Functional modulation of the metastatic suppressor Nm23-H1 by oncogenic viruses

FEBS Letters

Volumn 585, Issue 20, 2011, Pages 3174-3184

  Saha, Abhik ^a   Robertson, Erle S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cancer and tumor virus; Metastasis; Nm23

Indexed keywords

BINDING PROTEIN; COLLAGEN TYPE 4; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; ENDONUCLEASE; EPSTEIN BARR VIRUS ANTIGEN; EPSTEIN BARR VIRUS ANTIGEN 3C; EXONUCLEASE; GELATINASE A; GELATINASE B; H PRUNE PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; K RAS PROTEIN; KINASE SUPPRESSOR OF RAS PROTEIN; LATENCY ASSOCIATED NUCLEAR ANTIGEN; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; NECDIN; NUCLEASE; NUCLEOSIDE DIPHOSPHATASE; NUCLEOSIDE DIPHOSPHATE KINASE A; PROTEIN E6; PROTEIN E7; PROTEIN HISTIDINE KINASE; PROTEIN SERINE THREONINE KINASE; PROTEIN SERINE THREONINE KINASE RECEPTOR ASSOCIATED PROTEIN; SET PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; EPSTEIN BARR VIRUS ANTIGEN 1; KINASE SUPRESOR OF RAS; NUCLEOSIDE DIPHOSPHATE KINASE; PROTEIN EBNA3A; PROTEIN EBNA3B; PROTEIN EBNA3C; RAS PROTEIN; SERINE THREONINE KINASE RECEPTOR ASSOCIATED PROTEIN; VIRUS ANTIGEN; NME1 PROTEIN, HUMAN; NUCLEOSIDE DIPHOSPHATE KINASE NM23; TUMOR ANTIGEN; TUMOR SUPPRESSOR PROTEIN;

ANTIANGIOGENIC ACTIVITY; CANCER GROWTH; CANCER INVASION; CARCINOGENESIS; CELL DEATH; CELL MOTILITY; COMPLEX FORMATION; DNA DAMAGE; ENZYME ACTIVITY; EPSTEIN BARR VIRUS; GENE REPRESSION; HUMAN; HUMAN HERPESVIRUS 8; INFLAMMATION; METASTASIS; NONHUMAN; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; TUMOR VIRUS; WART VIRUS; CELL MIGRATION; EBNA 3A GENE; EBNA 3B GENE; EBNA 3C GENE; ENZYME REPRESSION; EPSTEIN BARR VIRUS INFECTION; KAPOSI SARCOMA; NM23 GENE; ONCOGENE; PAPILLOMAVIRUS INFECTION; TUMOR CELL; VIRUS GENE; ANIMAL; CELL MOTION; ENZYMOLOGY; GENETICS; METABOLISM; PATHOLOGY; VIRUS INFECTION;

HERPESVIRIDAE; HUMAN HERPESVIRUS 4; HUMAN PAPILLOMAVIRUS;

ANIMALS; ANTIGENS, NEOPLASM; ANTIGENS, VIRAL; CELL MOVEMENT; HUMANS; NEOPLASM METASTASIS; NM23 NUCLEOSIDE DIPHOSPHATE KINASES; ONCOGENIC VIRUSES; TUMOR SUPPRESSOR PROTEINS; TUMOR VIRUS INFECTIONS;

EID: 84856392194     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2011.08.007     Document Type: Review

References (166)

1. C.W. Rinker-Schaeffer, J.P. O'Keefe, D.R. Welch, and D. Theodorescu Metastasis suppressor proteins: discovery, molecular mechanisms, and clinical application Clin. Cancer Res. 12 2006 3882 3889 (Pubitemid 44078070)
2. M.L. Lacombe, L. Milon, A. Munier, J.G. Mehus, and D.O. Lambeth The human Nm23/nucleoside diphosphate kinases J. Bioenerg. Biomembr. 32 2000 247 258
3. K.L. van Golen, S. Risin, A. Staroselsky, D. Berger, M.A. Tainsky, S. Pathak, and J.E. Price Predominance of the metastatic phenotype in hybrids formed by fusion of mouse and human melanoma clones Clin. Exp. Metastasis 14 1996 95 106 (Pubitemid 26074273)
4. A.M. Rosengard Reduced Nm23/Awd protein in tumour metastasis and aberrant Drosophila development Nature 342 1989 177 180
5. J.A. Stahl, A. Leone, A.M. Rosengard, L. Porter, C.R. King, and P.S. Steeg Identification of a second human nm23 gene, nm23-H2 Cancer Res. 51 1991 445 449
6. D. Venturelli Overexpression of DR-nm23, a protein encoded by a member of the nm23 gene family, inhibits granulocyte differentiation and induces apoptosis in 32Dc13 myeloid cells Proc. Natl. Acad. Sci. USA 92 1995 7435 7439
7. L. Milon, M.F. Rousseau-Merck, A. Munier, M. Erent, I. Lascu, J. Capeau, and M.L. Lacombe Nm23-H4, a new member of the family of human nm23/nucleoside diphosphate kinase genes localised on chromosome 16p13 Hum. Genet. 99 1997 550 557 (Pubitemid 27152109)
8. A. Munier, C. Feral, L. Milon, V.P. Pinon, G. Gyapay, J. Capeau, G. Guellaen, and M.L. Lacombe A new human nm23 homologue (nm23-H5) specifically expressed in testis germinal cells FEBS Lett. 434 1998 289 294 (Pubitemid 29052242)
9. J.G. Mehus, P. Deloukas, and D.O. Lambeth NME6: a new member of the nm23/nucleoside diphosphate kinase gene family located on human chromosome 3p21.3 Hum. Genet. 104 1999 454 459 (Pubitemid 29370919)
10. H. Tsuiki A novel human nucleoside diphosphate (NDP) kinase, Nm23-H6, localizes in mitochondria and affects cytokinesis J. Cell. Biochem. 76 1999 254 269 (Pubitemid 30030773)
11. P. Padma, A. Hozumi, K. Ogawa, and K. Inaba Molecular cloning and characterization of a thioredoxin/nucleoside diphosphate kinase related dynein intermediate chain from the ascidian, Ciona intestinalis Gene 275 2001 177 183 (Pubitemid 32907341)
12. G. Nallamothu, J.A. Woolworth, V. Dammai, and T. Hsu Awd, the homolog of metastasis suppressor gene Nm23, regulates Drosophila epithelial cell invasion Mol. Cell. Biol. 28 2008 1964 1973 (Pubitemid 351342627)
13. R. Kaul, M. Murakami, T. Choudhuri, and E.S. Robertson Epstein-Barr virus latent nuclear antigens can induce metastasis in a nude mouse model J. Virol. 81 2007 10352 10361 (Pubitemid 47463310)
