Inhibition of androgen receptor functions by gelsolin FxxFF peptide delivered by transfection, cell-penetrating peptides, and lentiviral infection

Prostate

Volumn 71, Issue 3, 2011, Pages 241-253

  Van De Wijngaart, Dennis J ^a   Dubbink, Hendrikus J ^a   Molier, Michel ^a   De Vos, Carola ^a   Jenster, Guido ^a   Trapman, Jan ^a  

^a JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

Author keywords

androgen receptor; cell penetrating peptide; FxxFF; gene expression; TAT

Indexed keywords

ANDROGEN RECEPTOR; CELL PENETRATING PEPTIDE; GELSOLIN; GLUCOCORTICOID RECEPTOR; PROGESTERONE RECEPTOR;

ARTICLE; CELL STRAIN LNCAP; EXPRESSION VECTOR; GENE EXPRESSION; HORMONE BINDING; HORMONE INHIBITION; IN VITRO STUDY; INCUBATION TEMPERATURE; LENTIVIRUS INFECTION; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; TRANSIENT TRANSFECTION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANDROGEN RECEPTOR ANTAGONISTS; CELL-PENETRATING PEPTIDES; GELSOLIN; GENE EXPRESSION REGULATION; HUMANS; LENTIVIRUS; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ANDROGEN; TRANSFECTION;

EID: 78951475635     PISSN: 02704137     EISSN: 10970045     Source Type: Journal    
DOI: 10.1002/pros.21238     Document Type: Article

References (73)

