Advertisement

Cell Biochemistry and Biophysics

, Volume 77, Issue 3, pp 253–260 | Cite as

The Ribosomal Protein RPLP0 Mediates PLAAT4-induced Cell Cycle Arrest and Cell Apoptosis

  • Chun-Hua Wang
  • Lu-Kai Wang
  • Chang-Chieh Wu
  • Mao-Liang Chen
  • Ming-Cheng Lee
  • Yi-Ying Lin
  • Fu-Ming TsaiEmail author
Original Paper
  • 55 Downloads

Abstract

Phospholipase A and acyltransferase 4 (PLAAT4) is a member of the HREV107 tumor suppressor gene family. The expression of PLAAT4 has been shown to induce cell death; however, the underlying mechanism remains unknown. Here, we found that RPLP0, a ribosomal protein, can interact with PLAAT4, as determined by yeast two-hybrid screening, coimmunoprecipitation, and colocalization. The level of RPLP0 was suppressed in HtTA cervical cancer cells expressing PLAAT4. In PLAAT4-expressing or RPLP0-silenced cells, decreased cell viability and cell proliferation combined with increased cell death were observed. Furthermore, the levels of cell cycle-associated proteins and anti-apoptotic proteins decreased in PLAAT4-expressing or RPLP0-silenced cells. Similar patterns of cell viability and expression levels of cell-cycle-associated proteins and apoptosis-related proteins were observed in PLAAT4-expressing and RPLP0-knockdown cells, indicating that RPLP0 deficiency might be involved in PLAAT4-mediated growth inhibition and cellular apoptosis.

Keywords

Phospholipase A and acyltransferase 4 Retinoid-inducible gene 1 RPLP0 Apoptosis Cell cycle arrest 

