The prolyl isomerase pin1 regulates mRNA levels of genes with short half-lives by targeting specific RNA binding proteins

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Krishnan, Nithya ^a   Titus, Mark A ^c   Thapar, Roopa ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b RICE UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; HUR PROTEIN; MESSENGER RNA; PEPTIDYLPROLYL ISOMERASE PIN1; PHOSPHATIDYLINOSITOL; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; ARTICLE; AU RICH ELEMENT; CANCER GROWTH; CELL ADHESION; DNA MICROARRAY; DNA REPLICATION; ENZYME ACTIVITY; ENZYME REGULATION; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE SEQUENCE; GENE SILENCING; GENE TARGETING; GENETIC ASSOCIATION; HALF LIFE TIME; HELA CELL; HUMAN; IN VIVO STUDY; INTRACELLULAR SIGNALING; LEUKOCYTE MIGRATION; MAMMAL CELL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RNA INTERFERENCE; RNA STABILITY; SCORING SYSTEM; STATISTICAL ANALYSIS;

CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; DNA REPLICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENOME, HUMAN; HALF-LIFE; HEK293 CELLS; HELA CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN D; HISTONES; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PEPTIDYLPROLYL ISOMERASE; PHOSPHATIDYLINOSITOLS; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84897472520     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085427     Document Type: Article

References (62)

1. Liou YC, Zhou XZ, Lu KP (2011) Prolyl isomerase Pin1 as a molecular switch to determine the fate of phosphoproteins. Trends Biochem Sci 36: 501-514.
2. Driver JA, Lu KP (2010) Pin1: a new genetic link between Alzheimer's disease, cancer and aging. Curr Aging Sci 3: 158-165.
3. Ranganathan R, Lu KP, Hunter T, Noel JP (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation dependent. Cell 89: 875-886. (Pubitemid 27513514)
4. Zhou XZ, Kops O, Werner A, Lu PJ, Shen M, et al. (2000) Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tau proteins. Mol Cell 6: 873-883.
5. Stukenberg PT, Kirschner MW (2001) Pin1 acts catalytically to promote a conformational change in Cdc25. Mol Cell 7: 1071-1083. (Pubitemid 32525753)
6. Krishnan N, Lam TT, Fritz A, Rempinski D, O'Loughlin K, et al. (2012) The Prolyl Isomerase Pin1 Targets Stem-Loop Binding Protein (SLBP) To Dissociate the SLBP-Histone mRNA Complex Linking Histone mRNA Decay with SLBP Ubiquitination. Mol Cell Biol 32: 4306-4322.
7. Jentsch S, Siepe D (2009) Pin1, a novel switch in the ubiquitin pathway. Cell Cycle 8: 3800-3801.
8. Min SH, Lau AW, Lee TH, Inuzuka H, Wei S, et al. (2012) Negative regulation of the stability and tumor suppressor function of fbw7 by the pin1 prolyl isomerase. Mol Cell 46: 771-783.
9. Ryo A, Nakamura M, Wulf G, Liou YC, Lu KP (2001) Pin1 regulates turnover and subcellular localization of beta-catenin by inhibiting its interaction with APC. Nat Cell Biol 3: 793-801. (Pubitemid 32842684)
10. Lu KP, Zhou XZ (2007) The prolyl isomerase PIN1: a pivotal new twist in phosphorylation signalling and disease. Nat Rev Mol Cell Biol 8: 904-916. (Pubitemid 47622559)
11. Lee TH, Pastorino L, Lu KP (2011) Peptidyl-prolyl cis-trans isomerase Pin1 in ageing, cancer and Alzheimer disease. Expert Rev Mol Med 13: e21.
12. Esnault S, Shen ZJ, Malter JS (2008) Pinning down signaling in the immune system: the role of the peptidyl-prolyl isomerase Pin1 in immune cell function. Crit Rev Immunol 28: 45-60. (Pubitemid 351264074)
13. Rudrabhatla P, Pant HC (2010) Phosphorylation-specific peptidyl-prolyl isomerization of neuronal cytoskeletal proteins by Pin1: implications for therapeutics in neurodegeneration. J Alzheimers Dis 19: 389-403.
14. Wulf G, Garg P, Liou YC, Iglehart D, Lu KP (2004) Modeling breast cancer in vivo and ex vivo reveals an essential role of Pin1 in tumorigenesis. EMBO J 23: 3397-3407. (Pubitemid 39209163)
15. Girardini JE, Napoli M, Piazza S, Rustighi A, Marotta C, et al. (2011) A Pin1/mutant p53 axis promotes aggressiveness in breast cancer. Cancer Cell 20: 79-91.
