Wnt5a-Rac1-NF-κB homeostatic circuitry sustains innate immune functions in macrophages

Journal of Immunology

Volumn 192, Issue 9, 2014, Pages 4386-4397

  Naskar, Debdut ^a   Maiti, George ^a   Chakraborty, Arijit ^a   Roy, Arunava ^b   Chattopadhyay, Dhrubajyoti ^b   Sen, Malini ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

^b UNIVERSITY OF CALCUTTA   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; GROWTH FACTOR RECEPTOR; INTERFERON; PROTEIN FZ5; RAC1 PROTEIN; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; WNT5A PROTEIN;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; BACTERIAL IMMUNITY; CELL SURVIVAL; CHANDIPURA VIRUS; CONTROLLED STUDY; ESCHERICHIA COLI; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNOMODULATION; IN VITRO STUDY; INNATE IMMUNITY; MACROPHAGE FUNCTION; MOUSE; NONHUMAN; PARACRINE SIGNALING; PERITONEUM MACROPHAGE; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VIRUS; VIRUS IMMUNITY;

ANIMALS; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; NEUROPEPTIDES; NF-KAPPA B; RAC1 GTP-BINDING PROTEIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION; WNT PROTEINS;

EID: 84899548231     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302817     Document Type: Article

References (64)

