The perinucleolar compartment associates with malignancy

Yiping WEN, Chen WANG, Sui HUANG

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Front. Biol. ›› 2013, Vol. 8 ›› Issue (4) : 369-376. DOI: 10.1007/s11515-013-1265-z
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The perinucleolar compartment associates with malignancy

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Abstract

The perinucleolar compartment (PNC) is a unique nuclear substructure, forming predominantly in cancer cells both in vitro and in vivo. PNC prevalence (percentage of cells containing at least one PNC) has been found to positively correlate with disease progression in several cancers (breast, ovarian, and colon). While there is a clear association between PNCs and cancer, the molecular function of the PNC remains unclear. Here we summarize the current understanding of the association of PNCs with cancer and its possible functions in cancer cells.

Keywords

PNC / cancer / nuclear substructure / gene expression regulation / structure and function

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Yiping WEN, Chen WANG, Sui HUANG. The perinucleolar compartment associates with malignancy. Front Biol, 2013, 8(4): 369‒376 https://doi.org/10.1007/s11515-013-1265-z

References

[1]
Altman S (1990). Ribonuclease P. Postscript. J Biol Chem, 265(33): 20053-20056
[2]
Anderson J T, Wilson S M, (1993). NAB2: a yeast nuclear polyadenylated RNA-binding protein essential for cell viability. Mol Cell Biol, 13(5): 2730-2741
[3]
Apponi L H, Corbett A H, Pavlath G K (2011). RNA-binding proteins and gene regulation in myogenesis. Trends Pharmacol Sci, 32(11): 652-658
CrossRef Google scholar
[4]
Bond C S, Fox A H (2009). Paraspeckles: nuclear bodies built on long noncoding RNA. J Cell Biol, 186(5): 637-644
CrossRef Google scholar
[5]
Castelo-Branco P, Furger A, Wollerton M, Smith C, Moreira A, Proudfoot N (2004). Polypyrimidine tract binding protein modulates efficiency of polyadenylation. Mol Cell Biol, 24(10): 4174-4183
CrossRef Google scholar
[6]
Charlet B N, Savkur R S, Singh G, Philips A V, Grice E A, Cooper T A (2002). Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol Cell, 10(1): 45-53
CrossRef Google scholar
[7]
Chen M, Zhang J, Manley J L (2010). Turning on a fuel switch of cancer: hnRNP proteins regulate alternative splicing of pyruvate kinase mRNA. Cancer Res, 70(22): 8977-8980
CrossRef Google scholar
[8]
Clayton D A (1994). A nuclear function for RNase MRP. Proc Natl Acad Sci USA, 91(11): 4615-4617
CrossRef Google scholar
[9]
Esakova O, Krasilnikov A S (2010). Of proteins and RNA: the RNase P/MRP family. RNA, 16(9): 1725-1747
CrossRef Google scholar
[10]
Esakova O, Perederina A, Quan C, Berezin I, Krasilnikov A S (2011). Substrate recognition by ribonucleoprotein ribonuclease MRP. RNA, 17(2): 356-364
CrossRef Google scholar
[11]
Fox A H, Lamond A I (2010). Paraspeckles. Cold Spring Harb Perspect Biol, 2(7): a000687
CrossRef Google scholar
[12]
Frank R, Hargreaves R (2003). Clinical biomarkers in drug discovery and development. Nat Rev Drug Discov, 2(7): 566-580
CrossRef Google scholar
[13]
Ghetti A, Pinol-Roma S, Michael W M, Morandi C, Dreyfuss G (1992). hnRNP I, the polypyrimidine tract-binding protein: distinct nuclear localization and association with hnRNAs. Nucleic Acids Res, 20(14): 3671-3678
CrossRef Google scholar
[14]
Gromak N, Rideau A, Southby J, Scadden A D J, Gooding C, Hüttelmaier S, Singer R H, Smith C W J (2003). The PTB interacting protein raver1 regulates alpha-tropomyosin alternative splicing. EMBO J, 22(23): 6356-6364
