Differential control of Yorkie activity by LKB1/AMPK and the Hippo/Warts cascade in the central nervous system

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 37, 2015, Pages E5169-E5178

  Gailite, Ieva ^a   Aerne, Birgit L ^a   Tapon, Nicolas ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

Author keywords

Development; Growth control; Hippo; Neuroblast; Stem cells

Indexed keywords

GLUCOSE TRANSPORTER 3; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PROTEIN KINASE LKB1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTIONAL COACTIVATOR YORKIE; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; HPO PROTEIN, DROSOPHILA; LKB1 PROTEIN, DROSOPHILA; NUCLEAR PROTEIN; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; TRANSACTIVATOR PROTEIN; YORKIE PROTEIN, DROSOPHILA;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASYMMETRIC CELL DIVISION; BRAIN SIZE; CELL CYCLE REGULATION; CELL DIVISION; CELL POPULATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DROSOPHILA; GENE REPRESSION; HIPPO SIGNALING; LARVAL STAGE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NEUROEPITHELIUM; NONHUMAN; OPTIC LOBE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TISSUE GROWTH; VENTRAL ROOT; ANIMAL; BRAIN; CONFOCAL MICROSCOPY; CYTOLOGY; DROSOPHILA MELANOGASTER; EMBRYOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOTYPE; LARVA; METABOLISM; STEM CELL; TRANSGENIC ANIMAL;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BRAIN; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENOTYPE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LARVA; MICROSCOPY, CONFOCAL; NUCLEAR PROTEINS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; STEM CELLS; TRANS-ACTIVATORS;

EID: 84941662887     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1505512112     Document Type: Article

References (100)

