G-CSF-mediated inhibition of JNK is a key mechanism for Lactobacillus rhamnosus-induced suppression of TNF production in macrophages

Cellular Microbiology

Volumn 8, Issue 12, 2006, Pages 1958-1971

  Kim, Sung O ^a,b   Sheikh, Haroon I ^a   Ha, Soon Duck ^a   Martins, Andrew ^a   Reid, Gregor ^a,b  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE COLONY STIMULATING FACTOR RECEPTOR; LIPOPOLYSACCHARIDE; NEUTRALIZING ANTIBODY; PROBIOTIC AGENT; STAT3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENTEROCOCCUS FAECALIS; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME LOCALIZATION; ESCHERICHIA COLI; HUMAN; HUMAN CELL; IMMUNOMODULATION; KNOCKOUT MOUSE; LACTOBACILLUS RHAMNOSUS; MACROPHAGE; MACROPHAGE ACTIVATION; MONOCYTE; MOUSE; NONHUMAN; PARACRINE SIGNALING; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS;

ANIMALS; BONE MARROW CELLS; CELL LINE; CYTOKINES; ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; GRANULOCYTE COLONY-STIMULATING FACTOR; HUMANS; INTERLEUKIN-10; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LACTOBACILLUS RHAMNOSUS; MACROPHAGE ACTIVATION; MACROPHAGES; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROBIOTICS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TUMOR NECROSIS FACTOR-ALPHA;

ENTEROCOCCUS FAECALIS; ESCHERICHIA COLI; LACTOBACILLUS RHAMNOSUS;

EID: 33750585793     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00763.x     Document Type: Article

References (74)

1. Baharav, E., Mor, F., Halpern, M., and Weinberger, A. (2004) Lactobacillus GG bacteria ameliorate arthritis in Lewis rats. J Nutr 134: 1964-1969.
2. Bennett, B.L., Sasaki, D.T., Murray, B.W., O'Leary, E.C., Sakata, S.T., Xu, W., et al. (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci USA 98: 13681-13686.
3. van den Blink, B., Juffermans, N.P., ten Hove, T., Schultz, M.J., van Deventer, S.J., van der Poll, T., and Peppelenbosch, M.P. (2001) p38 mitogen-activated protein kinase inhibition increases cytokine release by macrophages in vitro and during infection in vivo. J Immunol 166: 582-587.
4. Boneberg, E.M., and Hartung, T. (2002) Molecular aspects of anti-inflammatory action of G-CSF. Inflamm Res 51: 119-128.
5. Border, J.R. (1988) Hypothesis: Sepsis, multiple systems organ failure, and the macrophage. Arch Surg 123: 285-286.
6. Borruel, N., Carol, M., Casellas, F., Antolin, M., de Lara, F., Espin, E., et al. (2002) Increased mucosal tumour necrosis factor alpha production in Crohn's disease can be downregulated ex vivo by probiotic bacteria. Gut 51: 659-664.
7. Bromberg, J.F., Wrzeszczynska, M.H., Devgan, G., Zhao, Y., Pestell, R.G., Albanese, C., and Darnell, J.E., Jr (1999) Stat3 as an oncogene. Cell 98: 295-303.
8. Butcher, B.A., Kim, L., Panopoulos, A.D., Watowich, S.S., Murray, P.J., and Denkers, E.Y. (2005) IL-10-independent STAT3 activation by Toxoplasma gondii mediates suppression of IL-12 and TNF-alpha in host macrophages. J Immunol 174: 3148-3152.
9. Cochran, F.R., and Finch-Arietta, M.B. (1992) Interleukin-6 can prime THP-1 macrophages for enhanced production of tumor necrosis factor-alpha in response to LPS. Immunopharmacology 23: 97-103.
