The p110α and p110β isoforms of class i phosphatidylinositol 3-kinase are involved in toll-like receptor 5 signaling in epithelial cells

Mediators of Inflammation

Volumn 2010, Issue , 2010, Pages

  Ivison, Sabine M ^a   Khan, Mohammed A S ^a   Graham, Nicholas R ^a   Shobab, Leila A ^a   Yao, Yu ^a   Kifayet, Arnawaz ^a   Sly, Laura M ^b   Steiner, Theodore S ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BC CHILDREN S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 (1H INDAZOL 4 YL) 6 (4 METHANESULFONYL 1 PIPERAZINYLMETHYL) 4 MORPHOLINOTHIENO[3,2 D]PYRIMIDINE; 2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; 2 MORPHOLINO 8 PHENYLCHROMONE; 3 (4 TERT BUTYLPHENYLSULFONYL) 2 PROPENENITRILE; 9 (1 ANILINOETHYL) 7 METHYL 2 MORPHOLINOPYRIDO[1,2 A]PYRIMIDIN 4 ONE; FLAGELLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; LY303511; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROTEIN P110; SHORT HAIRPIN RNA; TOLL LIKE RECEPTOR 5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRAIN CACO 2; COLON CARCINOMA; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DRUG DELIVERY SYSTEM; DRUG EFFECT; DRUG INHIBITION; ENZYME ACTIVATION; ENZYME ACTIVITY; EPITHELIUM CELL; FEMALE; IMMUNOPRECIPITATION; INFLAMMATION; MAMMAL CELL; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; CACO-2 CELLS; CLASS IA PHOSPHATIDYLINOSITOL 3-KINASE; EPITHELIAL CELLS; HUMANS; INFLAMMATION; INTERLEUKIN-6; INTERLEUKIN-8; MICE; MICE, INBRED C57BL; PHOSPHATIDYLINOSITOL 3-KINASES; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; TOLL-LIKE RECEPTOR 5;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 78349269947     PISSN: 09629351     EISSN: 14661861     Source Type: Journal    
DOI: 10.1155/2010/652098     Document Type: Article

References (54)

1. Felix G., Duran J. D., Volko S., Boller T., Plants have a sensitive perception system for the most conserved domain of bacterial flagellin Plant Journal 1999 18 3 265 276
2. Smith K. D., Ozinsky A., Toll-like receptor-5 and the innate immune response to bacterial flagellin Current Topics in Microbiology and Immunology 2002 270 93 108
3. Tallant T., Deb A., Kar N., Lupica J., de Veer M. J., DiDonato J. A., Flagellin acting via TLR5 is the major activator of key signaling pathways leading to NF- B and proinflammatory gene program activation in intestinal epithelial cells BMC Microbiology 2004 4, article 33
4. Gewirtz A. T., Navas T. A., Lyons S., Godowski P. J., Madara J. L., Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression Journal of Immunology 2001 167 4 1882 1885
5. Zeng H., Carlson A. Q., Guo Y., Yu Y., Collier-Hyams L. S., Madara J. L., Gewirtz A. T., Neish A. S., Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella Journal of Immunology 2003 171 7 3668 3674
6. Zhou X., Girn J. A., Torres A. G., Crawford J. A., Negrete E., Vogel S. N., Kaper J. B., Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 cells Infection and Immunity 2003 71 4 2120 2129
7. Steiner T. S., Nataro J. P., Poteet-Smith C. E., Smith J. A., Guerrant R. L., Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells Journal of Clinical Investigation 2000 105 12 1769 1777
8. Barton G. M., Medzhitov R., Toll-like receptor signaling pathways Science 2003 300 5625 1524 1525
9. Yu Y., Nagai S., Wu H., Neish A. S., Koyasu S., Gewirtz A. T., TLR5-mediated phosphoinositide 3-kinase activation negatively regulates flagellin-induced proinflammatory gene expression Journal of Immunology 2006 176 10 6194 6201
10. Khan M. A. S., Kang J., Steiner T. S., Enteroaggregative Escherichia coli flagellin-induced interleukin-8 secretion requires Toll-like receptor 5-dependent p38 MAP kinase activation Immunology 2004 112 4 651 660
