Cell cycle restriction is more important than apoptosis induction for RASSF1A Protein tumor suppression

Journal of Biological Chemistry

Volumn 289, Issue 45, 2014, Pages 31287-31295

  Donninger, Howard ^a   Clark, Jennifer A ^a   Monaghan, Megan K ^a   Lee Schmidt, M ^b   Vos, Michele ^c   Clark, Geoffrey J ^a  

^a University of Louisville School of Medicine   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; TUMORS;

APOPTOSIS INDUCTION; APOPTOTIC EFFECTS; CELL CYCLE REGULATION; CELL-CYCLE ARREST; MICROTUBULE ASSOCIATED PROTEIN; SINGLE-POINT MUTATION; TUMOR SUPPRESSION; TUMOR SUPPRESSORS;

PROTEINS;

CARRIER PROTEINS AND BINDING PROTEINS; CASPASE 3; CASPASE 7; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN 1A; MICROTUBULE ASSOCIATED PROTEIN 4; MICROTUBULE ASSOCIATED PROTEIN C19ORF5; PROTEIN NORE1A; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; TRANSCRIPTION FACTOR YAP1; TUBULIN; UNCLASSIFIED DRUG; GREEN FLUORESCENT PROTEIN; RAS PROTEIN; RASSF1 PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

AMINO ACID SUBSTITUTION; APOPTOSIS; ARTICLE; CANCER INHIBITION; CELL CYCLE CHECKPOINT; CELL CYCLE REGULATION; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; COS 7 CELL LINE; DIMERIZATION; ENZYME ACTIVATION; FAL MOTIF; G2 PHASE CELL CYCLE CHECKPOINT; GENETIC TRANSFECTION; GENETIC VARIABILITY; HEK293 CELL LINE; MICROTUBULE; MOLECULAR DYNAMICS; PHENOTYPE; POINT MUTATION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; CELL CYCLE; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; SEQUENCE HOMOLOGY; TUMOR CELL LINE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; GREEN FLUORESCENT PROTEINS; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; POINT MUTATION; RAS PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TUMOR SUPPRESSOR PROTEINS;

EID: 84909951720     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.609537     Document Type: Article

References (41)

