Mst1 and Mst2 kinases: Regulations and diseases

Cell and Bioscience

Volumn 3, Issue 1, 2013, Pages

  Qin, Funiu ^a   Tian, Jing ^a   Zhou, Dawang ^a   Chen, Lanfen ^a  

^a XIAMEN UNIVERSITY   (China)

Author keywords

Cancer; Immune diseases; Mst1; Mst2; Reactive oxygen species; The Hippo pathway; YAP

Indexed keywords

MAMMALIA; MURINAE;

EID: 84883108283     PISSN: None     EISSN: 20453701     Source Type: Journal    
DOI: 10.1186/2045-3701-3-31     Document Type: Review

References (79)

1. 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 2003, 114(4):445-456.
2. Harvey KF, Pfleger CM, Hariharan IK. The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 2003, 114(4):457-467.
3. Udan RS, Kango-Singh M, Nolo R, Tao C, Halder G. Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat Cell Biol 2003, 5(10):914-920.
4. Pantalacci S, Tapon N, Leopold P. The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat Cell Biol 2003, 5(10):921-927.
5. Jia J, Zhang W, Wang B, Trinko R, Jiang J. The Drosophila Ste20 family kinase dMST functions as a tumor suppressor by restricting cell proliferation and promoting apoptosis. Genes Dev 2003, 17(20):2514-2519.
6. Justice RW, Zilian O, Woods DF, Noll M, Bryant PJ. The Drosophila tumor suppressor gene warts encodes a homolog of human myotonic dystrophy kinase and is required for the control of cell shape and proliferation. Genes Dev 1995, 9(5):534-546.
7. Xu T, Wang W, Zhang S, Stewart RA, Yu W. Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 1995, 121(4):1053-1063.
8. Lai ZC, Wei X, Shimizu T, Ramos E, Rohrbaugh M, Nikolaidis N, Ho LL, Li Y. Control of cell proliferation and apoptosis by mob as tumor suppressor, mats. Cell 2005, 120(5):675-685.
9. Tapon N, Harvey KF, Bell DW, Wahrer DC, Schiripo TA, Haber DA, Hariharan IK. salvador Promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 2002, 110(4):467-478.
10. Kango-Singh M, Nolo R, Tao C, Verstreken P, Hiesinger PR, Bellen HJ, Halder G. Shar-pei mediates cell proliferation arrest during imaginal disc growth in Drosophila. Development 2002, 129(24):5719-5730.
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 2005, 122(3):421-434.
12. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, Gayyed MF, Anders RA, Maitra A, Pan D. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 2007, 130(6):1120-1133.
13. Creasy CL, Ambrose DM, Chernoff J. The Ste20-like protein kinase, Mst1, dimerizes and contains an inhibitory domain. J Biol Chem 1996, 271(35):21049-21053.
14. Creasy CL, Chernoff J. Cloning and characterization of a member of the MST subfamily of Ste20-like kinases. Gene 1995, 167(1-2):303-306.
15. Chan EH, Nousiainen M, Chalamalasetty RB, Schafer A, Nigg EA, Sillje HH. The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 2005, 24(12):2076-2086.
16. Praskova M, Xia F, Avruch J. MOBKL1A/MOBKL1B phosphorylation by MST1 and MST2 inhibits cell proliferation. Curr Biol 2008, 18(5):311-321.
17. Wei X, Shimizu T, Lai ZC. Mob as tumor suppressor is activated by Hippo kinase for growth inhibition in Drosophila. EMBO J 2007, 26(7):1772-1781.
18. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 2007, 21(21):2747-2761.
19. Sudol M, Shields DC, Farooq A. Structures of YAP protein domains reveal promising targets for development of new cancer drugs. Semin Cell Dev Biol 2012, 23(7):827-833.
20. Avruch J, Zhou D, Fitamant J, Bardeesy N, Mou F, Barrufet LR. Protein kinases of the Hippo pathway: regulation and substrates. Semin Cell Dev Biol 2012, 23(7):770-784.
21. Hong W, Guan KL. The YAP and TAZ transcription co-activators: key downstream effectors of the mammalian Hippo pathway. Semin Cell Dev Biol 2012, 23(7):785-793.
22. Chen L, Qin F, Deng X, Avruch J, Zhou D. Hippo pathway in intestinal homeostasis and tumorigenesis. Protein & cell 2012, 3(4):305-310.
