Protein arginine methyltransferase 5 functions in opposite ways in the cytoplasm and nucleus of prostate cancer cells

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Gu, Zhongping ^a,b   Li, Yirong ^c   Lee, Peng ^c   Liu, Tao ^d   Wan, Chidan ^d   Wang, Zhengxin ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^d HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN ARGININE METHYLTRANSFERASE 5; PROTEIN P44; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER CELL; CELL COUNT; CELL GROWTH; CELL NUCLEUS; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVITY; GENE EXPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; NONHUMAN; OPEN READING FRAME; PATHOGENESIS; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE, TUMOR; CELL NUCLEUS; CELL PROLIFERATION; CERCOPITHECUS AETHIOPS; COS CELLS; GENE SILENCING; HUMANS; MALE; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR LOCALIZATION SIGNALS; PROSTATIC NEOPLASMS; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEIN-ARGININE N-METHYLTRANSFERASES; SUBCELLULAR FRACTIONS; SUBSTRATE SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 84865429451     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044033     Document Type: Article

References (52)

1. Bedford MT, Clarke SG, (2009) Protein arginine methylation in mammals: who, what, and why. Mol Cell 33: 1-13.
2. Jansson M, Durant ST, Cho EC, Sheahan S, Edelmann M, et al. (2008) Arginine methylation regulates the p53 response. Nat Cell Biol 10: 1431-1439.
3. Bedford MT, Richard S, (2005) Arginine methylation: an emerging regulator of protein function. Mol Cell 18: 263-272.
4. Amente S, Napolitano G, Licciardo P, Monti M, Pucci P, et al. (2005) Identification of proteins interacting with the RNAPII FCP1 phosphatase: FCP1 forms a complex with arginine methyltransferase PRMT5 and it is a substrate for PRMT5-mediated methylation. FEBS Lett 579: 683-689.
5. Liu C, Lu F, Cui X, Cao X, (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61: 395-420.
6. Ren J, Wang Y, Liang Y, Zhang Y, Bao S, et al. (2010) Methylation of ribosomal protein S10 by protein-arginine methyltransferase 5 regulates ribosome biogenesis. J Biol Chem 285: 12695-12705.
7. Zhou Z, Sun X, Zou Z, Sun L, Zhang T, et al. (2010) PRMT5 regulates Golgi apparatus structure through methylation of the golgin GM130. Cell Res 20: 1023-1033.
8. Tee WW, Pardo M, Theunissen TW, Yu L, Choudhary JS, et al. (2010) Prmt5 is essential for early mouse development and acts in the cytoplasm to maintain ES cell pluripotency. Genes Dev 24: 2772-2777.
9. Nagamatsu G, Kosaka T, Kawasumi M, Kinoshita T, Takubo K, et al. (2011) A germ cell-specific gene, Prmt5, works in somatic cell reprogramming. J Biol Chem 286: 10641-10648.
10. Gonsalvez GB, Rajendra TK, Tian L, Matera AG, (2006) The Sm-protein methyltransferase, dart5, is essential for germ-cell specification and maintenance. Curr Biol 16: 1077-1089.
11. Yang M, Sun J, Sun X, Shen Q, Gao Z, et al. (2009) Caenorhabditis elegans protein arginine methyltransferase PRMT-5 negatively regulates DNA damage-induced apoptosis. PLoS Genet 5: e1000514.
12. Ancelin K, Lange UC, Hajkova P, Schneider R, Bannister AJ, et al. (2006) Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat Cell Biol 8: 623-630.
13. Vagin VV, Wohlschlegel J, Qu J, Jonsson Z, Huang X, et al. (2009) Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev 23: 1749-1762.
14. Le Guezennec X, Vermeulen M, Brinkman AB, Hoeijmakers WA, Cohen A, et al. (2006) MBD2/NuRD and MBD3/NuRD, two distinct complexes with different biochemical and functional properties. Mol Cell Biol 26: 843-851.
15. Pal S, Vishwanath SN, Erdjument-Bromage H, Tempst P, Sif S, (2004) Human SWI/SNF-associated PRMT5 methylates histone H3 arginine 8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes. Mol Cell Biol 24: 9630-9645.