10. Demetri, G.D., and Griffin, J.D. (1991) Granulocyte colony-stimulating factor and its receptor. Blood 78: 2791-2808.
11. Denys, A., Udalova, I.A., Smith, C., Williams, L.M., Ciesielski, C.J., Campbell, J., et al. (2002) Evidence for a dual mechanism for IL-10 suppression of TNF-alpha production that does not involve inhibition of p38 mitogen-activated protein kinase or NF-kappa B in primary human macrophages. J Immunol 168: 4837-4845.
12. Dieleman, L.A., Goerres, M.S., Arends, A., Sprengers, D., Torrice, C., Hoentjen, F., et al. (2003) Lactobacillus GG prevents recurrence of colitis in HLA-B27 transgenic rats after antibiotic treatment. Gut 52: 370-376.
13. Donnelly, R.P., Dickensheets, H., and Finbloom, D.S. (1999) The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes. J Interferon Cytokine Res 19: 563-573.
14. Doron, S., Snydman, D.R., and Gorbach, S.L. (2005) Lactobacillus GG: bacteriology and clinical applications. Gastroenterol Clin North Am 34: 483-498, ix.
15. Gardiner, G.E., Heinemann, C., Bruce, A.W., Beuerman, D., and Reid, G. (2002) Persistence of Lactobacillus fermentum RC-14 and Lactobacillus rhamnosus GR-1 but not L. rhamnosus GG in the human vagina as demonstrated by randomly amplified polymorphic DNA. Clin Diagn Lab Immunol 9: 92-96.
16. Goodridge, H.S., Wilson, E.H., Harnett, W., Campbell, C.C., Harnett, M.M., and Liew, F.Y. (2001) Modulation of macrophage cytokine production by ES-62, a secreted product of the filarial nematode Acanthocheilonema viteae. J Immunol 167: 940-945.
17. Gorbach, S.L. (2002) Probiotics in the third millennium. Dig Liver Dis 34 (Suppl. 2): S2-S7.
18. Gorgen, I., Hartung, T., Leist, M., Niehorster, M., Tiegs, G., Uhlig, S., et al. (1992) Granulocyte colony-stimulating factor treatment protects rodents against lipopolysaccharide-induced toxicity via suppression of systemic tumor necrosis factor-alpha. J Immunol 149: 918-924.
19. Guandalini, S. (2002) Use of Lactobacillus - GG in paediatric Crohn's disease. Dig Liver Dis 34 (Suppl. 2): S63-S65.
20. Haq, R., Halupa, A., Beattie, B.K., Mason, J.M., Zanke, B.W., and Barber, D.L. (2002) Regulation of erythropoietin-induced STAT serine phosphorylation by distinct mitogen-activated protein kinases. J Biol Chem 277: 17359-17366.
21. Hareng, L., Meergans, T., von Aulock, S., Volk, H.D., and Hartung, T. (2003) Cyclic AMP increases endogenous granulocyte colony-stimulating factor formation in monocytes and THP-1 macrophages despite attenuated TNF-alpha formation. Eur J Immunol 33: 2287-2296.
22. Hartmann, S., and Lucius, R. (2003) Modulation of host immune responses by nematode cystatins. Int J Parasitol 33: 1291-1302.
23. Hasegawa, T., Suzuki, K., Sakamoto, C., Ohta, K., Nishiki, S., Hino, M., et al. (2003) Expression of the inhibitor of apoptosis (IAP) family members in human neutrophils: Up-regulation of cIAP2 by granulocyte colony-stimulating factor and overexpression of cIAP2 in chronic neutrophilic leukemia. Blood 101: 1164-1171.
24. Hayes, M.P., and Zoon, K.C. (1993) Priming of human monocytes for enhanced lipopolysaccharide responses: Expression of alpha interferon, interferon regulatory factors, and tumor necrosis factor. Infect Immun 61: 3222-3227.
25. Houston, K.M., Wilson, E.H., Eyres, L., Brombacher, F., Harnett, M.M., Alexander, J., and Harnett, W. (2000) Presence of phosphorylcholine on a filarial nematode protein influences immunoglobulin G subclass response to the molecule by an interleukin-10-dependent mechanism. Infect Immun 68: 5466-5468.