23. Zhao B, Tumaneng K, Guan KL. The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat Cell Biol 2011, 13(8):877-883.
24. Radu M, Chernoff J. The DeMSTification of mammalian Ste20 kinases. Curr Biol 2009, 19(10):R421-R425.
25. Graves JD, Gotoh Y, Draves KE, Ambrose D, Han DK, Wright M, Chernoff J, Clark EA, Krebs EG. Caspase-mediated activation and induction of apoptosis by the mammalian Ste20-like kinase Mst1. EMBO J 1998, 17(8):2224-2234.
26. Chae JS, Gil Hwang S, Lim DS, Choi EJ. Thioredoxin-1 functions as a molecular switch regulating the oxidative stress-induced activation of MST1. Free Radic Biol Med 2012, 53(12):2335-2343.
27. Lehtinen MK, Yuan Z, Boag PR, Yang Y, Villen J, Becker EB, DiBacco S, de la Iglesia N, Gygi S, Blackwell TK, et al. A conserved MST-FOXO signaling pathway mediates oxidative-stress responses and extends life span. Cell 2006, 125(5):987-1001.
28. Yuan Z, Lehtinen MK, Merlo P, Villen J, Gygi S, Bonni A. Regulation of neuronal cell death by MST1-FOXO1 signaling. J Biol Chem 2009, 284(17):11285-11292.
29. Xiao L, Chen D, Hu P, Wu J, Liu W, Zhao Y, Cao M, Fang Y, Bi W, Zheng Z, et al. The c-Abl-MST1 signaling pathway mediates oxidative stress-induced neuronal cell death. J Neurosci Off J Soc Neurosci 2011, 31(26):9611-9619.
30. Liu W, Wu J, Xiao L, Bai Y, Qu A, Zheng Z, Yuan Z. Regulation of neuronal cell death by c-Abl-Hippo/MST2 signaling pathway. PloS one 2012, 7(5):e36562.
31. Sanphui P, Biswas SC. FoxO3a is activated and executes neuron death via Bim in response to beta-amyloid. Cell Death Dis 2013, 4:e625.
32. Lee JK, Shin JH, Hwang SG, Gwag BJ, McKee AC, Lee J, Kowall NW, Ryu H, Lim DS, Choi EJ. MST1 functions as a key modulator of neurodegeneration in a mouse model of ALS. Proc Natl Acad Sci U S A 2013, 110(29):12066-12071.
33. Chung C, Kim T, Kim M, Song H, Kim TS, Seo E, Lee SH, Kim H, Kim SK, Yoo G, et al. Hippo-Foxa2 signaling pathway plays a role in peripheral lung maturation and surfactant homeostasis. Proc Natl Acad Sci U S A 2013, 110(19):7732-7737.
34. Choi J, Oh S, Lee D, Oh HJ, Park JY, Lee SB, Lim DS. Mst1-FoxO signaling protects Naive T lymphocytes from cellular oxidative stress in mice. PloS one 2009, 4(11):e8011.
35. Abdollahpour H, Appaswamy G, Kotlarz D, Diestelhorst J, Beier R, Schaffer AA, Gertz EM, Schambach A, Kreipe HH, Pfeifer D, et al. The phenotype of human STK4 deficiency. Blood 2012, 119(15):3450-3457.
36. Valis K, Prochazka L, Boura E, Chladova J, Obsil T, Rohlena J, Truksa J, Dong LF, Ralph SJ, Neuzil J. Hippo/Mst1 stimulates transcription of the proapoptotic mediator NOXA in a FoxO1-dependent manner. Cancer Res 2011, 71(3):946-954.
37. Ohsawa S, Sato Y, Enomoto M, Nakamura M, Betsumiya A, Igaki T. Mitochondrial defect drives non-autonomous tumour progression through Hippo signalling in Drosophila. Nature 2012, 490(7421):547-551.
38. Matallanas D, Romano D, Al-Mulla F, O'Neill E, Al-Ali W, Crespo P, Doyle B, Nixon C, Sansom O, Drosten M, et al. Mutant K-Ras activation of the proapoptotic MST2 pathway is antagonized by wild-type K-Ras. Mol Cell 2011, 44(6):893-906.
39. Morinaka A, Funato Y, Uesugi K, Miki H. Oligomeric peroxiredoxin-I is an essential intermediate for p53 to activate MST1 kinase and apoptosis. Oncogene 2011, 30(40):4208-4218.
40. Rawat SJ, Creasy CL, Peterson JR, Chernoff J. The tumor suppressor Mst1 promotes changes in the cellular redox state by phosphorylation and inactivation of peroxiredoxin-1 protein. J Biol Chem 2013, 288(12):8762-8771.
41. Wu H, Xiao Y, Zhang S, Ji S, Wei L, Fan F, Geng J, Tian J, Sun X, Qin F, et al. The Ets transcription factor GABP is a component of the hippo pathway essential for growth and antioxidant defense. Cell reports 2013, 3(5):1663-1677.
42. Chinenov Y, Schmidt T, Yang XY, Martin ME. Identification of redox-sensitive cysteines in GA-binding protein-alpha that regulate DNA binding and heterodimerization. J Biol Chem 1998, 273(11):6203-6209.
