Toll-like receptor 2 and class B scavenger receptor type I are required for bacterial uptake by trophoblast giant cells

Molecular Immunology

Volumn 47, Issue 11-12, 2010, Pages 1989-1996

  Watanabe, Kenta ^a   Shin, Eun Kyung ^a   Hashino, Masanori ^a   Tachibana, Masato ^a   Watarai, Masahisa ^a  

^a YAMAGUCHI UNIVERSITY   (Japan)

Author keywords

Class B scavenger receptor type I; Phagocytosis; Toll like receptor 2; Trophoblast giant cell

Indexed keywords

BACTERIAL ANTIGEN; GAMMA INTERFERON; LIPOPEPTIDE; PATTERN RECOGNITION RECEPTOR; SCAVENGER RECEPTOR; SCAVENGER RECEPTOR BI; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ARTICLE; BRUCELLA ABORTUS; CONCENTRATION RESPONSE; CONTROLLED STUDY; ESCHERICHIA COLI; GIANT CELL; IMMUNE RESPONSE; INTERNALIZATION; LISTERIA MONOCYTOGENES; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; STEM CELL; TROPHOBLAST;

ANIMALS; BACTERIA; CELLS, CULTURED; GIANT CELLS; INTERFERON-GAMMA; MICE; PHAGOCYTOSIS; SCAVENGER RECEPTORS, CLASS B; TOLL-LIKE RECEPTOR 2; TROPHOBLASTS;

BACTERIA (MICROORGANISMS);

EID: 77953620557     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2010.04.013     Document Type: Article

References (51)