Notes

Acknowledgements

This work was supported by a grant (TCRD-TPE-108-9) from the Taipei Tzuchi Hospital through the Buddhist Tzuchi Medical Foundation, Taipei, Taiwan. We thank the Core Laboratory of the Buddhist Tzuchi General Hospital for support.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Ren, X., Lin, J., Jin, C., & Xia, B. (2010). 1H, 13C nd 15N resonance assignments of human H-REV107 N-terminal domain. Biomolecular NMR Assignments, 4(2), 175–178.CrossRefGoogle Scholar
  2. 2.
    Anantharaman, V., & Aravind, L. (2003). Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biology, 4(2), R11.CrossRefGoogle Scholar
  3. 3.
    DiSepio, D., Ghosn, C., Eckert, R. L., Deucher, A., Robinson, N., Duvic, M., Chandraratna, R. A., & Nagpal, S. (1998). Identification and characterization of a retinoid-induced class II tumor suppressor/growth regulatory gene. Proceedings of the National Academy of Sciences of The United States of America, 95(25), 14811–14815.Google Scholar
  4. 4.
    Higuchi, E., Chandraratna, R. A., Hong, W. K., & 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(30), 4627–4635.CrossRefGoogle Scholar
  5. 5.
    Huang, S. L., Shyu, R. Y., Yeh, M. Y., & Jiang, S. Y. (2000). Cloning and characterization of a novel retinoid-inducible gene 1(RIG1) deriving from human gastric cancer cells. Molecular and Cellular Endocrinology, 159, 15–24.CrossRefGoogle Scholar
  6. 6.
    Huang, S. L., Shyu, R. Y., Yeh, M. Y., & Jiang, S. Y. (2002). The retinoid-inducible gene I: effect on apoptosis and mitogen-activated kinase signal pathways. Anticancer Research, 22(2A), 799–804.Google Scholar
  7. 7.
    Jans, R., Sturniolo, M. T., & Eckert, R. L. (2008). Localization of the TIG3 transglutaminase interaction domain and demonstration that the amino-terminal region is required for TIG3 function as a keratinocyte differentiation regulator. Journal Of Investigative Dermatology, 128(3), 517–529.CrossRefGoogle Scholar
  8. 8.
    Sturniolo, M. T., Chandraratna, R. A., & Eckert, R. L. (2005). A novel transglutaminase activator forms a complex with type 1 transglutaminase. Oncogene, 24(18), 2963–2972.CrossRefGoogle Scholar
  9. 9.
    Sturniolo, M. T., Dashti, S. R., Deucher, A., Rorke, E. A., Broome, A. M., Chandraratna, R. A., Keepers, T., & Eckert, R. L. (2003). A novel tumor suppressor protein promotes keratinocyte terminal differentiation via activation of type I transglutaminase. Journal of Biological Chemistry, 278(48), 48066–48073.CrossRefGoogle Scholar
  10. 10.
    Tsai, F. M., Shyu, R. Y., Lin, S. C., Wu, C. C., & Jiang, S. Y. (2009). Induction of apoptosis by the retinoid inducible growth regulator RIG1 depends on the NC motif in HtTA cervical cancer cells. BMC Cell Biology, 10, 15.CrossRefGoogle Scholar
  11. 11.
    Hajnal, A., Klemenz, R., & Schafer, R. (1994). Subtraction cloning of H-rev107, a gene specifically expressed in H-ras resistant fibroblasts. Oncogene, 9(2), 479–490.Google Scholar
  12. 12.
    Deucher, A., Nagpal, S., Chandraratna, R. A., Di Sepio, D., Robinson, N. A., Dashti, S. R., & 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. International Journal of Oncology, 17(6), 1195–1203.Google Scholar
  13. 13.
    Tsai, F. M., Shyu, R. Y., & Jiang, S. Y. (2007). RIG1 suppresses Ras activation and induces cellular apoptosis at the Golgi apparatus. Cellular Signalling, 19(5), 989–999.CrossRefGoogle Scholar
  14. 14.
    Ban, N., Beckmann, R., Cate, J. H., Dinman, J. D., Dragon, F., Ellis, S. R., Lafontaine, D. L., Lindahl, L., Liljas, A., Lipton, J. M., McAlear, M. A., Moore, P. B., Noller, H. F., Ortega, J., Panse, V. G., Ramakrishnan, V., Spahn, C. M., Steitz, T. A., Tchorzewski, M., Tollervey, D., Warren, A. J., Williamson, J. R., Wilson, D., Yonath, A., & Yusupov, M. (2014). A new system for naming ribosomal proteins. Current Opinion in Structural Biology, 24, 165–169.CrossRefGoogle Scholar
  15. 15.
    Chan, D. S., Chu, L. O., Lee, K. M., Too, P. H., Ma, K. W., Sze, K. H., Zhu, G., Shaw, P. C., & Wong, K. B. (2007). Interaction between trichosanthin, a ribosome-inactivating protein, and the ribosomal stalk protein P2 by chemical shift perturbation and mutagenesis analyses. Nucleic Acids Research, 35(5), 1660–1672.CrossRefGoogle Scholar
  16. 16.
    McCluskey, A. J., Poon, G. M., Bolewska-Pedyczak, E., Srikumar, T., Jeram, S. M., Raught, B., & Gariepy, J. (2008). The catalytic subunit of shiga-like toxin 1 interacts with ribosomal stalk proteins and is inhibited by their conserved C-terminal domain. Journal Of Molecular Biology, 378(2), 375–386.CrossRefGoogle Scholar
  17. 17.
    Castro, M. E., Leal, J. F., Lleonart, M. E., Ramon, Y. C. S., & Carnero, A. (2008). Loss-of-function genetic screening identifies a cluster of ribosomal proteins regulating p53 function. Carcinogenesis, 29(7), 1343–1350.CrossRefGoogle Scholar
