The PTEN Long N-tail is intrinsically disordered: Increased viability for PTEN therapy

Molecular BioSystems

Volumn 9, Issue 11, 2013, Pages 2877-2888

  Malaney, Prerna ^a   Uversky, Vladimir N ^a,b,c   Davé, Vrushank ^a,d  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c INSTITUTE FOR BIOLOGICAL INSTRUMENTATION   (Russian Federation)

^d H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN BINDING;

ANIMAL; ARTICLE; BINDING SITE; BIOLOGY; CHEMISTRY; HUMAN; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROCESSING; SEQUENCE HOMOLOGY; PROCEDURES;

ANIMALS; BINDING SITES; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; HUMANS; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PTEN PHOSPHOHYDROLASE; SEQUENCE HOMOLOGY;

EID: 84885096545     PISSN: 1742206X     EISSN: 17422051     Source Type: Journal    
DOI: 10.1039/c3mb70267g     Document Type: Article

References (98)

1. H. Sun et al., PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-trisphosphate and Akt/protein kinase B signaling pathway Proc. Natl. Acad. Sci. U. S. A. 1999 96 6199 6204
2. T. Maehama J. E. Dixon The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate J. Biol. Chem. 1998 273 13375 13378
3. C. Blanco-Aparicio O. Renner J. F. M. Leal A. Carnero PTEN, more than the AKT pathway Carcinogenesis 2007 28 1379 1386
4. M. C. Hollander G. M. Blumenthal P. A. Dennis PTEN loss in the continuum of common cancers, rare syndromes and mouse models Nat. Rev. Cancer 2011 11 289 301
5. A. H. Ross A. Gericke Phosphorylation keeps PTEN phosphatase closed for business Proc. Natl. Acad. Sci. U. S. A. 2009 106 1297 1298
6. M. Rahdar et al., A phosphorylation-dependent intramolecular interaction regulates the membrane association and activity of the tumor suppressor PTEN Proc. Natl. Acad. Sci. U. S. A. 2009 106 480 485
7. L. Odriozola G. Singh T. Hoang A. M. Chan Regulation of PTEN activity by its carboxyl-terminal autoinhibitory domain J. Biol. Chem. 2007 282 23306 23315
8. J. O. Lee et al., Crystal structure of the PTEN tumor suppressor: implications for its phosphoinositide phosphatase activity and membrane association Cell 1999 99 323 334
9. P. Malaney R. R. Pathak B. Xue V. N. Uversky V. Dave Intrinsic Disorder in PTEN and its Interactome Confers Structural Plasticity and Functional Versatility Sci. rep. 2013 3 2035
10. M. S. Song L. Salmena P. P. Pandolfi The functions and regulation of the PTEN tumour suppressor Nat. Rev.: Mol. Cell Biol. 2012 13 283 296
11. C. Xiao et al., Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes Nat. Immunol. 2008 9 405 414
12. V. Olive et al., miR-19 is a key oncogenic component of mir-17-92 Genes Dev. 2009 23 2839 2849
13. K. J. Mavrakis et al., Genome-wide RNA-mediated interference screen identifies miR-19 targets in Notch-induced T-cell acute lymphoblastic leukaemia Nat. Cell Biol. 2010 12 372 379
14. F. Meng et al., MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer Gastroenterology 2007 133 647 658
15. X. Ma et al., Loss of the miR-21 allele elevates the expression of its target genes and reduces tumorigenesis Proc. Natl. Acad. Sci. U. S. A. 2011 108 10144 10149
16. L. Poliseno et al., A coding-independent function of gene and pseudogene mRNAs regulates tumour biology Nature 2010 465 1033 1038
17. N. R. Leslie V. G. Brunton Where Is PTEN? Science 2013 341 355 356
18. J. L. Liu et al., Nuclear PTEN-mediated growth suppression is independent of Akt down-regulation Mol. Cell. Biol. 2005 25 6211 6224
19. W. H. Shen et al., Essential role for nuclear PTEN in maintaining chromosomal integrity Cell 2007 128 157 170
20. U. Putz et al., The Tumor Suppressor PTEN Is Exported in Exosomes and Has Phosphatase Activity in Recipient Cells Sci. Signaling 2012 5 ra70
