Modulating effects of acyl-CoA synthetase 5-derived mitochondrial Wnt2B palmitoylation on intestinal Wnt activity

World Journal of Gastroenterology

Volumn 20, Issue 40, 2014, Pages 14855-14864

  Klaus, Christina ^a   Schneider, Ursula ^a   Hedberg, Christian ^b   Schütz, Anke K ^a   Bernhagen, Jürgen ^a   Waldmann, Herbert ^b   Gassler, Nikolaus ^a   Kaemmerer, Elke ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

Author keywords

Acyl CoA synthetases; Carcinogenesis; Intestinal barrier; Palmitoylation; Wnt signaling

Indexed keywords

APC PROTEIN; BETA CATENIN; COMPLEMENTARY DNA; LONG CHAIN FATTY ACID COENZYME A LIGASE; LONG CHAIN FATTY ACID COENZYME A LIGASE 5; UNCLASSIFIED DRUG; WNT PROTEIN; WNT2 PROTEIN; WNT2B PROTEIN; WNT3A PROTEIN; ACSL5 PROTEIN, HUMAN; GLYCOPROTEIN; PALMOSTATIN B; PROPIOLACTONE; WNT2B PROTEIN, HUMAN; WNT2B PROTEIN, MOUSE;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CACO 2 CELL LINE; CELL DIFFERENTIATION; CELL NUCLEUS; CHEMICAL MODIFICATION; COLON ADENOCARCINOMA; COLON CARCINOGENESIS; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; FATTY ACID METABOLISM; HCT116 CELL LINE; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; INTESTINE MUCOSA; LUCIFERASE ASSAY; MITOCHONDRION; MOLECULAR INTERACTION; NUCLEOTIDE SEQUENCE; PALMITOYLATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY; ACTIVE TRANSPORT; ADENOCARCINOMA; ADENOMA; ANALOGS AND DERIVATIVES; ANIMAL; CELL PROLIFERATION; COLORECTAL TUMOR; DRUG EFFECTS; ENZYMOLOGY; EPITHELIUM CELL; GENETIC TRANSFECTION; GENETICS; HT 29 CELL LINE; LIPOYLATION; METABOLISM; PATHOLOGY; RNA INTERFERENCE; TRANSGENIC MOUSE; TUMOR SUPPRESSOR GENE;

ACTIVE TRANSPORT, CELL NUCLEUS; ADENOCARCINOMA; ADENOMA; ANIMALS; CACO-2 CELLS; CELL PROLIFERATION; COENZYME A LIGASES; COLORECTAL NEOPLASMS; EPITHELIAL CELLS; GENES, APC; GLYCOPROTEINS; HCT116 CELLS; HT29 CELLS; HUMANS; INTESTINAL MUCOSA; LIPOYLATION; MICE, TRANSGENIC; MITOCHONDRIA; PROPIOLACTONE; RNA INTERFERENCE; TRANSFECTION; WNT PROTEINS; WNT SIGNALING PATHWAY; WNT3A PROTEIN;

EID: 84910632984     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i40.14855     Document Type: Article

References (45)