1. Yu FX, Guan KL (2013) The Hippo pathway: Regulators and regulations. Genes Dev 27(4):355-371.
2. Lin JI, Poon CL, Harvey KF (2013) The Hippo size control pathway-ever expanding. Sci Signal 6(259):pe4.
3. Nolo R, Morrison CM, Tao C, Zhang X, Halder G (2006) The bantam microRNA is a target of the hippo tumor-suppressor pathway. Curr Biol 16(19):1895-1904.
4. Thompson BJ, Cohen SM (2006) The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 126(4):767-774.
5. Huang J, Wu S, Barrera J, Matthews K, Pan D (2005) The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122(3):421-434.
6. Tapon N, et al. (2002) salvador Promotes both cell cycle exit and apoptosis in Dro-sophila and is mutated in human cancer cell lines. Cell 110(4):467-478.
7. Neto-Silva RM, de Beco S, Johnston LA (2010) Evidence for a growth-stabilizing regulatory feedback mechanism between Myc and Yorkie, the Drosophila homolog of Yap. Dev Cell 19(4):507-520.
8. Genevet A, Wehr MC, Brain R, Thompson BJ, Tapon N (2010) Kibra is a regulator of the Salvador/Warts/Hippo signaling network. Dev Cell 18(2):300-308.
9. Cho E, et al. (2006) Delineation of a Fat tumor suppressor pathway. Nat Genet 38(10):1142-1150.
10. Hamaratoglu F, et al. (2006) The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat Cell Biol 8(1):27-36.
11. Harvey KF, Zhang X, Thomas DM (2013) The Hippo pathway and human cancer. Nat Rev Cancer 13(4):246-257.
12. Johnson R, Halder G (2014) The two faces of Hippo: Targeting the Hippo pathway for regenerative medicine and cancer treatment. Nat Rev Drug Discov 13(1): 63-79.
13. Lian I, et al. (2010) The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev 24(11):1106-1118.
14. Qin H, et al. (2012) Transcriptional analysis of pluripotency reveals the Hippo pathway as a barrier to reprogramming. Hum Mol Genet 21(9):2054-2067.
15. Camargo FD, et al. (2007) YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol 17(23):2054-2060.
16. Zhang H, Pasolli HA, Fuchs E (2011) Yes-associated protein (YAP) transcriptional coactivator functions in balancing growth and differentiation in skin. Proc Natl Acad Sci USA 108(6):2270-2275.
17. Cao X, Pfaff SL, Gage FH (2008) YAP regulates neural progenitor cell number via the TEA domain transcription factor. Genes Dev 22(23):3320-3334.
18. Chen Q, et al. (2014) A temporal requirement for Hippo signaling in mammary gland differentiation, growth, and tumorigenesis. Genes Dev 28(5):432-437.
19. Cordenonsi M, et al. (2011) The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 147(4):759-772.
20. Yimlamai D, et al. (2014) Hippo pathway activity influences liver cell fate. Cell 157(6): 1324-1338.
21. Mahoney JE, Mori M, Szymaniak AD, Varelas X, Cardoso WV (2014) The hippo pathway effector Yap controls patterning and differentiation of airway epithelial progenitors. Dev Cell 30(2):137-150.
22. Shaw RL, et al. (2010) The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 137(24):4147-4158.
23. Reddy BV, Rauskolb C, Irvine KD (2010) Influence of fat-hippo and notch signaling on the proliferation and differentiation of Drosophila optic neuroepithelia. Development 137(14):2397-2408.
24. Huang J, Kalderon D (2014) Coupling of Hedgehog and Hippo pathways promotes stem cell maintenance by stimulating proliferation. J Cell Biol 205(3):325-338.
25. Karpowicz P, Perez J, Perrimon N (2010) The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 137(24):4135-4145.
26. Staley BK, Irvine KD (2010) Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation. Curr Biol 20(17):1580-1587.
27. Ren F, et al. (2010) Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proc Natl Acad Sci USA 107(49):21064-21069.
28. Harvey KF, Pfleger CM, Hariharan IK (2003) The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114(4):457-467.
29. Jia J, Zhang W, Wang B, Trinko R, Jiang J (2003) The Drosophila Ste20 family kinase dMST functions as a tumor suppressor by restricting cell proliferation and promoting apoptosis. Genes Dev 17(20):2514-2519.
30. Pantalacci S, Tapon N, Léopold P (2003) The Salvador partner Hippo promotes ap-optosis and cell-cycle exit in Drosophila. Nat Cell Biol 5(10):921-927.
31. Udan RS, Kango-Singh M, Nolo R, Tao C, Halder G (2003) Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat Cell Biol 5(10): 914-920.
32. Wu S, Huang J, Dong J, Pan D (2003) hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell 114(4):445-456.
33. Dong J, et al. (2007) Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130(6):1120-1133.
34. Hao Y, Chun A, Cheung K, Rashidi B, Yang X (2008) Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem 283(9):5496-5509.
35. Oka T, Mazack V, Sudol M (2008) Mst2 and Lats kinases regulate apoptotic function of Yes kinase-associated protein (YAP). J Biol Chem 283(41):27534-27546.
