MAP4K family kinases act in parallel to MST1/2 to activate LATS1/2 in the Hippo pathway

Nature Communications

Volumn 6, Issue , 2015, Pages

  Meng, Zhipeng ^a   Moroishi, Toshiro ^a   Mottier Pavie, Violaine ^b   Plouffe, Steven W ^a   Hansen, Carsten G ^a   Hong, Audrey W ^a   Park, Hyun Woo ^a   Mo, Jung Soon ^a   Lu, Wenqi ^a   Lu, Shicong ^a   Flores, Fabian ^a   Yu, Fa Xing ^c   Halder, Georg ^b   Guan, Kun Liang ^a  

^a San Diego   (United States)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LATS1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 4; MST1 PROTEIN; PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; GERMINAL CENTER KINASES; HEMATOPOIETIC PROGENITOR KINASE 1; HIPPO PROTEIN, HUMAN; HPO PROTEIN, DROSOPHILA; LATS1 PROTEIN, HUMAN; LATS2 PROTEIN, HUMAN; MACROPHAGE STIMULATING PROTEIN; MAP4K3 PROTEIN, HUMAN; MAP4K4 PROTEIN, HUMAN; MINK1 PROTEIN, HUMAN; NUCLEAR PROTEIN; ONCOPROTEIN; PROTEIN SERINE THREONINE KINASE; SCATTER FACTOR; SIGNAL PEPTIDE; STK3 PROTEIN, HUMAN; TAZ PROTEIN, HUMAN; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN; YY1AP1 PROTEIN, HUMAN;

CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; HOMEOSTASIS; PROTEIN; TUMOR;

ARTICLE; CELL DENSITY; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONTROLLED STUDY; DEPOLYMERIZATION; DROSOPHILA; GENETIC TRANSCRIPTION; HEK293 CELL LINE; HIPPO PATHWAY; HOMEOSTASIS; HUMAN; HUMAN CELL; IMAGINAL DISC; IN VITRO STUDY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; U2OS CELL LINE; ANIMAL; CARCINOGENESIS; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CARCINOGENESIS; CELL LINE, TUMOR; DROSOPHILA; DROSOPHILA PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; HEK293 CELLS; HEPATOCYTE GROWTH FACTOR; HOMEOSTASIS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84943327329     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9357     Document Type: Article

References (47)