21. B. D. Hopkins et al., A Secreted PTEN Phosphatase that Enters Cells to Alter Signaling and Survival Science 2013 341 399 402
22. K. Gabriel A. Ingram R. Austin A. Kapoor D. Tang et al., Regulation of the Tumor Suppressor PTEN through Exosomes: A Diagnostic Potential for Prostate Cancer PLoS ONE 2013 8 e70047 10.1371/journal.pone.0070047
23. S. Seton-Rogers Tumour suppressors: PTEN surprise Nat. Rev. Cancer 2013 13 520
24. M. Swami Tumor suppressors: A new PTEN translational variant Nat. Med. 2013 19 827
25. K. Legg PTEN goes paracrine Nat. Cell Biol. 2013 15 894
26. A. Papa M. Chen P. P. Pandolfi Pills of PTEN? In and out for tumor suppression Cell Res. 2013 10.1038/cr.2013.103
27. P. Romero et al., Sequence complexity of disordered protein Proteins 2001 42 38 48
28. K. Peng et al., Optimizing long intrinsic disorder predictors with protein evolutionary information J. Bioinf. Comput. Biol. 2005 3 35 60
29. B. Xue R. L. Dunbrack R. W. Williams A. K. Dunker V. N. Uversky PONDR-FIT: a meta-predictor of intrinsically disordered amino acids Biochim. Biophys. Acta 2010 1804 996 1010
30. C. J. Oldfield et al., Coupled folding and binding with alpha-helix-forming molecular recognition elements Biochemistry 2005 44 12454 12470
31. Y. Cheng et al., Mining alpha-helix-forming molecular recognition features with cross species sequence alignments Biochemistry 2007 46 13468 13477
32. K. Peng P. Radivojac S. Vucetic A. K. Dunker Z. Obradovic Length-dependent prediction of protein intrinsic disorder BMC Bioinf. 2006 7 208
33. J. Prilusky et al., FoldIndex: a simple tool to predict whether a given protein sequence is intrinsically unfolded Bioinformatics 2005 21 3435 3438
34. Z. Dosztanyi V. Csizmok P. Tompa I. Simon IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content Bioinformatics 2005 21 3433 3434
35. A. Campen et al., TOP-IDP-scale: a new amino acid scale measuring propensity for intrinsic disorder Protein Pept. Lett. 2008 15 956 963
36. G. G. Tartaglia et al., Prediction of aggregation-prone regions in structured proteins J. Mol. Biol. 2008 380 425 436
37. S. O. Garbuzynskiy M. Y. Lobanov O. V. Galzitskaya FoldAmyloid: a method of prediction of amyloidogenic regions from protein sequence Bioinformatics 2010 26 326 332
38. V. Vacic V. N. Uversky A. K. Dunker S. Lonardi Composition Profiler: a tool for discovery and visualization of amino acid composition differences BMC Bioinf. 2007 8 211
39. P. Radivojac et al., Identification, analysis, and prediction of protein ubiquitination sites Proteins 2010 78 365 380
40. L. M. Iakoucheva et al., The importance of intrinsic disorder for protein phosphorylation Nucleic Acids Res. 2004 32 1037 1049
41. N. Blom S. Gammeltoft S. Brunak Sequence and structure-based prediction of eukaryotic protein phosphorylation sites J. Mol. Biol. 1999 294 1351 1362
42. H. D. Huang T. Y. Lee S. W. Tzeng J. T. Horng KinasePhos: a web tool for identifying protein kinase-specific phosphorylation sites Nucleic Acids Res. 2005 33 W226 W229
43. R. Gupta S. Brunak Prediction of glycosylation across the human proteome and the correlation to protein function Pac. Symp. Biocomput. 2002 310 322
44. B. Meszaros I. Simon Z. Dosztanyi Prediction of protein binding regions in disordered proteins PLoS Comput. Biol. 2009 5 e1000376
45. Z. Dosztanyi B. Meszaros I. Simon ANCHOR: web server for predicting protein binding regions in disordered proteins Bioinformatics 2009 25 2745 2746
46. Z. Dosztanyi V. Csizmok P. Tompa I. Simon The pairwise energy content estimated from amino acid composition discriminates between folded and intrinsically unstructured proteins J. Mol. Biol. 2005 347 827 839
47. H. Dinkel et al., ELM - the database of eukaryotic linear motifs Nucleic Acids Res. 2012 40 D242 D251
48. A. Mohan et al., Analysis of molecular recognition features (MoRFs) J. Mol. Biol. 2006 362 1043 1059