  18. 18.
    Bortoluzzi, S., d’Alessi, F., Romualdi, C., & Danieli, G. A. (2001). Differential expression of genes coding for ribosomal proteins in different human tissues. Bioinformatics, 17(12), 1152–1157.CrossRefGoogle Scholar
  19. 19.
    Wang, H., Zhao, L. N., Li, K. Z., Ling, R., Li, X. J., & Wang, L. (2006). Overexpression of ribosomal protein L15 is associated with cell proliferation in gastric cancer. BMC Cancer, 6, 91.CrossRefGoogle Scholar
  20. 20.
    Barnard, G. F., Staniunas, R. J., Bao, S., Mafune, K., Steele, Jr., G. D., Gollan, J. L., & Chen, L. B. (1992). Increased expression of human ribosomal phosphoprotein P0 messenger RNA in hepatocellular carcinoma and colon carcinoma. Cancer Research, 52(11), 3067–3072.Google Scholar
  21. 21.
    Artero-Castro, A., Castellvi, J., Garcia, A., Hernandez, J., Ramon y Cajal, S., & Lleonart, M. E. (2011). Expression of the ribosomal proteins Rplp0, Rplp1, and Rplp2 in gynecologic tumors. Human Pathology, 42(2), 194–203.CrossRefGoogle Scholar
  22. 22.
    Teller, A., Jechorek, D., Hartig, R., Adolf, D., Reissig, K., Roessner, A., & Franke, S. (2015). Dysregulation of apoptotic signaling pathways by interaction of RPLP0 and cathepsin X/Z in gastric cancer. Pathology Research and Practice, 211(1), 62–70.CrossRefGoogle Scholar
  23. 23.
    Wang, C. H., Shyu, R. Y., Wu, C. C., Tsai, T. C., Wang, L. K., Chen, M. L., Jiang, S. Y., & Tsai, F. M. (2014). Phospholipase A/Acyltransferase enzyme activity of H-rev107 inhibits the H-RAS signaling pathway. Journal of Biomedical Science, 21, 36.CrossRefGoogle Scholar
  24. 24.
    Han, B. G., Cho, J. W., Cho, Y. D., Kim, S. Y., Yoon, H. J., Song, H. K., Cheong, H. K., Jeon, Y. H., Lee, D. K., Lee, S., & Lee, B. I. (2008). Expression, purification and biochemical characterization of the N-terminal regions of human TIG3 and HRASLS3 proteins. Protein Expression and Purification, 71(1), 103–107.CrossRefGoogle Scholar
  25. 25.
    Tsai, F. M., Chen, M. L., Wang, L. K., & Lee, M. C. (2015). H-rev107 regulates cytochrome P450 reductase activity and increases lipid accumulation. PLoS ONE, 10(9), e0138586.CrossRefGoogle Scholar
  26. 26.
    Jin, X. H., Uyama, T., Wang, J., Okamoto, Y., Tonai, T., & Ueda, N. (2009). cDNA cloning and characterization of human and mouse Ca(2+)-independent phosphatidylethanolamine N-acyltransferases. Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids, 1791(1), 32–38.CrossRefGoogle Scholar
  27. 27.
    Shyu, R. Y., Hsieh, Y. C., Tsai, F. M., Wu, C. C., & Jiang, S. Y. (2008). Cloning and functional characterization of the HRASLS2 gene. Amino Acids, 35(1), 129–137.Google Scholar
  28. 28.
    Tsai, F. M., Shyu, R. Y., & Jiang, S. Y. (2006). RIG1 inhibits the Ras/mitogen-activated protein kinase pathway by suppressing the activation of Ras. Cellular Signalling, 18(3), 349–358.CrossRefGoogle Scholar
  29. 29.
    Wu, C. C., Shyu, R. Y., Wang, C. H., Tsai, T. C., Wang, L. K., Chen, M. L., Jiang, S. Y., & Tsai, F. M. (2012). Involvement of the prostaglandin D2 signal pathway in retinoid-inducible gene 1 (RIG1)-mediated suppression of cell invasion in testis cancer cells. Biochimica et Biophysica Acta - Molecular Cell Research, 1823(12), 2227–2236.CrossRefGoogle Scholar
  30. 30.
    Barnard, G. F., Staniunas, R. J., Mori, M., Puder, M., Jessup, M. J., Steele, Jr., G. D., & Chen, L. B. (1993). Gastric and hepatocellular carcinomas do not overexpress the same ribosomal protein messenger RNAs as colonic carcinoma. Cancer Research, 53(17), 4048–4052.Google Scholar
  31. 31.
    Loging, W. T., & Reisman, D. (1999). Elevated expression of ribosomal protein genes L37, RPP-1, and S2 in the presence of mutant p53. Cancer Epidemiology Biomarkers & Prevention, 8(11), 1011–1016.Google Scholar
  32. 32.
    Artero-Castro, A., Kondoh, H., Fernandez-Marcos, P. J., Serrano, M., Ramon y Cajal, S., & Lleonart, M. E. (2009). Rplp1 bypasses replicative senescence and contributes to transformation. Experimental Cell Research, 315(8), 1372–1383.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Chun-Hua Wang
    • 1
    • 2
  • Lu-Kai Wang
    • 3
  • Chang-Chieh Wu
    • 4
  • Mao-Liang Chen
    • 5
  • Ming-Cheng Lee
    • 5
  • Yi-Ying Lin
    • 5
  • Fu-Ming Tsai
    • 5
    Email author
  1. 1.Department of Dermatology, Taipei Tzuchi HospitalBuddhist Tzuchi Medical FoundationNew Taipei CityTaiwan
  2. 2.School of MedicineTzu Chi UniversityHualienTaiwan
  3. 3.Radiation Biology Core Laboratory, Institute for Radiological ResearchChang Gung University/Chang Gung Memorial HospitalTaoyuanTaiwan
  4. 4.Department of Surgery, Tri-Service General Hospital Keelung BranchNational Defense Medical CenterKeelungTaiwan
  5. 5.Department of Research, Taipei Tzuchi HospitalBuddhist Tzuchi Medical FoundationNew Taipei CityTaiwan

Personalised recommendations