1. Feldman BJ, Feldman D,. The development of androgen-independent prostate cancer. Nat Rev Cancer 2001; 1: 34-45.
2. Trapman J, Brinkmann AO,. The androgen receptor in prostate cancer. Pathol Res Pract 1996; 192: 752-760.
3. van der Kwast TH, Schalken J, Ruizeveld de Winter JA, van Vroonhoven CC, Mulder E, Boersma W, Trapman J,. Androgen receptors in endocrine-therapy- resistant human prostate cancer. Int J Cancer 1991; 48: 189-193.
4. Balk SP,. Androgen receptor as a target in androgen-independent prostate cancer. Urology 2002; 60 (3 Suppl 1): 132-138; discussion 138-139.
5. Taplin ME,. Drug insight: Role of the androgen receptor in the development and progression of prostate cancer. Nat Clin Pract Oncol 2007; 4: 236-244.
6. Visakorpi T, Hyytinen E, Koivisto P, Tanner M, Keinanen R, Palmberg C, Palotie A, Tammela T, Isola J, Kallioniemi OP,. In vivo amplification of the androgen receptor gene and progression of human prostate cancer. Nat Genet 1995; 9: 401-406.
7. Mohler JL, Gregory CW, Ford OH III, Kim D, Weaver CM, Petrusz P, Wilson EM, French FS,. The androgen axis in recurrent prostate cancer. Clin Cancer Res 2004; 10: 440-448.
8. Mostaghel EA, Page ST, Lin DW, Fazli L, Coleman IM, True LD, Knudsen B, Hess DL, Nelson CC, Matsumoto AM, Bremner WJ, Gleave ME, Nelson PS,. Intraprostatic androgens and androgen-regulated gene expression persist after testosterone suppression: Therapeutic implications for castration-resistant prostate cancer. Cancer Res 2007; 67: 5033-5041.
9. Titus MA, Schell MJ, Lih FB, Tomer KB, Mohler JL,. Testosterone and dihydrotestosterone tissue levels in recurrent prostate cancer. Clin Cancer Res 2005; 11: 4653-4657.
10. Hermans KG, van der Korput HA, van Marion R, van de Wijngaart DJ, Ziel-van der Made A, Dits NF, Boormans JL, van der Kwast TH, van Dekken H, Bangma CH, Korsten H, Kraaij R, Jenster G, Trapman J,. Truncated ETV1, fused to novel tissue-specific genes, and full-length ETV1 in prostate cancer. Cancer Res 2008; 68: 7541-7549.
11. Hermans KG, van Marion R, van Dekken H, Jenster G, van Weerden WM, Trapman J,. TMPRSS2: ERG fusion by translocation or interstitial deletion is highly relevant in androgen-dependent prostate cancer, but is bypassed in late-stage androgen receptor-negative prostate cancer. Cancer Res 2006; 66: 10658-10663.
12. Tomlins SA, Laxman B, Dhanasekaran SM, Helgeson BE, Cao X, Morris DS, Menon A, Jing X, Cao Q, Han B, Yu J, Wang L, Montie JE, Rubin MA, Pienta KJ, Roulston D, Shah RB, Varambally S, Mehra R, Chinnaiyan AM,. Distinct classes of chromosomal rearrangements create oncogenic ETS gene fusions in prostate cancer. Nature 2007; 448: 595-599.
13. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, Lee C, Montie JE, Shah RB, Pienta KJ, Rubin MA, Chinnaiyan AM,. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005; 310: 644-648.
14. Bain DL, Heneghan AF, Connaghan-Jones KD, Miura MT,. Nuclear receptor structure: Implications for function. Annu Rev Physiol 2007; 69: 201-220.
15. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM,. The nuclear receptor superfamily: The second decade. Cell 1995; 83: 835-839.
16. Huang ZQ, Li J, Sachs LM, Cole PA, Wong J,. A role for cofactor-cofactor and cofactor-histone interactions in targeting p300, SWI/SNF and Mediator for transcription. EMBO J 2003; 22: 2146-2155.
17. Kang Z, Janne OA, Palvimo JJ,. Coregulator recruitment and histone modifications in transcriptional regulation by the androgen receptor. Mol Endocrinol 2004; 18: 2633-2648.
18. Louie MC, Yang HQ, Ma AH, Xu W, Zou JX, Kung HJ, Chen HW,. Androgen-induced recruitment of RNA polymerase II to a nuclear receptor-p160 coactivator complex. Proc Natl Acad Sci USA 2003; 100: 2226-2230.
19. Marshall TW, Link KA, Petre-Draviam CE, Knudsen KE,. Differential requirement of SWI/SNF for androgen receptor activity. J Biol Chem 2003; 278: 30605-30613.
