenoma predisposition caused by germline mutations in the AIP gene. Science 312: 1228-1230.
5. Leontiou CA, Gueorguiev M, van der Spuy J, Quinton R, Lolli F, et al. (2008) The role of the aryl hydrocarbon receptor-interacting protein gene in familial and sporadic pituitary adenomas. J Clin Endocrinol Metab 93: 2390-2401.
6. Chahal HS, Chapple JP, Frohman LA, Grossman AB, Korbonits M, (2010) Clinical, genetic and molecular characterization of patients with familial isolated pituitary adenomas (FIPA). Trends Endocrinol Metab 21: 419-427.
7. Linnert M, Haupt K, Lin YJ, Kissing S, Paschke AK, et al. (2012) NMR assignments of the FKBP-type PPIase domain of the human aryl-hydrocarbon receptor-interacting protein (AIP). Biomolecular NMR assignments 6: 209-212.
8. Carver LA, LaPres JJ, Jain S, Dunham EE, Bradfield CA, (1998) Characterization of the Ah receptor-associated protein, ARA9. J Biol Chem 273: 33580-33587.
9. Laenger A, Lang-Rollin I, Kozany C, Zschocke J, Zimmermann N, et al. (2009) XAP2 inhibits glucocorticoid receptor activity in mammalian cells. FEBS lett 583: 1493-1498.
10. Trivellin G, Korbonits M, (2011) AIP and its interacting partners. J Endocrinol 210: 137-155.
11. Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, et al. (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101: 199-210.
12. Zhang M, Windheim M, Roe SM, Peggie M, Cohen P, et al. (2005) Chaperoned ubiquitylation-crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol cell 20: 525-538.
13. Bolger GB, Peden AH, Steele MR, MacKenzie C, McEwan DG, et al. (2003) Attenuation of the activity of the cAMP-specific phosphodiesterase PDE4A5 by interaction with the immunophilin XAP2. J Biol Chem 278: 33351-33363.
14. Pearl LH, Prodromou C, Workman P, (2008) The Hsp90 molecular chaperone: an open and shut case for treatment. Biochem J 410: 439-453.
15. Prodromou C, (2012) The 'active life' of Hsp90 complexes. Biochim Biophys Acta 1823: 614-623.
16. Jackson SE (2012) Hsp90: Structure and Function. Topics in current chemistry.
17. Bukau B, Weissman J, Horwich A, (2006) Molecular chaperones and protein quality control. Cell 125: 443-451.
18. Mayer MP, Bukau B, (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cellular and molecular life sciences: CMLS 62: 670-684.
19. Perry AJ, Rimmer KA, Mertens HD, Waller RF, Mulhern TD, et al. (2008) Structure, topology and function of the translocase of the outer membrane of mitochondria. Plant physiology and biochemistry: PPB/Societe francaise de physiologie vegetale 46: 265-274.
20. Huang G, Elferink CJ, (2005) Multiple mechanisms are involved in Ah receptor-mediated cell cycle arrest. Mol Pharmacol 67: 88-96.
21. Marlowe JL, Knudsen ES, Schwemberger S, Puga A, (2004) The aryl hydrocarbon receptor displaces p300 from E2F-dependent promoters and represses S phase-specific gene expression. J Biol Chem 279: 29013-29022.
22. Puga A, Barnes SJ, Dalton TP, Chang C, Knudsen ES, et al. (2000) Aromatic hydrocarbon receptor interaction with the retinoblastoma protein potentiates repression of E2F-dependent transcription and cell cycle arrest. J Biol Chem 275: 2943-2950.
23. Kolluri SK, Weiss C, Koff A, Gottlicher M, (1999) p27(Kip1) induction and inhibition of proliferation by the intracellular Ah receptor in developing thymus and hepatoma cells. Genes Dev 13: 1742-1753.
24. Pang PH, Lin YH, Lee YH, Hou HH, Hsu SP, et al. (2008) Molecular mechanisms of p21 and p27 induction by 3-methylcholanthrene, an aryl-hydrocarbon receptor agonist, involved in antiproliferation of human umbilical vascular endothelial cells. J Cell Physiol 215: 161-171.
25. Heliovaara E, Raitila A, Launonen V, Paetau A, Arola J, et al. (2009) The expression of AIP-related molecules in elucidation of cellular pathways in pituitary adenomas. Am J Pathol 175: 2501-2507.
26. de Oliveira SK, Smolenski A, (2009) Phosphodiesterases link the aryl hydrocarbon receptor complex to cyclic nucleotide signaling. Biochem Pharmacol 77: 723-733.
27. de Oliveira SK, Hoffmeister M, Gambaryan S, Muller-Esterl W, Guimaraes JA, et al. (2007) Phosphodiesterase 2A forms a complex with the co-chaperone XAP2 and regulates nuclear translocation of the aryl hydrocarbon receptor. J Biol Chem 282: 13656-13663.
28. Feigelson HS, Henderson BE, (1996) Estrogens and breast cancer. Carcinogenesis 17: 2279-2284.
29. Persson I, Weiderpass E, Bergkvist L, Bergstrom R, Schairer C, (1999) Risks of breast and endometrial cancer after estrogen and estrogen-progestin replacement. Cancer Causes Control 10: 253-260.
30. Greiser CM, Greiser EM, Doren M, (2007) Menopausal hormone therapy and risk of ovarian cancer: systematic review and meta-analysis. Hum Reprod Update 13: 453-463.
31. Zeng Q, Chen G, Vlantis A, Tse G, van Hasselt C, (2008) The contributions of oestrogen receptor isoforms to the development of papillary and anaplastic thyroid carcinomas. J Pathol 214: 425-433.