43. Rosmarin AG, Resendes KK, Yang Z, McMillan JN, Fleming SL. GA-binding protein transcription factor: a review of GABP as an integrator of intracellular signaling and protein-protein interactions. Blood Cells Mol Dis 2004, 32(1):143-154.
44. Circu ML, Aw TY. Intestinal redox biology and oxidative stress. Semin Cell Dev Biol 2012, 23(7):729-737.
45. Zhang H, Forman HJ. Glutathione synthesis and its role in redox signaling. Semin Cell Dev Biol 2012, 23(7):722-728.
46. Zhou D, Conrad C, Xia F, Park JS, Payer B, Yin Y, Lauwers GY, Thasler W, Lee JT, Avruch J, et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 2009, 16(5):425-438.
47. Oh S, Lee D, Kim T, Kim TS, Oh HJ, Hwang CY, Kong YY, Kwon KS, Lim DS. Crucial role for Mst1 and Mst2 kinases in early embryonic development of the mouse. Mol Cell Biol 2009, 29(23):6309-6320.
48. Schlegelmilch K, Mohseni M, Kirak O, Pruszak J, Rodriguez JR, Zhou D, Kreger BT, Vasioukhin V, Avruch J, Brummelkamp TR, et al. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 2011, 144(5):782-795.
49. Lu L, Li Y, Kim SM, Bossuyt W, Liu P, Qiu Q, Wang Y, Halder G, Finegold MJ, Lee JS, et al. Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc Natl Acad Sci U S A 2010, 107(4):1437-1442.
50. Song H, Mak KK, Topol L, Yun K, Hu J, Garrett L, Chen Y, Park O, Chang J, Simpson RM, et al. Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc Natl Acad Sci U S A 2010, 107(4):1431-1436.
51. Lee KP, Lee JH, Kim TS, Kim TH, Park HD, Byun JS, Kim MC, Jeong WI, Calvisi DF, Kim JM, et al. The Hippo-Salvador pathway restrains hepatic oval cell proliferation, liver size, and liver tumorigenesis. Proc Natl Acad Sci U S A 2011, 107(18):8248-8253.
52. Zhou D, Zhang Y, Wu H, Barry E, Yin Y, Lawrence E, Dawson D, Willis JE, Markowitz SD, Camargo FD, et al. Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance. Proc Natl Acad Sci U S A 2011, 108(49):E1312-E1320.
53. Camargo FD, Gokhale S, Johnnidis JB, Fu D, Bell GW, Jaenisch R, Brummelkamp TR. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol 2007, 17(23):2054-2060.
54. Pannequin J, Bonnans C, Delaunay N, Ryan J, Bourgaux JF, Joubert D, Hollande F. The wnt target jagged-1 mediates the activation of notch signaling by progastrin in human colorectal cancer cells. Cancer Res 2009, 69(15):6065-6073.
55. Rodilla V, Villanueva A, Obrador-Hevia A, Robert-Moreno A, Fernandez-Majada V, Grilli A, Lopez-Bigas N, Bellora N, Alba MM, Torres F, et al. Jagged1 is the pathological link between Wnt and Notch pathways in colorectal cancer. Proc Natl Acad Sci U S A 2009, 106(15):6315-6320.
56. Cai J, Zhang N, Zheng Y, de Wilde RF, Maitra A, Pan D. The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program. Genes Dev 2010, 24(21):2383-2388.
57. Rosenbluh J, Nijhawan D, Cox AG, Li X, Neal JT, Schafer EJ, Zack TI, Wang X, Tsherniak A, Schinzel AC, et al. beta-Catenin-driven cancers require a YAP1 transcriptional complex for survival and tumorigenesis. Cell 2012, 151(7):1457-1473.
58. Spence JR, Lauf R, Shroyer NF. Vertebrate intestinal endoderm development. Dev Dyn 2011, 240(3):501-520.
59. Gao T, Zhou D, Yang C, Singh T, Penzo-Mendez A, Maddipati R, Tzatsos A, Bardeesy N, Avruch J, Stanger BZ. Hippo signaling regulates differentiation and maintenance in the exocrine pancreas. Gastroenterology 2013, 144(7):1543-1553. e1541.
60. George NM, Day CE, Boerner BP, Johnson RL, Sarvetnick NE. Hippo signaling regulates pancreas development through inactivation of Yap. Mol Cell Biol 2012, 32(24):5116-5128.
61. Stanger BZ, Hebrok M. Control of cell identity in pancreas development and regeneration. Gastroenterology 2013, 144(6):1170-1179.