36. Zhao B, et al. (2007) Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 21(21): 2747-2761.
37. Zhang J, Smolen GA, Haber DA (2008) Negative regulation of YAP by LATS1 underscores evolutionary conservation of the Drosophila Hippo pathway. Cancer Res 68(8):2789-2794.
38. Oh H, Irvine KD (2008) In vivo regulation of Yorkie phosphorylation and localization. Development 135(6):1081-1088.
39. Oh H, Irvine KD (2009) In vivo analysis of Yorkie phosphorylation sites. Oncogene 28(17):1916-1927.
40. Piccolo S, Dupont S, Cordenonsi M (2014) The biology of YAP/TAZ: Hippo signaling and beyond. Physiol Rev 94(4):1287-1312.
41. Shackelford DB, Shaw RJ (2009) The LKB1-AMPK pathway: Metabolism and growth control in tumour suppression. Nat Rev Cancer 9(8):563-575.
42. Hemminki A, et al. (1998) A serine/threonine kinase gene defective in Peutz-Jeghers syndrome. Nature 391(6663):184-187.
43. Jenne DE, et al. (1998) Peutz-Jeghers syndrome is caused by mutations in a novel serine threonine kinase. Nat Genet 18(1):38-43.
44. Hezel AF, Bardeesy N (2008) LKB1; linking cell structure and tumor suppression. Oncogene 27(55):6908-6919.
45. Ji H, et al. (2007) LKB1 modulates lung cancer differentiation and metastasis. Nature 448(7155):807-810.
46. Wingo SN, et al. (2009) Somatic LKB1 mutations promote cervical cancer progression. PLoS One 4(4):e5137.
47. Sanchez-Cespedes M, et al. (2002) Inactivation of LKB1/STK11 is a common event in adenocarcinomas of the lung. Cancer Res 62(13):3659-3662.
48. Calles A, et al. (2015) Immunohistochemical loss of LKB1 is a biomarker for more aggressive biology in KRAS-mutant lung adenocarcinoma. Clin Cancer Res 21(12): 2851-2860.
49. Lizcano JM, et al. (2004) LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J 23(4):833-843.
50. Woods A, et al. (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13(22):2004-2008.
51. Shaw RJ, et al. (2004) The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci USA 101(10):3329-3335.
52. Yuan HX, Xiong Y, Guan KL (2013) Nutrient sensing, metabolism, and cell growth control. Mol Cell 49(3):379-387.
53. Mohseni M, et al. (2014) A genetic screen identifies an LKB1-MARK signalling axis controlling the Hippo-YAP pathway. Nat Cell Biol 16(1):108-117.
54. Nguyen HB, Babcock JT, Wells CD, Quilliam LA (2013) LKB1 tumor suppressor regulates AMP kinase/mTOR-independent cell growth and proliferation via the phos-phorylation of Yap. Oncogene 32(35):4100-4109.
55. DeRan M, et al. (2014) Energy stress regulates hippo-YAP signaling involving AMPK-mediated regulation of angiomotin-like 1 protein. Cell Reports 9(2): 495-503.
56. Mo JS, et al. (2015) Cellular energy stress induces AMPK-mediated regulation of YAP and the Hippo pathway. Nat Cell Biol 17(4):500-510.
57. Wang W, et al. (2015) AMPK modulates Hippo pathway activity to regulate energy homeostasis. Nat Cell Biol 17(4):490-499.
58. Homem CC, Knoblich JA (2012) Drosophila neuroblasts: A model for stem cell biology. Development 139(23):4297-4310.
59. Sousa-Nunes R, Cheng LY, Gould AP (2010) Regulating neural proliferation in the Drosophila CNS. Curr Opin Neurobiol 20(1):50-57.
60. Urbach R, Schnabel R, Technau GM (2003) The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development 130(16):3589-3606.
61. Younossi-Hartenstein A, Nassif C, Green P, Hartenstein V (1996) Early neurogenesis of the Drosophila brain. J Comp Neurol 370(3):313-329.
62. Egger B, Boone JQ, Stevens NR, Brand AH, Doe CQ (2007) Regulation of spindle orientation and neural stem cell fate in the Drosophila optic lobe. Neural Dev 2:1.
63. Yasugi T, Umetsu D, Murakami S, Sato M, Tabata T (2008) Drosophila optic lobe neuroblasts triggered by a wave of proneural gene expression that is negatively regulated by JAK/STAT. Development 135(8):1471-1480.
64. Green P, Hartenstein AY, Hartenstein V (1993) The embryonic development of the Drosophila visual system. Cell Tissue Res 273(3):583-598.
65. Lee JH, et al. (2006) JNK pathway mediates apoptotic cell death induced by tumor suppressor LKB1 in Drosophila. Cell Death Differ 13(7):1110-1122.
66. Bonaccorsi S, et al. (2007) The Drosophila Lkb1 kinase is required for spindle formation and asymmetric neuroblast division. Development 134(11):2183-2193.
67. Bowman SK, et al. (2008) The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev Cell 14(4):535-546.
68. Lee CY, et al. (2006) Drosophila Aurora-A kinase inhibits neuroblast self-renewal by regulating aPKC/Numb cortical polarity and spindle orientation. Genes Dev 20(24): 3464-3474.
69. Lee CY, Robinson KJ, Doe CQ (2006) Lgl, Pins and aPKC regulate neuroblast self-renewal versus differentiation. Nature 439(7076):594-598.
70. Lee CY, Wilkinson BD, Siegrist SE, Wharton RP, Doe CQ (2006) Brat is a Miranda cargo protein that promotes neuronal differentiation and inhibits neuroblast self-renewal. Dev Cell 10(4):441-449.