26. Jain, N., Zhang, T., Fong, S.L., Lim, C.P., and Cao, X. (1998) Repression of Stat3 activity by activation of mitogen-activated protein kinase (MAPK). Oncogene 17: 3157-3167.
27. Kato, I., Endo-Tanaka, K., and Yokokura, T. (1998) Suppressive effects of the oral administration of Lactobacillus casei on type II collagen-induced arthritis in DBA/1 mice. Life Sci 63: 635-644.
28. Kelly, D., Campbell, J.I., King, T.P., Grant, G., Jansson, E.A., Coutts, A.G., et al. (2004) Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol 5: 104-112.
29. Kim, S.O., Ono, K., and Han, J. (2001) Apoptosis by pan-caspase inhibitors in lipopolysaccharide-activated macrophages. Am J Physiol Lung Cell Mol Physiol 281: L1095-L1105.
30. Kondo, S., Okamura, S., Asano, Y., Harada, M., and Niho, Y. (1991) Human granulocyte colony-stimulating factor receptors in acute myelogenous leukemia. Eur J Haematol 46: 223-230.
31. Kontoyiannis, D., Kotlyarov, A., Carballo, E., Alexopoulou, L., Blackshear, P.J., Gaestel, M., et al. (2001) Interleukin-10 targets p38 MAPK to modulate ARE-dependent TNF mRNA translation and limit intestinal pathology. EMBO J 20: 3760-3770.
32. Lang, R., Patel, D., Morris, J.J., Rutschman, R.L., and Murray, P.J. (2002) Shaping gene expression in activated and resting primary macrophages by IL-10. J Immunol 169: 2253-2263.
33. McCarthy, J., O'Mahony, L., O'Callaghan, L., Sheil, B., Vaughan, E.E., Fitzsimons, N., et al. (2003) Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut 52: 975-980.
34. Madsen, K.L., Doyle, J.S., Jewell, L.D., Tavernini, M.M., and Fedorak, R.N. (1999) Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 116: 1107-1114.
35. Mahida, Y.R. (2000) The key role of macrophages in the immunopathogenesis of inflammatory bowel disease. Inflamm Bowel Dis 6: 21-33.
36. Manning, A.M., and Davis, R.J. (2003) Targeting JNK for therapeutic benefit: From junk to gold? Nat Rev Drug Discov 2: 554-565.
37. Miettinen, M., Lehtonen, A., Julkunen, I., and Matikainen, S. (2000) Lactobacilli and Streptococci activate NF-kappa B and STAT signaling pathways in human macrophages. J Immunol 164: 3733-3740.
38. Miller, A.D., and Buttimore, C. (1986) Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Mol Cell Biol 6: 2895-2902.
39. Miraglia del Giudice, M., and De Luca, M.G. (2004) The role of probiotics in the clinical management of food allergy and atopic dermatitis. J Clin Gastroenterol 38: S84-S85.
40. Montrose, D.C., and Floch, M.H. (2005) Probiotics used in human studies. J Clin Gastroenterol 39: 469-484.
41. Moore, K.W., de Waal Malefyt, R., Coffman, R.L., and O'Garra, A. (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19: 683-765.
42. Morita, H., He, F., Fuse, T., Ouwehand, A.C., Hashimoto, H., Hosoda, M., et al. (2002) Cytokine production by the murine macrophage cell line J774.1 after exposure to lactobacilli. Biosci Biotechnol Biochem 66: 1963-1966.
43. Nagabhushanam, V., Solache, A., Ting, L.M., Escaron, C.J., Zhang, J.Y., and Ernst, J.D. (2003) Innate inhibition of adaptive immunity: Mycobacterium tuberculosis-induced IL-6 inhibits macrophage responses to IFN-gamma. J Immunol 171: 4750-4757.