14. M. Boissan, D. Wendum, S. Arnaud-Dabernat, A. Munier, M. Debray, I. Lascu, J.Y. Daniel, and M.L. Lacombe Increased lung metastasis in transgenic NM23-Null/SV40 mice with hepatocellular carcinoma J. Natl. Cancer Inst. 97 2005 836 845 (Pubitemid 40909126)
15. J.M. Backer Chromosomal localization and nucleoside diphosphate kinase activity of human metastasis-suppressor genes NM23-1 and NM23-2 Oncogene 8 1993 497 502 (Pubitemid 23073767)
16. Y.T. Tee, G.D. Chen, L.Y. Lin, J.L. Ko, and P.H. Wang Nm23-H1: a metastasis-associated gene Taiwan J. Obstet. Gynecol. 45 2006 107 113
17. M.H. Bosnar, J. De Gunzburg, R. Bago, L. Brecevic, I. Weber, and J. Pavelic Subcellular localization of A and B Nm23/NDPK subunits Exp. Cell Res. 298 2004 275 284 (Pubitemid 38887327)
18. P.S. Steeg, G. Bevilacqua, L. Kopper, U.P. Thorgeirsson, J.E. Talmadge, L.A. Liotta, and M.E. Sobel Evidence for a novel gene associated with low tumor metastatic potential J. Natl. Cancer Inst. 80 1988 200 204
19. T. Urano, K. Takamiya, K. Furukawa, and H. Shiku Molecular cloning and functional expression of the second mouse nm23/NDP kinase gene, nm23-M2 FEBS Lett. 309 1992 358 362
20. E. Lee, J. Jeong, S.E. Kim, E.J. Song, S.W. Kang, and K.J. Lee Multiple functions of Nm23-H1 are regulated by oxido-reduction system PLoS ONE 4 2009 e7949
21. J. Okabe-Kado, T. Kasukabe, Y. Honma, R. Hanada, A. Nakagawara, and Y. Kaneko Clinical significance of serum NM23-H1 protein in neuroblastoma Cancer Sci. 96 2005 653 660 (Pubitemid 41723541)
22. J. Sgouros, E. Galani, E. Gonos, P. Moutsatsou, M. Belechri, D. Skarlos, and A. Dionyssiou-Asteriou Correlation of nm23-H1 gene expression with clinical outcome in patients with advanced breast cancer In Vivo 21 2007 519 522 (Pubitemid 46901412)
23. M. Ilijas, K. Pavelic, B. Sarcevic, S. Kapitanovic, A. Kurjak, P. Stambrook, J. Gluckman, and Z. Pavelic Expression of nm23-h1 gene in squamous-cell carcinoma of the cervix correlates with 5-year survival Int. J. Oncol. 5 1994 1455 1457 (Pubitemid 24357495)
24. T. Ouatas, M. Salerno, D. Palmieri, and P.S. Steeg Basic and translational advances in cancer metastasis: Nm23 J. Bioenerg. Biomembr. 35 2003 73 79 (Pubitemid 36667583)
25. G. Bevilacqua NM23 gene expression and human breast cancer metastases Pathol. Biol. (Paris) 38 1990 774 775 (Pubitemid 20369160)
26. C. Hennessy, J.A. Henry, F.E. May, B.R. Westley, B. Angus, and T.W. Lennard Expression of anti-metastatic gene nm23 Br. J. Cancer 63 1991 1024
27. V.A. Florenes, S. Aamdal, O. Myklebost, G.M. Maelandsmo, O.S. Bruland, and O. Fodstad Levels of nm23 messenger RNA in metastatic malignant melanomas: inverse correlation to disease progression Cancer Res. 52 1992 6088 6091
28. M.M. van Noesel, and R. Versteeg Pediatric neuroblastomas: genetic and epigenetic 'danse macabre' Gene 325 2004 1 15 (Pubitemid 38030371)
29. C.L. Chang Nm23-H1 mutation in neuroblastoma Nature 370 1994 335 336
30. A. Yokoyama Evaluation by multivariate analysis of the differentiation inhibitory factor nm23 as a prognostic factor in acute myelogenous leukemia and application to other hematologic malignancies Blood 91 1998 1845 1851 (Pubitemid 28185483)
31. D.M. Kaetzel, J.R. McCorkle, M. Novak, M. Yang, and S.G. Jarrett Potential contributions of antimutator activity to the metastasis suppressor function of NM23-H1 Mol. Cell. Biochem. 329 2009 161 165
32. M.D. Rochdi Nm23-H2 interacts with a G protein-coupled receptor to regulate its endocytosis through an Rac1-dependent mechanism J. Biol. Chem. 279 2004 18981 18989 (Pubitemid 38623328)
33. N. Ishikawa, N. Shimada, Y. Takagi, Y. Ishijima, M. Fukuda, and N. Kimura Molecular evolution of nucleoside diphosphate kinase genes: conserved core structures and multiple-layered regulatory regions J. Bioenerg. Biomembr. 35 2003 7 18 (Pubitemid 36667576)
34. P.S. Steeg, C.E. Horak, and K.D. Miller Clinical-translational approaches to the Nm23-H1 metastasis suppressor Clin. Cancer Res. 14 2008 5006 5012
35. J.C. Marshall, J. Collins, N. Marino, and P. Steeg The Nm23-H1 metastasis suppressor as a translational target Eur. J. Cancer 46 2010 1278 1282
36. N.J. MacDonald, J.M. Freije, M.L. Stracke, R.E. Manrow, and P.S. Steeg Site-directed mutagenesis of nm23-H1. Mutation of proline 96 or serine 120 abrogates its motility inhibitory activity upon transfection into human breast carcinoma cells J. Biol. Chem. 271 1996 25107 25116 (Pubitemid 26337869)
37. P.D. Wagner, P.S. Steeg, and N.D. Vu Two-component kinase-like activity of nm23 correlates with its motility-suppressing activity Proc. Natl. Acad. Sci. USA 94 1997 9000 9005
38. M.T. Hartsough, D.K. Morrison, M. Salerno, D. Palmieri, T. Ouatas, M. Mair, J. Patrick, and P.S. Steeg Nm23-H1 metastasis suppressor phosphorylation of kinase suppressor of Ras via a histidine protein kinase pathway J. Biol. Chem. 277 2002 32389 32399 (Pubitemid 34969057)
