The MLK-related Kinase (MRK) is a novel RhoC effector that mediates lysophosphatidic acid (LPA)-stimulated tumor cell invasio

Journal of Biological Chemistry

Volumn 288, Issue 8, 2013, Pages 5364-5373

  Korkina, Olga ^a   Dong, Zhiwan ^b   Marullo, Allison ^c   Warshaw, Gregg ^d   Symons, Marc ^e   Ruggieri, Rosamaria ^e  

^a Celcuity LLC   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d REGENERON PHARMACEUTICALS INC   (United States)

^e FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSOPHOSPHATIDIC ACID; PROTEIN KINASE; SMALL GTPASE; TUMOR CELL INVASION; TUMOR CELLS; TUMOR METASTASIS;

PATHOLOGY; PHOSPHOLIPIDS;

ENZYMES;

LYSOPHOSPHATIDIC ACID; MLK RELATED KINASE; RHO KINASE; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CARCINOGENESIS; CELL INVASION; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME BINDING; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

CELL LINE, TUMOR; CELL MOVEMENT; COLLAGEN; DRUG COMBINATIONS; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; HUMANS; LAMININ; LYSOPHOSPHOLIPIDS; MODELS, BIOLOGICAL; MYOSINS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; OVARIAN NEOPLASMS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTEOGLYCANS; RHO GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 84874308869     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.414060     Document Type: Article

References (73)