62. Yamamoto S, Yang G, Zablocki D, Liu J, Hong C, Kim S-J, Soler S, Odashima M, Thaisz J, Yehia G, et al. Activation of Mst1 causes dilated cardiomyopathy by stimulating apoptosis without compensatory ventricular myocyte hypertrophy. J Clin Invest 2003, 111(10):1463-1474.
63. Yan G, Qin Q, Yi B, Chuprun K, Sun H, Huang S, Sun J. Protein-L-isoaspartate (D-aspartate) O-methyltransferase protects cardiomyocytes against hypoxia induced apoptosis through inhibiting proapoptotic kinase Mst1. Int J Cardiol 2013, S0167-5273(13):00629-00633.
64. Odashima M, Usui S, Takagi H, Hong C, Liu J, Yokota M, Sadoshima J. Inhibition of endogenous Mst1 prevents apoptosis and cardiac dysfunction without affecting cardiac hypertrophy after myocardial infarction. Circ Res 2007, 100(9):1344-1352.
65. Del Re DP, Matsuda T, Zhai P, Gao S, Clark GJ, Van Der Weyden L, Sadoshima J. Proapoptotic Rassf1A/Mst1 signaling in cardiac fibroblasts is protective against pressure overload in mice. J Clin Invest 2010, 120(10):3555-3567.
66. Heallen T, Zhang M, Wang J, Bonilla-Claudio M, Klysik E, Johnson RL, Martin JF. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 2011, 332(6028):458-461.
67. von Gise A, Lin Z, Schlegelmilch K, Honor LB, Pan GM, Buck JN, Ma Q, Ishiwata T, Zhou B, Camargo FD, et al. YAP1, the nuclear target of Hippo signaling, stimulates heart growth through cardiomyocyte proliferation but not hypertrophy. Proc Natl Acad Sci U S A 2012, 109(7):2394-2399.
68. Dong Y, Du X, Ye J, Han M, Xu T, Zhuang Y, Tao W. A cell-intrinsic role for Mst1 in regulating thymocyte egress. J Immunol 2009, 183(6):3865-3872.
69. Mou F, Praskova M, Xia F, van Buren D, Hock H, Avruch J, Zhou D. The Mst1 and Mst2 kinases control activation of rho family GTPases and thymic egress of mature thymocytes. J Exp Med 2012, 209(4):741-759.
70. Katagiri K, Imamura M, Kinashi T. Spatiotemporal regulation of the kinase Mst1 by binding protein RAPL is critical for lymphocyte polarity and adhesion. Nat Immunol 2006, 7(9):919-928.
71. Zhou D, Medoff BD, Chen L, Li L, Zhang XF, Praskova M, Liu M, Landry A, Blumberg RS, Boussiotis VA, et al. The Nore1B/Mst1 complex restrains antigen receptor-induced proliferation of naive T cells. Proc Natl Acad Sci U S A 2008, 105(51):20321-20326.
72. Katagiri K, Ueda Y, Tomiyama T, Yasuda K, Toda Y, Ikehara S, Nakayama KI, Kinashi T. Deficiency of Rap1-binding protein RAPL causes lymphoproliferative disorders through mislocalization of p27kip1. Immunity 2011, 34(1):24-38.
73. Katagiri K, Katakai T, Ebisuno Y, Ueda Y, Okada T, Kinashi T. Mst1 controls lymphocyte trafficking and interstitial motility within lymph nodes. EMBO J 2009, 28(9):1319-1331.
74. Nehme NT, Pachlopnik Schmid J, Debeurme F, Andre-Schmutz I, Lim A, Nitschke P, Rieux-Laucat F, Lutz P, Picard C, Mahlaoui N, et al. MST1 mutations in autosomal recessive primary immunodeficiency characterized by defective naive T cells survival. Blood 2012, 119(15):3458-3468.
75. Crequer A, Picard C, Patin E, D'Amico A, Abhyankar A, Munzer M, Debre M, Zhang SY, de Saint-Basile G, Fischer A, et al. Inherited MST1 deficiency underlies susceptibility to EV-HPV infections. PloS one 2012, 7(8):e44010.
76. Kliche S, Worbs T, Wang X, Degen J, Patzak I, Meineke B, Togni M, Moser M, Reinhold A, Kiefer F, et al. CCR7-mediated LFA-1 functions in T cells are regulated by 2 independent ADAP/SKAP55 modules. Blood 2012, 119(3):777-785.
77. Tybulewicz VL, Henderson RB. Rho family GTPases and their regulators in lymphocytes. Nat Rev Immunol 2009, 9(9):630-644.
78. Faroudi M, Hons M, Zachacz A, Dumont C, Lyck R, Stein JV, Tybulewicz VL. Critical roles for Rac GTPases in T-cell migration to and within lymph nodes. Blood 2010, 116(25):5536-5547.
79. Ueda Y, Katagiri K, Tomiyama T, Yasuda K, Habiro K, Katakai T, Ikehara S, Matsumoto M, Kinashi T. Mst1 regulates integrin-dependent thymocyte trafficking and antigen recognition in the thymus. Nat Commun 2012, 3:1098.