Sphingosine kinase-1 is required for toll mediated β-defensin 2 induction in human oral keratinocytes

PLoS ONE

Volumn 5, Issue 7, 2010, Pages

  Benakanakere, Manjunatha R ^a   Zhao, Jiawei ^a   Galicia, Johnah C ^a   Martin, Michael ^b   Kinane, Denis F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; BETA DEFENSIN; GLYCOGEN SYNTHASE KINASE 3BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; SPHINGOSINE KINASE 1; TOLL LIKE RECEPTOR 2; DEFB4A PROTEIN, HUMAN; ENZYME INHIBITOR; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; INDOLE DERIVATIVE; LITHIUM; MALEIMIDE DERIVATIVE; PHOSPHOTRANSFERASE; SPHINGOSINE KINASE; TLR2 PROTEIN, HUMAN;

ARTICLE; CATALYSIS; CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; KERATINOCYTE; MOUTH; PROTEIN FUNCTION; PROTEIN SECRETION; RNA INTERFERENCE; UPREGULATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG POTENTIATION; GENETICS; METABOLISM; POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

BETA-DEFENSINS; BLOTTING, WESTERN; CELLS, CULTURED; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; INDOLES; KERATINOCYTES; LITHIUM; MALEIMIDES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); POLYMERASE CHAIN REACTION; TOLL-LIKE RECEPTOR 2;

EID: 77955368940     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011512     Document Type: Article

References (79)