20. Shang Y, Myers M, Brown M,. Formation of the androgen receptor transcription complex. Mol Cell 2002; 9: 601-610.
21. Vijayvargia R, May MS, Fondell JD,. A coregulatory role for the mediator complex in prostate cancer cell proliferation and gene expression. Cancer Res 2007; 67: 4034-4041.
22. Wang Q, Carroll JS, Brown M,. Spatial and temporal recruitment of androgen receptor and its coactivators involves chromosomal looping and polymerase tracking. Mol Cell 2005; 19: 631-642.
23. van de Wijngaart DJ, Dubbink HJ, Molier M, de Vos C, Trapman J, Jenster G,. Functional screening of FxxLF-like peptide motifs identifies SMARCD1/BAF60a as an androgen receptor cofactor that modulates TMPRSS2 expression. Mol Endocrinol 2009; 23: 1776-1786.
24. Estebanez-Perpina E, Moore JM, Mar E, Delgado-Rodrigues E, Nguyen P, Baxter JD, Buehrer BM, Webb P, Fletterick RJ, Guy RK,. The molecular mechanisms of coactivator utilization in ligand-dependent transactivation by the androgen receptor. J Biol Chem 2005; 280: 8060-8068.
25. He B, Gampe RT, Jr., Kole AJ, Hnat AT, Stanley TB, An G, Stewart EL, Kalman RI, Minges JT, Wilson EM,. Structural basis for androgen receptor interdomain and coactivator interactions suggests a transition in nuclear receptor activation function dominance. Mol Cell 2004; 16: 425-438.
26. Hur E, Pfaff SJ, Payne ES, Gron H, Buehrer BM, Fletterick RJ,. Recognition and accommodation at the androgen receptor coactivator binding interface. PLoS Biol 2004; 2: E274.
27. Darimont BD, Wagner RL, Apriletti JW, Stallcup MR, Kushner PJ, Baxter JD, Fletterick RJ, Yamamoto KR,. Structure and specificity of nuclear receptor-coactivator interactions. Genes Dev 1998; 12: 3343-3356.
28. Ding XF, Anderson CM, Ma H, Hong H, Uht RM, Kushner PJ, Stallcup MR,. Nuclear receptor-binding sites of coactivators glucocorticoid receptor interacting protein 1 (GRIP1) and steroid receptor coactivator 1 (SRC-1): Multiple motifs with different binding specificities. Mol Endocrinol 1998; 12: 302-313.
29. Heery DM, Kalkhoven E, Hoare S, Parker MG,. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 1997; 387: 733-736.
30. Chang CY, Abdo J, Hartney T, McDonnell DP,. Development of peptide antagonists for the androgen receptor using combinatorial peptide phage display. Mol Endocrinol 2005; 19: 2478-2490.
31. Dubbink HJ, Hersmus R, Pike AC, Molier M, Brinkmann AO, Jenster G, Trapman J,. Androgen receptor ligand-binding domain interaction and nuclear receptor specificity of FXXLF and LXXLL motifs as determined by L/F swapping. Mol Endocrinol 2006; 20: 1742-1755.
32. Dubbink HJ, Hersmus R, Verma CS, van der Korput HA, Berrevoets CA, van Tol J, Ziel-van der Made AC, Brinkmann AO, Pike AC, Trapman J,. Distinct recognition modes of FXXLF and LXXLL motifs by the androgen receptor. Mol Endocrinol 2004; 18: 2132-2150.
33. He B, Kemppainen JA, Wilson EM,. FXXLF and WXXLF sequences mediate the NH2-terminal interaction with the ligand binding domain of the androgen receptor. J Biol Chem 2000; 275: 22986-22994.
34. Steketee K, Berrevoets CA, Dubbink HJ, Doesburg P, Hersmus R, Brinkmann AO, Trapman J,. Amino acids 3-13 and amino acids in and flanking the 23FxxLF27 motif modulate the interaction between the N-terminal and ligand-binding domain of the androgen receptor. Eur J Biochem 2002; 269: 5780-5791.
35. Askew EB, Gampe RT, Jr., Stanley TB, Faggart JL, Wilson EM,. Modulation of androgen receptor activation function 2 by testosterone and dihydrotestosterone. J Biol Chem 2007; 282: 25801-25816.
36. Callewaert L, Verrijdt G, Christiaens V, Haelens A, Claessens F,. Dual function of an amino-terminal amphipatic helix in androgen receptor-mediated transactivation through specific and nonspecific response elements. J Biol Chem 2003; 278: 8212-8218.