16. Friesen WJ, Paushkin S, Wyce A, Massenet S, Pesiridis GS, et al. (2001) The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins. Mol Cell Biol 21: 8289-8300.
17. Meister G, Eggert C, Buhler D, Brahms H, Kambach C, et al. (2001) Methylation of Sm proteins by a complex containing PRMT5 and the putative U snRNP assembly factor pICln. Curr Biol 11: 1990-1994.
18. Friesen WJ, Wyce A, Paushkin S, Abel L, Rappsilber J, et al. (2002) A novel WD repeat protein component of the methylosome binds Sm proteins. J Biol Chem 277: 8243-8247.
19. Brahms H, Meheus L, de Brabandere V, Fischer U, Luhrmann R, (2001) Symmetrical dimethylation of arginine residues in spliceosomal Sm protein B/B' and the Sm-like protein LSm4, and their interaction with the SMN protein. RNA 7: 1531-1542.
20. Friesen WJ, Massenet S, Paushkin S, Wyce A, Dreyfuss G, (2001) SMN, the product of the spinal muscular atrophy gene, binds preferentially to dimethylarginine-containing protein targets. Mol Cell 7: 1111-1117.
21. Meister G, Fischer U, (2002) Assisted RNP assembly: SMN and PRMT5 complexes cooperate in the formation of spliceosomal UsnRNPs. EMBO J 21: 5853-5863.
22. Neuenkirchen N, Chari A, Fischer U, (2008) Deciphering the assembly pathway of Sm-class U snRNPs. FEBS Lett 582: 1997-2003.
23. Boisvert FM, Cote J, Boulanger MC, Cleroux P, Bachand F, et al. (2002) Symmetrical dimethylarginine methylation is required for the localization of SMN in Cajal bodies and pre-mRNA splicing. J Cell Biol 159: 957-969.
24. Hosohata K, Li P, Hosohata Y, Qin J, Roeder RG, et al. (2003) Purification and identification of a novel complex which is involved in androgen receptor-dependent transcription. Mol Cell Biol 23: 7019-7029.
25. Zhou L, Wu H, Lee P, Wang Z, (2006) Roles of the androgen receptor cofactor p44 in the growth of prostate epithelial cells. J Mol Endocrinol 37: 283-300.
26. Peng Y, Chen F, Melamed J, Chiriboga L, Wei J, et al. (2008) Distinct nuclear and cytoplasmic functions of androgen receptor cofactor p44 and association with androgen-independent prostate cancer. Proc Natl Acad Sci USA 105: 5236-5241.
27. Gao S, Wu H, Wang F, Wang Z, (2011) Altered differentiation and proliferation of prostate epithelium in mice lacking the androgen receptor cofactor p44/WDR77. Endocrinology 151: 3941-3953.
28. Gu Z, Zhou L, Gao S, Wang Z, (2011) Nuclear transport signals control cellular localization and function of androgen receptor cofactor p44/WDR77. PLoS One 6: e22395.
29. Hayward SW, Baskin LS, Haughney PC, Cunha AR, Foster BA, et al. (1996) Epithelial development in the rat ventral prostate, anterior prostate and seminal vesicle. Acta Anat (Basel) 155: 81-93.
30. Cunha GR, Donjacour AA, Cooke PS, Mee S, Bigsby RM, et al. (1987) The endocrinology and developmental biology of the prostate. Endocr Rev 8: 338-362.
31. Timms BG, Mohs TJ, Didio LJ, (1994) Ductal budding and branching patterns in the developing prostate. J Urol 151: 1427-1432.
32. Kellokumpu-Lehtinen P, (1985) Development of sexual dimorphism in human urogenital sinus complex. Biol Neonate 48: 157-167.
33. Guderian G, Peter C, Wiesner J, Sickmann A, Schulze-Osthoff K, et al. (2011) RioK1, a new interactor of protein arginine methyltransferase 5 (PRMT5), competes with pICln for binding and modulates PRMT5 complex composition and substrate specificity. J Biol Chem 286: 1976-1986.