11. Dahan S., Busuttil V., Imbert V., Peyron J.-F., Rampal P., Czerucka D., Enterohemorrhagic Escherichia coli infection induces interleukin-8 production via activation of mitogen-activated protein kinases and the transcription factors NF- B and AP-1 in T84 cells Infection and Immunity 2002 70 5 2304 2310
12. Cantley L. C., The phosphoinositide 3-kinase pathway Science 2002 296 5573 1655 1657
13. Rhee S. H., Kim H., Moyer M. P., Pothoulakis C., Role of MyD88 in phosphatidylinositol 3-kinase activation by flagellin/Toll-like receptor 5 engagement in colonic epithelial cells Journal of Biological Chemistry 2006 281 27 18560 18568
14. Bnistant C., Chapuis H., Roche S., A specific function for phosphatidylinositol 3-kinase (p85 -p110 ) in cell survival and for phosphatidylinositol 3-kinase (p85 -p110 ) in de novo DNA synthesis of human colon carcinoma cells Oncogene 2000 19 44 5083 5090
15. Sasaki T., Irie-Sasaki J., Horie Y., Bachmaler K., Fata J. E., Li M., Suzuki A., Bouchard D., Ho A., Redston M., Gallinger S., Khokha R., Mak T. W., Hawkins P. T., Stephens L., Scherer S. W., Tsao M., Penninger J. M., Colorectal carcinomas in mice lacking the catalytic submit of PI(3)k Nature 2000 406 6798 897 902
16. Jackson S. P., Schoenwaelder S. M., Goncalves I., Nesbitt W. S., Yap C. L., Wright C. E., Kenche V., Anderson K. E., Dopheide S. M., Yuan Y., Sturgeon S. A., Prabaharan H., Thompson P. E., Smith G. D., Shepherd P. R., Daniele N., Kulkarni S., Abbott B., Saylik D., Jones C., Lu L., Giuliano S., Hughan S. C., Angus J. A., Robertson A. D., Salem H. H., PI 3-kinase p110 : a new target for antithrombotic therapy Nature Medicine 2005 11 5 507 514
17. Hmama Z., Nandan D., Sly L., Knutson K. L., Herrera-Velit P., Reiner N. E., 1,25-dihydroxyvitamin D3 -induced myeloid cell differentiation is regulated by a vitamin D receptor-phosphatidylinositol 3-kinase signaling complex Journal of Experimental Medicine 1999 190 11 1583 1594
18. Ivison S. M., Graham N. R., Bernales C. Q., Kifayet A., Ng N., Shobab L. A., Steiner T. S., Protein kinase D interaction with TLR5 is required for inflammatory signaling in response to bacterial flagellin Journal of Immunology 2007 178 9 5735 5743
19. Li X., Leu S., Cheong A., Zhang H., Baibakov B., Shih C., Birnbaum M. J., Donowitz M., Akt2, phosphatidylinositol 3-kinase, and PTEN are in lipid rafts of intestinal cells: role in absorption and differentiation Gastroenterology 2004 126 1 122 135
20. Cuevas B. D., Lu Y., Mao M., Zhang J., LaPushin R., Siminovitch K., Mills G. B., Tyrosine phosphorylation of p85 relieves its inhibitory activity on phosphatidylinositol 3-kinase Journal of Biological Chemistry 2001 276 29 27455 27461
21. Brunn G. J., Williams J., Sabers C., Wiederrecht G., Lawrence J. C. Jr., Abraham R. T., Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002 The EMBO Journal 1996 15 19 5256 5267
22. Kristof A. S., Pacheco-Rodriguez G., Schremmer B., Moss J., LY303511 (2-piperazinyl-8-phenyl-4 H -1-benzopyran-4-one) acts via phosphatidylinositol 3-kinase-independent pathways to inhibit cell proliferation via mammalian target of rapamycin (mTOR)- and non-mTOR-dependent mechanisms Journal of Pharmacology and Experimental Therapeutics 2005 314 3 1134 1143
23. Davies S. P., Reddy H., Caivano M., Cohen P., Specificity and mechanism of action of some commonly used protein kinase inhibitors Biochemical Journal 2000 351 1 95 105
24. Fruman D. A., Meyers R. E., Cantley L. C., Phosphoinositide kinases Annual Review of Biochemistry 1998 67 481 507
25. Chaussade C., Rewcastle G. W., Kendall J. D., Denny W. A., Cho K., Grnning L. M., Chong M. L., Anagnostou S. H., Jackson S. P., Daniele N., Shepherd P. R., Evidence for functional redundancy of class IA PI3K isoforms in insulin signalling Biochemical Journal 2007 404 3 449 458