1. Janeway, C. A., Jr., and R. Medzhitov. 2002. Innate immune recognition. Annu. Rev. Immunol. 20: 197-216
2. Twigg, H. L., III. 2004. Macrophages in innate and acquired immunity. Semin. Respir. Crit. Care Med. 25: 21-31
3. Gordon, S. B., and R. C. Read. 2002. Macrophage defences against respiratory tract infections. Br. Med. Bull. 61: 45-61
4. Pugin, J., I. D. Heumann, A. Tomasz, V. V. Kravchenko, Y. Akamatsu, M. Nishijima, M. P. Glauser, P. S. Tobias, and R. J. Ulevitch. 1994. CD14 is a pattern recognition receptor. Immunity 1: 509-516
5. Schiff, D. E., L. Kline, K. Soldau, J. D. Lee, J. Pugin, P. S. Tobias, and R. J. Ulevitch. 1997. Phagocytosis of gram-negative bacteria by a unique CD14-dependent mechanism. J. Leukoc. Biol. 62: 786-794
6. Ghosh, S., M. J. May, and E. B. Kopp. 1998. NF-kappa B and Rel proteins: Evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16: 225-260
7. Baldwin, A. S., Jr. 1996. The NF-k B and I k B proteins: New discoveries and insights. Annu. Rev. Immunol. 14: 649-683
8. Hoffmann, A., and D. Baltimore. 2006. Circuitry of nuclear factor kappaB signaling. Immunol. Rev. 210: 171-186
9. Maiti, G., D. Naskar, and M. Sen. 2012. The Wingless homolog Wnt5a stimulates phagocytosis but not bacterial killing. Proc. Natl. Acad. Sci. USA 109: 16600-16605
10. Pereira, C., D. J. Schaer, E. B. Bachli, M. O. Kurrer, and G. Schoedon. 2008. Wnt5A/CaMKII signaling contributes to the inflammatory response of macrophages and is a target for the antiinflammatory action of activated protein C and interleukin-10. Arterioscler. Thromb. Vasc. Biol. 28: 504-510
11. Blumenthal, A., S. Ehlers, J. Lauber, J. Buer, C. Lange, T. Goldmann, H. Heine, E. Brandt, and N. Reiling. 2006. The Wingless homolog WNT5A and its receptor Frizzled-5 regulate inflammatory responses of human mononuclear cells induced by microbial stimulation. Blood 108: 965-973
12. Cadigan, K. M., and R. Nusse. 1997. Wnt signaling: A common theme in animal development. Genes Dev. 11: 3286-3305
13. Logan, C. Y., and R. Nusse. 2004. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20: 781-810
14. Liu, X., T. Liu, D. C. Slusarski, J. Yang-Snyder, C. C. Malbon, R. T. Moon, and H. Wang. 1999. Activation of a frizzled-2/b-adrenergic receptor chimera promotes Wnt signaling and differentiation of mouse F9 teratocarcinoma cells via Galphao and Galphat. Proc. Natl. Acad. Sci. USA 96: 14383-14388
15. Schulte, G., and V. Bryja. 2007. The Frizzled family of unconventional Gprotein-coupled receptors. Trends Pharmacol. Sci. 28: 518-525
16. Kuhl, M., L. C. Sheldahl, M. Park, J. R. Miller, and R. T. Moon. 2000. The Wnt/ Ca2+ pathway: A new vertebrate Wnt signaling pathway takes shape. Trends Genet. 16: 279-283
17. Veeman, M. T., J. D. Axelrod, and R. T. Moon. 2003. A second canon. Functions and mechanisms of b-catenin-independent Wnt signaling. Dev. Cell 5: 367-377
18. Mikels, A. J., and R. Nusse. 2006. Purified Wnt5a protein activates or inhibits b-catenin-TCF signaling depending on receptor context. PLoS Biol. 4.4: E115
19. Slusarski, D. C., V. G. Corces, and R. T. Moon. 1997. Interaction of Wnt and a Frizzled homologue triggers G-protein-linked phosphatidylinositol signalling. Nature 390: 410-413
20. He, X., J. P. Saint-Jeannet, Y. Wang, J. Nathans, I. Dawid, and H. Varmus. 1997. A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 275: 1652-1654
21. Minami, Y., I. Oishi, M. Endo, and M. Nishita. 2010. Ror-family receptor tyrosine kinases in noncanonical Wnt signaling: Their implications in developmental morphogenesis and human diseases. Dev. Dyn. 239: 1-15
22. Chen, W., D. ten Berge, J. Brown, S. Ahn, L. A. Hu, W. E. Miller, M. G. Caron, L. S. Barak, R. Nusse, and R. J. Lefkowitz. 2003. Dishevelled 2 recruits betaarrestin 2 to mediate Wnt5A-stimulated endocytosis of Frizzled 4. Science 301: 1391-1394
23. Ishida-Takagishi, M., A. Enomoto, N. Asai, K. Ushida, T. Watanabe, T. Hashimoto, T. Kato, L. Weng, S. Matsumoto, M. Asai, et al. 2012. The Dishevelled-associating protein Daple controls the non-canonical Wnt/Rac pathway and cell motility. Nat. Commun. 3: 859
