Axin1 prevents salmonella invasiveness and inflammatory response in intestinal epithelial cells

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Zhang, Yong Guo ^a   Wu, Shaoping ^a   Xia, Yinglin ^b   Chen, Di ^a   Petrof, Elaine O ^c   Claud, Erika C ^d   Hsu, Wei ^e   Sun, Jun ^a,e  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

^c QUEEN S UNIVERSITY   (Canada)

^d UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

^e UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN; AXIN1; AXIN2; BACTERIAL PROTEIN; PROTEIN DIX; SERINE; UNCLASSIFIED DRUG; WNT PROTEIN; AXIN1 PROTEIN, MOUSE; AXIN2 PROTEIN, MOUSE; BETA CATENIN;

ARTICLE; BACTERIAL COLONIZATION; CONTROLLED STUDY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; INFLAMMATION; INTESTINE EPITHELIUM CELL; MICROBIAL ACTIVITY; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; SALMONELLA; SALMONELLOSIS; SUMOYLATION; TRANSCRIPTION REGULATION; UBIQUITINATION; ANIMAL; C57BL MOUSE; CELL STRAIN CACO 2; CELL STRAIN HCT116; CELL STRAIN HT29; DISEASE MODEL; EPITHELIUM CELL; GENE EXPRESSION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MOUSE; PATHOGENICITY; WNT SIGNALING PATHWAY;

BACTERIA (MICROORGANISMS); SALMONELLA;

ANIMALS; AXIN PROTEIN; BETA CATENIN; CACO-2 CELLS; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; GENE EXPRESSION; HCT116 CELLS; HOST-PATHOGEN INTERACTIONS; HT29 CELLS; HUMANS; IMMUNITY, INNATE; INFLAMMATION; MICE; MICE, INBRED C57BL; SALMONELLA; SALMONELLA INFECTIONS; UBIQUITINATION; WNT SIGNALING PATHWAY;

EID: 84859612128     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034942     Document Type: Article

References (45)

