Mechanisms of the HRSL3 tumor suppressor fuction in ovarian carcinoma cells

Journal of Cell Science

Volumn 120, Issue 8, 2007, Pages 1393-1404

  Nazarenko, Irina ^a   Schäfer, Reinhold ^a   Sers, Christine ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Apoptosis; HRSL3; PP2A; Tumor suppressor

Indexed keywords

PHOSPHATASE; PHOSPHATASE 2A; PROTEIN HRSL3; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER GROWTH; CARCINOMA CELL; CATALYSIS; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TWO HYBRID SYSTEM;

APOPTOSIS; BASE SEQUENCE; CATALYSIS; CELL LINE, TUMOR; DNA PRIMERS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENES, TUMOR SUPPRESSOR; HUMANS; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROSCOPY, CONFOCAL; OVARIAN NEOPLASMS; PHOSPHOPROTEIN PHOSPHATASE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEINS;

MAMMALIA;

EID: 34249027747     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.000018     Document Type: Article

References (85)

1. Abraham, D., Podar, K., Pacher, M., Kubicek, M., Welzel, N., Hemmings, B. A., Dilworth, S. M., Mischak, H., Kolch, W. and Baccarini, M. (2000). Raf-1-associated protein phosphatase 2A as a positive regulator of kinase activation. J. Biol. Chem. 275, 22300-22304.
2. Alessi, D. R., Gomez, N., Moorhead, G., Lewis, T., Keyse, S. M. and Cohen, P. (1995). Inactivation of p42 MAP kinase by protein phosphatase 2A and a protein tyrosine phosphatase, but not CL100, in various cell lines. Curr. Biol. 5, 283-295.
3. Anantharaman, V. and Aravind, L. (2003). Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol. 4, R11.
4. Andreola, E, Giandomenico, V., Spero, R. and De Luca, L. M. (2000). Expression of a smaller lecithin:retinol acyl transferase transcript and reduced retinol esterification in MCF-7 cells. Biochem. Biophys. Res. Commun. 279, 920-924.
5. Bastians, H. and Ponstingl, H. (1996). The novel human protein serine/threonine phosphatase 6 is a functional homologue of budding yeast Sit4p and fission yeast ppe1, which are involved in cell cycle regulation. J. Cell Sci. 109, 2865-2874.
6. Bennin, D. A., Don, A. S., Brake, T., McKenzie, J. L., Rosenbaum, H., Ortiz, L., DePaoli-Roach, A. A. and Horne, M. C. (2002). Cyclin G2 associates with protein phosphatase 2A catalytic and regulatory B' subunits in active complexes and induces nuclear aberrations and a G1/S phase cell cycle arrest. J. Biol. Chem. 277, 27449-27467.
7. Boorjian, S, Tickoo, S. K., Mongan, N. P., Yu, H., Bok, D, Rando, R. R., Nanus, D. M., Scherr, D. S. and Gudas, L. J. (2004). Reduced lecithin: retinol acyltransferase expression correlates with increased pathologic tumor stage in bladder cancer. Clin. Cancer Res. 10, 3429-3437.
8. Boudreau, R. T. and Hoskin, D. W. (2005). The use of okadaic acid to elucidate the intracellular role(s) of protein phosphatase 2A: lessons from the mast cell model system. Int. Immunopharmacol. 5, 1507-1518.
9. Brewis, N. D., Street, A. J., Prescott, A. R. and Cohen, P. T. (1993). PPX, a novel protein serine/threonine phosphatase localized to centrosomes. EMBO J. 12, 987-996.
10. Bryant, J. C., Westphal, R. S. and Wadzinski, B. E. (1999). Methylated C-terminal leucine residue of PP2A catalytic subunit is important for binding of regulatory Balpha subunit. Biochem. J. 339, 241-246.
11. Chen, J., Peterson, R. T. and Schreiber, S. L. (1998). Alpha 4 associates with protein phosphatases 2A, 4, and 6. Biochem. Biophys. Res. Commun. 247, 827-832.