26. Folkes A. J., Ahmadi K., Alderton W. K., Alix S., Baker S. J., Box G., Chuckowree I. S., Clarke P. A., Depledge P., Eccles S. A., Friedman L. S., Hayes A., Hancox T. C., Kugendradas A., Lensun L., Moore P., Olivero A. G., Pang J., Patel S., Pergl-Wilson G.H., Raynaud F. I., Robson A., Saghir N., Salphati L., Sohal S., Ultsch M. H., Valenti M., Wallweber H. J.A., Nan C. W., Wiesmann C., Workman P., Zhyvoloup A., Zvelebil M. J., Shuttleworth S. J., The identification of 2-(1 H -indazol-4-yl)-6-(4-methanesulfonyl-piperazin- 1-ylmethyl)-4- morpholin-4-yl-thieno[3,2-d]pyrimidine (GDC-0941) as a potent, selective, orally bioavailable inhibitor of class I PI3 kinase for the treatment of cancer Journal of Medicinal Chemistry 2008 51 18 5522 5532
27. Ito K., Caramori G., Adcock I. M., Therapeutic potential of phosphatidylinositol 3-kinase inhibitors in inflammatory respiratory disease Journal of Pharmacology and Experimental Therapeutics 2007 321 1 1 8
28. Knight Z. A., Gonzalez B., Feldman M. E., Zunder E. R., Goldenberg D. D., Williams O., Loewith R., Stokoe D., Balla A., Toth B., Balla T., Weiss W. A., Williams R. L., Shokat K. M., A pharmacological map of the PI3-K family defines a role for p110 in insulin signaling Cell 2006 125 4 733 747
29. Raynaud F., Eccles S., Clarke P., Pharmacological properties of a potent inhibitor of the phosphatidylinositol 3-kinase (PI3K) family Annals of Oncology 2007 18 supplement 4 iv23
30. Gewirtz A. T., Vijay-Kumar M., Brant S. R., Duerr R. H., Nicolae D. L., Cho J. H., Dominant-negative TLR5 polymorphism reduces adaptive immune response to flagellin and negatively associates with Crohn's disease American Journal of Physiology 2006 290 6 G1157 G1163
31. Hawn T. R., Wu H., Grossman J. M., Hahn B. H., Tsao B. P., Aderem A., A stop codon polymorphism of Toll-like receptor 5 is associated with resistance to systemic lupus erythematosus Proceedings of the National Academy of Sciences of the United States of America 2005 102 30 10593 10597
32. Hawn T. R., Verbon A., Lettinga K. D., Zhao L. P., Li S. S., Laws R. J., Skerrett S. J., Beutler B., Schroeder L., Nachman A., Ozinsky A., Smith K. D., Aderem A., A common dominant TLR5 stop codon polymorphism abolishes flagellin signaling and is associated with susceptibility to legionnaires' disease Journal of Experimental Medicine 2003 198 10 1563 1572
33. Toker A., Cantley L. C., Signalling through the lipid products of phosphoinositide-3-OH kinase Nature 1997 387 6634 673 676
34. Marqus M., Kumar A., Poveda A. M., Zuluaga S., Hernndez C., Jackson S., Pasero P., Carrera A. C., Specific function of phosphoinositide 3-kinase beta in the control of DNA replication Proceedings of the National Academy of Sciences of the United States of America 2009 106 18 7525 7530
35. Laird M. H. W., Rhee S. H., Perkins D. J., Medvedev A. E., Piao W., Fenton M. J., Vogel S. N., TLR4/MyD88/PI3K interactions regulate TLR4 signaling Journal of Leukocyte Biology 2009 85 6 966 977
36. Weaver S. A., Russo M. P., Wright K. L., Kolios G., Jobin C., Robertson D. A. F., Ward S. G., Regulatory role of phosphatidylinositol 3-kinase on TNF- -induced cyclooxygenase 2 expression in colonic epithelial cells Gastroenterology 2001 120 5 1117 1127
37. Lee J. Y., Ye J., Gao Z., Youn H. S., Lee W. H., Zhao L., Sizemore N., Hwang D. H., Reciprocal modulation of Toll-like receptor-4 signaling pathways involving MyD88 and phosphatidylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids Journal of Biological Chemistry 2003 278 39 37041 37051
38. Tang S., Leung J. C. K., Abe K., Chan K. W., Chan L. Y. Y., Chan T. M., Lai K. N., Albumin stimulates interleukin-8 expression in proximal tubular epithelial cells in vitro and in vivo Journal of Clinical Investigation 2003 111 4 515 527
39. Osawa Y., Nagaki M., Banno Y., Brenner D. A., Asano T., Nozawa Y., Moriwaki H., Nakashima S., Tumor necrosis factor alpha-induced interleukin-8 production via NF- B and phosphatidylinositol 3-kinase/Akt pathways inhibits cell apoptosis in human hepatocytes Infection and Immunity 2002 70 11 6294 6301