39. N.J. MacDonald, A. De la Rosa, M.A. Benedict, J.M. Freije, H. Krutsch, and P.S. Steeg A serine phosphorylation of Nm23, and not its nucleoside diphosphate kinase activity, correlates with suppression of tumor metastatic potential J. Biol. Chem. 268 1993 25780 25789 (Pubitemid 23358195)
40. H.D. Kim, B. Youn, T.S. Kim, S.H. Kim, H.S. Shin, and J. Kim Regulators affecting the metastasis suppressor activity of Nm23-H1 Mol. Cell. Biochem. 329 2009 167 173
41. N. Wettschureck, and S. Offermanns Mammalian G proteins and their cell type specific functions Physiol. Rev. 85 2005 1159 1204 (Pubitemid 41362268)
42. S.M. Rumjahn, K.A. Baldwin, and I.L. Buxton P2y receptor-mediated angiogenesis via vascular endothelial growth factor receptor 2 signaling Proc. West. Pharmacol. Soc. 50 2007 58 60
43. D. Chowdhury, P.J. Beresford, P. Zhu, D. Zhang, J.S. Sung, B. Demple, F.W. Perrino, and J. Lieberman The exonuclease TREX1 is in the SET complex and acts in concert with NM23-H1 to degrade DNA during granzyme A-mediated cell death Mol. Cell 23 2006 133 142 (Pubitemid 43963449)
44. P.J. Beresford, D. Zhang, D.Y. Oh, Z. Fan, E.L. Greer, M.L. Russo, M. Jaju, and J. Lieberman Granzyme A activates an endoplasmic reticulum-associated caspase-independent nuclease to induce single-stranded DNA nicks J. Biol. Chem. 276 2001 43285 43293
45. Z. Fan, P.J. Beresford, D.Y. Oh, D. Zhang, and J. Lieberman Tumor suppressor NM23-H1 is a granzyme A-activated DNase during CTL-mediated apoptosis, and the nucleosome assembly protein SET is its inhibitor Cell 112 2003 659 672 (Pubitemid 36331778)
46. S.C. Goswami, J.H. Yoon, B.M. Abramczyk, G.P. Pfeifer, and E.H. Postel Molecular and functional interactions between Escherichia coli nucleoside-diphosphate kinase and the uracil-DNA glycosylase Ung J. Biol. Chem. 281 2006 32131 32139 (Pubitemid 46036767)
47. H.A. Seong, H. Jung, H.S. Choi, K.T. Kim, and H. Ha Regulation of transforming growth factor-beta signaling and PDK1 kinase activity by physical interaction between PDK1 and serine-threonine kinase receptor-associated protein J. Biol. Chem. 280 2005 42897 42908 (Pubitemid 43049252)
48. H.A. Seong, H. Jung, and H. Ha NM23-H1 tumor suppressor physically interacts with serine-threonine kinase receptor-associated protein, a transforming growth factor-beta (TGF-beta) receptor-interacting protein, and negatively regulates TGF-beta signaling J. Biol. Chem. 282 2007 12075 12096 (Pubitemid 47100716)
49. H. Jung, H.A. Seong, and H. Ha NM23-H1 tumor suppressor and its interacting partner STRAP activate p53 function J. Biol. Chem. 282 2007 35293 35307 (Pubitemid 350232484)
50. A. Reymond, S. Volorio, G. Merla, M. Al-Maghtheh, O. Zuffardi, A. Bulfone, A. Ballabio, and M. Zollo Evidence for interaction between human PRUNE and nm23-H1 NDPKinase Oncogene 18 1999 7244 7252 (Pubitemid 30032103)
51. A. Forus Amplification and overexpression of PRUNE in human sarcomas and breast carcinomas-a possible mechanism for altering the nm23-H1 activity Oncogene 20 2001 6881 6890 (Pubitemid 33054105)
52. A. D'Angelo Prune cAMP phosphodiesterase binds nm23-H1 and promotes cancer metastasis Cancer Cell 5 2004 137 149 (Pubitemid 38283800)
53. N. Oue, K. Yoshida, T. Noguchi, K. Sentani, A. Kikuchi, and W. Yasui Increased expression of h-prune is associated with tumor progression and poor survival in gastric cancer Cancer Sci. 98 2007 1198 1205 (Pubitemid 46993540)
54. L. Garzia Phosphorylation of nm23-H1 by CKI induces its complex formation with h-prune and promotes cell motility Oncogene 27 2008 1853 1864 (Pubitemid 351430816)
55. Y. Otsuki, M. Tanaka, S. Yoshii, N. Kawazoe, K. Nakaya, and H. Sugimura Tumor metastasis suppressor nm23H1 regulates Rac1 GTPase by interaction with Tiam1 Proc. Natl. Acad. Sci. USA 98 2001 4385 4390 (Pubitemid 32294986)
56. M. Murakami, P.I. Meneses, J.S. Knight, K. Lan, R. Kaul, S.C. Verma, and E.S. Robertson Nm23-H1 modulates the activity of the guanine exchange factor Dbl-1 Int. J. Cancer 123 2008 500 510 (Pubitemid 351898406)
57. C.D. Curtis, V.S. Likhite, I.X. McLeod, J.R. Yates, and A.M. Nardulli Interaction of the tumor metastasis suppressor nonmetastatic protein 23 homologue H1 and estrogen receptor alpha alters estrogen-responsive gene expression Cancer Res. 67 2007 10600 10607 (Pubitemid 350070837)
58. J. Zhu, Y.H. Tseng, J.D. Kantor, C.J. Rhodes, B.R. Zetter, J.S. Moyers, and C.R. Kahn Interaction of the Ras-related protein associated with diabetes rad and the putative tumor metastasis suppressor NM23 provides a novel mechanism of GTPase regulation Proc. Natl. Acad. Sci. USA 96 1999 14911 14918 (Pubitemid 30019739)
59. C.H. Switzer, R.Y. Cheng, T.M. Vitek, D.J. Christensen, D.A. Wink, and M.P. Vitek Targeting SET/I(2)PP2A oncoprotein functions as a multi-pathway strategy for cancer therapy Oncogene 30 2011 2504 2513
60. Marino, N., Marshall, J.C. and Steeg, P.S. (2011). Protein-protein interactions: a mechanism regulating the anti-metastatic properties of Nm23-H1. Naunyn Schmiedebergs Arch. Pharmacol. [Epub ahead of print].