44. Neish, A.S., Gewirtz, A.T., Zeng, H., Young, A.N., Hobert, M.E., Karmali, V., et al. (2000) Prokaryotic regulation of epithelial responses by inhibition of IkappaB-alpha ubiquitination. Science 289: 1560-1563.
45. Nicola, N.A., and Metcalf, D. (1985) Binding of 125I-labeled granulocyte colony-stimulating factor to normal murine hemopoietic cells. J Cell Physiol 124: 313-321.
46. Nicola, N.A., Vadas, M.A., and Lopez, A.F. (1986) Down-modulation of receptors for granulocyte colony-stimulating factor on human neutrophils by granulocyte-activating agents. J Cell Physiol 128: 501-509.
47. Nishiki, S., Hato, F., Kamata, N., Sakamoto, E., Hasegawa, T., Kimura-Eto, A., et al. (2004) Selective activation of STAT3 in human monocytes stimulated by G-CSF: Implication in inhibition of LPS-induced TNF-alpha production. Am J Physiol Cell Physiol 286: C1302-C1311.
48. Noverr, M.C., and Huffnagle, G.B. (2004) Does the microbiota regulate immune responses outside the gut? Trends Microbiol 12: 562-568.
49. O'Farrell, A.M., Liu, Y., Moore, K.W., and Mui, A.L. (1998) IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: Evidence for Stat3-dependent and -independent pathways. EMBO J 17: 1006-1018.
50. O'Mahony, L., Feeney, M., O'Halloran, S., Murphy, L., Kiely, B., Fitzgibbon, J., et al. (2001) Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knockout mice. Aliment Pharmacol Ther 15: 1219-1225.
51. Ojaniemi, M., Glumoff, V., Harju, K., Liljeroos, M., Vuori, K., and Hallman, M. (2003) Phosphatidylinositol 3-kinase is involved in Toll-like receptor 4-mediated cytokine expression in mouse macrophages. Eur J Immunol 33: 597-605.
52. Pena, J.A., and Versalovic, J. (2003) Lactobacillus rhamnosus GG decreases TNF-alpha production in lipopolysaccharide-activated murine macrophages by a contact-independent mechanism. Cell Microbiol 5: 277-285.
53. Pena, J.A., Rogers, A.B., Ge, Z., Ng, V., Li, S.Y., Fox, J.G., and Versalovic, J. (2005) Probiotic Lactobacillus spp. diminish Helicobacter hepaticus -induced inflammatory bowel disease in interleukin-10-deficient mice. Infect Immun 73: 912-920.
54. Petrof, E.O., Kojima, K., Ropeleski, M.J., Musch, M.W., Tao, Y., De Simone, C., and Chang, E.B. (2004) Probiotics inhibit nuclear factor-kappaB and induce heat shock proteins in colonic epithelial cells through proteasome inhibition. Gastroenterology 127: 1474-1487.
55. Poltorak, A., Smirnova, I., He, X., Liu, M.Y., Van Huffel, C., McNally, O., et al. (1998) Genetic and physical mapping of the Lps locus: identification of the toll-4 receptor as a candidate gene in the critical region. Blood Cells Mol Dis 24: 340-355.
56. Reid, G., and Bruce, A.W. (2001) Selection of lactobacillus strains for urogenital probiotic applications. J Infect Dis 183 (Suppl. 1): S77-S80.
57. Reid, G., McGroarty, J.A., Angotti, R., and Cook, R.L. (1988) Lactobacillus inhibitor production against Escherichia coli and coaggregation ability with uropathogens. Can J Microbiol 34: 344-351.
58. Reid, G., Sanders, M.E., Gaskins, H.R., Gibson, G.R., Mercenier, A., Rastall, R., et al. (2003) New scientific paradigms for probiotics and prebiotics. J Clin Gastroenterol 37: 105-118.
59. Reuter, G. (2001) The Lactobacillus and Bifidobacterium microflora of the human intestine: Composition and succession. Curr Issues Intest Microbiol 2: 43-53.