CrossRef Google scholar
[15]
Hall M P, Huang S, (2004). Differentiation-induced colocalization of the KH-type splicing regulatory protein with polypyrimidine tract binding protein and the c-src pre-mRNA. Mol Biol Cell, 15(2): 774-786
CrossRef Google scholar
[16]
Hellen C U, Pestova T V, (1994). The cellular polypeptide p57 (pyrimidine tract-binding protein) binds to multiple sites in the poliovirus 5′ nontranslated region. J Virol, 68(2): 941-950
[17]
Ho T H, Bundman D, Armstrong, D L, Cooper, T A (2005). Transgenic mice expressing CUG-BP1 reproduce splicing mis-regulation observed in myotonic dystrophy. Hum Mol Genet, 14(11): 1539-1547
CrossRef Google scholar
[18]
Huang S, Deerinck T J, Ellisman M H, Spector D L (1997). The dynamic organization of the perinucleolar compartment in the cell nucleus. J Cell Biol, 137(5): 965-974
CrossRef Google scholar
[19]
Huang S, Deerinck T J, Ellisman M H, Spector D L (1998). The perinucleolar compartment and transcription. J Cell Biol, 143(1): 35-47
CrossRef Google scholar
[20]
Huttelmaier S, Illenberger S, Grosheva I, Rudiger M, Singer R H, and Jockusch B M (2001). Raver1, a dual compartment protein, is a ligand for PTB/hnRNPI and microfilament attachment proteins. J Cell Biol, 155(5): 775-786
CrossRef Google scholar
[21]
Jackson D A, Hassan A B, Errington P R (1993). Visualization of focal sites of transcription within human nuclei. EMBO J, 12: 1059-1065
[22]
Jacobson M R, Cao L G, Wang Y L, Pederson T (1995). Dynamic localization of RNase MRP RNA in the nucleolus observed by fluorescent RNA cytochemistry in living cells. J Cell Biol, 131(6 Pt 2): 1649-1658
CrossRef Google scholar
[23]
Jarrous N (2002). Human ribonuclease P: subunits, function, and intranuclear localization. RNA, 8(1): 1-7
CrossRef Google scholar
[24]
Jones K, Timchenko L, Timchenko N A (2012). The role of CUGBP1 in age-dependent changes of liver functions. Ageing Res Rev, 11(4): 442-449
CrossRef Google scholar
[25]
Kafasla P, Mickleburgh I, Llorian M, Coelho M, Gooding C, Cherny D, Joshi A, Kotik-Kogan O, Curry S, Eperon I C, Jackson R J, Smith C W J (2012). Defining the roles and interactions of PTB. Biochem Soc Trans, 40(4): 815-820
CrossRef Google scholar
[26]
Kamath R V, Leary D J, Huang S (2001). Nucleocytoplasmic shuttling of polypyrimidine tract-binding protein is uncoupled from RNA export. Mol Biol Cell, 12(12): 3808-3820
[27]
Kamath R V, Thor A D, Wang C, Edgerton SM, Slusarczyk A, Leary D J, Wang J, Wiley E L, Jovanovic B, Wu Q, Nayar R, Kovarik P, Shi F, Huang S (2005). Perinucleolar compartment prevalence has an independent prognostic value for breast cancer. Cancer Res, 65(1): 246-253
[28]
Kaminski A, Hunt S L, Patton J G, Jackson- Rna R J (1995). Direct evidence that polypyrimidine tract binding protein (PTB) is essential for internal initiation of translation of encephalomyocarditis virus RNA. RNA, 1(9): 924-938
[29]
Lee B, Matera A G, Ward D C, Craft J (1996). Association of RNase mitochondrial RNA processing enzyme with ribonuclease P in higher ordered structures in the nucleolus: a possible coordinate role in ribosome biogenesis. Proc Natl Acad Sci USA, 93(21): 11471-11476
CrossRef Google scholar
[30]
Liu Y, Norton J T, Witschi M A, Xu Q, Lou G, Wang C, H Appella D, Chen Z, Huang S (2011). Methoxyethylamino-numonafide is an efficacious and minimally toxic amonafide derivative in murine models of human cancer. Neoplasia, 13(5): 453-460
[31]
Lou H, Gagel R F, Berget S M (1996). An intron enhancer recognized by splicing factors activates polyadenylation. Genes Dev, 10(2): 208-219
