The kinase domain of Drosophila Tribbles is required for turnover of fly C/EBP during cellmigration

Developmental Biology

Volumn 375, Issue 1, 2013, Pages 33-44

  Masoner, Venessa ^a   Das, Rahul ^a   Pence, Laramie ^a   Anand, Gaurav ^a   LaFerriere, Holly ^b,c   Zars, Troy ^b   Bouyain, Samuel ^a   Dobens, Leonard L ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

^c Culver Stockton College   (United States)

Author keywords

Drosophila oogenesis; Trib protein family

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; NUCLEAR PROTEIN; TRIBBLE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; GENE EXPRESSION; GENE REPRESSION; NEGATIVE FEEDBACK; NONHUMAN; NULL ALLELE; OVARY FOLLICLE CELL; POINT MUTATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; TRANSGENE; TRBL GENE; UPREGULATION;

MAMMALIA;

EID: 84873523703     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.12.016     Document Type: Article

References (50)

1. Abdelilah-Seyfried S., Chan Y.M., Zeng C., Justice N.J., Younger-Shepherd S., Sharp L.E., Barbel S., Meadows S.A., Jan L.Y., Jan Y.N. A gain-of-function screen for genes that affect the development of the Drosophila adult external sensory organ. Genetics 2000, 155:733-752.
2. Angyal A., Kiss-Toth E. The tribbles gene family and lipoprotein metabolism. Curr. Opin. Lipidol. 2012, 23:122-126.
3. Batlle E., Sancho E., Franci C., Dominguez D., Monfar M., Baulida J., Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2000, 2:84-89.
4. Bischof J., Basler K. Recombinases and their use in gene activation, gene inactivation, and transgenesis. Methods Mol. Biol. 2008, 420:175-195.
5. Cano A., Perez-Moreno M.A., Rodrigo I., Locascio A., Blanco M.J., del Barrio M.G., Portillo F., Nieto M.A. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2000, 2:76-83.
6. Chan M.C., Nguyen P.H., Davis B.N., Ohoka N., Hayashi H., Du K., Lagna G., Hata A. A novel regulatory mechanism of the bone morphogenetic protein (BMP) signaling pathway involving the carboxyl-terminal tail domain of BMP type II receptor. Mol. Cell Biol. 2007, 27:5776-5789.
7. Dobens L.L.J., Bouyain S. Developmental roles of tribbles protein family members. Dev. Dyn. 2012, 241:1239-1248.
8. Dobens L., Petersen J., Treisman J., Raftery L. Drosophila bunched integrates opposing DPP and EGF signals to set the operculum boundary. Development 2000, 127:745-754.
9. Eder K., Guan H., Sung H.Y., Francis S.E., Crossman D.C., Kiss-Toth E. LDL uptake by monocytes in response to inflammation is MAPK dependent but independent of tribbles protein expression. Immunol. Lett. 2008, 116:178-183.
10. Fichelson P., Gho M. Mother-daughter precursor cell fate transformation after Cdc2 down-regulation in the Drosophila bristle lineage. Dev. Biol. 2004, 276:367-377.
11. Grosshans J., Wieschaus E. A genetic link between morphogenesis and cell division during formation of the ventral furrow in Drosophila. Cell 2000, 101:523-531.
12. Hegedus Z., Czibula A., Kiss-Toth E. Tribbles: novel regulators of cell function; evolutionary aspects. Cell. Mol. Life Sci. 2006, 63:1632-1641.
13. Hegedus Z., Czibula A., Kiss-Toth E. Tribbles: a family of kinase-like proteins with potent signalling regulatory function. Cell. Signal. 2007, 19:238-250.
14. Herranz N., Pasini D., Diaz V.M., Franci C., Gutierrez A., Dave N., Escriva M., Hernandez-Munoz I., Di Croce L., Helin K., Garcia de Herreros A., Peiro S. Polycomb complex 2is required for E-cadherin repression by the Snail1 transcription factor. Mol. Cell. Biol. 2008, 28:4772-4781.
15. Hua F., Mu R., Liu J., Xue J., Wang Z., Lin H., Yang H., Chen X., Hu Z. TRB3 interacts with SMAD3 promoting tumor cell migration and invasion. J. Cell Sci. 2011, 124:3235-3246.