61. C. Subramanian, M.A. Cotter 2nd, and E.S. Robertson Epstein-Barr virus nuclear protein EBNA-3C interacts with the human metastatic suppressor Nm23-H1: a molecular link to cancer metastasis Nat. Med. 7 2001 350 355 (Pubitemid 32224352)
62. M. Murakami, R. Kaul, P. Kumar, and E.S. Robertson Nucleoside diphosphate kinase/Nm23 and Epstein-Barr virus Mol. Cell. Biochem. 329 2009 131 139
63. A. Saha, R. Kaul, M. Murakami, and E.S. Robertson Tumor viruses and cancer biology: Modulating signaling pathways for therapeutic intervention Cancer Biol. Ther. 10 2010 961 978
64. A. Saha, S. Halder, S.K. Upadhyay, J. Lu, P. Kumar, M. Murakami, Q. Cai, and E.S. Robertson Epstein-Barr virus nuclear antigen 3C facilitates G1-S transition by stabilizing and enhancing the function of cyclin D1 PLoS Pathog. 7 2011 e1001275
65. A. Saha, and E.S. Robertson Epstein-Barr virus-associated B-cell lymphomas: pathogenesis and clinical outcomes Clin. Cancer Res. 17 2011 3056 3063
66. Y. Wang, X. Liu, X. Xing, Y. Cui, C. Zhao, and B. Luo Variations of Epstein-Barr virus nuclear antigen 1 gene in gastric carcinomas and nasopharyngeal carcinomas from Northern China Virus Res. 147 2010 258 264
67. S. Maruo, Y. Wu, S. Ishikawa, T. Kanda, D. Iwakiri, and K. Takada Epstein-Barr virus nuclear protein EBNA3C is required for cell cycle progression and growth maintenance of lymphoblastoid cells Proc. Natl. Acad. Sci. USA 103 2006 19500 19505 (Pubitemid 46026060)
68. K.M. Kaye, K.M. Izumi, and E. Kieff Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation Proc. Natl. Acad. Sci. USA 90 1993 9150 9154 (Pubitemid 23306469)
69. M.A. Lee, M.E. Diamond, and J.L. Yates Genetic evidence that EBNA-1 is needed for efficient, stable latent infection by Epstein-Barr virus J. Virol. 73 1999 2974 2982 (Pubitemid 29135686)
70. J.I. Cohen, F. Wang, J. Mannick, and E. Kieff Epstein-Barr virus nuclear protein 2 is a key determinant of lymphocyte transformation Proc. Natl. Acad. Sci. USA 86 1989 9558 9562 (Pubitemid 20010466)
71. B. Tomkinson, E. Robertson, and E. Kieff Epstein-Barr virus nuclear proteins EBNA-3A and EBNA-3C are essential for B-lymphocyte growth transformation J. Virol. 67 1993 2014 2025 (Pubitemid 23088375)
72. S. Apcher, C. Daskalogianni, B. Manoury, and R. Fahraeus Epstein Barr virus-encoded EBNA1 interference with MHC class I antigen presentation reveals a close correlation between mRNA translation initiation and antigen presentation PLoS Pathog. 6 2010 e1001151
73. M.S. Kang Epstein-Barr virus nuclear antigen 1 does not induce lymphoma in transgenic FVB mice Proc. Natl. Acad. Sci. USA 102 2005 820 825
74. M.S. Kang, V. Soni, R. Bronson, and E. Kieff Epstein-Barr virus nuclear antigen 1 does not cause lymphoma in C57BL/6J mice J. Virol. 82 2008 4180 4183 (Pubitemid 351521255)
75. J.B. Wilson, J.L. Bell, and A.J. Levine Expression of Epstein-Barr virus nuclear antigen-1 induces B cell neoplasia in transgenic mice EMBO J. 15 1996 3117 3126 (Pubitemid 26187759)
76. S.E. Lindner, and B. Sugden The plasmid replicon of Epstein-Barr virus: mechanistic insights into efficient, licensed, extrachromosomal replication in human cells Plasmid 58 2007 1 12 (Pubitemid 46874590)
77. D.R. Rawlins, G. Milman, S.D. Hayward, and G.S. Hayward Sequence-specific DNA binding of the Epstein-Barr virus nuclear antigen (EBNA-1) to clustered sites in the plasmid maintenance region Cell 42 1985 859 868
78. J.L. Yates, N. Warren, and B. Sugden Stable replication of plasmids derived from Epstein-Barr virus in various mammalian cells Nature 313 1985 812 815 (Pubitemid 15130835)
79. V. Marechal, A. Dehee, R. Chikhi-Brachet, T. Piolot, M. Coppey-Moisan, and J.C. Nicolas Mapping EBNA-1 domains involved in binding to metaphase chromosomes J. Virol. 73 1999 4385 4392 (Pubitemid 29189885)
80. J. Dheekollu, and P.M. Lieberman The replisome pausing factor timeless is required for episomal maintenance of latent epstein-barr virus J. Virol. 85 2011 5853 5863
81. J. Sears, M. Ujihara, S. Wong, C. Ott, J. Middeldorp, and A. Aiyar The amino terminus of Epstein-Barr Virus (EBV) nuclear antigen 1 contains AT hooks that facilitate the replication and partitioning of latent EBV genomes by tethering them to cellular chromosomes J. Virol. 78 2004 11487 11505 (Pubitemid 39390736)
82. S.C. Hung, M.S. Kang, and E. Kieff Maintenance of Epstein-Barr virus (EBV) oriP-based episomes requires EBV-encoded nuclear antigen-1 chromosome-binding domains, which can be replaced by high-mobility group-I or histone H1 Proc. Natl. Acad. Sci. USA 98 2001 1865 1870 (Pubitemid 32165589)