1. Barry, E. R., Camargo, F. D. The Hippo superhighway: signaling crossroads converging on the Hippo/Yap pathway in stem cells and development. Curr. Opin. Cell Biol. 25, 247-253 (2013).
2. Varelas, X. The Hippo pathway effectors TAZ and YAP in development, homeostasis and disease. Development 141, 1614-1626 (2014).
3. Yu, F. X., Meng, Z., Plouffe, S. W., Guan, K. L. Hippo pathway regulation of gastrointestinal tissues. Annu. Rev. Physiol. 77, 201-227 (2014).
4. Moroishi, T., Hansen, C. G., Guan, K. L. The emerging roles of YAP and TAZ in cancer. Nat. Rev. Cancer. 15, 73-79 (2015).
5. Piccolo, S., Dupont, S., Cordenonsi, M. The biology of YAP/TAZ: hippo signaling and beyond. Physiol. Rev. 94, 1287-1312 (2014).
6. Yu, F. X., Guan, K. L. The Hippo pathway: regulators and regulations. Genes Dev. 27, 355-371 (2013).
7. Johnson, R., Halder, G. The two faces of Hippo: targeting the Hippo pathway for regenerative medicine and cancer treatment. Nat. Rev. Drug. Discov. 13, 63-79 (2014).
8. Wu, S., Huang, J., Dong, J., Pan, D. hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 114, 445-456 (2003).
9. Udan, R. S., Kango-Singh, M., Nolo, R., Tao, C., Halder, G. Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat. Cell Biol. 5, 914-920 (2003).
10. Pantalacci, S., Tapon, N., Leopold, P. The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat. Cell Biol. 5, 921-927 (2003).
11. Huang, J., Wu, S., Barrera, J., Matthews, K., Pan, D. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122, 421-434 (2005).
12. Dong, J. et al. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130, 1120-1133 (2007).
13. Pan, D. The hippo signaling pathway in development and cancer. Dev. Cell 19, 491-505 (2010).
14. Harvey, K. F., Pfleger, C. M., Hariharan, I. K. The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114, 457-467 (2003).
15. Zhou, D. et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 16, 425-438 (2009).
16. Camargo, F. D. et al. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr. Biol. 17, 2054-2060 (2007).
17. Harvey, K. F., Zhang, X., Thomas, D. M. The Hippo pathway and human cancer. Nat. Rev. Cancer. 13, 246-257 (2013).
18. Gumbiner, B. M., Kim, N. G. The Hippo-YAP signaling pathway and contact inhibition of growth. J. Cell Sci. 127, 709-717 (2014).
19. Yu, F. X. et al. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150, 780-791 (2012).
20. DeRan, M. et al. Energy stress regulates hippo-YAP signaling involving AMPK-mediated regulation of angiomotin-like 1 protein. Cell Rep. 9, 495-503 (2014).
21. Mo, J. S. et al. Cellular energy stress induces AMPK-mediated regulation of YAP and the Hippo pathway. Nat. Cell Biol. 17, 500-510 (2015).
22. Wang, W. et al. AMPK modulates Hippo pathway activity to regulate energy homeostasis. Nat. Cell Biol. 17, 490-499 (2015).
23. Yu, F. X. et al. Protein kinase A activates the Hippo pathway to modulate cell proliferation and differentiation. Genes Dev. 27, 1223-1232 (2013).
24. Zhao, B. et al. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev. 26, 54-68 (2012).
25. Dupont, S. et al. Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183 (2011).
26. Halder, G., Dupont, S., Piccolo, S. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat. Rev. Mol. Cell Biol. 13, 591-600 (2012).
27. Aragona, M. et al. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154, 1047-1059 (2013).
28. Kim, N. G., Koh, E., Chen, X., Gumbiner, B. M. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc. Natl Acad. Sci. USA 108, 11930-11935 (2011).
29. Cong, L. et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013).
30. Chan, E. H. et al. The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 24, 2076-2086 (2005).
31. Taipale, M. et al. Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition. Cell 150, 987-1001 (2012).
32. Manning, G., Whyte, D. B., Martinez, R., Hunter, T., Sudarsanam, S. The protein kinase complement of the human genome. Science 298, 1912-1934 (2002).
33. Dan, I., Watanabe, N. M., Kusumi, A. The Ste20 group kinases as regulators of MAP kinase cascades. Trends. Cell Biol. 11, 220-230 (2001).
34. Madaule, P. et al. A novel partner for the GTP-bound forms of rho and rac. FEBS Lett. 377, 243-248 (1995).
35. Sultan, M. et al. A global view of gene activity and alternative splicing by deep sequencing of the human transcriptome. Science 321, 956-960 (2008).
36. Yin, F. et al. Spatial organization of Hippo signaling at the plasma membrane mediated by the tumor suppressor Merlin/NF2. Cell 154, 1342-1355 (2013).
37. Boggiano, J. C., Vanderzalm, P. J., Fehon, R. G. Tao-1 phosphorylates Hippo/MST kinases to regulate the Hippo-Salvador-Warts tumor suppressor pathway. Dev. Cell 21, 888-895 (2011).
38. Poon, C. L., Lin, J. I., Zhang, X., Harvey, K. F. The sterile 20-like kinase Tao-1 controls tissue growth by regulating the Salvador-Warts-Hippo pathway. Dev. Cell 21, 896-906 (2011).
39. Hamaratoglu, F. et al. The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat. Cell Biol. 8, 27-36 (2006).
40. Mohseni, M. et al. A genetic screen identifies an LKB1-MARK signalling axis controlling the Hippo-YAP pathway. Nat. Cell Biol. 16, 108-117 (2014).
41. Karpowicz, P., Perez, J., Perrimon, N. The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 137, 4135-4145 (2010).
42. Shaw, R. L. et al. The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 137, 4147-4158 (2010).
43. Ren, F. et al. Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proc. Natl Acad. Sci. USA 107, 21064-21069 (2010).
44. Staley, B. K., Irvine, K. D. Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation. Curr. Biol. 20, 1580-1587 (2010).
45. Poernbacher, I., Baumgartner, R., Marada, S. K., Edwards, K., Stocker, H. Drosophila Pez acts in Hippo signaling to restrict intestinal stem cell proliferation. Curr. Biol. 22, 389-396 (2012).
46. Li, Q. et al. The conserved misshapen-warts-Yorkie pathway acts in enteroblasts to regulate intestinal stem cells in Drosophila. Dev. Cell 31, 291-304 (2014).
47. Ran, F. A. et al. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308 (2013).