32. Fujimoto M, Yoshino E, Hirakawa K, Chihara K, Ibata Y, (1987) Studies on estrogen induced pituitary tumor in the rat with special reference to the relationship of the tuberoinfundibular dopamine neuron system. J Neurooncol 5: 151-159.
33. Heaney AP, Horwitz GA, Wang Z, Singson R, Melmed S, (1999) Early involvement of estrogen-induced pituitary tumor transforming gene and fibroblast growth factor expression in prolactinoma pathogenesis. Nat Med 5: 1317-1321.
34. Spengler D, Villalba M, Hoffmann A, Pantaloni C, Houssami S, et al. (1997) Regulation of apoptosis and cell cycle arrest by Zac1, a novel zinc finger protein expressed in the pituitary gland and the brain. EMBO J 16: 2814-2825.
35. Chahal HS, Trivellin G, Leontiou CA, Alband N, Fowkes RC, et al. (2012) Somatostatin Analogs Modulate AIP in Somatotroph Adenomas: The Role of the ZAC1 Pathway. J Clin Endocrinol Metab 97: E1411-1420.
36. Ozfirat Z, Korbonits M, (2010) AIP gene and familial isolated pituitary adenomas. Mol Cell Endocrinol 326: 71-79.
37. Afonine PV, Grosse-Kunstleve RW, Echols N, Headd JJ, Moriarty NW, et al. (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr D Biol Crystallogr 68: 352-367.
38. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35: W375-383.
39. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
40. Krissinel EB, Winn MD, Ballard CC, Ashton AW, Patel P, et al. (2004) The new CCP4 Coordinate Library as a toolkit for the design of coordinate-related applications in protein crystallography. Acta Crystallogr D Biol Crystallogr 60: 2250-2255.
41. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N, (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38: W529-533.
42. Landau M, Mayrose I, Rosenberg Y, Glaser F, Martz E, et al. (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res 33: W299-302.
43. Glaser F, Pupko T, Paz I, Bell RE, Bechor-Shental D, et al. (2003) ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics 19: 163-164.
44. Siligardi G, Hu B, Panaretou B, Piper PW, Pearl LH, et al. (2004) Co-chaperone regulation of conformational switching in the Hsp90 ATPase cycle. J Biol Chem 279: 51989-51998.
45. Prodromou C, Siligardi G, O'Brien R, Woolfson DN, Regan L, et al. (1999) Regulation of Hsp90 ATPase activity by tetratricopeptide repeat (TPR)-domain co-chaperones. EMBO J 18: 754-762.
46. Panaretou B, Siligardi G, Meyer P, Maloney A, Sullivan JK, et al. (2002) Activation of the ATPase activity of hsp90 by the stress-regulated cochaperone aha1. Mol Cell 10: 1307-1318.
47. Yano M, Terada K, Mori M, (2003) AIP is a mitochondrial import mediator that binds to both import receptor Tom20 and preproteins. The Journal of cell biology 163: 45-56.
48. Bell DR, Poland A, (2000) Binding of aryl hydrocarbon receptor (AhR) to AhR-interacting protein. The role of hsp90. J Biol Chem 275: 36407-36414.
49. Hollingshead BD, Petrulis JR, Perdew GH, (2004) The aryl hydrocarbon (Ah) receptor transcriptional regulator hepatitis B virus X-associated protein 2 antagonizes p23 binding to Ah receptor-Hsp90 complexes and is dispensable for receptor function. J Biol Chem 279: 45652-45661.
50. Chahal HS, Stals K, Unterlander M, Balding DJ, Thomas MG, et al. (2011) AIP mutation in pituitary adenomas in the 18th century and today. N Engl J Med 364: 43-50.
51. Daly AF, Tichomirowa MA, Petrossians P, Heliovaara E, Jaffrain-Rea ML, et al. (2010) Clinical characteristics and therapeutic responses in patients with germ-line AIP mutations and pituitary adenomas: an international collaborative study. J Clin Endocrinol Metab 95: E373-383.
52. Igreja S, Chahal HS, King P, Bolger GB, Srirangalingam U, et al. (2010) Characterization of aryl hydrocarbon receptor interacting protein (AIP) mutations in familial isolated pituitary adenoma families. Hum Mutat 31: 950-960.
53. Muller P, Ruckova E, Halada P, Coates PJ, Hrstka R, et al. (2012) C-terminal phosphorylation of Hsp70 and Hsp90 regulates alternate binding to co-chaperones CHIP and HOP to determine cellular protein folding/degradation balances. Oncogene.
54. Cook C, Petrucelli L (2012) Tau Triage Decisions Mediated by the Chaperone Network. Journal of Alzheimer's disease: JAD.
55. Raitila A, Lehtonen HJ, Arola J, Heliovaara E, Ahlsten M, et al. (2010) Mice with inactivation of aryl hydrocarbon receptor-interacting protein (Aip) display complete penetrance of pituitary adenomas with aberrant ARNT expression. Am J Pathol 177: 1969-1976.
56. Pocar P, Fischer B, Klonisch T, Hombach-Klonisch S, (2005) Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction. Reproduction 129: 379-389.
57. Safe S, Wormke M, Samudio I, (2000) Mechanisms of inhibitory aryl hydrocarbon receptor-estrogen receptor crosstalk in human breast cancer cells. J Mammary Gland Biol Neoplasia 5: 295-306.
58. Cai W, Kramarova TV, Berg P, Korbonits M, Pongratz I, (2011) The immunophilin-like protein XAP2 is a negative regulator of estrogen signaling through interaction with estrogen receptor alpha. PLoS One 6: e25201.