12. Chen, W., Possemato, R., Campbell, K. T., Plattner, C. A., Pallas, D. C. and Hahn, W. C. (2004). Identification of specific PP2A complexes involved in human cell transformation. Cancer Cell 5, 127-136.
13. Chen, W., Arroyo, J. D., Timmons, J. C., Possemato, R. and Hahn, W. C. (2005). Cancer-associated PP2A Aalpha subunits induce functional haploinsufficiency and tumorigenicity. Cancer Res. 65, 8193-8192.
14. Chung, H., Nairn, A. C., Murata, K. and Brautigan, D. L. (1999). Mutation of Tyr307 and Leu309 in the protein phosphatase 2A catalytic subunit favors association with the alpha 4 subunit which promotes dephosphorylation of elongation factor-2. Biochemistry 38, 10371-10376.
15. Cohen, P. T., Chen, M. X. and Armstrong, C. G. (1996). Novel protein phosphatases that may participate in cell signaling. Adv. Pharmacol. 36, 67-89.
16. Deucher, A., Nagpal, S., Chandraratna, R. A. S., Di Sepio, D., Robinson, N. A., Dashti, S. R. and Eckert, R. L. (2000). The carboxy-terminal hydrophobic domain of TIG3, a class II tumor suppressor protein, is required for appropriate cellular localization and optimal biological activity. Int. J. Oncol. 17, 1195-1203.
17. DiSepio, D., Ghosn, C., Eckert, R. L., Deucher, A., Robinson, N., Duvic, M., Chandraratna, R. A. S. and Nagpal, S. (1998). Identification and characterization of a retinoid-induced class II tumor suppressor growth regulatory gene. Proc. Natl. Acad. Sci. USA 95, 14811-14815.
18. Duvic, M., Helekar, B, Schulz, C., Cho, M., DiSepio, D., Hager, C., Dimao, D., Hazarika, P., Jackson, B., Breuer-McHam, J. et al. (2000). Expression of a retinoid-inducible tumor suppressor, Tazarotene-inducible gene-3, is decreased in psoriasis and skin cancer. Clin. Cancer Res. 6, 3249-3259.
19. Duvic, M., Ni, X., Talpur, R., Herne, K., Schulz, C., Sui, D., Ward, S., Joseph, A. and Hazarika, P. (2003). Tazarotene-induced gene 3 is suppressed in basal cell carcinomas and reversed in vivo by tazarotene application. J Invest. Dermatol. 121, 902-909.
20. Favre, B., Turowski, P. and Hemmings, B. A. (1997). Differential inhibition and posttranslational modification of protein phosphatase 1 and 2A in MCF7 cells treated with calyculin-A, okadaic acid, and tautomycin. J. Biol. Chem. 272, 13856-13863.
21. Gao, Z. H., Seeling, J. M., Hill, V., Yochum, A. and Virshup, D. M. (2002). Casein kinase I phosphorylates and destabilizes the beta-catenin degradation complex. Proc. Natl. Acad. Sci. USA 99, 1182-1187.
22. Garcia, A., Cayla, X., Guergnon, J., Dessauge, F., Hospital, V., Rebollo, M. P., Fleischer, A. and Rebollo, A. (2003). Serine/ threonine protein phosphatases PP1 and PP2A are key players in apoptosis. Biochimie 85, 721-726.
23. Gotz, J., Probst, A., Mistl, C., Nitsch, R. M. and Ehler, E. (2000). Distinct role of protein phosphatase 2A subunit Calpha in the regulation of E-cadherin and beta-catenin during development. Mech. Dev. 93, 83-93.
24. Grethe, S. and Porn-Ares, M. I. (2005). p38 MAPK regulates phosphorylation of Bad via PP2A-dependent suppression of the MEK1/2-ERK1/ 2 survival pathway in TNF-alpha induced endothelial apoptosis. Cell. Signal. 18, 531-540.
25. Griegel, S., Traub, O., Willecke, K. and Schäfer, R. (1986). Suppression and re-expression of transformed phenotype in hybrids of HA-ras-1-transformed rat-1 cells and early-passage rat embryonic fibroblasts. Int. J. Cancer 5, 697-705.