16. Avila MA, Lu KP (2007) Hepatitis B virus x protein and pin1 in liver cancer: "les liaisons dangereuses". Gastroenterology 132: 1180-1183. (Pubitemid 46440882)
17. Ayala G, Wang D, Wulf G, Frolov A, Li R, et al. (2003) The prolyl isomerase Pin1 is a novel prognostic marker in human prostate cancer. Cancer Res 63: 6244-6251. (Pubitemid 37255170)
18. Ryo A, Uemura H, Ishiguro H, Saitoh T, Yamaguchi A, et al. (2005) Stable suppression of tumorigenicity by Pin1-targeted RNA interference in prostate cancer. Clin Cancer Res 11: 7523-7531. (Pubitemid 41507714)
19. Chen SY, Wulf G, Zhou XZ, Rubin MA, Lu KP, et al. (2006) Activation of betacatenin signaling in prostate cancer by peptidyl-prolyl isomerase Pin1-mediated abrogation of the androgen receptor-beta-catenin interaction. Mol Cell Biol 26: 929-939. (Pubitemid 43146487)
20. Bao L, Kimzey A, Sauter G, Sowadski JM, Lu KP, et al. (2004) Prevalent overexpression of prolyl isomerase Pin1 in human cancers. Am J Pathol 164: 1727-1737. (Pubitemid 38529775)
21. Anderson P (2005) Pin1: a proline isomerase that makes you wheeze? Nat Immunol 6: 1211-1212.
22. Guo C, Hou X, Dong L, Dagostino E, Greasley S, et al. (2009) Structure-based design of novel human Pin1 inhibitors (I). Bioorg Med Chem Lett 19: 5613-5616.
23. Dong L, Marakovits J, Hou X, Guo C, Greasley S, et al. (2010) Structure-based design of novel human Pin1 inhibitors (II). Bioorg Med Chem Lett 20: 2210-2214.
24. Moore JD, Potter A (2013) Pin1 inhibitors: Pitfalls, progress and cellular pharmacology. Bioorg Med Chem Lett 23: 4283-4291.
25. Potter A, Oldfield V, Nunns C, Fromont C, Ray S, et al. (2010) Discovery of cell-active phenyl-imidazole Pin1 inhibitors by structure-guided fragment evolution. Bioorg Med Chem Lett 20: 6483-6488.
26. Tatara Y, Lin YC, Bamba Y, Mori T, Uchida T (2009) Dipentamethylene thiuram monosulfide is a novel inhibitor of Pin1. Biochem Biophys Res Commun 384: 394-398.
27. Mori T, Hidaka M, Lin YC, Yoshizawa I, Okabe T, et al. (2011) A dual inhibitor against prolyl isomerase Pin1 and cyclophilin discovered by a novel real-time fluorescence detection method. Biochem Biophys Res Commun 406: 439-443.
28. Wildemann D, Erdmann F, Alvarez BH, Stoller G, Zhou XZ, et al. (2006) Nanomolar inhibitors of the peptidyl prolyl cis/trans isomerase Pin1 from combinatorial peptide libraries. J Med Chem 49: 2147-2150.
29. Liu T, Liu Y, Kao HY, Pei D (2010) Membrane permeable cyclic peptidyl inhibitors against human Peptidylprolyl Isomerase Pin1. J Med Chem 53: 2494-2501.
30. Duncan KE, Dempsey BR, Killip LE, Adams J, Bailey ML, et al. (2011) Discovery and characterization of a nonphosphorylated cyclic peptide inhibitor of the peptidylprolyl isomerase, Pin1. J Med Chem 54: 3854-3865.
31. Wulf GM, Ryo A, Wulf GG, Lee SW, Niu T, et al. (2001) Pin1 is over-expressed in breast cancer and cooperates with Ras signaling in increasing the transcriptional activity of c-Jun towards cyclin D1. EMBO J 20: 3459-3472. (Pubitemid 32634353)
32. Rajbhandari P, Schalper KA, Solodin NM, Ellison-Zelski SJ, Ping Lu K, et al. (2013) Pin1 modulates ERalpha levels in breast cancer through inhibition of phosphorylation-dependent ubiquitination and degradation. Oncogene.
33. Rajbhandari P, Finn G, Solodin NM, Singarapu KK, Sahu SC, et al. (2012) Regulation of estrogen receptor alpha N-terminus conformation and function by peptidyl prolyl isomerase Pin1. Mol Cell Biol 32: 445-457.
34. La Montagna R, Caligiuri I, Maranta P, Lucchetti C, Esposito L, et al. (2012) Androgen receptor serine 81 mediates Pin1 interaction and activity. Cell Cycle 11: 3415-3420.
35. Esnault S, Shen ZJ, Whitesel E, Malter JS (2006) The peptidyl-prolyl isomerase Pin1 regulates granulocyte-macrophage colony-stimulating factor mRNA stability in T lymphocytes. J Immunol 177: 6999-7006. (Pubitemid 44715066)
36. Nechama M, Uchida T, Mor Yosef-Levi I, Silver J, Naveh-Many T (2009) The peptidyl-prolyl isomerase Pin1 determines parathyroid hormone mRNA levels and stability in rat models of secondary hyperparathyroidism. J Clin Invest 119: 3102-3114.
37. Naveh-Many T (2010) Minireview: the play of proteins on the parathyroid hormone messenger ribonucleic Acid regulates its expression. Endocrinology 151: 1398-1402.
38. Gratacos FM, Brewer G (2010) The role of AUF1 in regulated mRNA decay. Wiley Interdiscip Rev RNA 1: 457-473.
39. von Roretz C, Di Marco S, Mazroui R, Gallouzi IE (2011) Turnover of AU-rich-containing mRNAs during stress: a matter of survival. Wiley Interdiscip Rev RNA 2: 336-347.