60. Saniabadi, A.R., Hanai, H., Takeuchi, K., Umemura, K., Nakashima, M., Adachi, T., et al. (2003) Adacolumn, an adsorptive carrier based granulocyte and monocyte apheresis device for the treatment of inflammatory and refractory diseases associated with leukocytes. Ther Apher Dial 7: 48-59.
61. Sansonetti, P.J. (2004) War and peace at mucosal surfaces. Nat Rev Immunol 4: 953-964.
62. Seabra, S.H., de Souza, W., and Damatta, R.A. (2004) Toxoplasma gondii exposes phosphatidylserine inducing a TGF-beta1 autocrine effect orchestrating macrophage evasion. Biochem Biophys Res Commun 324: 744-752.
63. Sheil, B., McCarthy, J., O'Mahony, L., Bennett, M.W., Ryan, P., Fitzgibbon, J.J., et al. (2004) Is the mucosal route of administration essential for probiotic function? Subcutaneous administration is associated with attenuation of murine colitis and arthritis. Gut 53: 694-700.
64. Shuai, K., Horvath, C.M., Huang, L.H., Qureshi, S.A., Cowburn, D., and Darnell, J.E., Jr (1994) Interferon activation of the transcription factor Stat91 involves dimerization through SH2-phosphotyrosyl peptide interactions. Cell 76: 821-828.
65. Swantek, J.L., Cobb, M.H., and Geppert, T.D. (1997) Jun N-terminal kinase/stress-activated protein kinase (JNK/SAPK) is required for lipopolysaccharide stimulation of tumor necrosis factor alpha (TNF-alpha) translation: Glucocorticoids inhibit TNF-alpha translation by blocking JNK/SAPK. Mol Cell Biol 17: 6274-6282.
66. Takeda, K., Clausen, B.E., Kaisho, T., Tsujimura, T., Terada, N., Forster, I., and Akira, S. (1999) Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 10: 39-49.
67. Tian, Z.J., and An, W. (2004) ERK1/2 contributes negative regulation to STAT3 activity in HSS-transfected HepG2 cells. Cell Res 14: 141-147.
68. Watanabe, N., Ikuta, K., Okazaki, K., Nakase, H., Tabata, Y., Matsuura, M., et al. (2003) Elimination of local macrophages in intestine prevents chronic colitis in interleukin-10-deficient mice. Dig Dis Sci 48: 408-414.
69. Welte, T., Zhang, S.S., Wang, T., Zhang, Z., Hesslein, D.G., Yin, Z., et al. (2003) STAT3 deletion during hematopoiesis causes Crohn's disease-like pathogenesis and lethality: A critical role of STAT3 in innate immunity. Proc Natl Acad Sci USA 100: 1879-1884.
70. Wierenga, A.T., Vogelzang, I., Eggen, B.J., and Vellenga, E. (2003) Erythropoietin-induced serine 727 phosphorylation of STAT3 in erythroid cells is mediated by a MEK-, ERK-, and MSK1-dependent pathway. Exp Hematol 31: 398-405.
71. Williams, L., Bradley, L., Smith, A., and Foxwell, B. (2004) Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages. J Immunol 172: 567-576.
72. Woetmann, A., Nielsen, M., Christensen, S.T., Brockdorff, J., Kaltoft, K., Engel, A.M., et al. (1999) Inhibition of protein phosphatase 2A induces serine/threonine phosphorylation, subcellular redistribution, and functional inhibition of STAT3. Proc Natl Acad Sci USA 96: 10620-10625.
73. Wohlleben, G., Trujillo, C., Muller, J., Ritze, Y., Grunewald, S., Tatsch, U., and Erb, K.J. (2004) Helminth infection modulates the development of allergen-induced airway inflammation. Int Immunol 16: 585-596.
74. Yang, J., New, L., Jiang, Y., Han, J., and Su, B. (1998) Molecular cloning and characterization of a human protein kinase that specifically activates c-Jun N-terminal kinase. Gene 212: 95-102.