Bystin-like protein is upregulated in hepatocellular carcinoma and required for nucleologenesis in cancer cell proliferation

Cell Research

Volumn 19, Issue 10, 2009, Pages 1150-1164

  Wang, Hanzhi ^a,b   Xiao, Wei ^c   Zhou, Qinbo ^a,b   Chen, Yun ^d   Yang, Shuo ^a   Sheng, Jiansong ^a   Yin, Yanqing ^b   Fan, Jia ^e   Zhou, Jiawei ^a,b  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b Chinese Academy of Sciences   (China)

^c Department of Pathology   (China)

^d No 411 Hospital of PLA   (China)

^e FUDAN UNIVERSITY   (China)

Author keywords

Bystin like; Cell growth; Hepatocellular carcinoma; Nucleolar proteins; Nucleologenesis

Indexed keywords

BYSL PROTEIN, HUMAN; CELL ADHESION MOLECULE; SMALL INTERFERING RNA;

ADULT; ANIMAL; APOPTOSIS; ARTICLE; CELL CYCLE G2 PHASE; CELL DIVISION; CELL PROLIFERATION; CHEMISTRY; FEMALE; HUMAN; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; MITOSIS; MOUSE; NUCLEOLUS; PHYSIOLOGY; TUMOR CELL LINE; UPREGULATION;

ADULT; ANIMALS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL ADHESION MOLECULES; CELL DIVISION; CELL LINE, TUMOR; CELL NUCLEOLUS; CELL PROLIFERATION; FEMALE; G2 PHASE; HUMANS; LIVER NEOPLASMS; MICE; MITOSIS; RNA, SMALL INTERFERING; UP-REGULATION;

MUS MUSCULUS;

EID: 70349772938     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2009.99     Document Type: Article

References (54)