16. Kato S., Du K. TRB3 modulates C2C12 differentiation by interfering with Akt activation. Biochem. Biophys. Res. Commun. 2007, 353:933-938.
17. Keeshan K., Bailis W., Dedhia P.H., Vega M.E., Shestova O., Xu L., Toscano K., Uljon S.N., Blacklow S.C., Pear W.S. Transformation by Tribbles homolog 2 (Trib2) requires both the Trib2 kinase domain and COP1 binding. Blood 2010, 116:4948-4957.
18. Keeshan K., He Y., Wouters B.J., Shestova O., Xu L., Sai H., Rodriguez C.G., Maillard I., Tobias J.W., Valk P., Carroll M., Aster J.C., Delwel R., Pear W.S. Tribbles homolog 2inactivates C/EBPalpha and causes acute myelogenous leukemia. Cancer Cell 2006, 10:401-411.
19. Keeshan K., Shestova O., Ussin L., Pear W.S. Tribbles homolog 2 (Trib2) and HoxA9 cooperate to accelerate acute myelogenous leukemia. Blood Cells Mol. Dis. 2008, 40:119-121.
20. Kiss-Toth E. Tribbles: 'puzzling' regulators of cell signalling. Biochem. Soc. Trans. 2011, 39:684-687.
21. Kiss-Toth E., Wyllie D.H., Holland K., Marsden L., Jozsa V., Oxley K.M., Polgar T., Qwarnstrom E.E., Dower S.K. Functional mapping and identification of novel regulators for the Toll/Interleukin-1 signalling network by transcription expression cloning. Cell. Signal. 2006, 18:202-214.
22. Levine B., Hackney J.F., Bergen A., Dobens L.r., Truesdale A., Dobens L. Opposing interactions between Drosophila cut and the C/EBP encoded by slow border cells direct apical constriction and epithelial invagination. Dev. Biol. 2010, 344:196-209.
23. Liew C.W., Bochenski J., Kawamori D., Hu J., Leech C.A., Wanic K., Malecki M., Warram J.H., Qi L., Krolewski A.S., Kulkarni R.N. The pseudokinase tribbles homolog 3interacts with ATF4 to negatively regulate insulin exocytosis in human and mouse beta cells. J. Clin. Invest. 2010, 120:2876-2888.
24. Lin K.R., Lee S.F., Hung C.M., Li C.L., Yang-Yen H.F., Yen J.J. Survival factor withdrawal-induced apoptosis of TF-1 cells involves a TRB2-Mcl-1 axis-dependent pathway. J. Biol. Chem. 2007, 282:21962-21972.
25. Mata J., Curado S., Ephrussi A., Rorth P. Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell 2000, 101:511-522.
26. Mathieu J., Sung H.H., Pugieux C., Soetaert J., Rorth P. A sensitized PiggyBac-based screen for regulators of border cell migration in Drosophila. Genetics 2007, 176:1579-1590.
27. McQuilton P., Pierre S.E.S. FlyBase 101-the basics of navigating FlyBase. Nucleic Acids Res. 2012.
28. Montell D.J., Rorth P., Spradling A.C. Slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes Drosophila C/EBP. Cell 1992, 71:51-62.
29. Naiki T., Saijou E., Miyaoka Y., Sekine K., Miyajima A. TRB2, a mouse Tribbles ortholog, suppresses adipocyte differentiation by inhibiting AKT and C/EBPbeta. J. Biol. Chem. 2007, 282:24075-24082.
30. Norga K.K., Gurganus M.C., Dilda C.L., Yamamoto A., Lyman R.F., Patel P.H., Rubin G.M., Hoskins R.A., Mackay T.F., Bellen H.J. Quantitative analysis of bristle number in Drosophila mutants identifies genes involved in neural development. Curr. Biol. 2003, 13:1388-1396.
31. Ohoka N., Yoshii S., Hattori T., Onozaki K., Hayashi H. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 2005, 24:1243-1255.
32. Parrini M.C., Lei M., Harrison S.C., Mayer B.J. Pak1 kinase homodimers are autoinhibited in trans and dissociated upon activation by Cdc42 and Rac1. Mol. Cell 2002, 9:73-83.
33. Pignoni F., Zipursky S.L. Induction of Drosophila eye development by Decapentaplegic. Development 1997, 124:271-278.
34. Prudente S., Sesti G., Pandolfi A., Andreozzi F., Consoli A., Trischitta V. The Mammalian Tribbles Homolog TRIB3, Glucose Homeostasis, and Cardiovascular Diseases. Endocr. Rev. 2012.