26. Guo, X. and Gudas, L. J. (1998). Metabolism of all-trans-retinol in normal human cell strains and squamous cell carcinoma (SCC) lines from the oral cavity and skin: reduced esterification of retinol in SCC lines. Cancer Res. 58, 166-176.
27. Guo, X., Ruiz, A., Rando, R. R., Bok, D. and Gudas, L. J. (2000). Esterification of all-trans-retinol in normal human epithelial cell strains and carcinoma lines from oral cavity, skin and breast: reduced expression of lecithin:retinol acyltransferase in carcinoma lines. Carcinogenesis 21, 1925-1933.
28. Guo, X., Nanus, D. M., Ruiz, A., Rando, R. R., Bok, D. and Gudas, L. J. (2001). Reduced levels of retinyl esters and vitamin A in human renal cancers. Cancer Res. 61, 2774-2781.
29. Guo, X, Knudsen, B. S., Peehl, D. M., Ruiz, A, Bok, D., Rando, R. R., Rhim, J. S, Nanus, D. M. and Gudas, L. J. (2002). Retinol metabolism and lecithin:retinol acyltransferase levels are reduced in cultured human prostate cancer cells and tissue specimens. Cancer Res. 62, 1654-1661.
30. Hajnal, A., Klemenz, R. and Schäfer, R. (1994). Subtraction cloning of H-Rev107, a gene specificafly expressed in H-Ras resistant fibroblasts. Oncogene 9, 479-490.
31. Hemmati, P. G., Gillissen, B., von Haefen, C., Wendt, J., Starck, L., Guner, D., Dorken, B. and Daniel, P. T. (2002). Adenovirus-mediated overexpression of p14(ARF) induces p53 and Bax-independent apoptosis. Oncogene 21, 3149-3161.
32. Higuchi, E., Chandraratna, R. A., Hong, W. K. and Lotan, R. (2003). Induction of TIG3, a putative class II tumor suppressor gene, by retinoic acid in head and neck and lung carcinoma cells and its association with suppression of the transformed phenotype. Oncogene 22, 4627-4635.
33. Holmes, C. F., Luu, H. A., Carrier, F. and Schmitz, F. J. (1990). Inhibition of protein phosphatases-1 and -2A with acanthifolicin. Comparison with diarrhetic shellfish toxins and identification of a region on okadaic acid important for phosphatase inhibition. FEBS Lett. 270, 216-218.
34. Huang, S. L., Shyu, R. Y., Yeh, M. Y. and Jiang, S. Y. (2000). Cloning and characterization of a novel retinoid-inducible gene 1 (RIG1) deriving from human gastric cancer cells. Mol. Cell. Endocrinol. 159, 15-24.
35. Huang, S. L., Shyu, R. Y., Yeh, M. Y. and Jiang, S. Y. (2002). The retinoid-inducible gene I: Effect on apoptosis and mitogen-activated kinase signal pathways. Anticancer Res. 22, 799-804.
36. Hughes, P. J. and Stanway, G. (2000). The 2A proteins of three diverse picornaviruses are related to each other and to the H-rev107 family of proteins involved in the control of cell proliferation. J. Gen. Virol. 81, 201-207.
37. Husmann, K., Sers, C., Fietze, E., Mincheva, A., Lichter, P. and Schäfer, R. (1998). Transcriptional and translational downregulation of H-REV107, a class II tumour suppressor gene located on human chromosome 11q11-12. Oncogene 17, 1305-1312.
38. Ikeda, S., Kishida, M., Matsuura, Y., Usui, H. and Kikuchi, A. (2000). GSK-3beta-dependent phosphorylation of adenomatous polyposis coli gene product can be modulated by beta-catenin and protein phosphatase 2A complexed with Axin. Oncogene 19, 537-545.