1. Gordon JI, Hooper LV, McNevin MS, Wong M, Bry L. Epithelial cell growth and differentiation. III. Promoting diversity in the intestine: conversations between the microflora, epithelium, and diffuse GALT. Am J Physiol 1997; 273: G565-G570 [PMID: 9316460]
2. Potten CS. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos Trans R Soc Lond B Biol Sci 1998; 353: 821-830 [PMID: 9684279 DOI: 10.1098/rstb.1998.0246]
3. Heath JP. Epithelial cell migration in the intestine. Cell Biol Int 1996; 20: 139-146 [PMID: 8935158 DOI: 10.1006/cbir.1996.0018]
4. Gerbe F, van Es JH, Makrini L, Brulin B, Mellitzer G, Robine S, Romagnolo B, Shroyer NF, Bourgaux JF, Pignodel C, Clevers H, Jay P. Distinct ATOH1 and Neurog3 requirements define tuft cells as a new secretory cell type in the intestinal epithelium. J Cell Biol 2011; 192: 767-780 [PMID: 21383077 DOI: 10.1083/jcb.201010127]
5. Solanas G, Cortina C, Sevillano M, Batlle E. Cleavage of E-cadherin by ADAM10 mediates epithelial cell sorting downstream of EphB signalling. Nat Cell Biol 2011; 13: 1100-1107 [PMID: 21804545 DOI: 10.1038/ncb2298]
6. Gassler N, Roth W, Funke B, Schneider A, Herzog F, Tischendorf JJ, Grund K, Penzel R, Bravo IG, Mariadason J, Ehemann V, Sykora J, Haas TL, Walczak H, Ganten T, Zentgraf H, Erb P, Alonso A, Autschbach F, Schirmacher P, Knüchel R, Kopitz J. Regulation of enterocyte apoptosis by acyl-CoA synthetase 5 splicing. Gastroenterology 2007; 133: 587-598 [PMID: 17681178 DOI: 10.1053/j.gastro.2007.06.005]
7. Mashima T, Sato S, Sugimoto Y, Tsuruo T, Seimiya H. Promotion of glioma cell survival by acyl-CoA synthetase 5 under extracellular acidosis conditions. Oncogene 2009; 28: 9-19 [PMID: 18806831 DOI: 10.1038/onc.2008.355]
8. Lewin TM, Kim JH, Granger DA, Vance JE, Coleman RA. Acyl-CoA synthetase isoforms 1, 4, and 5 are present in different subcellular membranes in rat liver and can be inhibited independently. J Biol Chem 2001; 276: 24674-24679 [PMID: 11319232 DOI: 10.1074/jbc.M102036200]
9. Coleman RA, Lewin TM, Van Horn CG, Gonzalez-Baró MR. Do long-chain acyl-CoA synthetases regulate fatty acid entry into synthetic versus degradative pathways? J Nutr 2002; 132: 2123-2126 [PMID: 12163649]
10. Liu C, Li Y, Semenov M, Han C, Baeg GH, Tan Y, Zhang Z, Lin X, He X. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002; 108: 837-847 [PMID: 11955436 DOI: 10.1016/S0092-8674(02)00685-2]
11. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006; 127: 469-480 [PMID: 17081971 DOI: 10.1016/j.cell.2006.10.018]
12. Wodarz A, Nusse R. Mechanisms of Wnt signaling in development. Annu Rev Cell Dev Biol 1998; 14: 59-88 [PMID: 9891778 DOI: 10.1146/annurev.cellbio.14.1.59]
13. Gordon MD, Nusse R. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 2006; 281: 22429-22433 [PMID: 16793760 DOI: 10.1074/jbc.R600015200]
14. Klaus A, Birchmeier W. Wnt signalling and its impact on development and cancer. Nat Rev Cancer 2008; 8: 387-398 [PMID: 18432252 DOI: 10.1038/nrc2389]
15. Harris TJ, Peifer M. Decisions, decisions: beta-catenin chooses between adhesion and transcription. Trends Cell Biol 2005; 15: 234-237 [PMID: 15866026 DOI: 10.1016/j.tcb.2005.03.002]