24. Gon, H., K. Fumoto, Y. Ku, S. Matsumoto, and A. Kikuchi. 2013. Wnt5a signaling promotes apical and basolateral polarization of single epithelial cells. Mol. Biol. Cell. 24: 3764-3774
25. Wang, Q., A. J. Symes, C. A. Kane, A. Freeman, J. Nariculam, P. Munson, C. Thrasivoulou, J. R. W. Masters, and A. Ahmed. 2010. A novel role for Wnt/ Ca2+ signaling in actin cytoskeleton remodeling and cell motility in prostate cancer. PLoS ONE 5: E10456
26. Weeraratna, A. T., Y. Jiang, G. Hostetter, K. Rosenblatt, P. Duray, M. Bittner, and J. M. Trent. 2002. Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 1: 279-288
27. Sato, A., H. Yamamoto, H. Sakane, H. Koyama, and A. Kikuchi. 2010. Wnt5a regulates distinct signalling pathways by binding to Frizzled2. EMBO J. 29: 41-54
28. Sen, M. 2005. Wnt signalling in rheumatoid arthritis. Rheumatology (Oxford) 44: 708-713
29. Sen, M., M. Chamorro, J. Reifert, M. Corr, and D. A. Carson. 2001. Blockade of Wnt-5A/frizzled 5 signaling inhibits rheumatoid synoviocyte activation. Arthritis Rheum. 44: 772-781
30. Murphy, L. L. S., and C. C. W. Hughes. 2002. Endothelial cells stimulate T cell NFAT nuclear translocation in the presence of cyclosporin A: Involvement of the wnt/glycogen synthase kinase-3 b pathway. J. Immunol. 169: 3717-3725
31. Kim, J., J. Kim, D. W. Kim, Y. Ha, M. H. Ihm, H. Kim, K. Song, and I. Lee. 2010. Wnt5a induces endothelial inflammation via b-catenin-independent signaling. J. Immunol. 185: 1274-1282
32. Frankenberger, M., A. Pforte, T. Sternsdorf, B. Passlick, P. A. Baeuerle, and H. W. L. Ziegler-Heitbrock. 1994. Constitutive nuclear NF-kappa B in cells of the monocyte lineage. Biochem. J. 304: 87-94
33. Liu, J., D. Yang, Y. Minemoto, M. Leitges, M. R. Rosner, and A. Lin. 2006. NFkappaB is required for UV-induced JNK activation via induction of PKCdelta. Mol. Cell 21: 467-480
34. Marim, F. M., T. N. Silveira, D. S. Lima, Jr., and D. S. Zamboni. 2010. A method for generation of bone marrow-derived macrophages from cryopreserved mouse bone marrow cells. PLoS ONE 5: E15263
35. Zhang, X., R. Goncalves, and D. M. Mosser. 2008. The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. Chapter 14: Unit 14.1
36. Ghisletti, S., C. Meda, A. Maggi, and E. Vegeto. 2005. 17beta estradiol inhibits inflammatory gene expression by controlling NF-kappaB intracellular localization. Mol. Cell. Biol. 25: 2957-2968
37. Roy, A., M. Mukherjee, S. Mukhopadhyay, S. S. Maity, S. Ghosh, and D. Chattopadhyay. 2013. Characterization of the Chandipura virus leader RNAphosphoprotein interaction using single tryptophan mutants and its detection in viral infected cells. Biochimie 95: 180-194
38. Kumar, S. and V. A. Arankalle. 2010. Intracranial administration of P gene siRNA protects mice from lethal Chandipura virus encephalitis. PLos ONE 5: E8615
39. Randall, R. E., and S. Goodbourn. 2008. Interferons and viruses: An interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89: 1-47
40. Schafer, S. L., R. Lin, P. A. Moore, J. Hiscott, and P. M. Pitha. 1998. Regulation of type I interferon gene expression by interferon regulatory factor-3. J. Biol. Chem. 273: 2714-2720
41. Boehm, U., T. Klamp, M. Groot, and J. C. Howard. 1997. Cellular responses to interferon-g. Annu. Rev. Immunol. 15: 749-795
42. Sica, A., L. Dorman, V. Viggiano, M. Cippitelli, P. Ghosh, N. Rice, and H. A. Young. 1997. Interaction of NF-kappaB and NFAT with the interferon-g promoter. J. Biol. Chem. 272: 30412-30420
43. Katoh, M., and M. Katoh. 2009. Transcriptional mechanisms of WNT5A based on NF-kappaB, Hedgehog, TGFbeta, and Notch signaling cascades. Int. J. Mol. Med. 23: 763-769
44. Chen, B., M. E. Dodge, W. Tang, J. Lu, Z. Ma, C. W. Fan, S. Wei, W. Hao, J. Kilgore, N. S. Williams, et al. 2009. Small molecule-mediated disruption of Wnt-dependent signaling in tissue regeneration and cancer. Nat. Chem. Biol. 5: 100-107
45. Chen, Q., R. Takada, and S. Takada. 2012. Loss of Porcupine impairs convergent extension during gastrulation in zebrafish. J. Cell Sci. 125: 2224-2234