1. Sahai, E., and Marshall, C. J. (2002) RHO-GTPases and cancer. Nat. Rev. Cancer 2, 133-142
2. Karlsson, R., Pedersen, E. D., Wang, Z., and Brakebusch, C. (2009) Rho GTPase function in tumorigenesis. Biochim. Biophys. Acta 1796, 91-98
3. Kamai, T., Arai, K., Tsujii, T., Honda, M., and Yoshida, K. (2001) Overexpression of RhoA mRNA is associated with advanced stage in testicular germ cell tumour. BJU. Int. 87, 227-231
4. Suwa, H., Ohshio, G., Imamura, T., Watanabe, G., Arii, S., Imamura, M., Narumiya, S., Hiai, H., and Fukumoto, M. (1998) Overexpression of the rhoC gene correlates with progression of ductal adenocarcinoma of the pancreas. Br. J. Cancer 77, 147-152
5. van Golen, K. L., Davies, S., Wu, Z. F., Wang, Y., Bucana, C. D., Root, H., Chandrasekharappa, S., Strawderman, M., Ethier, S. P., and Merajver, S. D. (1999) A novel putative low-affinity insulin-like growth factor-binding protein, LIBC (lost in inflammatory breast cancer), and RhoC GTPase correlate with the inflammatory breast cancer phenotype. Clin. Cancer Res. 5, 2511-2519
6. Fritz, G., Just, I., and Kaina, B. (1999) Rho GTPases are overexpressed in human tumors. Int. J. Cancer 81, 682-687
7. Fritz, G., Brachetti, C., Bahlmann, F., Schmidt, M., and Kaina, B. (2002) Rho GTPases in human breast tumours: expression and mutation analyses and correlation with clinical parameters. Br. J. Cancer 87, 635-644
8. Horiuchi, A., Imai, T., Wang, C., Ohira, S., Feng, Y., Nikaido, T., and Konishi, I. (2003) Up-regulation of small GTPases, RhoA and RhoC, is associated with tumor progression in ovarian carcinoma. Lab. Invest. 83, 861-870
9. Vega, F. M., and Ridley, A. J. (2008) Rho GTPases in cancer cell biology. FEBS Lett. 582, 2093-2101
10. Clark, E. A., Golub, T. R., Lander, E. S., and Hynes, R. O. (2000) Genomic analysis of metastasis reveals an essential role for RhoC. Nature 406, 532-535
11. Hakem, A., Sanchez-Sweatman, O., You-Ten, A., Duncan, G., Wakeham, A., Khokha, R., and Mak, T. W. (2005) RhoC is dispensable for embryogenesis and tumor initiation but essential for metastasis. Genes Dev. 19, 1974-1979
12. Wang, W., Wu, F., Fang, F., Tao, Y., and Yang, L. (2008) Inhibition of invasion and metastasis of hepatocellular carcinoma cells via targeting RhoC in vitro and in vivo. Clin. Cancer Res. 14, 6804-6812
13. Kondo, T., Sentani, K., Oue, N., Yoshida, K., Nakayama, H., and Yasui, W. (2004) Expression of RHOC is associated with metastasis of gastric carcinomas. Pathobiology 71, 19-25
14. Shikada, Y., Yoshino, I., Okamoto, T., Fukuyama, S., Kameyama, T., and Maehara, Y. (2003) Higher expression of RhoC is related to invasiveness in non-small cell lung carcinoma. Clin. Cancer Res. 9, 5282-5286
15. Kleer, C. G., Griffith, K. A., Sabel, M. S., Gallagher, G., van Golen, K. L., Wu, Z. F., and Merajver, S. D. (2005) RhoC-GTPase is a novel tissue biomarker associated with biologically aggressive carcinomas of the breast. Breast Cancer Res. Treat. 93, 101-110
16. Boone, B., Van Gele, M., Lambert, J., Haspeslagh, M., and Brochez, L. (2009) The role of RhoC in growth and metastatic capacity of melanoma. J. Cutan. Pathol. 36, 629-636
17. Wheeler, A. P., and Ridley, A. J. (2004) Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Exp. Cell Res. 301, 43-49
18. Simpson, K. J., Dugan, A. S., and Mercurio, A. M. (2004) Functional analysis of the contribution of RhoA and RhoC GTPases to invasive breast carcinoma. Cancer Res. 64, 8694-8701
19. Pillé, J. Y., Denoyelle, C., Varet, J., Bertrand, J. R., Soria, J., Opolon, P., Lu, H., Pritchard, L. L., Vannier, J. P., Malvy, C., Soria, C., and Li, H. (2005) Anti-RhoA and anti-RhoC siRNAs inhibit the proliferation and invasiveness of MDA-MB-231 breast cancer cells in vitro and in vivo. Mol. Ther. 11, 267-274
20. Bellovin, D. I., Simpson, K. J., Danilov, T., Maynard, E., Rimm, D. L., Oettgen, P., and Mercurio, A. M. (2006) Reciprocal regulation of RhoA and RhoC characterizes the EMT and identifies RhoC as a prognostic marker of colon carcinoma. Oncogene 25, 6959-6967
21. Hutchison, N., Hendry, B. M., and Sharpe, C. C. (2009) Rho isoforms have distinct and specific functions in the process of epithelial to mesenchymal transition in renal proximal tubular cells. Cell Signal. 21, 1522-1531
22. Dietrich, K. A., Schwarz, R., Liska, M., Grass, S., Menke, A., Meister, M., Kierschke, G., Längle, C., Genze, F., and Giehl, K. (2009) Specific induction of migration and invasion of pancreatic carcinoma cells by RhoC, which differs from RhoA in its localisation and activity. Biol. Chem. 390, 1063-1077