35. Qi L., Heredia J.E., Altarejos J.Y., Screaton R., Goebel N., Niessen S., Macleod I.X., Liew C.W., Kulkarni R.N., Bain J., Newgard C., Nelson M., Evans R.M., Yates J., Montminy M. TRB3 links the E3 ubiquitin ligase COP1 to lipid metabolism. Science 2006, 312:1763-1766.
36. Remenyi A., Good M.C., Lim W.A. Docking interactions in protein kinase and phosphatase networks. Curr. Opin. Struct. Biol. 2006, 16:676-685.
37. Rorth P., Szabo K., Texido G. The level of C/EBP protein is critical for cell migration during Drosophila oogenesis and is tightly controlled by regulated degradation. Mol. Cell 2000, 6:23-30.
38. Saka Y., Smith J.C. A Xenopus tribbles orthologue is required for the progression of mitosis and for development of the nervous system. Dev. Biol. 2004, 273:210-225.
39. Sathyanarayana P., Dev A., Fang J., Houde E., Bogacheva O., Bogachev O., Menon M., Browne S., Pradeep A., Emerson C., Wojchowski D.M. EPO receptor circuits for primary erythroblast survival. Blood 2008, 111:5390-5399.
40. Schulz C., Kiger A.A., Tazuke S.I., Yamashita Y.M., Pantalena-Filho L.C., Jones D.L., Wood C.G., Fuller M.T. A misexpression screen reveals effects of bag-of-marbles and TGF beta class signaling on the Drosophila male germ-line stem cell lineage. Genetics 2004, 167:707-723.
41. Seher T.C., Leptin M. Tribbles, a cell-cycle brake that coordinates proliferation and morphogenesis during Drosophila gastrulation. Curr. Biol. 2000, 10:623-629.
42. Selim E., Frkanec J.T., Cunard R. Fibrates upregulate TRB3 in lymphocytes independent of PPAR alpha by augmenting CCAAT/enhancer-binding protein beta (C/EBP beta) expression. Mol. Immunol. 2007, 44:1218-1229.
43. Sung H.Y., Guan H., Czibula A., King A.R., Eder K., Heath E., Suvarna S.K., Dower S.K., Wilson A.G., Francis S.E., Crossman D.C., Kiss-Toth E. Human tribbles-1 controls proliferation and chemotaxis of smooth muscle cells via MAPK signaling pathways. J. Biol. Chem. 2007, 282:18379-18387.
44. Szafranski P., Goode S. A Fasciclin 2morphogenetic switch organizes epithelial cell cluster polarity and motility. Development 2004, 131:2023-2036.
45. Takahashi Y., Ohoka N., Hayashi H., Sato R. TRB3 suppresses adipocyte differentiation by negatively regulating PPARgamma transcriptional activity. J. Lipid Res. 2008, 49:880-892.
46. Thibault S.T., Singer M.A., Miyazaki W.Y., Milash B., Dompe N.A., Singh C.M., Buchholz R., Demsky M., Fawcett R., Francis-Lang H.L., Ryner L., Cheung L.M., Chong A., Erickson C., Fisher W.W., Greer K., Hartouni S.R., Howie E., Jakkula L., Joo D., Killpack K., Laufer A., Mazzotta J., Smith R.D., Stevens L.M., Stuber C., Tan L.R., Ventura R., Woo A., Zakrajsek I., Zhao L., Chen F., Swimmer C., Kopczynski C., Duyk G., Winberg M.L., Margolis J. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac.[see comment]. Nat. Genet. 2004, 36:283-287.
47. Wang S.P., Wang W.L., Chang Y.L., Wu C.T., Chao Y.C., Kao S.H., Yuan A., Lin C.W., Yang S.C., Chan W.K., Li K.C., Hong T.M., Yang P.C. p53 controls cancer cell invasion by inducing the MDM2-mediated degradation of Slug. Nat. Cell Biol. 2009, 11:694-704.
48. Xu T., Rubin G.M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 1993, 117:1223-1237.
49. Yamamoto M., Uematsu S., Okamoto T., Matsuura Y., Sato S., Kumar H., Satoh T., Saitoh T., Takeda K., Ishii K.J., Takeuchi O., Kawai T., Akira S. Enhanced TLR-mediated NF-IL6 dependent gene expression by Trib1 deficiency. J. Exp. Med. 2007, 204:2233-2239.
50. Yokoyama T., Nakamura T. Tribbles in disease: signaling pathways important for cellular function and neoplastic transformation. Cancer Sci. 2011, 102:1115-1122.