83. J. Norseen, F.B. Johnson, and P.M. Lieberman Role for G-quadruplex RNA binding by Epstein-Barr virus nuclear antigen 1 in DNA replication and metaphase chromosome attachment J. Virol. 83 2009 10336 10346
84. G. Habeshaw, Q.Y. Yao, A.I. Bell, D. Morton, and A.B. Rickinson Epstein-barr virus nuclear antigen 1 sequences in endemic and sporadic Burkitt's lymphoma reflect virus strains prevalent in different geographic areas J. Virol. 73 1999 965 975 (Pubitemid 29036747)
85. J. Levitskaya, M. Coram, V. Levitsky, S. Imreh, P.M. Steigerwald-Mullen, G. Klein, M.G. Kurilla, and M.G. Masucci Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1 Nature 375 1995 685 688
86. N. Blake Human CD8+ T cell responses to EBV EBNA1: HLA class I presentation of the (Gly-Ala)-containing protein requires exogenous processing Immunity 7 1997 791 802 (Pubitemid 28064892)
87. S.A. Kamranvar, B. Gruhne, A. Szeles, and M.G. Masucci Epstein-Barr virus promotes genomic instability in Burkitt's lymphoma Oncogene 26 2007 5115 5123 (Pubitemid 47206955)
88. B. Gruhne, R. Sompallae, D. Marescotti, S.A. Kamranvar, S. Gastaldello, and M.G. Masucci The Epstein-Barr virus nuclear antigen-1 promotes genomic instability via induction of reactive oxygen species Proc. Natl. Acad. Sci. USA 106 2009 2313 2318
89. T.J. Owen Epstein-Barr virus-encoded EBNA1 enhances RNA polymerase III-dependent EBER expression through induction of EBER-associated cellular transcription factors Mol. Cancer 9 2010 241
90. T.C. Cheng, S.S. Hsieh, W.L. Hsu, Y.F. Chen, H.H. Ho, and L.F. Sheu Expression of Epstein-Barr nuclear antigen 1 in gastric carcinoma cells is associated with enhanced tumorigenicity and reduced cisplatin sensitivity Int. J. Oncol. 36 2010 151 160
91. G. Kennedy, J. Komano, and B. Sugden Epstein-Barr virus provides a survival factor to Burkitt's lymphomas Proc. Natl. Acad. Sci. USA 100 2003 14269 14274 (Pubitemid 37499226)
92. M. Hong Suppression of Epstein-Barr nuclear antigen 1 (EBNA1) by RNA interference inhibits proliferation of EBV-positive Burkitt's lymphoma cells J. Cancer Res. Clin. Oncol. 132 2006 1 8 (Pubitemid 41712800)
93. Q. Yin, and E.K. Flemington SiRNAs against the Epstein Barr virus latency replication factor, EBNA1, inhibit its function and growth of EBV-dependent tumor cells Virology 346 2006 385 393 (Pubitemid 43357882)
94. L. Skalska, R.E. White, M. Franz, M. Ruhmann, and M.J. Allday Epigenetic repression of p16(INK4A) by latent Epstein-Barr virus requires the interaction of EBNA3A and EBNA3C with CtBP PLoS Pathog. 6 2010 e1000951
95. A. Le Roux, B. Kerdiles, D. Walls, J.F. Dedieu, and M. Perricaudet The Epstein-Barr virus determined nuclear antigens EBNA-3A, -3B, and -3C repress EBNA-2-mediated transactivation of the viral terminal protein 1 gene promoter Virology 205 1994 596 602 (Pubitemid 24371708)
96. I. Cludts, and P.J. Farrell Multiple functions within the Epstein-Barr virus EBNA-3A protein J. Virol. 72 1998 1862 1869 (Pubitemid 28100737)
97. L. Waltzer, M. Perricaudet, A. Sergeant, and E. Manet Epstein-Barr virus EBNA3A and EBNA3C proteins both repress RBP-J kappa-EBNA2-activated transcription by inhibiting the binding of RBP-J kappa to DNA J. Virol. 70 1996 5909 5915 (Pubitemid 26266803)
98. S. Maruo, B. Zhao, E. Johannsen, E. Kieff, J. Zou, and K. Takada Epstein-Barr virus nuclear antigens 3C and 3A maintain lymphoblastoid cell growth by repressing p16INK4A and p14ARF expression Proc. Natl. Acad. Sci. USA 108 2011 1919 1924
99. J. Lin, E. Johannsen, E. Robertson, and E. Kieff Epstein-Barr virus nuclear antigen 3C putative repression domain mediates coactivation of the LMP1 promoter with EBNA-2 J. Virol. 76 2002 232 242 (Pubitemid 33139008)
100. J.S. Knight, N. Sharma, and E.S. Robertson Epstein-Barr virus latent antigen 3C can mediate the degradation of the retinoblastoma protein through an SCF cellular ubiquitin ligase Proc. Natl. Acad. Sci. USA 102 2005 18562 18566 (Pubitemid 43011265)
101. S.A. Radkov, R. Touitou, A. Brehm, M. Rowe, M. West, T. Kouzarides, and M.J. Allday Epstein-Barr virus nuclear antigen 3C interacts with histone deacetylase to repress transcription J. Virol. 73 1999 5688 5697 (Pubitemid 29274854)
102. B.G. Bajaj, M. Murakami, Q. Cai, S.C. Verma, K. Lan, and E.S. Robertson Epstein-Barr virus nuclear antigen 3C interacts with and enhances the stability of the c-Myc oncoprotein J. Virol. 82 2008 4082 4090 (Pubitemid 351521243)