CrossRef Google scholar
[32]
Lou H, Helfman D M, Gagel R F, Berget S M (1999). Polypyrimidine tract-binding protein positively regulates inclusion of an alternative 3′-terminal exon. Mol Cell Biol, 19(1): 78-85
[33]
Mahadevan M S (2012). Myotonic dystrophy: is a narrow focus obscuring the rest of the field? Curr Opin Neurol, 25(5): 609-613
CrossRef Google scholar
[34]
Matera A G, Frey M R, Margelot K, Wolin S L (1995). A perinucleolar compartment contains several RNA polymerase III transcripts as well as the polypyrimidine tract-binding protein, hnRNP I. J Cell Biol, 129(5): 1181-1193
CrossRef Google scholar
[35]
Norton J T, Pollock C B, Wang C, Schink J C, Kim J J, Huang S (2008). Perinucleolar compartment prevalence is a phenotypic pancancer marker of malignancy. Cancer, 113(4): 861-869
CrossRef Google scholar
[36]
Norton J T, Titus S A, Dexter D, Austin C P, Zheng W, Huang S (2009). Automated high-content screening for compounds that disassemble the perinucleolar compartment. J Biomol Screen, 14(9): 1045-1053
CrossRef Google scholar
[37]
Norton J T, Wang C, Gjidoda A, Henry R W, Huang S (2009). The perinucleolar compartment is directly associated with DNA. J Biol Chem, 284(7): 4090-4101
CrossRef Google scholar
[38]
Norton J T, Witschi M A, Luong L, Kawamura A, Ghosh S, Sharon Stack M, Sim E, Avram M J, Appella D H, Huang S (2008). Synthesis and anticancer activities of 6-amino amonafide derivatives. Anticancer Drugs, 19(1): 23-36
CrossRef Google scholar
[39]
O'Keefe R T, Mayeda A, Sadowski C L, Krainer A R, and Spec-tor D L (1994). Disruption of pre-mRNA splicing in vivo results in reorganization of splicing factors. J Cell Biol, 124(3): 249-260
CrossRef Google scholar
[40]
Paillard L, Legagneux V, Osborne H B (2003). A functional deadenylation assay identifies human CUG-BP as a deadenylation factor. Biol Cell, 95(2): 107-113
CrossRef Google scholar
[41]
Perederina A, Esakova O, Quan C, Khanova E, Krasilnikov A S (2010). Eukaryotic ribonucleases P/MRP: the crystal structure of the P3 domain. EMBO J, 29(4): 761-769
CrossRef Google scholar
[42]
Perez I, Lin C H, Mcafee J, Patton J (1997). Mutation of PTB binding sites causes misregulation of alternative 3′ splice site selection in vivo. RNA, 3(7): 764-778
[43]
Pettaway C A, Pathak S, Greene G, Ramirez E, Wilson M R, Killion J J, Fidler I J (1996). Selection of highly metastatic variants of different human prostatic carcinomas using orthotopic implantation in nude mice. Clin Cancer Res, 2(9): 1627-1636
[44]
Pianese G (1896). Beitrag zur histologie und aetiologie der carcinoma. Histologische und experimentelle untersuchungen. Beitr Pathol Anat Allgem Pathol, 142(1): 193
[45]
Pickering B M, Mitchell S A, Evans J R, Willis A E (2003). Polypyrimidine tract binding protein and poly r(C) binding protein 1 interact with the BAG-1 IRES and stimulate its activity in vitro and in vivo. Nucleic Acids Res, 31(2): 639-646
CrossRef Google scholar
[46]
Pollock C, Daily K, Nguyen V T, Wang C, Lewandowska M A, Bensaude O, Huang S (2011). Characterization of MRP RNA-protein interactions within the perinucleolar compartment. Mol Biol Cell, 22(6): 858-866
CrossRef Google scholar
[47]
Savkur R S, Philips A V, Cooper T A (2001). Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat Genet, 29(1): 40-47
CrossRef Google scholar
[48]
Sawicka K, Bushell M, Spriggs K A, Willis A E (2008). Polypyrimidine-tract-binding protein: a multifunctional RNA-binding protein. Biochem Soc Trans, 36(Pt 4): 641-647
CrossRef Google scholar
[49]