16. Moon RT, Kohn AD, De Ferrari GV, Kaykas A. WNT and beta-catenin signalling: diseases and therapies. Nat Rev Genet 2004; 5: 691-701 [PMID: 15372092 DOI: 10.1038/nrg1427]
17. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005; 434: 843-850 [PMID: 15829953 DOI: 10.1038/nature03319]
18. Kuniyasu H. The Roles of Dietary PPARgamma Ligands for Metastasis in Colorectal Cancer. PPAR Res 2008; 2008: 529720 [PMID: 18551182 DOI: 10.1155/2008/529720]
19. Blasband A, Schryver B, Papkoff J. The biochemical properties and transforming potential of human Wnt-2 are similar to Wnt-1. Oncogene 1992; 7: 153-161 [PMID: 1371336]
20. Shimizu H, Julius MA, Giarré M, Zheng Z, Brown AM, Kitajewski J. Transformation by Wnt family proteins correlates with regulation of beta-catenin. Cell Growth Differ 1997; 8: 1349-1358 [PMID: 9419423]
21. Goss AM, Tian Y, Tsukiyama T, Cohen ED, Zhou D, Lu MM, Yamaguchi TP, Morrisey EE. Wnt2/2b and betacatenin signaling are necessary and sufficient to specify lung progenitors in the foregut. Dev Cell 2009; 17: 290-298 [PMID: 19686689 DOI: 10.1016/j.devcel.2009.06.005]
22. Katoh M. Frequent up-regulation of WNT2 in primary gastric cancer and colorectal cancer. Int J Oncol 2001; 19: 1003-1007 [PMID: 11605001]
23. Katoh M, Kirikoshi H, Terasaki H, Shiokawa K. WNT2B2 mRNA, up-regulated in primary gastric cancer, is a positive regulator of the WNT- beta-catenin-TCF signaling pathway. Biochem Biophys Res Commun 2001; 289: 1093-1098 [PMID: 11741304 DOI: 10.1006/bbrc.2001.6076]
24. Poulain M, Ober EA. Interplay between Wnt2 and Wnt2bb controls multiple steps of early foregut-derived organ development. Development 2011; 138: 3557-3568 [PMID: 21771809 DOI: 10.1242/dev.055921]
25. Struewing IT, Toborek A, Mao CD. Mitochondrial and nuclear forms of Wnt13 are generated via alternative promoters, alternative RNA splicing, and alternative translation start sites. J Biol Chem 2006; 281: 7282-7293 [PMID: 16407296 DOI: 10.1074/jbc.M511182200]
26. Bunaciu RP, Tang T, Mao CD. Differential expression of Wnt13 isoforms during leukemic cell differentiation. Oncol Rep 2008; 20: 195-201 [PMID: 18575737]
27. Tang T, Rector K, Barnett CD, Mao CD. Upstream open reading frames regulate the expression of the nuclear Wnt13 isoforms. Biochem Biophys Res Commun 2008; 366: 1081-1088 [PMID: 18155664 DOI: 10.1016/j.bbrc.2007.12.092]
28. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 2000; 1: 31-39 [PMID: 11413487 DOI: 10.1038/35036052]
29. Doubravska L, Krausova M, Gradl D, Vojtechova M, Tumova L, Lukas J, Valenta T, Pospichalova V, Fafilek B, Plachy J, Sebesta O, Korinek V. Fatty acid modification of Wnt1 and Wnt3a at serine is prerequisite for lipidation at cysteine and is essential for Wnt signalling. Cell Signal 2011; 23: 837-848 [PMID: 21244856 DOI: 10.1016/j.cellsig.2011.01.007]
30. Gao X, Arenas-Ramirez N, Scales SJ, Hannoush RN. Membrane targeting of palmitoylated Wnt and Hedgehog revealed by chemical probes. FEBS Lett 2011; 585: 2501-2506 [PMID: 21740904 DOI: 10.1016/j.febslet.2011.06.033]
31. Schotte P, Van Criekinge W, Van de Craen M, Van Loo G, Desmedt M, Grooten J, Cornelissen M, De Ridder L, Vandekerckhove J, Fiers W, Vandenabeele P, Beyaert R. Cathepsin B-mediated activation of the proinflammatory caspase-11. Biochem Biophys Res Commun 1998; 251: 379-387 [PMID: 9790964 DOI: 10.1006/bbrc.1998.9425]