49. V. Vacic et al., Characterization of molecular recognition features, MoRFs, and their binding partners J. Proteome Res. 2007 6 2351 2366
50. F. M. Disfani W.-L. Hsu M. J. Mizianty C. J. Oldfield B. Xue A. K. Dunker V. N. Uversky L. Kurgan MoRFpred, a computational tool for sequence-based prediction and characterization of disorder-to-order transitioning binding sites in proteins Bioinformatics 2012 i75 i83
51. J. Kim M. Mosior L. A. Chung H. Wu S. McLaughlin Binding of peptides with basic residues to membranes containing acidic phospholipids Biophys. J. 1991 60 135 148
52. I. Braakman N. J. Bulleid Protein folding and modification in the mammalian endoplasmic reticulum Annu. Rev. Biochem. 2011 80 71 99
53. G. G. Tartaglia M. Vendruscolo The Zyggregator method for predicting protein aggregation propensities Chem. Soc. Rev. 2008 37 1395 1401
54. E. Monsellier M. Ramazzotti N. Taddei F. Chiti Aggregation propensity of the human proteome PLoS Comput. Biol. 2008 4 e1000199
55. D. Xu J. Gao Correlation between posttranslational modification and intrinsic disorder in protein. Biocomputing 2012 94 103
56. S. I. Buschow J. M. Liefhebber R. Wubbolts W. Stoorvogel Exosomes contain ubiquitinated proteins Blood Cells, Mol., Dis. 2005 35 398 403
57. M. Simons G. Raposo Exosomes-vesicular carriers for intercellular communication Curr. Opin. Cell Biol. 2009 21 575 581
58. A. Golks D. Guerini The O-linked N-acetylglucosamine modification in cellular signalling and the immune system. 'Protein modifications: beyond the usual suspects' review series EMBO Rep. 2008 9 748 753
59. F. M. Disfani et al., MoRFpred, a computational tool for sequence-based prediction and characterization of short disorder-to-order transitioning binding regions in proteins Bioinformatics 2012 28 i75 i83
60. T. M. Handel et al., Regulation of protein function by glycosaminoglycans-as exemplified by chemokines Annu. Rev. Biochem. 2005 74 385 410
61. G. W. Yip M. Smollich M. Gotte Therapeutic value of glycosaminoglycans in cancer Mol. Cancer Ther. 2006 5 2139 2148
62. A. C. Prats G. De Billy P. Wang J. L. Darlix CUG initiation codon used for the synthesis of a cell surface antigen coded by the murine leukemia virus J. Mol. Biol. 1989 205 363 372
63. J. Curran D. Kolakofsky Ribosomal initiation from an ACG codon in the Sendai virus P/C mRNA EMBO J. 1988 7 245 251
64. M. Strubin E. O. Long B. Mach Two forms of the Ia antigen-associated invariant chain result from alternative initiations at two in-phase AUGs Cell 1986 47 619 625
65. L. Kazak et al., Alternative translation initiation augments the human mitochondrial proteome Nucleic Acids Res. 2013 41 2354 2369
66. I. P. Ivanov A. E. Firth A. M. Michel J. F. Atkins P. V. Baranov Identification of evolutionarily conserved non-AUG-initiated N-terminal extensions in human coding sequences Nucleic Acids Res. 2011 39 4220 4234
67. J. Sambrook Adenovirus amazes at Cold Spring Harbor Nature 1977 268 101 104
68. D. L. Black Mechanisms of alternative pre-messenger RNA splicing Annu. Rev. Biochem. 2003 72 291 336
69. W. Gilbert Why genes in pieces? Nature 1978 271 501
70. G. Ast How did alternative splicing evolve? Nat. Rev. Genet. 2004 5 773 782
71. M. Irimia J. L. Rukov D. Penny S. W. Roy Functional and evolutionary analysis of alternatively spliced genes is consistent with an early eukaryotic origin of alternative splicing BMC Evol. Biol. 2007 7 188
72. B. R. Graveley Alternative splicing: increasing diversity in the proteomic world Trends Genet 2001 17 100 107
73. K. P. Minneman Splice variants of G protein-coupled receptors Mol. interventions 2001 1 108 116
74. T. H. Thai J. F. Kearney Distinct and opposite activities of human terminal deoxynucleotidyltransferase splice variants J. Immunol. 2004 173 4009 4019