Schneider R, Agol V I, Andino R, Bayard F, Cavener D R, Chappell S A, Chen J J, Darlix J L, Dasgupta A, Donze O (2001). New ways of initiating translation in eukaryotes. Mol Cell Biol, 21(23): 8238-8246
CrossRef Google scholar
[50]
Slusarczyk A, Kamath R, Wang C, Anchel D, Pollock C, Lewandowska M A, Fitzpatrick T, Bazett-Jones D P, Huang S (2010). Structure and function of the perinucleolar compartment in cancer cells. Cold Spring Harb Symp Quant Biol, 75(0): 599-605
CrossRef Google scholar
[51]
Steinberg T H, Burgess R R (1992). Tagetitoxin inhibition of RNA polymerase III transcription results from enhanced pausing at discrete sites and is template-dependent. J Biol Chem, 267(28): 20204-20211
[52]
Steinberg T H, Mathews D E, Durbin R D, Burgess R R (1990). Tagetitoxin: a new inhibitor of eukaryotic transcription by RNA polymerase III. J Biol Chem, 265(1): 499-505
[53]
Timchenko L T, Miller J W, Timchenko N A, DeVore D R, Datar K V, Lin L, Roberts R, Caskey C T, Swanson M S (1996). Identification of a (CUG)n triplet repeat RNA-binding protein and its expression in myotonic dystrophy. Nucleic Acids Res, 24(22): 4407-4414
CrossRef Google scholar
[54]
Valcarcel J, Gebauer F (1997). Post-transcriptional regulation: the dawn of PTB. Curr Biol, 7(11): R705-R708
CrossRef Google scholar
[55]
Van Eenennaam H, Vogelzangs J H, Lugtenberg D, Van Den Hoogen F H J, Van Venrooij W J, Pruijn G J M (2002). Identity of the RNase MRP- and RNase P-associated Th/To autoantigen. Arthritis Rheum, 46(12): 3266-3272
CrossRef Google scholar
[56]
Wagner E J, Carstens R P, Garcia-Blanco M A (1999). A novel isoform ratio switch of the polypyrimidine tract binding protein. Electrophoresis, 20(4-5): 1082-1086
CrossRef Google scholar
[57]
Wagner E J, Garcia-Blanco M A (2002). RNAi-mediated PTB depletion leads to enhanced exon definition. Mol Cell, 10(4): 943-949
CrossRef Google scholar
[58]
Wang C, Politz J C, Pederson T, Huang S (2003). RNA polymerase III transcripts and the PTB protein are essential for the integrity of the perinucleolar compartment. Mol Biol Cell, 14(6): 2425-2435
CrossRef Google scholar
[59]
Wansink D G, Schul W, van der Kraan I, van Steensel B, van Driel R, de Jong L (1993). Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus. J Cell Biol, 122(2): 283-293
CrossRef Google scholar
[60]
Witherell G W, Schultz-Witherell C S, Wimmer E C K A R D (1995). Cis-acting elements of the encephalomyocarditis virus internal ribosomal entry site. Virology, 214(2): 660-663
CrossRef Google scholar
[61]
Xiao S, Scott F, Fierke C A, Engelke D R (2002). EUKARYOTIC RIBONUCLEASE P: A Plurality of Ribonucleoprotein Enzymes. Annu Rev Biochem, 71(1): 165-189
CrossRef Google scholar
[62]
Xie J, Lee J A, Kress T L, Mowry K L, Black D L (2003). Protein kinase A phosphorylation modulates transport of the polypyrimidine tract-binding protein. Proc Natl Acad Sci USA, 100(15): 8776-8781
CrossRef Google scholar
[63]
Zhang W, Liu H, Han K, Grabowski P J (2002). Region-specific alternative splicing in the nervous system: implications for regulation by the RNA-binding protein NAPOR. RNA, 8(5): 671-685
CrossRef Google scholar
[64]
Zwerger M, Ho C Y, Lammerding J (2011). Nuclear mechanics in disease. Annu Rev Biomed Eng, 13(1): 397-428
CrossRef Google scholar

Acknowledgements

We thank the support from NIH grant (2R01GM078555-05) and from the Robert H. Lurie Comprehensive Cancer Center.
Compliance with ethics guidelines

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2014 Higher Education Press and Springer-Verlag Berlin Heidelberg
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