23. Kitzing, T. M., Wang, Y., Pertz, O., Copeland, J. W., and Grosse, R. (2010) Formin-like 2 drives amoeboid invasive cell motility downstream of RhoC. Oncogene 29, 2441-2448
24. Vega, F. M., Fruhwirth, G., Ng, T., and Ridley, A. J. (2011) RhoA and RhoC have distinct roles in migration and invasion by acting through different targets. J. Cell Biol. 193, 655-665
25. Bian, D., Mahanivong, C., Yu, J., Frisch, S. M., Pan, Z. K., Ye, R. D., and Huang, S. (2006) The G12/13-RhoA signaling pathway contributes to efficient lysophosphatidic acid-stimulated cell migration. Oncogene 25, 2234-2244
26. Buhl, A. M., Johnson, N. L., Dhanasekaran, N., and Johnson, G. L. (1995)G alpha 12 and G+13 stimulate Rho-dependent stress fiber formation and focal adhesion assembly. J. Biol. Chem. 270, 24631-24634
27. Hart, M. J., Jiang, X., Kozasa, T., Roscoe, W., Singer, W. D., Gilman, A. G., Sternweis, P. C., and Bollag, G. (1998) Direct stimulation of the guanine nucleotide exchange activity of p115 RhoGEF by G+13. Science 280, 2112-2114
28. Moolenaar, W. H., van Meeteren, L. A., and Giepmans, B. N. (2004) The ins and outs of lysophosphatidic acid signaling. Bioessays 26, 870-881
29. Hama, K., Aoki, J., Fukaya, M., Kishi, Y., Sakai, T., Suzuki, R., Ohta, H., Yamori, T., Watanabe, M., Chun, J., and Arai, H. (2004) Lysophosphatidic acid and autotaxin stimulate cell motility of neoplastic and non-neoplastic cells through LPA1. J. Biol. Chem. 279, 17634-17639
30. Offermanns, S., Mancino, V., Revel, J. P., and Simon, M. I. (1997) Vascular system defects and impaired cell chemokinesis as a result of G+13 deficiency. Science 275, 533-536
31. Parks, S., and Wieschaus, E. (1991) The Drosophila gastrulation gene concertina encodes a G β-like protein. Cell 64, 447-458
32. Radhika, V., Onesime, D., Ha, J. H., and Dhanasekaran, N. (2004) G+13 stimulates cell migration through cortactin-interacting protein Hax-1. J. Biol. Chem. 279, 49406-49413
33. Hill, C. S., Wynne, J., and Treisman, R. (1995) The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 81, 1159-1170
34. Teramoto, H., Crespo, P., Coso, O. A., Igishi, T., Xu, N., and Gutkind, J. S. (1996) The small GTP-binding protein rho activates c-Jun N-terminal kinases/stress-activated protein kinases in human kidney 293T cells. Evidence for a Pak-independent signaling pathway. J. Biol. Chem. 271, 25731-25734
35. Jia, Z., Vadnais, J., Lu, M. L., Noël, J., and Nabi, I. R. (2006) Rho/ROCKdependent pseudopodial protrusion and cellular blebbing are regulated by p38 MAPK in tumour cells exhibiting autocrine c-Met activation. Biol. Cell 98, 337-351
36. Marinissen, M. J., Chiariello, M., and Gutkind, J. S. (2001) Regulation of gene expression by the small GTPase Rho through the ERK6 (p38+) MAP kinase pathway. Genes Dev. 15, 535-553
37. Marinissen, M. J., Chiariello, M., Tanos, T., Bernard, O., Narumiya, S., and Gutkind, J. S. (2004) The small GTP-binding protein RhoA regulates c-jun by a ROCK-JNK signaling axis. Mol. Cell 14, 29-41
38. Gross, E. A., Callow, M. G., Waldbaum, L., Thomas, S., and Ruggieri, R. (2002) MRK, a mixed lineage kinase-related molecule that plays a role in β-radiation-induced cell cycle arrest. J. Biol. Chem. 277, 13873-13882
39. Gotoh, I., Adachi, M., and Nishida, E. (2001) Identification and characterization of a novel MAP kinase kinase kinase, MLTK. J. Biol. Chem. 276, 4276-4286
40. Liu, T. C., Huang, C. J., Chu, Y. C., Wei, C. C., Chou, C. C., Chou, M. Y., Chou, C. K., and Yang, J. J. (2000) Cloning and expression of ZAK, a mixed lineage kinase-like protein containing a leucine-zipper and a sterile-+ motif. Biochem. Biophys. Res. Commun. 274, 811-816
41. Tosti, E., Waldbaum, L., Warshaw, G., Gross, E. A., and Ruggieri, R. (2004) The stress kinase MRK contributes to regulation of DNA damage checkpoints through a p38 β-independent pathway. J. Biol. Chem. 279, 47652-47660
42. Self, A. J., and Hall, A. (1995) Purification of recombinant Rho/Rac/G25K from Escherichia coli. Methods Enzymol. 256, 3-10
43. Valster, A., Tran, N. L., Nakada, M., Berens, M. E., Chan, A. Y., and Symons, M. (2005) Cell migration and invasion assays. Methods 37, 208-215
44. Chuang, Y. Y., Tran, N. L., Rusk, N., Nakada, M., Berens, M. E., and Symons, M. (2004) Role of synaptojanin 2 in glioma cell migration and invasion. Cancer Res. 64, 8271-8275
45. Crabtree, G. R., and Schreiber, S. L. (1996) Three-part inventions: intracellular signaling and induced proximity. Trends Biochem. Sci. 21, 418-422
46. Sahai, E., and Marshall, C. J. (2002) ROCK and Dia have opposing effects on adherens junctions downstream of Rho. Nat. Cell Biol. 4, 408-415