40. Bancroft C. C., Chen Z., Yeh J., Sunwoo J. B., Yeh N. T., Jackson S., Jackson C., Van Waes C., Effects of pharmacologic antagonists of epidermal growth factor receptor, PI3K and MEK signal kinases on NF- B and AP-1 activation and IL-8 and VEGF expression in human head and neck squamous cell carcinoma lines International Journal of Cancer 2002 99 4 538 548
41. Schulte R., Zumbihl R., Kampik D., Fauconnier A., Autenrieth I. B., Wortmannin blocks Yersinia invasin-triggered internalization, but not interleukin-8 production by epithelial cells Medical Microbiology and Immunology 1998 187 1 53 60
42. Re F., Strominger J. L., Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells Journal of Biological Chemistry 2001 276 40 37692 37699
43. Arbibe L., Mira J.-P., Teusch N., Kline L., Guha M., Mackman N., Godowski P. J., Ulevitch R. J., Knaus U. G., Toll-like receptor 2-mediated NF- B activation requires a Rac I-dependent pathway Nature Immunology 2000 1 6 533 540
44. Ozes O. N., Mayo L. D., Gustin J. A., Pfeffer S. R., Pfeffer L. M., Donner D. B., NF- B activation by tumour necrosis factor requires tie Akt serine- threonine kinase Nature 1999 401 6748 82 85
45. Martin M., Schifferle R. E., Cuesta N., Vogel S. N., Katz J., Michalek S. M., Role of the phosphatidylinositol 3 kinase-Akt pathway in the regulation of IL-10 and IL-12 by Porphyromonas gingivalis lipopolysaccharide Journal of Immunology 2003 171 2 717 725
46. Kane L. P., Shapiro V. S., Stokoe D., Weiss A., Induction of NF- B by the Akt/PKB kinase Current Biology 1999 9 11 601 604
47. Sizemore N., Leung S., Stark G. R., Activation of phosphatidylinositol 3-kinase in response to interleukin- 1 leads to phosphorylation and activation of the NF- B p65/RelA subunit Molecular and Cellular Biology 1999 19 7 4798 4805
48. El-Kholy W., Macdonald P. E., Lin J. H., Wang J., Fox J. M., Light P. E., Wang Q., Tsushima R. G., Wheeler M. B., The phosphatidylinositol 3-kinase inhibitor LY294002 potently blocks K(V) currents via a direct mechanism The FASEB Journal 2003 17 6 720 722
49. Choi E.-K., Park H.-J., Ma J.-S., Lee H.-C., Kang H.-C., Kim B.-G., Kang I.-C., LY294002 inhibits monocyte chemoattractant protein-1 expression through a phosphatidylinositol 3-kinase-independent mechanism FEBS Letters 2004 559 1-3 141 144
50. Hazeki K., Kinoshita S., Matsumura T., Nigorikawa K., Kubo H., Hazeki O., Opposite effects of wortmannin and 2-(4-morpholinyl)-8-phenyl-1(4 H)- benzopyran-4-one hydrochloride on Toll-like receptor-mediated nitric oxide production: negative regulation of nuclear factor- B by phosphoinositide 3-kinase Molecular Pharmacology 2006 69 5 1717 1724
51. Utsugi M., Dobashi K., Ono A., Ishizuka T., Matsuzaki S., Hisada T., Shimizu Y., Kawata T., Aoki H., Kamide Y., Mori M., PI3K p110beta positively regulates lipopolysaccharide-induced IL-12 production in human macrophages and dendritic cells and JNK1 plays a novel role Journal of Immunology 2009 182 9 5225 5231
52. Tsukamoto K., Hazeki K., Hoshi M., Nigorikawa K., Inoue N., Sasaki T., Hazeki O., Critical roles of the p110 subtype of phosphoinositide 3-kinase in lipopolysaccharide-induced Akt activation and negative regulation of nitrite production in RAW 264.7 cells Journal of Immunology 2008 180 4 2054 2061
53. Sly L. M., Hamilton M. J., Kuroda E., Ho V. W., Antignano F. L., Omeis S. L., Van Netten-Thomas C. J., Wong D., Brugger H. K., Williams O., Feldman M. E., Houseman B. T., Fiedler D., Shokat K. M., Krystal G., SHIP prevents lipopolysaccharide from triggering an antiviral response in mice Blood 2009 113 13 2945 2954
54. Kato K., Lu W., Kai H., Kim K. C., Phosphoinositide 3-kinase is activated by MUC1 but not responsible for MUC1-induced suppression of Toll-like receptor 5 signaling American Journal of Physiology 2007 293 3 L686 L692