1. Donninger, H., Vos, M. D., and Clark, G. J. (2007) The RASSF1A tumor suppressor. J. Cell Sci. 120, 3163-3172
2. van der Weyden, L., and Adams, D. J. (2007) The Ras-association domain family (RASSF) members and their role in human tumourigenesis. Biochim. Biophys. Acta 1776, 58-85
3. Dallol, A., Agathanggelou, A., Fenton, S. L., Ahmed-Choudhury, J., Hesson, L., Vos, M. D., Clark, G. J., Downward, J., Maher, E. R., and Latif, F. (2004) RASSF1A interacts with microtubule-associated proteins and modulates microtubule dynamics. Cancer Res. 64, 4112-4116
4. El-Kalla, M., Onyskiw, C., and Baksh, S. (2010) Functional importance of RASSF1A microtubule localization and polymorphisms. Oncogene 29, 5729-5740
5. Vos, M. D., Martinez, A., Elam, C., Dallol, A., Taylor, B. J., Latif, F., and Clark, G. J. (2004) A role for the RASSF1A tumor suppressor in the regulation of tubulin polymerization and genomic stability. Cancer Res. 64, 4244-4250
6. Song, M. S., Song, S. J., Ayad, N. G., Chang, J. S., Lee, J. H., Hong, H. K., Lee, H., Choi, N., Kim, J., Kim, H., Kim, J. W., Choi, E. J., Kirschner, M. W., and Lim, D. S. (2004) The tumour suppressor RASSF1A regulates mitosis by inhibiting the APC-Cdc20 complex. Nat. Cell Biol. 6, 129-137
7. Liu, L., Tommasi, S., Lee, D. H., Dammann, R., and Pfeifer, G. P. (2003) Control of microtubule stability by the RASSF1A tumor suppressor. Oncogene 22, 8125-8136
8. Agathanggelou, A., Cooper, W. N., and Latif, F. (2005) Role of the Rasassociation domain family 1 tumor suppressor gene in human cancers. Cancer Res. 65, 3497-3508
9. Dammann, R., Schagdarsurengin, U., Seidel, C., Strunnikova, M., Rastetter, M., Baier, K., and Pfeifer, G. P. (2005) The tumor suppressor RASSF1A in human carcinogenesis: an update. Histol. Histopathol. 20, 645-663
10. Rong, R., Jin, W., Zhang, J., Sheikh, M. S., and Huang, Y. (2004) Tumor suppressor RASSF1A is a microtubule-binding protein that stabilizes microtubules and induces G2/M arrest. Oncogene 23, 8216-8230
11. Liu, L., Vo, A., and McKeehan, W. L. (2005) Specificity of the methylationsuppressed A isoform of candidate tumor suppressor RASSF1 for microtubule hyperstabilization is determined by cell death inducer C19ORF5. Cancer Res. 65, 1830-1838
12. Donninger, H., Barnoud, T., Nelson, N., Kassler, S., Clark, J., Cummins, T. D., Powell, D. W., Nyante, S., Millikan, R. C., and Clark, G. J. (2011) RASSF1A and the rs2073498 Cancer Associated SNP. Front Oncol. 1, 54
13. Baksh, S., Tommasi, S., Fenton, S., Yu, V. C., Martins, L. M., Pfeifer, G. P., Latif, F., Downward, J., and Neel, B. G. (2005) The tumor suppressor RASSF1A and MAP-1 link death receptor signaling to Bax conformational change and cell death. Mol. Cell 18, 637-650
14. Vos, M. D., Dallol, A., Eckfeld, K., Allen, N. P., Donninger, H., Hesson, L. B., Calvisi, D., Latif, F., and Clark, G. J. (2006) The RASSF1A tumor suppressor activates Bax via MOAP-1. J. Biol. Chem. 281, 4557-4563
15. Avruch, J., Praskova, M., Ortiz-Vega, S., Liu, M., and Zhang, X. F. (2006) Nore1 and RASSF1 regulation of cell proliferation and of the MST1/2 kinases. Methods Enzymol. 407, 290-310
16. Donninger, H., Allen, N., Henson, A., Pogue, J., Williams, A., Gordon, L., Kassler, S., Dunwell, T., Latif, F., and Clark, G. J. (2011) Salvador protein is a tumor suppressor effector of RASSF1A with hippo pathway-independent functions. J. Biol. Chem. 286, 18483-18491
17. Guo, C., Tommasi, S., Liu, L., Yee, J. K., Dammann, R., and Pfeifer, G. P. (2007) RASSF1A is part of a complex similar to the Drosophila Hippo/ Salvador/Lats tumor-suppressor network. Curr. Biol. 17, 700-705
18. Matallanas, D., Romano, D., Yee, K., Meissl, K., Kucerova, L., Piazzolla, D., Baccarini, M., Vass, J. K., Kolch, W., and O'Neill, E. (2007) RASSF1A elicits apoptosis through an MST2 pathway directing proapoptotic transcription by the p73 tumor suppressor protein. Mol. Cell 27, 962-975
19. Vos, M. D., Ellis, C. A., Bell, A., Birrer, M. J., and Clark, G. J. (2000) Ras uses the novel tumor suppressor RASSF1 as an effector to mediate apoptosis. J. Biol. Chem. 275, 35669-35672
20. Fiordalisi, J. J., Johnson, R. L., 2nd, Ulkü, A. S., Der, C. J., and Cox, A. D. (2001) Mammalian expression vectors for Ras family proteins: generation and use of expression constructs to analyze Ras family function. Methods Enzymol. 332, 3-36
21. Dallol, A., Cooper, W. N., Al-Mulla, F., Agathanggelou, A., Maher, E. R., and Latif, F. (2007) Depletion of the Ras association domain family 1, isoform A-associated novel microtubule-associated protein, C19ORF5/ MAP1S, causes mitotic abnormalities. Cancer Res. 67, 492-500