1. Aderem A., Ulevitch R.J. Toll-like receptors in the induction of the innate immune response. Nature 2000, 406:782-787.
2. Akira S., Takeda K. Toll-like receptor signalling. Nat. Rev. Immunol. 2004, 4:499-511.
3. Akira S., Takeda K., Kaisho T. Toll-like receptors: critical proteins linking innate and acquired immunity. Nat. Immunol. 2001, 2:675-680.
4. Alarcon R., Fuenzalida C., Santibanez M., von Bernhardi R. Expression of scavenger receptors in glial cells. Comparing the adhesion of astrocytes and microglia from neonatal rats to surface-bound beta-amyloid. J. Biol. Chem. 2005, 280:30406-30415.
5. Albieri A., Hoshida M.S., Gagioti S.M., Leanza E.C., Abrahamsohn I., Croy A., Ashkar A.A., Bevilacqua E. Interferon-gamma alters the phagocytic activity of the mouse trophoblast. Reprod. Biol. Endocrinol. 2005, 3:34.
6. Amarante-Paffaro A., Queiroz G.S., Correa S.T., Spira B., Bevilacqua E. Phagocytosis as a potential mechanism for microbial defense of mouse placental trophoblast cells. Reproduction 2004, 128:207-218.
7. 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-kappa B activation requires a Rac1-dependent pathway. Nat. Immunol. 2000, 1:533-540.
8. Bevilacqua E., Abrahamsohn P.A. Invasiveness of mouse trophoblastic cells in connective tissue. Acta Anat. (Basel) 1994, 150:246-252.
9. Bevilacqua E.M., Abrahamsohn P.A. Ultrastructure of trophoblast giant cell transformation during the invasive stage of implantation of the mouse embryo. J. Morphol. 1988, 198:341-351.
10. Boschiroli M.L., Foulongne V., O'Callaghan D. Brucellosis: a worldwide zoonosis. Curr. Opin. Microbiol. 2001, 4:58-64.
11. Buechler C., Ritter M., Quoc C.D., Agildere A., Schmitz G. Lipopolysaccharide inhibits the expression of the scavenger receptor Cla-1 in human monocytes and macrophages. Biochem. Biophys. Res. Commun. 1999, 262:251-254.
12. Burgos P.V., Klattenhoff C., de la Fuente E., Rigotti A., Gonzalez A. Cholesterol depletion induces PKA-mediated basolateral-to-apical transcytosis of the scavenger receptor class B type I in MDCK cells. Proc. Natl. Acad. Sci. USA 2004, 101:3845-3850.
13. Campos M.A., Rosinha G.M., Almeida I.C., Salgueiro X.S., Jarvis B.W., Splitter G.A., Qureshi N., Bruna-Romero O., Gazzinelli R.T., Oliveira S.C. Role of Toll-like receptor 4 in induction of cell-mediated immunity and resistance to Brucella abortus infection in mice. Infect. Immun. 2004, 72:176-186.
14. Copin R., De Baetselier P., Carlier Y., Letesson J.J., Muraille E. MyD88-dependent activation of B220-CD11b+LY-6C+ dendritic cells during Brucella melitensis infection. J. Immunol. 2007, 178:5182-5191.
15. El Kasmi K.C., Qualls J.E., Pesce J.T., Smith A.M., Thompson R.W., Henao-Tamayo M., Basaraba R.J., Konig T., Schleicher U., Koo M.S., Kaplan G., Fitzgerald K.A., Tuomanen E.I., Orme I.M., Kanneganti T.D., Bogdan C., Wynn T.A., Murray P.J. Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat. Immunol. 2008, 9:1399-1406.
16. Faure E., Thomas L., Xu H., Medvedev A., Equils O., Arditi M. Bacterial lipopolysaccharide and IFN-gamma induce Toll-like receptor 2 and Toll-like receptor 4 expression in human endothelial cells: role of NF-kappa B activation. J. Immunol. 2001, 166:2018-2024.
17. Flo T.H., Ryan L., Latz E., Takeuchi O., Monks B.G., Lien E., Halaas O., Akira S., Skjak-Braek G., Golenbock D.T., Espevik T. Involvement of toll-like receptor (TLR) 2 and TLR4 in cell activation by mannuronic acid polymers. J. Biol. Chem. 2002, 277:35489-35495.
18. Gantner B.N., Simmons R.M., Canavera S.J., Akira S., Underhill D.M. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J. Exp. Med. 2003, 197:1107-1117.
19. Graf G.A., Matveev S.V., Smart E.J. Class B scavenger receptors, caveolae and cholesterol homeostasis. Trends Cardiovasc. Med. 1999, 9:221-225.
20. Gray M.L., Killinger A.H. Listeria monocytogenes and listeric infections. Bacteriol. Rev. 1966, 30:309-382.
21. Huang L.Y., Ishii K.J., Akira S., Aliberti J., Golding B. Th1-like cytokine induction by heat-killed Brucella abortus is dependent on triggering of TLR9. J. Immunol. 2005, 175:3964-3970.
22. Jia T., Leiner I., Dorothee G., Brandl K., Pamer E.G. MyD88 and Type I interferon receptor-mediated chemokine induction and monocyte recruitment during Listeria monocytogenes infection. J. Immunol. 2009, 183:1271-1278.
23. Kaisho T., Akira S. Regulation of dendritic cell function through Toll-like receptors. Curr. Mol. Med. 2003, 3:373-385.
24. Kawai T., Akira S. TLR signaling. Semin. Immunol. 2007, 19:24-32.
25. Kim S., Watarai M., Suzuki H., Makino S., Kodama T., Shirahata T. Lipid raft microdomains mediate class A scavenger receptor-dependent infection of Brucella abortus. Microb. Pathog. 2004, 37:11-19.
26. Krieger M. Scavenger receptor class B type I is a multiligand HDL receptor that influences diverse physiologic systems. J. Clin. Invest. 2001, 108:793-797.
27. Macedo G.C., Magnani D.M., Carvalho N.B., Bruna-Romero O., Gazzinelli R.T., Oliveira S.C. Central role of MyD88-dependent dendritic cell maturation and proinflammatory cytokine production to control Brucella abortus infection. J. Immunol. 2008, 180:1080-1087.