71. Bello B, Reichert H, Hirth F (2006) The brain tumor gene negatively regulates neural progenitor cell proliferation in the larval central brain of Drosophila. Development 133(14):2639-2648.
72. Wang H, et al. (2006) Aurora-A acts as a tumor suppressor and regulates self-renewal of Drosophila neuroblasts. Genes Dev 20(24):3453-3463.
73. Richter C, Oktaba K, Steinmann J, Müller J, Knoblich JA (2011) The tumour suppressor L(3)mbt inhibits neuroepithelial proliferation and acts on insulator elements. Nat Cell Biol 13(9):1029-1039.
74. Martin SG, St Johnston D (2003) A role for Drosophila LKB1 in anterior-posterior axis formation and epithelial polarity. Nature 421(6921):379-384.
75. Goulev Y, et al. (2008) SCALLOPED interacts with YORKIE, the nuclear effector of the hippo tumor-suppressor pathway in Drosophila. Curr Biol 18(6):435-441.
76. Nicolay BN, Frolov MV (2008) Context-dependent requirement for dE2F during on-cogenic proliferation. PLoS Genet 4(10):e1000205.
77. Neumüller RA, et al. (2011) Genome-wide analysis of self-renewal in Drosophila neural stem cells by transgenic RNAi. Cell Stem Cell 8(5):580-593.
78. Zhu S, Barshow S, Wildonger J, Jan LY, Jan YN (2011) Ets transcription factor Pointed promotes the generation of intermediate neural progenitors in Drosophila larval brains. Proc Natl Acad Sci USA 108(51):20615-20620.
79. Varelas X (2014) The Hippo pathway effectors TAZ and YAP in development, ho-meostasis and disease. Development 141(8):1614-1626.
80. Carney TD, et al. (2012) Functional genomics identifies neural stem cell sub-type expression profiles and genes regulating neuroblast homeostasis. Dev Biol 361(1): 137-146.
81. Gold KS, Brand AH (2014) Optix defines a neuroepithelial compartment in the optic lobe of the Drosophila brain. Neural Dev 9:18.
82. Badouel C, et al. (2009) The FERM-domain protein Expanded regulates Hippo pathway activity via direct interactions with the transcriptional activator Yorkie. Dev Cell 16(3):411-420.
83. Oh H, Reddy BV, Irvine KD (2009) Phosphorylation-independent repression of Yorkie in Fat-Hippo signaling. Dev Biol 335(1):188-197.
84. Berger C, et al. (2012) FACS purification and transcriptome analysis of drosophila neural stem cells reveals a role for Klumpfuss in self-renewal. Cell Reports 2(2): 407-418.
85. Andersen RO, Turnbull DW, Johnson EA, Doe CQ (2012) Sgt1 acts via an LKB1/AMPK pathway to establish cortical polarity in larval neuroblasts. Dev Biol 363(1): 258-265.
86. Mihaylova MM, Shaw RJ (2011) The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 13(9):1016-1023.
87. Hardie DG, Ross FA, Hawley SA (2012) AMPK: A nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13(4):251-262.
88. Cheng LY, et al. (2011) Anaplastic lymphoma kinase spares organ growth during nutrient restriction in Drosophila. Cell 146(3):435-447.
89. Gumbiner BM, Kim NG (2014) The Hippo-YAP signaling pathway and contact inhibition of growth. J Cell Sci 127(Pt 4):709-717.
90. Gordon GM, Zhang T, Zhao J, Du W (2013) Deregulated G1-S control and energy stress contribute to the synthetic-lethal interactions between inactivation of RB and TSC1 or TSC2. J Cell Sci 126(Pt 9):2004-2013.
91. Lee JH, et al. (2007) Energy-dependent regulation of cell structure by AMP-activated protein kinase. Nature 447(7147):1017-1020.
92. Amin N, et al. (2009) LKB1 regulates polarity remodeling and adherens junction formation in the Drosophila eye. Proc Natl Acad Sci USA 106(22):8941-8946.
93. Baas AF, et al. (2004) Complete polarization of single intestinal epithelial cells upon activation of LKB1 by STRAD. Cell 116(3):457-466.
94. Wang JW, Imai Y, Lu B (2007) Activation of PAR-1 kinase and stimulation of tau phosphorylation by diverse signals require the tumor suppressor protein LKB1. J Neurosci 27(3):574-581.
95. Shulman JM, Benton R, St Johnston D (2000) The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskeleton and directs oskar mRNA localization to the posterior pole. Cell 101(4):377-388.
96. Maitra S, Kulikauskas RM, Gavilan H, Fehon RG (2006) The tumor suppressors Merlin and Expanded function cooperatively to modulate receptor endocytosis and signaling. Curr Biol 16(7):702-709.
97. Xu T, Wang W, Zhang S, Stewart RA, Yu W (1995) Identifying tumor suppressors in genetic mosaics: The Drosophila lats gene encodes a putative protein kinase. Development 121(4):1053-1063.
98. Wehr MC, et al. (2013) Salt-inducible kinases regulate growth through the Hippo signalling pathway in Drosophila. Nat Cell Biol 15(1):61-71.
99. Bischof J, Maeda RK, Hediger M, Karch F, Basler K (2007) An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci USA 104(9):3312-3317.
100. Venken KJ, He Y, Hoskins RA, Bellen HJ (2006) P[acman]: A BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314(5806):1747-1751.