1. Zeng L, Fagotto F, Zhang T, Hsu W, Vasicek TJ, et al. (1997) The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation. Cell 90: 181-192.
2. Yu HM, Jerchow B, Sheu TJ, Liu B, Costantini F, et al. (2005) The role of Axin2 in calvarial morphogenesis and craniosynostosis. Development 132: 1995-2005.
3. Logan CY, Nusse R, (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810.
4. Clevers H, (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480.
5. Kishida S, Yamamoto H, Ikeda S, Kishida M, Sakamoto I, et al. (1998) Axin, a negative regulator of the wnt signaling pathway, directly interacts with adenomatous polyposis coli and regulates the stabilization of beta-catenin. J Biol Chem 273: 10823-10826.
6. Itoh K, Krupnik VE, Sokol SY, (1998) Axis determination in Xenopus involves biochemical interactions of axin, glycogen synthase kinase 3 and beta-catenin. Curr Biol 8: 591-594.
7. Ikeda S, Kishida S, Yamamoto H, Murai H, Koyama S, et al. (1998) Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin. EMBO J 17: 1371-1384.
8. Hsu W, Zeng L, Costantini F, (1999) Identification of a domain of Axin that binds to the serine/threonine protein phosphatase 2A and a self-binding domain. J Biol Chem 274: 3439-3445.
9. Yu HM, Liu B, Costantini F, Hsu W, (2007) Impaired neural development caused by inducible expression of Axin in transgenic mice. Mech Dev 124: 146-156.
10. Hsu W, Shakya R, Costantini F, (2001) Impaired mammary gland and lymphoid development caused by inducible expression of Axin in transgenic mice. J Cell Biol 155: 1055-1064.
11. Julius MA, Schelbert B, Hsu W, Fitzpatrick E, Jho E, et al. (2000) Domains of axin and disheveled required for interaction and function in wnt signaling. Biochem Biophys Res Commun 276: 1162-1169.
12. Li Q, Lin S, Wang X, Lian G, Lu Z, et al. (2009) Axin determines cell fate by controlling the p53 activation threshold after DNA damage. Nat Cell Biol 11: 1128-1134.
13. Luo W, Ng WW, Jin LH, Ye Z, Han J, et al. (2003) Axin utilizes distinct regions for competitive MEKK1 and MEKK4 binding and JNK activation. J Biol Chem 278: 37451-37458.
14. Patel JC, Rossanese OW, Galan JE, (2005) The functional interface between Salmonella and its host cell: opportunities for therapeutic intervention. Trends Pharmacol Sci 26: 564-570.
15. Du F, Galan JE, (2009) Selective inhibition of type III secretion activated signaling by the Salmonella effector AvrA. PLoS Pathog 5: e1000595.
16. Liu X, Wu S, Xia Y, Li XE, Zhou ZD, et al. (2011) Wingless homolog Wnt11 suppresses bacterial invasion and inflammation in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol.
17. Liu X, Lu R, Wu S, Zhang YG, Xia Y, et al. (2011) Wnt2 inhibits enteric bacterial-induced inflammation in intestinal epithelial cells. Inflamm Bowel Dis.
18. Liu X, Lu R, Wu S, Sun J, (2010) Salmonella regulation of intestinal stem cells through the Wnt/beta-catenin pathway. FEBS Lett 584: 911-916.
19. Ye Z, Petrof EO, Boone D, Claud EC, Sun J, (2007) Salmonella effector AvrA regulation of colonic epithelial cell inflammation by deubiquitination. Am J Pathol 171: 882-892.
20. Duan Y, Liao AP, Kuppireddi S, Ye Z, Ciancio MJ, et al. (2007) beta-Catenin activity negatively regulates bacteria-induced inflammation. Lab Invest 87: 613-624.
21. Sun J, Hobert ME, Duan Y, Rao AS, He TC, et al. (2005) Crosstalk between NF-kappaB and beta-catenin pathways in bacterial-colonized intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 289: G129-137.
22. Sun J, Hobert ME, Rao AS, Neish AS, Madara JL, (2004) Bacterial activation of beta-catenin signaling in human epithelia. Am J Physiol Gastrointest Liver Physiol 287: G220-227.
23. Jones RM, Wu H, Wentworth C, Luo L, Collier-Hyams L, et al. (2008) Salmonella AvrA Coordinates Suppression of Host Immune and Apoptotic Defenses via JNK Pathway Blockade. Cell Host Microbe 3: 233-244.
24. Wu S, Ye Z, Liu X, Zhao Y, Xia Y, et al. (2010) Salmonella typhimurium infection increases p53 acetylation in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 298: G784-794.
25. Kim MJ, Chia IV, Costantini F, (2008) SUMOylation target sites at the C terminus protect Axin from ubiquitination and confer protein stability. FASEB J 22: 3785-3794.
26. Rui HL, Fan E, Zhou HM, Xu Z, Zhang Y, et al. (2002) SUMO-1 modification of the C-terminal KVEKVD of Axin is required for JNK activation but has no effect on Wnt signaling. J Biol Chem 277: 42981-42986.
27. Luo W, Zou H, Jin L, Lin S, Li Q, et al. (2005) Axin contains three separable domains that confer intramolecular, homodimeric, and heterodimeric interactions involved in distinct functions. J Biol Chem 280: 5054-5060.
28. Behrens J, Jerchow BA, Wurtele M, Grimm J, Asbrand C, et al. (1998) Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta. Science 280: 596-599.
29. Mai M, Qian C, Yokomizo A, Smith DI, Liu W, (1999) Cloning of the human homolog of conductin (AXIN2), a gene mapping to chromosome 17q23-q24. Genomics 55: 341-344.
30. Yamamoto H, Kishida S, Uochi T, Ikeda S, Koyama S, et al. (1998) Axil, a member of the Axin family, interacts with both glycogen synthase kinase 3beta and beta-catenin and inhibits axis formation of Xenopus embryos. Mol Cell Biol 18: 2867-2875.
31. Liu X, Lu R, Wu S, Sun J, (2010) Salmonella regulation of intestinal stem cells through the Wnt/beta-catenin pathway. FEBS Lett 584: 911-916.
32. Lee E, Salic A, Kruger R, Heinrich R, Kirschner MW, (2003) The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway. PLoS Biol 1: E10.
33. Sen M, Ghosh G, (2008) Transcriptional outcome of Wnt-Frizzled signal transduction in inflammation: evolving concepts. J Immunol 181: 4441-4445.
34. You J, Nguyen AV, Albers CG, Lin F, Holcombe RF, (2008) Wnt pathway-related gene expression in inflammatory bowel disease. Dig Dis Sci 53: 1013-1019.
35. Wehkamp J, Wang G, Kubler I, Nuding S, Gregorieff A, et al. (2007) The Paneth cell alpha-defensin deficiency of ileal Crohn's disease is linked to Wnt/Tcf-4. J Immunol 179: 3109-3118.
36. Schaale K, Neumann J, Schneider D, Ehlers S, Reiling N, (2010) Wnt signaling in macrophages: Augmenting and inhibiting mycobacteria-induced inflammatory responses. Eur J Cell Biol.
37. Mao J, Wang J, Liu B, Pan W, Farr GH 3rd, et al. (2001) Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol Cell 7: 801-809.
38. Zhang Y, Neo SY, Han J, Lin SC, (2000) Dimerization choices control the ability of axin and dishevelled to activate c-Jun N-terminal kinase/stress-activated protein kinase. J Biol Chem 275: 25008-25014.
39. Nakamura T, Hamada F, Ishidate T, Anai K, Kawahara K, et al. (1998) Axin, an inhibitor of the Wnt signalling pathway, interacts with beta-catenin, GSK-3beta and APC and reduces the beta-catenin level. Genes Cells 3: 395-403.
40. Rui Y, Xu Z, Lin S, Li Q, Rui H, et al. (2004) Axin stimulates p53 functions by activation of HIPK2 kinase through multimeric complex formation. EMBO J 23: 4583-4594.
41. Xie R, Jiang R, Chen D, (2010) Generation of Axin1 conditional mutant mice. Genesis.
42. Miller SI, Mekalanos JJ, (1990) Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J Bacteriol 172: 2485-2490.
43. Liao AP, Petrof EO, Kuppireddi S, Zhao Y, Xia Y, et al. (2008) Salmonella type III effector AvrA stabilizes cell tight junctions to inhibit inflammation in intestinal epithelial cells. PLoS ONE 3: e2369.
44. Wu S, Liao AP, Xia Y, Li YC, Li JD, et al. (2010) Vitamin D receptor negatively regulates bacterial-stimulated NF-kappaB activity in intestine. Am J Pathol 177: 686-697.
45. McCormick BA, Colgan SP, Delp-Archer C, Miller SI, Madara JL, (1993) Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol 123: 895-907.