103. M. Murakami, K. Lan, C. Subramanian, and E.S. Robertson Epstein-Barr virus nuclear antigen 1 interacts with Nm23-H1 in lymphoblastoid cell lines and inhibits its ability to suppress cell migration J. Virol. 79 2005 1559 1568 (Pubitemid 40459103)
104. C. Subramanian, and E.S. Robertson The metastatic suppressor Nm23-H1 interacts with EBNA3C at sequences located between the glutamine- and proline-rich domains and can cooperate in activation of transcription J. Virol. 76 2002 8702 8709 (Pubitemid 34864065)
105. R. Kaul, M. Murakami, K. Lan, T. Choudhuri, and E.S. Robertson EBNA3C can modulate the activities of the transcription factor Necdin in association with metastasis suppressor protein Nm23-H1 J. Virol. 83 2009 4871 4883
106. P.A. Barker, and A. Salehi The MAGE proteins: emerging roles in cell cycle progression, apoptosis, and neurogenetic disease J. Neurosci. Res. 67 2002 705 712 (Pubitemid 34226281)
107. M. Niinobe, K. Koyama, and K. Yoshikawa Cellular and subcellular localization of necdin in fetal and adult mouse brain Dev. Neurosci. 22 2000 310 319
108. K. Matsumoto, H. Taniura, T. Uetsuki, and K. Yoshikawa Necdin acts as a transcriptional repressor that interacts with multiple guanosine clusters Gene 272 2001 173 179 (Pubitemid 32695410)
109. K. Hasegawa, and K. Yoshikawa Necdin regulates p53 acetylation via Sirtuin1 to modulate DNA damage response in cortical neurons J. Neurosci. 28 2008 8772 8784
110. H.E. Moon, M.Y. Ahn, J.A. Park, K.J. Min, Y.W. Kwon, and K.W. Kim Negative regulation of hypoxia inducible factor-1alpha by necdin FEBS Lett. 579 2005 3797 3801 (Pubitemid 40897727)
111. W.L. Smith, D.L. DeWitt, and R.M. Garavito Cyclooxygenases: structural, cellular, and molecular biology Annu. Rev. Biochem. 69 2000 145 182
112. H.R. Herschman Prostaglandin synthase 2 Biochim. Biophys. Acta 1299 1996 125 140 (Pubitemid 26007741)
113. G.N. Levy Prostaglandin H synthases, nonsteroidal anti-inflammatory drugs, and colon cancer FASEB J. 11 1997 234 247 (Pubitemid 27118324)
114. P. Needleman, J. Turk, B.A. Jakschik, A.R. Morrison, and J.B. Lefkowith Arachidonic acid metabolism Annu. Rev. Biochem. 55 1986 69 102 (Pubitemid 16070764)
115. H. Sano Expression of cyclooxygenase-1 and -2 in human colorectal cancer Cancer Res. 55 1995 3785 3789
116. H. Wolff, K. Saukkonen, S. Anttila, A. Karjalainen, H. Vainio, and A. Ristimaki Expression of cyclooxygenase-2 in human lung carcinoma Cancer Res. 58 1998 4997 5001 (Pubitemid 28521147)
117. D. Hwang, D. Scollard, J. Byrne, and E. Levine Expression of cyclooxygenase-1 and cyclooxygenase-2 in human breast cancer J. Natl. Cancer Inst. 90 1998 455 460 (Pubitemid 28160637)
118. A. Ristimaki, N. Honkanen, H. Jankala, P. Sipponen, and M. Harkonen Expression of cyclooxygenase-2 in human gastric carcinoma Cancer Res. 57 1997 1276 1280 (Pubitemid 27152551)
119. K.C. Zimmermann, M. Sarbia, A.A. Weber, F. Borchard, H.E. Gabbert, and K. Schror Cyclooxygenase-2 expression in human esophageal carcinoma Cancer Res. 59 1999 198 204 (Pubitemid 29062978)
120. M.A. Molina, M. Sitja-Arnau, M.G. Lemoine, M.L. Frazier, and F.A. Sinicrope Increased cyclooxygenase-2 expression in human pancreatic carcinomas and cell lines: growth inhibition by nonsteroidal anti-inflammatory drugs Cancer Res. 59 1999 4356 4362 (Pubitemid 29418754)
121. J.P. Peng, H.C. Chang, C.F. Hwang, and W.C. Hung Overexpression of cyclooxygenase-2 in nasopharyngeal carcinoma and association with lymph node metastasis Oral Oncol. 41 2005 903 908
122. H. Sawaoka, S. Kawano, S. Tsuji, M. Tsujii, E.S. Gunawan, Y. Takei, K. Nagano, and M. Hori Cyclooxygenase-2 inhibitors suppress the growth of gastric cancer xenografts via induction of apoptosis in nude mice Am. J. Physiol. 274 1998 G1061 G1067
123. R. Kaul, S.C. Verma, M. Murakami, K. Lan, T. Choudhuri, and E.S. Robertson Epstein-Barr virus protein can upregulate cyclo-oxygenase-2 expression through association with the suppressor of metastasis Nm23-H1 J. Virol. 80 2006 1321 1331 (Pubitemid 43134089)
124. S. Murono, H. Inoue, T. Tanabe, I. Joab, T. Yoshizaki, M. Furukawa, and J.S. Pagano Induction of cyclooxygenase-2 by Epstein-Barr virus latent membrane protein 1 is involved in vascular endothelial growth factor production in nasopharyngeal carcinoma cells Proc. Natl. Acad. Sci. USA 98 2001 6905 6910 (Pubitemid 32538315)