1. Leong TY, Leong AS. Epidemiology and carcinogenesis of hepatocellular carcinoma. HPB (Oxford) 2005; 7:5-15.
2. Kodousek R, Dusek J. Demonstration of the nucleolar organizer region by silver staining (AgNOR method) in research and in histopathological practice. Acta Univ Palacki Olomuc Fac Med 1991; 131:9-37.
3. Derenzini M, Sirri V, Trere D, Ochs RL. The quantity of nucleolar proteins nucleolin and protein B23 is related to cell doubling time in human cancer cells. Lab Invest 1995; 73:497-502.
4. Sirri V, Roussel P, Hernandez-Verdun D. The AgNOR proteins: qualitative and quantitative changes during the cell cycle. Micron 2000; 31:121-126.
5. Dundr M, Misteli T, Olson MO. The dynamics of postmitotic reassembly of the nucleolus. J Cell Biol 2000; 150:433-446.
6. Yun JP, Miao J, Chen GG, et al. Increased expression of nucleophosmin/B23 in hepatocellular carcinoma and correlation with clinicopathological parameters. Br J Cancer 2007; 96:477-484.
7. Storck S, Shukla M, Dimitrov S, Bouvet P. Functions of the histone chaperone nucleolin in diseases. Subcell Biochem 2007; 41:125-144.
8. Kondoh N, Shuda M, Tanaka K, et al. Enhanced expression of S8, L12, L23a, L27 and L30 ribosomal protein mRNAs in human hepatocellular carcinoma. Anticancer Res 2001; 21:2429-2433.
9. Bassoe CF, Bruserud O, Pryme IF, Vedeler A. Ribosomal proteins sustain morphology, function and phenotype in acute myeloid leukemia blasts. Leuk Res 1998; 22:329-339.
10. Alon U, Barkai N, Notterman DA, et al. Broad patterns of gene expression revealed by clustering analysis of tumor and normal colon tissues probed by oligonucleotide arrays. Proc Natl Acad Sci USA 1999; 96:6745-6750.
11. Ferrari S, Manfredini R, Tagliafico E, et al. Noncoordinated expression of S6, S11, and S14 ribosomal protein genes in leukemic blast cells. Cancer Res 1990; 50:5825-5828.
12. Ruggero D, Grisendi S, Piazza F, et al. Dyskeratosis congen- ita and cancer in mice deficient in ribosomal RNA modification. Science 2003; 299:259-262.
13. Ruggero D, Pandolfi PP. Does the ribosome translate cancer? Nat Rev Cancer 2003; 3:179-192.
14. Willig TN, Draptchinskaia N, Dianzani I, et al. Mutations in ribosomal protein S19 gene and iamond blackfan anemia: wide variations in phenotypic expression. Blood 1999; 94:4294-4306.
15. Miyoshi M, Okajima T, Matsuda T, Fukuda MN, Nadano D. Bystin in human cancer cells: intracellular localization and function in ribosome biogenesis. Biochem J 2007; 404:373-381.
16. Adachi K, Soeta-Saneyoshi C, Sagara H, Iwakura Y. A crucial role of Bysl in mammalian preimplantation development as an integral factor for 40S ribosome biogenesis. Mol Cell Biol 2007; 27:2202-2214.
17. Chen W, Bucaria J, Band DA, Sutton A, Sternglanz R. Enp1, a yeast protein associated with U3 and U14 snoRNAs, is required for pre-rRNA processing and 40S subunit synthesis. Nucleic Acids Res 2003; 31:690-699.
18. Schafer T, Strauss D, Petfalski E, Tollervey D, Hurt E. The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J 2003; 22:1370-1380.
19. Aoki R, Suzuki N, Paria BC, et al. The Bysl gene product, bystin, is essential for survival of mouse embryos. FEBS Lett 2006; 580:6062-6068.
20. Basso K, Margolin AA, Stolovitzky G, et al. Reverse engineering of regulatory networks in human B cells. Nat Genet 2005; 37:382-390.
21. Facchini LM, Penn LZ. The molecular role of Myc in growth and transformation: recent discoveries lead to new insights. FASEB J 1998; 12:633-651.
22. Henriksson M, Luscher B. Proteins of the Myc network: essential regulators of cell growth and differentiation. Adv Cancer Res 1996; 68:109-182.
23. Pascale RM, De Miglio MR, Muroni MR, et al. c-myc amplification in pre-malignant and malignant lesions induced in rat liver by the resistant hepatocyte model. Int J Cancer 1996; 68:136-142.
24. De Miglio MR, Simile MM, Muroni MR, et al. Correlation of c-myc overexpression and amplification with progression of preneoplastic liver lesions to malignancy in the poorly susceptible Wistar rat strain. Mol Carcinog 1999; 25:21-29.
25. Yaswen P, Goyette M, Shank PR, Fausto N. Expression of c-Ki-ras, c-Ha-ras, and c-myc in specific cell types during he- patocarcinogenesis. Mol Cell Biol 1985; 5:780-786.
26. Wang Y, Wu MC, Sham JS, et al. Prognostic significance of c-myc and AIB1 amplification in hepatocellular carcinoma. A broad survey using high-throughput tissue microarray. Cancer 2002; 95:2346-2352.
27. Abou-Elella A, Gramlich T, Fritsch C, Gansler T. c-myc amplification in hepatocellular carcinoma predicts unfavorable prognosis. Mod Pathol 1996; 9:95-98.
28. Zhang XK, Huang DP, Qiu DK, Chiu JF. The expression of c- myc and c-N-ras in human cirrhotic livers, hepatocellular carcinomas and liver tissue surrounding the tumors. Oncogene 1990; 5:909-914.