28. Muntener M., Hsu Y.C. Development of trophoblast and placenta of the mouse. A reinvestigation with regard to the in vitro culture of mouse trophoblast and placenta. Acta Anat. (Basel) 1977, 98:241-252.
29. Murao K., Yu X., Imachi H., Cao W.M., Chen K., Matsumoto K., Nishiuchi T., Wong N.C., Ishida T. Hyperglycemia suppresses hepatic scavenger receptor class B type I expression. Am. J. Physiol. Endocrinol. Metab. 2008, 294:E78-87.
30. Peiser L., De Winther M.P., Makepeace K., Hollinshead M., Coull P., Plested J., Kodama T., Moxon E.R., Gordon S. The class A macrophage scavenger receptor is a major pattern recognition receptor for Neisseria meningitidis which is independent of lipopolysaccharide and not required for secretory responses. Infect. Immun. 2002, 70:5346-5354.
31. Peiser L., Gough P.J., Kodama T., Gordon S. Macrophage class A scavenger receptor-mediated phagocytosis of Escherichia coli: role of cell heterogeneity, microbial strain, and culture conditions in vitro. Infect. Immun. 2000, 68:1953-1963.
32. Philips J.A., Rubin E.J., Perrimon N. Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 2005, 309:1251-1253.
33. Poltorak A., He X., Smirnova I., Liu M.Y., Van Huffel C., Du X., Birdwell D., Alejos E., Silva M., Galanos C., Freudenberg M., Ricciardi-Castagnoli P., Layton B., Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 1998, 282:2085-2088.
34. Ribes S., Ebert S., Czesnik D., Regen T., Zeug A., Bukowski S., Mildner A., Eiffert H., Hanisch U.K., Hammerschmidt S., Nau R. Toll-like receptor prestimulation increases phagocytosis of Escherichia coli DH5alpha and Escherichia coli K1 strains by murine microglial cells. Infect. Immun. 2009, 77:557-564.
35. Rigotti A., Miettinen H.E., Krieger M. The role of the high-density lipoprotein receptor SR-BI in the lipid metabolism of endocrine and other tissues. Endocr. Rev. 2003, 24:357-387.
36. Rigotti A., Trigatti B., Babitt J., Penman M., Xu S., Krieger M. Scavenger receptor BI-a cell surface receptor for high density lipoprotein. Curr. Opin. Lipidol. 1997, 8:181-188.
37. Seki E., Tsutsui H., Tsuji N.M., Hayashi N., Adachi K., Nakano H., Futatsugi-Yumikura S., Takeuchi O., Hoshino K., Akira S., Fujimoto J., Nakanishi K. Critical roles of myeloid differentiation factor 88-dependent proinflammatory cytokine release in early phase clearance of Listeria monocytogenes in mice. J. Immunol. 2002, 169:3863-3868.
38. Seveau S., Bierne H., Giroux S., Prevost M.C., Cossart P. Role of lipid rafts in E-cadherin and HGF-R/Met mediated entry of Listeria monocytogenes into host cells. J. Cell Biol. 2004, 166:743-753.
39. Soong G., Reddy B., Sokol S., Adamo R., Prince A. TLR2 is mobilized into an apical lipid raft receptor complex to signal infection in airway epithelial cells. J. Clin. Invest. 2004, 113:1482-1489.
40. Stuart E.S., Webley W.C., Norkin L.C. Lipid rafts, caveolae, caveolin-1, and entry by Chlamydiae into host cells. Exp. Cell Res. 2003, 287:67-78.
41. Takeuchi O., Hoshino K., Kawai T., Sanjo H., Takada H., Ogawa T., Takeda K., Akira S. Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components. Immunity 1999, 11:443-451.
42. Torres D., Barrier M., Bihl F., Quesniaux V.J., Maillet I., Akira S., Ryffel B., Erard F. Toll-like receptor 2 is required for optimal control of Listeria monocytogenes infection. Infect. Immun. 2004, 72:2131-2139.
43. Triantafilou M., Manukyan M., Mackie A., Morath S., Hartung T., Heine H., Triantafilou K. Lipoteichoic acid and toll-like receptor 2 internalization and targeting to the Golgi are lipid raft-dependent. J. Biol. Chem. 2004, 279:40882-40889.
44. Underhill D.M., Ozinsky A. Phagocytosis of microbes: complexity in action. Annu. Rev. Immunol. 2002, 20:825-852.
45. Underhill D.M., Ozinsky A., Hajjar A.M., Stevens A., Wilson C.B., Bassetti M., Aderem A. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 1999, 401:811-815.
46. Vishnyakova T.G., Kurlander R., Bocharov A.V., Baranova I.N., Chen Z., Abu-Asab M.S., Tsokos M., Malide D., Basso F., Remaley A., Csako G., Eggerman T.L., Patterson A.P. CLA-1 and its splicing variant CLA-2 mediate bacterial adhesion and cytosolic bacterial invasion in mammalian cells. Proc. Natl. Acad. Sci. USA 2006, 103:16888-16893.
47. Watanabe K., Tachibana M., Kim S., Watarai M. Participation of ezrin in bacterial uptake by trophoblast giant cells. Reprod. Biol. Endocrinol. 2009, 7:95.
48. Watanabe K., Tachibana M., Tanaka S., Furuoka H., Horiuchi M., Suzuki H., Watarai M. Heat shock cognate protein 70 contributes to Brucella invasion into trophoblast giant cells that cause infectious abortion. BMC Microbiol. 2008, 8:212.
49. Watarai M., Makino S., Fujii Y., Okamoto K., Shirahata T. Modulation of Brucella-induced macropinocytosis by lipid rafts mediates intracellular replication. Cell Microbiol. 2002, 4:341-355.
50. Weiss D.S., Takeda K., Akira S., Zychlinsky A., Moreno E. MyD88, but not toll-like receptors 4 and 2, is required for efficient clearance of Brucella abortus. Infect. Immun. 2005, 73:5137-5143.
51. Welsh A.O., Enders A.C. Trophoblast-decidual cell interactions and establishment of maternal blood circulation in the parietal yolk sac placenta of the rat. Anat. Rec. 1987, 217:203-219.