125. N. Ray, M.E. Bisher, and L.W. Enquist Cyclooxygenase-1 and -2 are required for production of infectious pseudorabies virus J. Virol. 78 2004 12964 12974 (Pubitemid 39507804)
126. I. Stamenkovic Matrix metalloproteinases in tumor invasion and metastasis Semin. Cancer Biol. 10 2000 415 433 (Pubitemid 32181912)
127. G. Giannelli, J. Falk-Marzillier, O. Schiraldi, W.G. Stetler-Stevenson, and V. Quaranta Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5 Science 277 1997 225 228 (Pubitemid 27446075)
128. K.B. Reddy, J.S. Krueger, S.B. Kondapaka, and C.A. Diglio Mitogen-activated protein kinase (MAPK) regulates the expression of progelatinase B (MMP-9) in breast epithelial cells Int. J. Cancer 82 1999 268 273 (Pubitemid 29293787)
129. S. Murono, T. Yoshizaki, H. Sato, H. Takeshita, M. Furukawa, and J.S. Pagano Aspirin inhibits tumor cell invasiveness induced by Epstein-Barr virus latent membrane protein 1 through suppression of matrix metalloproteinase-9 expression Cancer Res. 60 2000 2555 2561 (Pubitemid 30262452)
130. P. Gaudin TIMP-1/MMP-9 imbalance in an EBV-immortalized B lymphocyte cellular model: evidence for TIMP-1 multifunctional properties Biochim. Biophys. Acta 1499 2000 19 33
131. C. Trocme, P. Gaudin, S. Berthier, C. Barro, P. Zaoui, and F. Morel Human B lymphocytes synthesize the 92-kDa gelatinase, matrix metalloproteinase-9 J. Biol. Chem. 273 1998 20677 20684 (Pubitemid 28377640)
132. H. Takeshita, T. Yoshizaki, W.E. Miller, H. Sato, M. Furukawa, J.S. Pagano, and N. Raab-Traub Matrix metalloproteinase 9 expression is induced by Epstein-Barr virus latent membrane protein 1 C-terminal activation regions 1 and 2 J. Virol. 73 1999 5548 5555 (Pubitemid 29274838)
133. T. Yoshizaki, H. Sato, M. Furukawa, and J.S. Pagano The expression of matrix metalloproteinase 9 is enhanced by Epstein-Barr virus latent membrane protein 1 Proc. Natl. Acad. Sci. USA 95 1998 3621 3626
134. D.A. Kuppers, K. Lan, J.S. Knight, and E.S. Robertson Regulation of matrix metalloproteinase 9 expression by Epstein-Barr virus nuclear antigen 3C and the suppressor of metastasis Nm23-H1 J. Virol. 79 2005 9714 9724 (Pubitemid 41022314)
135. R.O. Hynes Integrins: versatility, modulation, and signaling in cell adhesion Cell 69 1992 11 25
136. Z. Zhang, A.O. Morla, K. Vuori, J.S. Bauer, R.L. Juliano, and E. Ruoslahti The alpha v beta 1 integrin functions as a fibronectin receptor but does not support fibronectin matrix assembly and cell migration on fibronectin J. Cell Biol. 122 1993 235 242 (Pubitemid 23188814)
137. D.T. Denhardt, and X. Guo Osteopontin: a protein with diverse functions FASEB J. 7 1993 1475 1482 (Pubitemid 24003267)
138. M. Busk, R. Pytela, and D. Sheppard Characterization of the integrin alpha v beta 6 as a fibronectin-binding protein J. Biol. Chem. 267 1992 5790 5796
139. I.F. Charo, L. Nannizzi, J.W. Smith, and D.A. Cheresh The vitronectin receptor alpha v beta 3 binds fibronectin and acts in concert with alpha 5 beta 1 in promoting cellular attachment and spreading on fibronectin J. Cell Biol. 111 1990 2795 2800 (Pubitemid 120014560)
140. J.W. Smith, D.J. Vestal, S.V. Irwin, T.A. Burke, and D.A. Cheresh Purification and functional characterization of integrin alpha v beta 5. An adhesion receptor for vitronectin J. Biol. Chem. 265 1990 11008 11013
141. P. Brodt, L. Fallavollita, R.J. Sawka, P. Shibata, J. Nip, U. Kim, and H. Shibata Tumor cell adhesion to frozen lymph node sections-a correlate of lymphatic metastasis in breast carcinoma models of human and rat origin Breast Cancer Res. Treat. 17 1990 109 120
142. E.J. Filardo, P.C. Brooks, S.L. Deming, C. Damsky, and D.A. Cheresh Requirement of the NPXY motif in the integrin beta 3 subunit cytoplasmic tail for melanoma cell migration in vitro and in vivo J. Cell Biol. 130 1995 441 450
143. S.M. Albelda, S.A. Mette, D.E. Elder, R. Stewart, L. Damjanovich, M. Herlyn, and C.A. Buck Integrin distribution in malignant melanoma: association of the beta 3 subunit with tumor progression Cancer Res. 50 1990 6757 6764 (Pubitemid 20348810)
144. P.C. Brooks, S. Stromblad, L.C. Sanders, T.L. von Schalscha, R.T. Aimes, W.G. Stetler-Stevenson, J.P. Quigley, and D.A. Cheresh Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3 Cell 85 1996 683 693 (Pubitemid 26181048)
145. S. Huang, D. Stupack, A. Liu, D. Cheresh, and G.R. Nemerow Cell growth and matrix invasion of EBV-immortalized human B lymphocytes is regulated by expression of alpha(v) integrins Oncogene 19 2000 1915 1923 (Pubitemid 30219034)