1. Martin GS, Mannino DM, Eaton S, Moss M (2003) The epidemiology of sepsis in the United States from 1979 through 2000. N Engl J Med 348: 1546-1554.
2. Danai P, Martin GS (2005) Epidemiology of sepsis: recent advances. Curr Infect Dis Rep 7: 329-334.
3. Danai PA, Sinha S, Moss M, Haber MJ, Martin GS (2007) Seasonal variation in the epidemiology of sepsis. Crit Care Med 35: 410-415.
4. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415: 389-395.
5. Scott MG, Hancock RE (2000) Cationic antimicrobial peptides and their multifunctional role in the immune system. Crit Rev Immunol 20: 407-431.
6. Lehrer RI, Ganz T (1999) Antimicrobial peptides in mammalian and insect host defence. Curr Opin Immunol 11: 23-27.
7. Ganz T (2002) Antimicrobial polypeptides in host defense of the respiratory tract. J Clin Invest 109: 693-697.
8. Ganz T (2003) Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 3: 710-720.
9. Ganz T (2004) Defensins: antimicrobial peptides of vertebrates. C R Biol 327: 539-549.
10. Huttner KM, Bevins CL (1999) Antimicrobial peptides as mediators of epithelial host defense. Pediatr Res 45: 785-794.
11. Kaiser V, Diamond G (2000) Expression of mammalian defensin genes. J Leukoc Biol 68: 779-784.
12. Diamond G, Kaiser V, Rhodes J, Russell JP, Bevins CL (2000) Transcriptional regulation of beta-defensin gene expression in tracheal epithelial cells. Infect Immun 68: 113-119.
13. Hait NC, Allegood J, Maceyka M, Strub GM, Harikumar KB, et al. (2009) Regulation of histone acetylation in the nucleus by sphingosine-1-phosphate. Science 325: 1254-1257.
14. Shida D, Takabe K, Kapitonov D, Milstien S, Spiegel S (2008) Targeting SphK1 as a new strategy against cancer. Curr Drug Targets 9: 662-673.
15. Spiegel S, Milstien S (2002) Sphingosine 1-phosphate, a key cell signaling molecule. J Biol Chem 277: 25851-25854.
16. Karliner JS (2009) Sphingosine kinase and sphingosine 1-phosphate in cardioprotection. J Cardiovasc Pharmacol 53: 189-197.
17. Kennedy S, Kane KA, Pyne NJ, Pyne S (2009) Targeting sphingosine-1-phosphate signalling for cardioprotection. Curr Opin Pharmacol 9: 194-201.
18. Means CK, Brown JH (2009) Sphingosine-1-phosphate receptor signalling in the heart. Cardiovasc Res 82: 193-200.
19. Lee MJ, Van Brocklyn JR, Thangada S, Liu CH, Hand AR, et al. (1998) Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 279: 1552-1555.
20. Pitson SM, Moretti PA, Zebol JR, Lynn HE, Xia P, et al. (2003) Activation of sphingosine kinase 1 by ERK1/2-mediated phosphorylation. EMBO J 22: 5491-5500.
21. Garg SK, Santucci MB, Panitti M, Pucillo L, Bocchino M, et al. (2006) Does sphingosine 1-phosphate play a protective role in the course of pulmonary tuberculosis? Clin Immunol 121: 260-264.
22. Garg SK, Valente E, Greco E, Santucci MB, De Spirito M, et al. (2006) Lysophosphatidic acid enhances antimycobacterial activity both in vitro and ex vivo. Clin Immunol 121: 23-28.
23. Garg SK, Volpe E, Palmieri G, Mattei M, Galati D, et al. (2004) Sphingosine 1-phosphate induces antimicrobial activity both in vitro and in vivo. J Infect Dis 189: 2129-2138.
24. Kinane DF, Shiba H, Stathopoulou PG, Zhao H, Lappin DF, et al. (2006) Gingival epithelial cells heterozygous for Toll-like receptor 4 polymorphisms Asp299Gly and Thr399ile are hypo-responsive to Porphyromonas gingivalis. Genes Immun 7: 190-200.
25. Shiba H, Venkatesh SG, Gorr SU, Barbieri G, Kurihara H, et al. (2005) Parotid secretory protein is expressed and inducible in human gingival keratinocytes. J Periodontal Res 40: 153-157.
26. Benakanakere MR, Li Q, Eskan MA, Singh AV, Zhao J, et al. (2009) Modulation of TLR2 protein expression by miR-105 in human oral keratinocytes. J Biol Chem 284: 23107-23115.
27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
28. Shida D, Fang X, Kordula T, Takabe K, Lepine S, et al. (2008) Cross-talk between LPA1 and epidermal growth factor receptors mediates up-regulation of sphingosine kinase 1 to promote gastric cancer cell motility and invasion. Cancer Res 68: 6569-6577.
29. Spiegel S, Milstien S (2003) Sphingosine-1-phosphate: an enigmatic signaling lipid. Nat Rev Mol Cell Biol 4: 397-407.
30. Markeeva N, Lisovskiy I, Lyzogubov V, Usenko V, Soldatkina M, et al. (2005) Expression of beta-defensin-2 in human gastric tumors: a pilot study. Exp Oncol 27: 130-135.
31. Haider AS, Peters SB, Kaporis H, Cardinale I, Fei J, et al. (2006) Genomic analysis defines a cancer-specific gene expression signature for human squamous cell carcinoma and distinguishes malignant hyperproliferation from benign hyperplasia. J Invest Dermatol 126: 869-881.