37. He B, Lee LW, Minges JT, Wilson EM,. Dependence of selective gene activation on the androgen receptor NH2- and COOH-terminal interaction. J Biol Chem 2002; 277: 25631-25639.
38. van Royen ME, Cunha SM, Brink MC, Mattern KA, Nigg AL, Dubbink HJ, Verschure PJ, Trapman J, Houtsmuller AB,. Compartmentalization of androgen receptor protein-protein interactions in living cells. J Cell Biol 2007; 177: 63-72.
39. Hsu CL, Chen YL, Yeh S, Ting HJ, Hu YC, Lin H, Wang X, Chang C,. The use of phage display technique for the isolation of androgen receptor interacting peptides with (F/W)XXL(F/W) and FXXLY new signature motifs. J Biol Chem 2003; 278: 23691-23698.
40. van de Wijngaart DJ, van Royen ME, Hersmus R, Pike AC, Houtsmuller AB, Jenster G, Trapman J, Dubbink HJ,. Novel FXXFF and FXXMF motifs in androgen receptor cofactors mediate high affinity and specific interactions with the ligand-binding domain. J Biol Chem 2006; 281: 19407-19416.
41. Vives E, Brodin P, Lebleu B,. A truncated HIV-1 Tat protein basic domain rapidly translocates through the plasma membrane and accumulates in the cell nucleus. J Biol Chem 1997; 272: 16010-16017.
42. Wender PA, Mitchell DJ, Pattabiraman K, Pelkey ET, Steinman L, Rothbard JB,. The design, synthesis, and evaluation of molecules that enable or enhance cellular uptake: Peptoid molecular transporters. Proc Natl Acad Sci USA 2000; 97: 13003-13008.
43. Doesburg P, Kuil CW, Berrevoets CA, Steketee K, Faber PW, Mulder E, Brinkmann AO, Trapman J,. Functional in vivo interaction between the amino-terminal, transactivation domain and the ligand binding domain of the androgen receptor. Biochemistry 1997; 36: 1052-1064.
44. Jenster G, van der Korput HA, Trapman J, Brinkmann AO,. Identification of two transcription activation units in the N-terminal domain of the human androgen receptor. J Biol Chem 1995; 270: 7341-7346.
45. Brinkmann AO, Faber PW, van Rooij HC, Kuiper GG, Ris C, Klaassen P, van der Korput JA, Voorhorst MM, van Laar JH, Mulder E, Trapman J,. The human androgen receptor: Domain structure, genomic organization and regulation of expression. J Steroid Biochem 1989; 34: 307-310.
46. Cleutjens KB, van Eekelen CC, van der Korput HA, Brinkmann AO, Trapman J,. Two androgen response regions cooperate in steroid hormone regulated activity of the prostate-specific antigen promoter. J Biol Chem 1996; 271: 6379-6388.
47. Jenster G, Spencer TE, Burcin MM, Tsai SY, Tsai MJ, O'Malley BW,. Steroid receptor induction of gene transcription: A two-step model. Proc Natl Acad Sci USA 1997; 94: 7879-7884.
48. Ozers MS, Marks BD, Gowda K, Kupcho KR, Ervin KM, De Rosier T, Qadir N, Eliason HC, Riddle SM, Shekhani MS,. The androgen receptor T877A mutant recruits LXXLL and FXXLF peptides differently than wild-type androgen receptor in a time-resolved fluorescence resonance energy transfer assay. Biochemistry 2007; 46: 683-695.
49. Chang C, Norris JD, Gron H, Paige LA, Hamilton PT, Kenan DJ, Fowlkes D, McDonnell DP,. Dissection of the LXXLL nuclear receptor-coactivator interaction motif using combinatorial peptide libraries: Discovery of peptide antagonists of estrogen receptors alpha and beta. Mol Cell Biol 1999; 19: 8226-8239.
50. He B, Minges JT, Lee LW, Wilson EM,. The FXXLF motif mediates androgen receptor-specific interactions with coregulators. J Biol Chem 2002; 277: 10226-10235.
51. Wang L, Hsu CL, Ni J, Wang PH, Yeh S, Keng P, Chang C,. Human checkpoint protein hRad9 functions as a negative coregulator to repress androgen receptor transactivation in prostate cancer cells. Mol Cell Biol 2004; 24: 2202-2213.
52. Eichler J,. Peptides as protein binding site mimetics. Curr Opin Chem Biol 2008; 12: 707-713.
53. Rubinstein M, Niv MY,. Peptidic modulators of protein-protein interactions: Progress and challenges in computational design. Biopolymers 2009; 91: 505-513.