146. T. Choudhuri, S.C. Verma, K. Lan, and E.S. Robertson Expression of alpha V integrin is modulated by Epstein-Barr virus nuclear antigen 3C and the metastasis suppressor Nm23-H1 through interaction with the GATA-1 and Sp1 transcription factors Virology 351 2006 58 72 (Pubitemid 44041081)
147. J.L. Klosky, H.L. Gamble, S.L. Spunt, M.E. Randolph, D.M. Green, and M.M. Hudson Human papillomavirus vaccination in survivors of childhood cancer Cancer 115 2009 5627 5636
148. C. Foresta, C. Patassini, A. Bertoldo, M. Menegazzo, F. Francavilla, L. Barzon, and A. Ferlin Mechanism of human papillomavirus binding to human spermatozoa and fertilizing ability of infected spermatozoa PLoS ONE 6 2011 e15036
149. L. Koutsky Epidemiology of genital human papillomavirus infection Am. J. Med. 102 1997 3 8 (Pubitemid 127695953)
150. A.R. Giuliano Epidemiology of human papillomavirus infection in men, cancers other than cervical and benign conditions Vaccine 26 Suppl. 10 2008 K17 K28
151. M. Schiffman, P.E. Castle, J. Jeronimo, A.C. Rodriguez, and S. Wacholder Human papillomavirus and cervical cancer Lancet 370 2007 890 907 (Pubitemid 47371147)
152. S. Duensing, L.Y. Lee, A. Duensing, J. Basile, S. Piboonniyom, S. Gonzalez, C.P. Crum, and K. Munger The human papillomavirus type 16 E6 and E7 oncoproteins cooperate to induce mitotic defects and genomic instability by uncoupling centrosome duplication from the cell division cycle Proc. Natl. Acad. Sci. USA 97 2000 10002 10007
153. K. Munger, J.R. Basile, S. Duensing, A. Eichten, S.L. Gonzalez, M. Grace, and V.L. Zacny Biological activities and molecular targets of the human papillomavirus E7 oncoprotein Oncogene 20 2001 7888 7898 (Pubitemid 33135315)
154. W. Zwerschke, and P. Jansen-Durr Cell transformation by the E7 oncoprotein of human papillomavirus type 16: interactions with nuclear and cytoplasmic target proteins Adv. Cancer Res. 78 2000 1 29
155. A.M. Mileo, E. Piombino, A. Severino, A. Tritarelli, M.G. Paggi, and D. Lombardi Multiple interference of the human papillomavirus-16 E7 oncoprotein with the functional role of the metastasis suppressor Nm23-H1 protein J. Bioenerg. Biomembr. 38 2006 215 225 (Pubitemid 44946229)
156. Q. Cai, S.C. Verma, J. Lu, and E.S. Robertson Molecular biology of Kaposi's sarcoma-associated herpesvirus and related oncogenesis Adv. Virus Res. 78 2010 87 142
157. T. Vanni, E. Sprinz, M.W. Machado, C. Santana Rde, B.A. Fonseca, and G. Schwartsmann Systemic treatment of AIDS-related Kaposi sarcoma: current status and perspectives Cancer Treat. Rev. 32 2006 445 455 (Pubitemid 44309251)
158. F. Bonnet Malignancy-related causes of death in human immunodeficiency virus-infected patients in the era of highly active antiretroviral therapy Cancer 101 2004 317 324 (Pubitemid 38890835)
159. E.A. Engels Cancer risk in people infected with human immunodeficiency virus in the United States Int. J. Cancer 123 2008 187 194 (Pubitemid 351705208)
160. S.M. Gregory, J.A. West, P.J. Dillon, C. Hilscher, D.P. Dittmer, and B. Damania Toll-like receptor signaling controls reactivation of KSHV from latency Proc. Natl. Acad. Sci. USA 106 2009 11725 11730
161. L.W. Qian, J. Xie, F. Ye, and S.J. Gao Kaposi's sarcoma-associated herpesvirus infection promotes invasion of primary human umbilical vein endothelial cells by inducing matrix metalloproteinases J. Virol. 81 2007 7001 7010 (Pubitemid 46986636)
162. D.L. Di Bartolo, M. Cannon, Y.F. Liu, R. Renne, A. Chadburn, C. Boshoff, and E. Cesarman KSHV LANA inhibits TGF-beta signaling through epigenetic silencing of the TGF-beta type II receptor Blood 111 2008 4731 4740
163. G. Platt, A. Carbone, and S. Mittnacht P16INK4a loss and sensitivity in KSHV associated primary effusion lymphoma Oncogene 21 2002 1823 1831 (Pubitemid 34259184)
164. M. Shamay, A. Krithivas, J. Zhang, and S.D. Hayward Recruitment of the de novo DNA methyltransferase Dnmt3a by Kaposi's sarcoma-associated herpesvirus LANA Proc. Natl. Acad. Sci. USA 103 2006 14554 14559 (Pubitemid 44484788)
165. Z. Qin, L. Dai, B. Toole, E. Robertson, and C. Parsons Regulation of Nm23-H1 and cell invasiveness by Kaposi's sarcoma-associated herpesvirus J. Virol. 85 2011 3596 3606
166. Y.H. Tseng, D. Vicent, J. Zhu, Y. Niu, A. Adeyinka, J.S. Moyers, P.H. Watson, and C.R. Kahn Regulation of growth and tumorigenicity of breast cancer cells by the low molecular weight GTPase Rad and nm23 Cancer Res. 61 2001 2071 2079 (Pubitemid 32692029)