32. Arimura Y, Ashitani J, Yanagi S, Tokojima M, Abe K, et al. (2004) Elevated serum beta-defensins concentrations in patients with lung cancer. Anticancer Res 24: 4051-4057.
33. Mizukawa N, Sawaki K, Yamachika E, Fukunaga J, Ueno T, et al. (2000) Presence of human beta-defensin-2 in oral squamous cell carcinoma. Anticancer Res 20: 2005-2007.
34. Eskan MA, Hajishengallis G, Kinane DF (2007) Differential activation of human gingival epithelial cells and monocytes by Porphyromonas gingivalis fimbriae. Infect Immun 75: 892-898.
35. Jang BC, Lim KJ, Paik JH, Kwon YK, Shin SW, et al. (2004) Up-regulation of human beta-defensin 2 by interleukin-1beta in A549 cells: involvement of PI3K, PKC, p38 MAPK, JNK, and NF-kappaB. Biochem Biophys Res Commun 320: 1026-1033.
36. Harder J, Bartels J, Christophers E, Schroder JM (1997) A peptide antibiotic from human skin. Nature 387: 861.
37. Harder J, Meyer-Hoffert U, Wehkamp K, Schwichtenberg L, Schroder JM (2004) Differential gene induction of human beta-defensins (hBD-1, -2, -3, and -4) in keratinocytes is inhibited by retinoic acid. J Invest Dermatol 123: 522-529.
38. O'Neil DA, Porter EM, Elewaut D, Anderson GM, Eckmann L, et al. (1999) Expression and regulation of the human beta-defensins hBD-1 and hBD-2 in intestinal epithelium. J Immunol 163: 6718-6724.
39. Garcia CA, Wang H, Benakanakere MR, Barrett E, Kinane DF, et al. (2009) c-Jun controls the ability of IL-12 to induce IL-10 production from human memory CD4+ T cells. J Immunol 183: 4475-4482.
40. Garcia CA, Benakanakere MR, Alard P, Kosiewicz MM, Kinane DF, et al. (2008) Antigenic experience dictates functional role of glycogen synthase kinase-3 in human CD4+ T cell responses. J Immunol 181: 8363-8371.
41. Martin M, Rehani K, Jope RS, Michalek SM (2005) Toll-like receptor-mediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat Immunol 6: 777-784.
42. Carretero M, Escamez MJ, Garcia M, Duarte B, Holguin A, et al. (2008) In vitro and in vivo wound healing-promoting activities of human cathelicidin LL-37. J Invest Dermatol 128: 223-236.
43. Donnarumma G, Paoletti I, Buommino E, Iovene MR, Tudisco L, et al. (2007) Anti-inflammatory effects of moxifloxacin and human beta-defensin 2 association in human lung epithelial cell line (A549) stimulated with lipopolysaccharide. Peptides 28: 2286-2292.
44. Rehani K, Scott DA, Renaud D, Hamza H, Williams LR, et al. (2008) Cotinineinduced convergence of the cholinergic and PI3 kinase-dependent anti-inflammatory pathways in innate immune cells. Biochim Biophys Acta 1783: 375-382.
45. Eldar-Finkelman H, Argast GM, Foord O, Fischer EH, Krebs EG (1996) Expression and characterization of glycogen synthase kinase-3 mutants and their effect on glycogen synthase activity in intact cells. Proc Natl Acad Sci U S A 93: 10228-10233.
46. Olivera A, Kohama T, Edsall L, Nava V, Cuvillier O, et al. (1999) Sphingosine kinase expression increases intracellular sphingosine-1-phosphate and promotes cell growth and survival. J Cell Biol 147: 545-558.
47. Markeeva N, Lysovskiy I, Zhuravel E, Soldatkina M, Lyzogubov V, et al. (2005) Involvement of human beta-defensin-2 in proliferation of transformed cells of human cervix. Exp Oncol 27: 308-313.
48. Zhi L, Leung BP, Melendez AJ (2006) Sphingosine kinase 1 regulates proinflammatory responses triggered by TNFalpha in primary human monocytes. J Cell Physiol 208: 109-115.
49. Gould IM (2009) Antibiotic resistance: the perfect storm. Int J Antimicrob Agents 34 Suppl 3: S2-5.
50. Travis SM, Singh PK, Welsh MJ (2001) Antimicrobial peptides and proteins in the innate defense of the airway surface. Curr Opin Immunol 13: 89-95.
51. Hancock RE, Sahl HG (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24: 1551-1557.
52. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4: 499-511.
53. Yang D, Biragyn A, Hoover DM, Lubkowski J, Oppenheim JJ (2004) Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil-derived neurotoxin in host defense. Annu Rev Immunol 22: 181-215.
54. White SH, Wimley WC, Selsted ME (1995) Structure, function, and membrane integration of defensins. Curr Opin Struct Biol 5: 521-527.
55. Yang D, Biragyn A, Kwak LW, Oppenheim JJ (2002) Mammalian defensins in immunity: more than just microbicidal. Trends Immunol 23: 291-296.
56. Yang D, Chen Q, Hoover DM, Staley P, Tucker KD, et al. (2003) Many chemokines including CCL20/MIP-3alpha display antimicrobial activity. J Leukoc Biol 74: 448-455.