47. Ho, T. T., Merajver, S. D., Lapière, C. M., Nusgens, B. V., and Deroanne, C. F. (2008) RhoA-GDP regulates RhoB protein stability. Potential involvement of RhoGDI+. J. Biol. Chem. 283, 21588-21598
48. Sengupta, S., Wang, Z., Tipps, R., and Xu, Y. (2004) Biology of LPA in health and disease. Semin. Cell Dev. Biol. 15, 503-512
49. Pua, T. L., Wang, F. Q., and Fishman, D. A. (2009) Roles of LPA in ovarian cancer development and progression. Future Oncol. 5, 1659-1673
50. Leung, I. W., and Lassam, N. (1998) Dimerization via tandem leucine zippers is essential for the activation of the mitogen-activated protein kinase kinase kinase, MLK-3. J. Biol. Chem. 273, 32408-32415
51. Vacratsis, P. O., and Gallo, K. A. (2000) Zipper-mediated oligomerization of the mixed lineage kinase SPRK/MLK-3 is not required for its activation by the GTPase cdc 42 but Is necessary for its activation of the JNK pathway. Monomeric SPRK L410P does not catalyze the activating phosphor-ylation of Thr258 of murine MITOGEN-ACTIVATED protein kinase kinase 4. J. Biol. Chem. 275, 27893-27900
52. Chakraborti, S., Mandal, M., Das, S., Mandal, A., and Chakraborti, T. (2003) Regulation of matrix metalloproteinases: an overview. Mol. Cell Biochem. 253, 269-285
53. Reddy, K. B., Nabha, S. M., and Atanaskova, N. (2003) Role of MAP kinase in tumor progression and invasion. Cancer Metastasis Rev. 22, 395-403
54. Huang, C., Jacobson, K., and Schaller, M. D. (2004) MAP kinases and cell migration. J. Cell Sci. 117, 4619-4628
55. del Barco Barrantes, I and Nebreda, A. R. (2012) Roles of p38 MAPKs in invasion and metastasis. Biochem. Soc. Trans. 40, 79-84
56. Katoh, K., Kano, Y., and Noda, Y. (2011) Rho-associated kinase-dependent contraction of stress fibres and the organization of focal adhesions. J.R. Soc. Interface 8, 305-311
57. Minden, A., Lin, A., Claret, F. X., Abo, A., and Karin, M. (1995) Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81, 1147-1157
58. Du, Y., Böck, B. C., Schachter, K. A., Chao, M., and Gallo, K. A. (2005) Cdc42 induces activation loop phosphorylation and membrane targeting of mixed lineage kinase 3. J. Biol. Chem. 280, 42984-42993
59. Ridley, A. J. (2001) Rho family proteins: coordinating cell responses. Trends Cell Biol. 11, 471-477
60. Bravo-Cordero, J. J., Oser, M., Chen, X., Eddy, R., Hodgson, L., and Condeelis, J. (2011) A novel spatiotemporal RhoC activation pathway locally regulates cofilin activity at invadopodia. Curr. Biol. 21, 635-644
61. Pan, C. Q., Sudol, M., Sheetz, M., and Low, B. C. (2012) Modularity and functional plasticity of scaffold proteins as p (l) acemakers in cell signaling. Cell Signal. 24, 2143-2165
62. Riento, K., and Ridley, A. J. (2003) Rocks: multifunctional kinases in cell behaviour. Nat. Rev. Mol. Cell Biol. 4, 446-456
63. Narumiya, S., Tanji, M., and Ishizaki, T. (2009) Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev. 28, 65-76
64. Street, C. A., and Bryan, B. A. (2011) Rho kinase proteins-pleiotropic modulators of cell survival and apoptosis. Anticancer Res. 31, 3645-3657
65. Xia, D., Stull, J. T., and Kamm, K. E. (2005) Myosin phosphatase targeting subunit 1 affects cell migration by regulating myosin phosphorylation and actin assembly. Exp. Cell Res. 304, 506-517
66. Vicente-Manzanares, M., Ma, X., Adelstein, R. S., and Horwitz, A. R. (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 10, 778-790
67. Mills, G. B., and Moolenaar, W. H. (2003) The emerging role of lysophosphatidic acid in cancer. Nat. Rev. Cancer 3, 582-591
68. Stracke, M. L., Krutzsch, H. C., Unsworth, E. J., Arestad, A., Cioce, V., Schiffmann, E., and Liotta, L. A. (1992) Identification, purification, and partial sequence analysis of autotaxin, a novel motility-stimulating protein. J. Biol. Chem. 267, 2524-2529
69. Schmitz, A. A., Govek, E. E., Böttner, B., and Van Aelst, L. (2000) Rho GTPases: signaling, migration, and invasion. Exp. Cell Res. 261, 1-12
70. Faried, A., Faried, L. S., Kimura, H., Nakajima, M., Sohda, M., Miyazaki, T., Kato, H., Usman, N., and Kuwano, H. (2006) RhoA and RhoC proteins promote both cell proliferation and cell invasion of human oesophageal squamous cell carcinoma cell lines in vitro and in vivo. Eur.J. Cancer 42, 1455-1465
71. Fritz, G., and Kaina, B. (2006) Rho GTPases: promising cellular targets for novel anticancer drugs. Curr. Cancer Drug Targets 6, 1-14
72. Islam, M., Lin, G., Brenner, J. C., Pan, Q., Merajver, S. D., Hou, Y., Kumar, P., and Teknos, T. N. (2009) RhoC expression and head and neck cancer metastasis. Mol. Cancer Res. 7, 1771-1780
73. Symons, M. (1995) The Rac and Rho pathways as a source of drug targets for Ras-mediated malignancies. Curr. Opin. Biotechnol. 6, 668-674