22. Cooper, W. N., Hesson, L. B., Matallanas, D., Dallol, A., von Kriegsheim, A., Ward, R., Kolch, W., and Latif, F. (2009) RASSF2 associates with and stabilizes the proapoptotic kinase MST2. Oncogene 28, 2988-2998
23. Chien, C. L., Lu, K. S., Lin, Y. S., Hsieh, C. J., and Hirokawa, N. (2005) The functional cooperation of MAP1A heavy chain and light chain 2 in the binding of microtubules. Exp. Cell Res. 308, 446-458
24. Creasy, C. L., and Chernoff, J. (1995) Cloning and characterization of a human protein kinase with homology to Ste20. J. Biol. Chem. 270, 21695-21700
25. Donninger, H., Binder, A., Bohm, L., and Parker, M. I. (2008) Differential effects of novel tumour-derived p53 mutations on the transformation of NIH-3T3 cells. Biol. Chem. 389, 57-67
26. Ortiz-Vega, S., Khokhlatchev, A., Nedwidek, M., Zhang, X. F., Dammann, R., Pfeifer, G. P., and Avruch, J. (2002) The putative tumor suppressor RASSF1A homodimerizes and heterodimerizes with the Ras-GTP binding protein Nore1. Oncogene 21, 1381-1390
27. Clark, J., Freeman, J., and Donninger, H. (2012) Loss of RASSF2 enhances tumorigencity of lung cancer cells and confers resistance to chemotherapy. Mol. Biol. Int. 2012, 705948
28. Matallanas, D., Romano, D., Al-Mulla, F., O'Neill, E., Al-Ali, W., Crespo, P., Doyle, B., Nixon, C., Sansom, O., Drosten, M., Barbacid, M., and Kolch, W. (2011) Mutant K-Ras activation of the proapoptotic MST2 pathway is antagonized by wild-type K-Ras. Mol. Cell 44, 893-906
29. Stieglitz, B., Bee, C., Schwarz, D., Yildiz, O., Moshnikova, A., Khokhlatchev, A., and Herrmann, C. (2008) Novel type of Ras effector interaction established between tumour suppressor NORE1A and Ras switch II. EMBO J. 27, 1995-2005
30. Moshnikova, A., Kuznetsov, S., and Khokhlatchev, A. V. (2008) Interaction of the growth and tumour suppressor NORE1A with microtubules is not required for its growth-suppressive function. BMC Res. Notes 1, 13
31. Burbee, D. G., Forgacs, E., Zöchbauer-Müller, S., Shivakumar, L., Fong, K., Gao, B., Randle, D., Kondo, M., Virmani, A., Bader, S., Sekido, Y., Latif, F., Milchgrub, S., Toyooka, S., Gazdar, A. F., Lerman, M. I., Zabarovsky, E., White, M., and Minna, J. D. (2001) Epigenetic inactivation of RASSF1A in lung and breast cancers and malignant phenotype suppression. J. Natl. Cancer Inst. 93, 691-699
32. Malumbres, M., and Pellicer, A. (1998) RAS pathways to cell cycle control and cell transformation. Front. Biosci. 3, d887-d912
33. Chen, Z., Otto, J. C., Bergo, M. O., Young, S. G., and Casey, P. J. (2000) The C-terminal polylysine region and methylation of K-Ras are critical for the interaction between K-Ras and microtubules. J. Biol. Chem. 275, 41251-41257
34. Demir, O., Korulu, S., Yildiz, A., Karabay, A., and Kurnaz, I. A. (2009) Elk-1 interacts with neuronal microtubules and relocalizes to the nucleus upon phosphorylation. Mol. Cell Neurosci. 40, 111-119
35. Thissen, J. A., Gross, J. M., Subramanian, K., Meyer, T., and Casey, P. J. (1997) Prenylation-dependent association of Ki-Ras with microtubules: evidence for a role in subcellular trafficking. J. Biol. Chem. 272, 30362-30370
36. Casar, B., Arozarena, I., Sanz-Moreno, V., Pinto, A., Agudo-Ibáñez, L., Marais, R., Lewis, R. E., Berciano, M. T., and Crespo, P. (2009) Ras subcellular localization defines extracellular signal-regulated kinase 1 and 2 substrate specificity through distinct utilization of scaffold proteins. Mol. Cell. Biol. 29, 1338-1353
37. Arnette, C., Efimova, N., Zhu, X., Clark, G. J., and Kaverina, I. (2014) Microtubule segment stabilization by RASSF1A is required for proper microtubule dynamics and Golgi integrity Mol. Biol. Cell 25, 800-810
38. Rong, R., Jiang, L. Y., Sheikh, M. S., and Huang, Y. (2007) Mitotic kinase Aurora-A phosphorylates RASSF1A and modulates RASSF1A-mediated microtubule interaction and M-phase cell cycle regulation. Oncogene 26, 7700-7708
39. Thaler, S., Hähnel, P. S., Schad, A., Dammann, R., and Schuler, M. (2009) RASSF1A mediates p21Cip1/Waf1-dependent cell cycle arrest and senescence through modulation of the Raf-MEK-ERK pathway and inhibition of Akt. Cancer Res. 69, 1748-1757
40. Dammann, R., Li, C., Yoon, J. H., Chin, P. L., Bates, S., and Pfeifer, G. P. (2000) Epigenetic inactivation of a RAS association domain family protein from the lung tumour suppressor locus 3p21.3. Nat. Genet. 25, 315-319
41. Liu, L., Vo, A., Liu, G., and McKeehan, W. L. (2005) Putative tumor suppressor RASSF1 interactive protein and cell death inducer C19ORF5 is a DNA binding protein. Biochem. Biophys. Res. Commun. 332, 670-676