32. Chomczynski P. A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques 1993; 15: 532-54, 532-54, [PMID: 7692896]
33. Reinartz A, Ehling J, Leue A, Liedtke C, Schneider U, Kopitz J, Weiss T, Hellerbrand C, Weiskirchen R, Knüchel R, Gassler N. Lipid-induced up-regulation of human acyl-CoA synthetase 5 promotes hepatocellular apoptosis. Biochim Biophys Acta 2010; 1801: 1025-1035 [PMID: 20470896 DOI: 10.1016/j.bbalip.2010.04.010]
34. Moser AR, Pitot HC, Dove WF. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990; 247: 322-324 [PMID: 2296722 DOI: 10.1126/science.2296722]
35. Sääf AM, Halbleib JM, Chen X, Yuen ST, Leung SY, Nelson WJ, Brown PO. Parallels between global transcriptional programs of polarizing Caco-2 intestinal epithelial cells in vitro and gene expression programs in normal colon and colon cancer. Mol Biol Cell 2007; 18: 4245-4260 [PMID: 17699589 DOI: 10.1091/mbc.E07-04-0309]
36. Gujral TS, MacBeath G. A system-wide investigation of the dynamics of Wnt signaling reveals novel phases of transcriptional regulation. PLoS One 2010; 5: e10024 [PMID: 20383323 DOI: 10.1371/journal.pone.0010024]
37. Shein HM, Enders JF. Transformation induced by simian virus 40 in human renal cell cultures. I. Morphology and growth characteristics. Proc Natl Acad Sci USA 1962; 48: 1164-1172 [PMID: 13911592 DOI: 10.1073/pnas.48.7.1164]
38. Linder ME, Deschenes RJ. Palmitoylation: policing protein stability and traffic. Nat Rev Mol Cell Biol 2007; 8: 74-84 [PMID: 17183362 DOI: 10.1038/nrm2084]
39. Flatmark K, Maelandsmo GM, Martinsen M, Rasmussen H, Fodstad Ø. Twelve colorectal cancer cell lines exhibit highly variable growth and metastatic capacities in an orthotopic model in nude mice. Eur J Cancer 2004; 40: 1593-1598 [PMID: 15196545 DOI: 10.1016/j.ejca.2004.02.023]
40. Mashek DG, Li LO, Coleman RA. Rat long-chain acyl-CoA synthetase mRNA, protein, and activity vary in tissue distribution and in response to diet. J Lipid Res 2006; 47: 2004-2010 [PMID: 16772660 DOI: 10.1194/jlr.M600150-JLR200]
41. Takemaru KI, Moon RT. The transcriptional coactivator CBP interacts with beta-catenin to activate gene expression. J Cell Biol 2000; 149: 249-254 [PMID: 10769018 DOI: 10.1083/jcb.149.2.249]
42. Draper JM, Smith CD. Palmitoyl acyltransferase assays and inhibitors (Review). Mol Membr Biol 2009; 26: 5-13 [PMID: 19152182 DOI: 10.1080/09687680802683839]
43. Wang HW, Fang JS, Kuang X, Miao LY, Wang C, Xia GL, King ML, Zhang J. Activity of long-chain acyl-CoA synthetase is required for maintaining meiotic arrest in Xenopus laevis. Biol Reprod 2012; 87: 74 [PMID: 22786823 DOI: 10.1095/biolreprod.112.100511]
44. Kaemmerer E, Peuscher A, Reinartz A, Liedtke C, Weiskirchen R, Kopitz J, Gassler N. Human intestinal acyl-CoA synthetase 5 is sensitive to the inhibitor triacsin C. World J Gastroenterol 2011; 17: 4883-4889 [PMID: 22171129 DOI: 10.3748/wjg.v17.i44.4883]
45. Galluzzo P, Caiazza F, Moreno S, Marino M. Role of ERbeta palmitoylation in the inhibition of human colon cancer cell proliferation. Endocr Relat Cancer 2007; 14: 153-167 [PMID: 17395984 DOI: 10.1677/ERC-06-0020]