29. Gautier T, Fomproix N, Masson C, et al. Fate of specific nucleolar perichromosomal proteins during mitosis: cellular distribution and association with U3 snoRNA. Biol Cell 1994; 82:81-93.
30. Azum-Gelade MC, Noaillac-Depeyre J, Caizergues-Ferrer M, Gas N. Cell cycle redistribution of U3 snRNA and fibrillarin. Presence in the cytoplasmic nucleolus remnant and in the pre- nucleolar bodies at telophase. J Cell Sci 1994; 107(Pt 2):463-475.
31. Jimenez-Garcia LF, Segura-Valdez ML, Ochs RL, et al. Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis. Mol Biol Cell 1994; 5:955-966.
32. Angelier N, Tramier M, Louvet E, et al. Tracking the interactions of rRNA processing proteins during nucleolar assembly in living cells. Mol Biol Cell 2005; 16:2862-2871.
33. Savino TM, Gebrane-Younes J, De Mey J, Sibarita JB, Hernandez-Verdun D. Nucleolar assembly of the rRNA processing machinery in living cells. J Cell Biol 2001; 153:1097-1110.
34. Calvisi DF, Conner EA, Ladu S, et al. Activation of the canonical Wnt/beta-catenin pathway confers growth advantages in c-Myc/E2F1 transgenic mouse model of liver cancer. J He- patol 2005; 42:842-849.
35. Dundr M, Olson MO. Partially processed pre-rRNA is preserved in association with processing components in nucleo- lus-derived foci during mitosis. Mol Biol Cell 1998; 9:2407-2422.
36. Russell J, Zomerdijk JC. The RNA polymerase I transcription machinery. Biochem Soc Symp 2006 (73):203-216.
37. Tollervey D, Kiss T. Function and synthesis of small nucleo- lar RNAs. Curr Opin Cell Biol 1997; 9:337-342.
38. Kasugai Y, Tagawa H, Kameoka Y, et al. Identification of CCND3 and BYSL as candidate targets for the 6p21 amplification in diffuse large B-cell lymphoma. Clin Cancer Res 2005; 11:8265-8272.
39. Suzuki N, Zara J, Sato T, et al. A cytoplasmic protein, bystin, interacts with trophinin, tastin, and cytokeratin and may be involved in trophinin-mediated cell adhesion between tropho- blast and endometrial epithelial cells. Proc Natl Acad Sci USA 1998; 95:5027-5032.
40. Marcu KB, Bossone SA, Patel AJ. myc function and regulation. Annu Rev Biochem 1992; 61:809-860.
41. Paria BC, Dey SK, Andrews GK. Antisense c-myc effects on preimplantation mouse embryo development. Proc Natl Acad Sci USA 1992; 89:10051-10055.
42. Fomproix N, Gebrane-Younes J, Hernandez-Verdun D. Effects of anti-fibrillarin antibodies on building of functional nucleoli at the end of mitosis. J Cell Sci 1998; 111(Pt 3):359-372.
43. Hernandez-Verdun D. Nucleolus: from structure to dynamics. Histochem Cell Biol 2006; 125:127-137.
44. Sirri V, Hernandez-Verdun D, Roussel P. Cyclin-dependent kinases govern formation and maintenance of the nucleolus. J Cell Biol 2002; 156:969-981.
45. Sugihara K, Sugiyama D, Byrne J, et al. Trophoblast cell activation by trophinin ligation is implicated in human embryo implantation. Proc Natl Acad Sci USA 2007; 104:3799-3804.
46. Fukuda MN, Nozawa S. Trophinin, tastin, and bystin: a complex mediating unique attachment between trophoblastic and endometrial epithelial cells at their respective apical cell membranes. Semin Reprod Endocrinol 1999; 17:229-234.
47. Suzuki N, Nakayama J, Shih IM, et al. Expression of trophi- nin, tastin, and bystin by trophoblast and endometrial cells in human placenta. Biol Reprod 1999; 60:621-627.
48. Hatakeyama S, Ohyama C, Minagawa S, et al. Functional correlation of trophinin expression with the malignancy of testicular germ cell tumor. Cancer Res 2004; 64:4257-4262.
49. Yang S, Liu X, Yin Y, Fukuda MN, Zhou J. Tastin is required for bipolar spindle assembly and centrosome integrity during mitosis. FASEB J 2008; 22:1960-1972.
50. Zhu DH, Wang JB. Cultivating of QSG-7701 cell line and comparing it with liver cancer cell. Res Cancer Prev Treat 1979; 5:7-9.
51. Pan QW, Zhong SY, Liu BS, et al. Enhanced sensitivity of hepatocellular carcinoma cells to chemotherapy with a Smac- armed oncolytic adenovirus. Acta Pharmacol Sin 2007; 28:1996-2004.
52. Guo SY, Shen X, Yang J, et al. TIMP-1 mediates the inhibitory effect of interleukin-6 on the proliferation of a hepatocar- cinoma cell line in a STAT3-dependent manner. Braz J Med Biol Res 2007; 40:621-631.
53. Alley MC, Scudiero DA, Monks A, et al. Feasibility of drug screening with panels of human tumor cell lines using a mi- croculture tetrazolium assay. Cancer Res 1988; 48:589-601.
54. Savino TM, Bastos R, Jansen E, Hernandez-Verdun D. The nucleolar antigen Nop52, the human homologue of the yeast ribosomal RNA processing RRP1, is recruited at late stages of nucleologenesis. J Cell Sci 1999; 112(Pt 12):1889-1900.