40. Gherzi R, Chen CY, Trabucchi M, Ramos A, Briata P (2010) The role of KSRP in mRNA decay and microRNA precursor maturation. Wiley Interdiscip Rev RNA 1: 230-239.
41. Shen ZJ, Esnault S, Rosenthal LA, Szakaly RJ, Sorkness RL, et al. (2008) Pin1 regulates TGF-beta1 production by activated human and murine eosinophils and contributes to allergic lung fibrosis. J Clin Invest 118: 479-490. (Pubitemid 351206539)
42. Shen ZJ, Braun RK, Hu J, Xie Q, Chu H, et al. (2012) Pin1 protein regulates Smad protein signaling and pulmonary fibrosis. J Biol Chem 287: 23294-23305.
43. Kumar R (2009) Pin1 regulates parathyroid hormone mRNA stability. J Clin Invest 119: 2887-2891.
44. Marzluff WF, Wagner EJ, Duronio RJ (2008) Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat Rev Genet 9: 843-854.
45. Alterman RB, Ganguly S, Schulze DH, Marzluff WF, Schildkraut CL, et al. (1984) Cell cycle regulation of mouse H3 histone mRNA metabolism. Mol Cell Biol 4: 123-132. (Pubitemid 14180053)
46. Heintz N, Sive HL, Roeder RG (1983) Regulation of human histone gene expression: kinetics of accumulation and changes in the rate of synthesis and in the half-lives of individual histone mRNAs during the HeLa cell cycle. Mol Cell Biol 3: 539-550. (Pubitemid 13136537)
47. Wang ZF, Whitfield ML, Ingledue TC, 3rd, Dominski Z, Marzluff WF (1996) The protein that binds the 39 end of histone mRNA: a novel RNA-binding protein required for histone pre-mRNA processing. Genes Dev 10: 3028-3040. (Pubitemid 26412529)
48. Dominski Z, Zheng LX, Sanchez R, Marzluff WF (1999) Stem-loop binding protein facilitates 39-end formation by stabilizing U7 snRNP binding to histone pre-mRNA. Mol Cell Biol 19: 3561-3570. (Pubitemid 29193815)
49. Sullivan KD, Mullen TE, Marzluff WF, Wagner EJ (2009) Knockdown of SLBP results in nuclear retention of histone mRNA. RNA 15: 459-472.
50. Sanchez R, Marzluff WF (2002) The stem-loop binding protein is required for efficient translation of histone mRNA in vivo and in vitro. Mol Cell Biol 22: 7093-7104.
51. Kaygun H, Marzluff WF (2005) Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat Struct Mol Biol 12: 794-800. (Pubitemid 43086254)
52. Dennis G Jr., Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
53. Draghici S, Khatri P, Tarca AL, Amin K, Done A, et al. (2007) A systems biology approach for pathway level analysis. Genome Res 17: 1537-1545. (Pubitemid 47529438)
54. Marzluff WF, Gongidi P, Woods KR, Jin J, Maltais LJ (2002) The human and mouse replication-dependent histone genes. Genomics 80: 487-498. (Pubitemid 35333791)
55. Akiyama H, Misawa T, Ono M, Uchida C, Uchida T (2011) Prolyl isomerase pin1 protects mice from endotoxin shock. PLoS One 6: e14656.
56. Shen ZJ, Esnault S, Malter JS (2005) The peptidyl-prolyl isomerase Pin1 regulates the stability of granulocyte-macrophage colony-stimulating factor mRNA in activated eosinophils. Nat Immunol 6: 1280-1287. (Pubitemid 43045640)
57. Chen CY, Xu N, Shyu AB (2002) Highly selective actions of HuR in antagonizing AU-rich element-mediated mRNA destabilization. Mol Cell Biol 22: 7268-7278.
58. Brennan CM, Steitz JA (2001) HuR and mRNA stability. Cell Mol Life Sci 58: 266-277. (Pubitemid 32217358)
59. Doller A, Huwiler A, Muller R, Radeke HH, Pfeilschifter J, et al. (2007) Protein kinase C alpha-dependent phosphorylation of the mRNA-stabilizing factor HuR: implications for posttranscriptional regulation of cyclooxygenase-2. Mol Biol Cell 18: 2137-2148. (Pubitemid 46911365)
60. Doller A, Akool el S, Huwiler A, Muller R, Radeke HH, et al. (2008) Posttranslational modification of the AU-rich element binding protein HuR by protein kinase Cdelta elicits angiotensin II-induced stabilization and nuclear export of cyclooxygenase 2 mRNA. Mol Cell Biol 28: 2608-2625.
61. Kim HH, Abdelmohsen K, Lal A, Pullmann R Jr., Yang X, et al. (2008) Nuclear HuR accumulation through phosphorylation by Cdk1. Genes Dev 22: 1804-1815. (Pubitemid 351915505)
62. Kim HH, Gorospe M (2008) Phosphorylated HuR shuttles in cycles. Cell Cycle 7: 3124-3126.