39. Janssens, V. and Goris, J. (2001). Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem. J. 353, 417-439.
40. Janssens, V., Goris, J. and Van Hoof, C. (2005). PP2A: the expected tumor suppressor. Curr. Opin. Genet. Dev. 15, 34-41.
41. Jaumot, M. and Hancock, J. F. (2001). Protein phosphatases 1 and 2A promote Raf-1 activation by regulating 14-3-3 interactions. Oncogene 20, 3949-3958.
42. Jurukovski, V. and Simon, M. (1999). Reduced lecithin:retinol acyl transferase activity in cultured squamous cell carcinoma lines results in increased substrate-driven retinoic acid synthesis. Biochim. Biophys. Acta 1436, 479-490.
43. Kaneda, A., Kaminishi, M, Yanagihara, K., Sugimura, T. and Ushijima, T. (2002). Identification of silencing of nine genes in human gastric cancers. Cancer Res. 62, 6645-6650.
44. Li, L., Ren, C. H., Tahir, S. A., Ren, C. and Thompson, T. C. (2003). Caveolin-1 maintains activated Akt in prostate cancer cells through scaffolding domain binding site interactions with and inhibition of serine/threonine protein phosphatases PP1 and PP2A. Mol. Cell. Biol. 23, 9389-9404.
45. Li, X., Yost, H. J., Virshup, D. M. and Seeling, J. M. (2001). Protein phosphatase 2A and its B56 regulatory subunit inhibit Wnt signaling in Xenopus. EMBO J. 20, 4122-4131.
46. Li, X., Scuderi, A., Letsou, A. and Virshup, D. M. (2002). B56-associated protein phosphatase 2A is required for survival and protects from apoptosis in Drosophila melanogaster. Mol. Cell. Biol. 22, 3674-3684.
47. Lotz, K., Kellner, T., Heitmann, M., Nazarenko, I., Noske, A., Malek, A., Gontarewiez, A., Schäfer, R. and Sers, C. (2005). Suppression of the TIG3 tumor suppressor gene in human ovarian carcinomas is mediated via mitogen-activated kinase-dependent and independent mechanisms. Int. J. Cancer 116, 894-902.
48. MacDonald, P. N. and Ong, D. E. (1988). Evidence for a lecithin-retinol acyltransferase activity in the rat small intestine. J. Biol. Chem. 263, 12478-12482.
49. MacKeigen, J. P., Murphy, L. O. and Blenis, J. (2005). Sensitized RNAi screen of human kinases and pbosphatases identifies new regulators of apoptosis and chemoresistance. Nat. Cell Biol. 7, 591-600.
50. McCluskey, A., Sim, A. T. and Sakoff, J. A. (2002). Serine-threonine protein phosphatase inhibitors: development of potential therapeutic strategies. J Med Chem. 45, 1151-1175.
51. Millward, T. A., Zolnierowicz, S. and Hemmings, B. A. (1999). Regulation of protein kinase cascades by protein phosphatase 2A. Trends Biochem. Sci. 24, 186-191.
52. Mondal, M. S., Ruiz, A., Bok, D. and Rando, R. R. (2000). Lecithin retinol acyltransferase contains cysteine residues essential for catalysis. Biochemistry 39, 5215-5220.
53. Mondal, M. S., Ruiz, A., Hu, J., Bok, D. and Rando, R. R. (2001). Two histidine residues are essential for catalysis by lecithin retinol acyl transferase. FEBS Lett. 489, 14-18.
54. Nunbhakdi-Craig, V., Machleidt, T., Ogris, E., Bellotto, D., White, C. L., III and Sontag, E. (2002). Protein phosphatase 2A associates with and regulates atypical PKC and the epithelial tight junction complex. J. Cell Biol. 158, 967-978.
55. Prickett, T. D. and Brautigan, D. L. (2004). Overlapping binding sites in protein phosphatase 2A for association with regulatory A and alpha-4 (mTap42) subunits. J. Biol. Chem. 279, 38912-38920.
56. Ratcliffe, M. J., Itoh, K. and Sokol, S. Y. (2000). A positive role for the PP2A catalytic subunit in Wnt signal transduction. J. Biol. Chem. 275, 35680-35683.