34. Kroiss M, Brunger KM, Wiesner J, Grimmler M, Sickmann A, et al. (2009) Native purification of protein and RNA-protein complexes using a novel affinity procedure. Fly (Austin) 3: 221-228.
35. Hou Z, Peng H, Ayyanathan K, Yan KP, Langer EM, et al. (2008) The LIM protein AJUBA recruits protein arginine methyltransferase 5 to mediate SNAIL-dependent transcriptional repression. Mol Cell Biol 28: 3198-3207.
36. Liang JJ, Wang Z, Chiriboga L, Greco MA, Shapiro E, et al. (2007) The expression and function of androgen receptor coactivator p44 and protein arginine methyltransferase 5 in the developing testis and testicular tumors. J Urol 177: 1918-1922.
37. Peng Y, Li CX, Chen F, Wang Z, Ligr M, et al. (2008) Stimulation of prostate cancer cellular proliferation and invasion by the androgen receptor co-activator ARA70. Am J Pathol 172: 225-235.
38. Rho J, Choi S, Seong YR, Cho WK, Kim SH, et al. (2001) Prmt5, which forms distinct homo-oligomers, is a member of the protein-arginine methyltransferase family. J Biol Chem 276: 11393-11401.
39. Pal S, Baiocchi RA, Byrd JC, Grever MR, Jacob ST, et al. (2007) Low levels of miR-92b/96 induce PRMT5 translation and H3R8/H4R3 methylation in mantle cell lymphoma. EMBO J 26: 3558-3569.
40. Spector DL, (2001) Nuclear domains. J Cell Sci 114: 2891-2893.
41. Gall JG, (2000) Cajal bodies: the first 100 years. Annu Rev Cell Dev Biol 16: 273-300.
42. Morgan GT, Doyle O, Murphy C, Gall JG, (2000) RNA polymerase II in Cajal bodies of amphibian oocytes. J Struct Biol 129: 258-268.
43. Shen J, Zhau HE, Hursting SD, Chung LW, (1998) Androgen regulation of the human pseudoautosomal gene MIC2, a potential marker for prostate cancer. Mol Carcinog 23: 13-19.
44. Fornerod M, Ohno M, Yoshida M, Mattaj IW, (1997) CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90: 1051-1060.
45. Pollack BP, Kotenko SV, He W, Izotova LS, Barnoski BL, et al. (1999) The human homologue of the yeast proteins Skb1 and Hsl7p interacts with Jak kinases and contains protein methyltransferase activity. J Biol Chem 274: 31531-31542.
46. Pesiridis GS, Diamond E, Van Duyne GD, (2009) Role of pICLn in methylation of Sm proteins by PRMT5. J Biol Chem 284: 21347-21359.
47. Branscombe TL, Frankel A, Lee JH, Cook JR, Yang Z, et al. (2001) PRMT5 (Janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J Biol Chem 276: 32971-32976.
48. Zhao Q, Rank G, Tan YT, Li H, Moritz RL, et al. (2009) PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat Struct Mol Biol 16: 304-311.
49. Eguizabal C, Shovlin TC, Durcova-Hills G, Surani A, McLaren A, (2009) Generation of primordial germ cells from pluripotent stem cells. Differentiation 78: 116-123.
50. Durcova-Hills G, Tang F, Doody G, Tooze R, Surani MA, (2008) Reprogramming primordial germ cells into pluripotent stem cells. PLoS One 3: e3531.
51. Eckert D, Biermann K, Nettersheim D, Gillis AJ, Steger K, et al. (2008) Expression of BLIMP1/PRMT5 and concurrent histone H2A/H4 arginine 3 dimethylation in fetal germ cells, CIS/IGCNU and germ cell tumors. BMC Dev Biol 8: 106.
52. Lacroix M, El Messaoudi S, Rodier G, Le Cam A, Sardet C, et al. (2008) The histone-binding protein COPR5 is required for nuclear functions of the protein arginine methyltransferase PRMT5. EMBO Rep 9: 452-458.