57. Krisanaprakornkit S, Kimball JR, Dale BA (2002) Regulation of human betadefensin-2 in gingival epithelial cells: the involvement of mitogen-activated protein kinase pathways, but not the NF-kappaB transcription factor family. J Immunol 168: 316-324.
58. Nakayama K, Furusu A, Xu Q, Konta T, Kitamura M (2001) Unexpected transcriptional induction of monocyte chemoattractant protein 1 by proteasome inhibition: involvement of the c-Jun N-terminal kinase-activator protein 1 pathway. J Immunol 167: 1145-1150.
59. Yamaguchi Y, Nagase T, Makita R, Fukuhara S, Tomita T, et al. (2002) Identification of multiple novel epididymis-specific beta-defensin isoforms in humans and mice. J Immunol 169: 2516-2523.
60. Biragyn A, Ruffini PA, Leifer CA, Klyushnenkova E, Shakhov A, et al. (2002) Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science 298: 1025-1029.
61. Vora P, Youdim A, Thomas LS, Fukata M, Tesfay SY, et al. (2004) Betadefensin-2 expression is regulated by TLR signaling in intestinal epithelial cells. J Immunol 173: 5398-5405.
62. Liu L, Roberts AA, Ganz T (2003) By IL-1 signaling, monocyte-derived cells dramatically enhance the epidermal antimicrobial response to lipopolysaccharide. J Immunol 170: 575-580.
63. Foster SL, Hargreaves DC, Medzhitov R (2007) Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447: 972-978.
64. Yoshida A, Inagawa H, Kohchi C, Nishizawa T, Soma G (2009) The role of tolllike receptor 2 in survival strategies of Mycobacterium tuberculosis in macrophage phagosomes. Anticancer Res 29: 907-910.
65. Eskan MA, Rose BG, Benakanakere MR, Zeng Q, Fujioka D, et al. (2008) TLR4 and S1P receptors cooperate to enhance inflammatory cytokine production in human gingival epithelial cells. Eur J Immunol 38: 1138-1147.
66. Burns E, Bachrach G, Shapira L, Nussbaum G (2006) Cutting Edge: TLR2 is required for the innate response to Porphyromonas gingivalis: activation leads to bacterial persistence and TLR2 deficiency attenuates induced alveolar bone resorption. J Immunol 177: 8296-8300.
67. Burns E, Eliyahu T, Uematsu S, Akira S, Nussbaum G TLR2-dependent inflammatory response to Porphyromonas gingivalis is MyD88 independent, whereas MyD88 is required to clear infection. J Immunol 184: 1455-1462.
68. Hajishengallis G, Wang M, Liang S (2009) Induction of distinct TLR2-mediated proinflammatory and proadhesive signaling pathways in response to Porphyromonas gingivalis fimbriae. J Immunol 182: 6690-6696.
69. Ruse M, Knaus UG (2006) New players in TLR-mediated innate immunity: PI3K and small Rho GTPases. Immunol Res 34: 33-48.
70. Pitson SM, Xia P, Leclercq TM, Moretti PA, Zebol JR, et al. (2005) Phosphorylation-dependent translocation of sphingosine kinase to the plasma membrane drives its oncogenic signalling. J Exp Med 201: 49-54.
71. Kota S, Sabbah A, Chang TH, Harnack R, Xiang Y, et al. (2008) Role of human beta-defensin-2 during tumor necrosis factor-alpha/NF-kappaB-mediated innate antiviral response against human respiratory syncytial virus. J Biol Chem 283: 22417-22429.
72. Falco A, Chico V, Marroqui L, Perez L, Coll JM, et al. (2008) Expression and antiviral activity of a beta-defensin-like peptide identified in the rainbow trout (Oncorhynchus mykiss) EST sequences. Mol Immunol 45: 757-765.
73. Quinones-Mateu ME, Lederman MM, Feng Z, Chakraborty B, Weber J, et al. (2003) Human epithelial beta-defensins 2 and 3 inhibit HIV-1 replication. AIDS 17: F39-48.
74. Chong KT, Xiang L, Wang X, Jun EL, Xi LF, et al. (2006) High level expression of human epithelial beta-defensins (hBD-1, 2 and 3) in papillomavirus induced lesions. Virol J 3: 75.
75. Yamane D, Zahoor MA, Mohamed YM, Azab W, Kato K, et al. (2009) Inhibition of sphingosine kinase by bovine viral diarrhea virus NS3 is crucial for efficient viral replication and cytopathogenesis. J Biol Chem 284: 13648-13659.
76. Mandala S, Hajdu R, Bergstrom J, Quackenbush E, Xie J, et al. (2002) Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science 296: 346-349.
77. Martin M, Schifferle RE, Cuesta N, Vogel SN, Katz J, et al. (2003) Role of the phosphatidylinositol 3 kinase-Akt pathway in the regulation of IL-10 and IL-12 by Porphyromonas gingivalis lipopolysaccharide. J Immunol 171: 717-725.
78. Jiang K, Zhong B, Gilvary DL, Corliss BC, Hong-Geller E, et al. (2000) Pivotal role of phosphoinositide-3 kinase in regulation of cytotoxicity in natural killer cells. Nat Immunol 1: 419-425.
79. Wang Q, Zhou Y, Wang X, Evers BM (2006) Glycogen synthase kinase-3 is a negative regulator of extracellular signal-regulated kinase. Oncogene 25: 43-50.