54. Chene P,. Inhibiting the p53-MDM2 interaction: An important target for cancer therapy. Nat Rev Cancer 2003; 3: 102-109.
55. Fischer PM,. Peptide, peptidomimetic, and small-molecule antagonists of the p53-HDM2 protein-protein interaction. Int J Pept Res Ther 2006; 12 (1): 3-19.
56. Murray JK, Gellman SH,. Targeting protein-protein interactions: Lessons from p53/MDM2. Biopolymers 2007; 88: 657-686.
57. Kussie PH, Gorina S, Marechal V, Elenbaas B, Moreau J, Levine AJ, Pavletich NP,. Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science 1996; 274: 948-953.
58. Picksley SM, Vojtesek B, Sparks A, Lane DP,. Immunochemical analysis of the interaction of p53 with MDM2âFine mapping of the MDM2 binding site on p53 using synthetic peptides. Oncogene 1994; 9: 2523-2529.
59. Kurebayashi S, Nakajima T, Kim SC, Chang CY, McDonnell DP, Renaud JP, Jetten AM,. Selective LXXLL peptides antagonize transcriptional activation by the retinoid-related orphan receptor RORgamma. Biochem Biophys Res Commun 2004; 315: 919-927.
60. Mettu NB, Stanley TB, Dwyer MA, Jansen MS, Allen JE, Hall JM, McDonnell DP,. The nuclear receptor-coactivator interaction surface as a target for peptide antagonists of the peroxisome proliferator-activated receptors. Mol Endocrinol 2007; 21: 2361-2377.
61. Pathrose P, Barmina O, Chang CY, McDonnell DP, Shevde NK, Pike JW,. Inhibition of 1,25-dihydroxyvitamin D3-dependent transcription by synthetic LXXLL peptide antagonists that target the activation domains of the vitamin D and retinoid X receptors. J Bone Miner Res 2002; 17: 2196-2205.
62. Carraz M, Zwart W, Phan T, Michalides R, Brunsveld L,. Perturbation of estrogen receptor alpha localization with synthetic nona-arginine LXXLL-peptide coactivator binding inhibitors. Chem Biol 2009; 16: 702-711.
63. Gaillard S, Dwyer MA, McDonnell DP,. Definition of the molecular basis for estrogen receptor-related receptor-alpha-cofactor interactions. Mol Endocrinol 2007; 21: 62-76.
64. Hsu CL, Chen YL, Ting HJ, Lin WJ, Yang Z, Zhang Y, Wang L, Wu CT, Chang HC, Yeh S, Pimplikar SW, Chang C,. Androgen receptor (AR) NH2- and COOH-terminal interactions result in the differential influences on the AR-mediated transactivation and cell growth. Mol Endocrinol 2005; 19: 350-361.
65. Dietz GP, Bahr M,. Delivery of bioactive molecules into the cell: The Trojan horse approach. Mol Cell Neurosci 2004; 27: 85-131.
66. Schwarze SR, Ho A, Vocero-Akbani A, Dowdy SF,. In vivo protein transduction: Delivery of a biologically active protein into the mouse. Science 1999; 285: 1569-1572.
67. Fonseca SB, Pereira MP, Kelley SO,. Recent advances in the use of cell-penetrating peptides for medical and biological applications. Adv Drug Deliv Rev 2009; 61: 953-964.
68. Snyder EL, Dowdy SF,. Recent advances in the use of protein transduction domains for the delivery of peptides, proteins and nucleic acids in vivo. Expert Opin Drug Deliv 2005; 2: 43-51.
69. Vives E, Schmidt J, Pelegrin A,. Cell-penetrating and cell-targeting peptides in drug delivery. Biochim Biophys Acta 2008; 1786: 126-138.
70. Derossi D, Joliot AH, Chassaing G, Prochiantz A,. The third helix of the Antennapedia homeodomain translocates through biological membranes. J Biol Chem 1994; 269: 10444-10450.
71. Mitchell DJ, Kim DT, Steinman L, Fathman CG, Rothbard JB,. Polyarginine enters cells more efficiently than other polycationic homopolymers. J Pept Res 2000; 56: 318-325.
72. Alen P, Claessens F, Verhoeven G, Rombauts W, Peeters B,. The androgen receptor amino-terminal domain plays a key role in p160 coactivator-stimulated gene transcription. Mol Cell Biol 1999; 19: 6085-6097.
73. Bevan CL, Hoare S, Claessens F, Heery DM, Parker MG,. The AF1 and AF2 domains of the androgen receptor interact with distinct regions of SRC1. Mol Cell Biol 1999; 19: 8383-8392.