46. Janot, L., T. Secher, D. Torres, I. Maillet, J. Pfeilschifter, V. F. J. Quesniaux, R. Landmann, B. Ryffel, and F. Erard. 2008. CD14 works with toll-like receptor 2 to contribute to recognition and control of Listeria monocytogenes infection. J. Infect. Dis. 198: 115-124
47. Wennerås, C., P. Ave, M. Huerre, J. Arondel, R. Ulevitch, J. Mathison, and P. Sansonetti. 2001. Blockade of CD14 aggravates experimental shigellosis. J. Endotoxin Res. 7: 442-446
48. Bernheiden, M., J. M. Heinrich, G. Minigo, C. Schutt, F. Stelter, M. Freeman, D. Golenbock, and R. S. Jack. 2001. LBP, CD14, TLR4 and the murine innate immune response to a peritoneal Salmonella infection. J. Endotoxin Res. 7: 447-450
49. Baumann, C. L., I. M. Aspalter, O. Sharif, A. Pichlmair, S. Bluml, F. Grebien, M. Bruckner, P. Pasierbek, K. Aumayr, M. Planyavsky, et al. 2010. CD14 is a coreceptor of Toll-like receptors 7 and 9. J. Exp. Med. 207: 2689-2701
50. Elson, G., I. Dunn-Siegrist, B. Daubeuf, and J. Pugin. 2007. Contribution of Tolllike receptors to the innate immune response to Gram-negative and Grampositive bacteria. Blood 109: 1574-1583
51. Zanoni, I., R. Ostuni, L. R. Marek, S. Barresi, R. Barbalat, G. M. Barton, F. Granucci, and J. C. Kagan. 2011. CD14 controls the LPS-induced endocytosis of Toll-like receptor 4. Cell 147: 868-880
52. Podolin, P. L., J. F. Callahan, B. J. Bolognese, Y. H. Li, K. Carlson, T. G. Davis, G. W. Mellor, C. EVans, and A. K. Roshak. 2005. Attenuation of murine collagen-induced arthritis by a novel, potent, selective small molecule inhibitor of IkappaB Kinase 2, TPCA-1 (2-[(aminocarbonyl)amino]-5-(4- fluorophenyl)-3-thiophenecarboxamide), occurs via reduction of proinflammatory cytokines and antigen-induced T cell Proliferation. J. Pharmacol. Exp. Ther. 312: 373-381
53. Yang, F., E. Tang, K. Guan, and C. Y. Wang. 2003. IKK b plays an essential role in the phosphorylation of RelA/p65 on serine 536 induced by lipopolysaccharide. J. Immunol. 170: 5630-5635
54. Dwivedi, S., D. Pandey, A. L. Khandoga, R. Brandl, and W. Siess. 2010. Rac1-mediated signaling plays a central role in secretion-dependent platelet aggregation in human blood stimulated by atherosclerotic plaque. J. Transl. Med. 8: 128
55. Gao, Y., J. B. Dickerson, F. Guo, J. Zheng, and Y. Zheng. 2004. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc. Natl. Acad. Sci. USA 101: 7618-7623
56. Kurt-Jones, E. A., L. Popova, L. Kwinn, L. M. Haynes, L. P. Jones, R. A. Tripp, E. E. Walsh, M. W. Freeman, D. T. Golenbock, L. J. Anderson, and R. W. Finberg. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1: 398-401
57. Jiang, Z., P. Georgel, X. Du, L. Shamel, S. Sovath, S. Mudd, M. Huber, C. Kalis, S. Keck, C. Galanos, M. Freudenberg, and B. Beutler. 2005. CD14 is required for MyD88-independent LPS signaling. Nat. Immunol. 6: 565-570
58. Anukumar, B., and P. Shahir. 2012. Chandipura virus infection in mice: The role of toll like receptor 4 in pathogenesis. BMC Infect. Dis. 12: 125
59. Basak, S., A. Mondal, S. Polley, S. Mukhopadhyay, and D. Chattopadhyay. 2007. Reviewing Chandipura: A vesiculovirus in human epidemics. Biosci. Rep. 27: 275-298
60. Anas, A., T.Van Der Poll, and A.F. De Vos. 2010. Role of CD14 in lung inflammation and infection. Crit. Care. 142: 209
61. Haziot, A., E. Ferrero, F. Köntgen, N. Hijiya, S. Yamamoto, J. Silver, C. L. Stewart, and S. M. Goyert. 1996. Resistance to endotoxin shock and reduced dissemination of gram-negative bacteria in CD14-deficient mice. Immunity 4: 407-414
62. Joseph, S. B., M. N. Bradley, A. Castrillo, K. W. Bruhn, P. A. Mak, L. Pei, J. Hogenesch, R. M. O?connell, G. Cheng, E. Saez, et al. 2004. LXR-dependent gene expression is important for macrophage survival and the innate immune response. Cell 119: 299-309
63. Mathes, E., E. L. O?Dea, A. Hoffmann, and G. Ghosh. 2008. NF-kappaB dictates the degradation pathway of IkappaBalpha. EMBO J. 27: 1357-1367
64. O?Dea, E. L., D. Barken, R. Q. Peralta, K. T. Tran, S. L. Werner, J. D. Kearns, A. Levchenko, and A. Hoffmann. 2007. A homeostatic model of IkappaB metabolism to control constitutive NF-kappaB activity. Mol. Syst. Biol. 3: 111