57. Ricciarelli, R. and Azzi, A. (1998). Regulation of recombinant PKC alpha activity by protein phosphatase 1 and protein phosphatase 2A. Arch. Biochem. Biophys. 355, 197-200.
58. Ruiz, A., Winston, A., Lim, Y. H., Gilbert, B. A., Rando, R. R. and Bok, D. (1999). Molecular and biochemical characterization of lecithin retinol acyltransferase. J. Biol. Chem. 274, 3834-3841.
59. Sager, R. (1997). Expression genetics in cancer: shifting the, focus from DNA to RNA. Proc. Natl. Acad. Sci. USA 94, 952-955.
60. Sasaki, K., Murata, M., Yasumoto, T., Mieskes, G. and Takai, A. (1994). Affinity of okadaic acid to type-1 and type-2A protein phosphatases is markedly reduced by oxidation of its 27-hydroxyl group. Biochem. J. 298, 259-262.
61. Schonthal, A. H. (1998). Role of PP2A in intracellular signal transduction pathways. Front. Biosci. 3, D1262-D1273.
62. Seeling, J. M., Miller, J. R., Gil, R., Moon, R. T., White, R. and Virshup, D. M. (1999). Regulation of beta-catenin signaling by the B56 subunit of protein phosphatase 2A. Science 283, 2089-2091.
63. Sers, C., Emmenegger, U., Husmann, K., Bucher, K., Andres, A. C. and Schäfer, R. (1997). Growth-inhibitory activity and downregulation of the class II tumor-suppressor gene H-rev107 in tumor cell lines and experimental tumors. J. Cell Biol. 136, 935-944.
64. Sers, C., Husmann, K., Nazarenko, I., Reich, S., Wiechen, K., Zhumabayeva, B., Adhikari, P., Schroder, K., Gontarewicz, A. and Schäfer, R. (2002). The class II tumour suppressor gene H-REV107-1 is a target of interferon-regulatory factor-1 and is involved in IFNgamma-induced cell death in human ovarian carcinoma cells. Oncogene 21, 2829-2839.
65. Shyu, R. Y., Jiang, S. Y., Chou, J. M., Shih, Y. L., Lee, M. S., Yu, J. C., Chao, P. C., Hsu, Y. J. and Jao, S. W. (2003). RARRES3 expression positively correlated to tumour differentiation in tissues of colorectal adenocarcinoma. Br. J. Cancer 89, 146-151.
66. Siegrist, S., Feral, C., Chami, M., Solhonne, B., Mattei, M. G., Rajpert-De Meyts, E., Guellaen, G. and Bulle, F. (2001). hH-Rev107, a class II tumor suppressor gene, is expressed by post-meiotic testicular germ cells and CIS cells but not by human testicular germ cell tumors. Oncogene 20, 5155-5163.
67. Silverstein, A. M., Barrow, C. A., Davis, A. J. and Mumby, M. C. (2002). Actions of PP2A on the MAP kinase pathway and apoptosis are mediated by distinct regulatory subunits. Proc. Natl. Acad. Sci. USA 99, 4221-4226.
68. Sim, A. T. and Scott, J. D. (1999). Targeting of PKA, PKC and protein phosphatases to cellular microdomains. Cell Calcium 26, 209-217.
69. Simmons, D. P., Andreola, F. and De Luca, L. M. (2002). Human melanomas of fibroblast and epithelial morphology differ widely in their ability to synthesize retinyl esters. Carcinogenesis 23, 1821-1830.
70. Sontag, E. (2001). Protein phosphatase 2A: the Trojan Horse of cellular signaling. Cell. Signal. 13, 7-16.
71. Sontag, E., Sontag, J. M. and Garcia, A. (1997). Protein phosphatase 2A is a critical regulator of protein kinase C zeta signaling targeted by SV40 small t to promote cell growth and NF-kappaB activation. EMBO J. 16, 5662-5671.