75. W. Scheper R. Zwart F. Baas Alternative splicing in the N-terminus of Alzheimer's presenilin 1 Neurogenetics 2004 5 223 227
76. P. R. Romero et al., Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms Proc. Natl. Acad. Sci. U. S. A. 2006 103 8390 8395
77. V. N. Uversky Intrinsic disorder-based protein interactions and their modulators Curr. Pharm. Des. 2013 19 4191 4213
78. E. Kovacs P. Tompa K. Liliom L. Kalmar Dual coding in alternative reading frames correlates with intrinsic protein disorder Proc. Natl. Acad. Sci. U. S. A. 2010 107 5429 5434
79. M. Buljan et al., Tissue-specific splicing of disordered segments that embed binding motifs rewires protein interaction networks Mol. Cell 2012 46 871 883
80. M. Buljan et al., Alternative splicing of intrinsically disordered regions and rewiring of protein interactions Curr. Opin. Struct. Biol. 2013 23 443 450
81. C. Helwick, Targeting KRAS in GI Cancers: The Hunt for the Holy Grail in Cancer Research, The ASCO Post, vol. 3, 2012
82. A. D. Cox C. J. Der Ras history: The saga continues Small GTPases 2010 1 2 27
83. W. H. Chappell et al., Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR inhibitors: rationale and importance to inhibiting these pathways in human health Oncotarget 2011 2 135 164
84. K. D. Courtney R. B. Corcoran J. A. Engelman The PI3K Pathway As Drug Target in Human Cancer J. Clin. Oncol. 2010 28 1075 1083
85. B. T. Hennessy D. L. Smith P. T. Ram Y. Lu G. B. Mills Exploiting the PI3K/AKT pathway for cancer drug discovery Nat. Rev. Drug Discovery 2005 4 988 1004
86. A. Carracedo et al., Inhibition of mTORC1 leads to MAPK pathway activation through a PI3K-dependent feedback loop in human cancer J. Clin. Invest. 2008 118 3065 3074
87. J. Tamburini et al., Mammalian target of rapamycin (mTOR), inhibition activates phosphatidylinositol 3-kinase/Akt by up-regulating insulin-like growth factor-1 receptor signaling in acute myeloid leukemia: rationale for therapeutic inhibition of both pathways Blood 2008 111 379 382
88. P. Lito et al., Relief of Profound Feedback Inhibition of Mitogenic Signaling by RAF Inhibitors Attenuates Their Activity in BRAFV600E Melanomas Cancer Cell 2012 22 668 682
89. H. Wang H. Y. Han S. Mousses D. D. Von Hoff Targeting loss-of-function mutations in tumor-suppressor genes as a strategy for development of cancer therapeutic agents Semin. Oncol. 2006 33 513 520
90. M. Shehata et al., Reconstitution of PTEN activity by CK2 inhibitors and interference with the PI3-K/Akt cascade counteract the antiapoptotic effect of human stromal cells in chronic lymphocytic leukemia Blood 2010 116 2513 2521
91. G. Singh A. M. Chan Post-Translational Modifications of PTEN and their Potential Therapeutic Implications Curr. Cancer Drug Targets 2011 11 536 547
92. S. Miwa et al., Caffeine activates tumor suppressor PTEN in sarcoma cells Int. J. Oncol. 2011 39 465 472
93. M. H. Traka et al., The dietary isothiocyanate sulforaphane modulates gene expression and alternative gene splicing in a PTEN null preclinical murine model of prostate cancer Mol. Cancer 2010 9 189
94. Y. Wang et al., Resveratrol regulates the PTEN/AKT pathway through androgen receptor-dependent and -independent mechanisms in prostate cancer cell lines Hum. Mol. Genet. 2010 19 4319 4329
95. M. J. Bissell W. C. Hines Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression Nat. Med. 2011 17 320 329
96. S. Chowdhury et al., Restoration of PTEN activity decreases metastases in an orthotopic model of colon cancer J. Surg. Res. 2013 10.1016/j.jss.2013.03. 035
97. A. Bronisz et al., Reprogramming of the tumour microenvironment by stromal PTEN-regulated miR-320 Nat. Cell Biol. 2012 14 159 167
98. A. J. Trimboli et al., Pten in stromal fibroblasts suppresses mammary epithelial tumours Nature 2009 461 1084 1091