72. Standaert, M. L., Bandyopadhyay, G., Sajan, M. P., Cong, L., Quon, M. J. and Farese, R. V. (1999). Okadaic acid activates atypical protein kinase C (zeta/lambda) in rat and 3T3/L1 adipocytes. An apparent requirement for activation of Glut4 translocation and glucose transport. J. Biol. Chem. 274, 14074-14078.
73. Strack, S., Cribbs, J. T. and Gomez, L. (2004). Critical role for protein phosphatase 2A heterotrimers in mammalian cell survival. J Biol. Chem. 279, 47732-47739.
74. Sturniolo, M. T., Dashti S. R., Deucher, A., Rorke, E. A., Broome, A. M., Chandraratna, R. A. S., Keepers, T. and Eckert, R. L. (2003). A novel tumor suppressor protein promotes keratinocyte terminal differentiation via activation of type I transglutaminase. J. Biol. Chem. 278, 48066-48073.
75. Tsai, F. M., Shyu, R. Y. and Jiang, S. Y. (2006). RIG1 inhibits the Rash/mitogen-activated protein kinase pathway by suppressing the activation of Ras. Cell. Signal. 18, 349-358.
76. Turowski, P., Fernandez, A., Favre, B., Lamb, N. J. and Hemmings, B. A. (1995). Differential methylation and altered conformation of cytoplasmic and nuclear forms of protein phosphatase 2A during cell cycle progression. J. Cell Biol. 129, 397-410.
77. Wu, J., Tolstykh, T., Lee, J., Boyd, K., Stock, J. B. and Broach, J. R. (2000). Carboxyl methylation of the phosphoprotein phosphatase 2A catalytic subunit promotes its functional association with regulatory subunits in vivo. EMBO J. 19, 5672-5681.
78. Xue, L. and Rando, R. R. (2004). Roles of cysteine 161 and tyrosine 154 in the lecithin-retinol acyltransferase mechanism. Biochemistry 43, 6120-6126.
79. Xue, L., Jahng, W. J., Gollapalli, D. and Rando, R. R. (2006). Palmitoyl transferase activity of lecithin retinol acyl transferase. Biochemistry 45, 10710-10718.
80. Yamamoto, H., Hinoi, T., Michiue, T., Fukui, A., Usui, H., Janssens, V., Van Hoof, C., Goris, J., Asashima, M. and Kikuchi, A. (2001). Inhibition of the Wnt signaling pathway by the PR61 subunit of protein phosphatase 2A. J. Biol. Chem. 276, 26875-26882.
81. Yang, J., Wu, J., Tan, C. and Klein, P. S. (2003). PP2A:B56epsilon is required for Wnt/beta-catenin signaling during embryonic development. Development 130, 5569-5578.
82. Zhan, H. C., Gudas, L. J., Bok, D., Rando, R., Nanus, D. M. and Tickoo, S. K. (2003). Differential expression of the enzyme that esterifies refinol, lecithin:retinol acyltransferase, in subtypes of human renal cancer and normal kidney. Clin. Cancer Res. 9, 4897-4905.
83. Zhang, L., Huang, J., Yang, N., Liang, S., Barchetti, A., Giannakakis, A., Cadungog, M. G., O'Brien-Jenkins, A., Massobrio, M., Roby, K. F. et al. (2006). Integrative genomic analysis of protein kinase C (PKC) family identifies PKCiota as a biomarker and potential oncogene in ovarian carcinoma. Cancer Res. 66, 4627-4635.
84. Zhou, B., Wan, Z. X., Zhao, Y., Brautigan, D. L. and Zhang, Z. Y. (2002). The specificity of extracellular signal-regulated kinase 2 dephosphorylation by protein phosphatases. J. Biol. Chem. 277, 31818-31825.
85. Zuluaga, S., Alvarez-Barrientos, A., Gutierrez-Uzquiza, A., Benito, M., Nebreda, A. R. and Porras, A. (2007). Negative regulation of Akt activity by p38alpha MAP kinase in cardiomyocytes involves membrane localization of PP2A through interaction with caveolin-1. Cell. Signal. 19, 62-74.