TLR-dependent phagosome tubulation in dendritic cells promotes phagosome cross-talk to optimize MHC-II antigen presentation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 43, 2014, Pages 15508-15513

  Mantegazza, Adriana R ^a,b   Zajac, Allison L ^b,c   Twelvetrees, Alison ^b   Holzbaur, Erika L F ^b   Amigorena, Sebastián ^d,e   Marks, Michael S ^a,b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b Department of Physiology ^*  (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d INSTITUT CURIE   (France)

^e PSL RESEARCH UNIVERSITY   (France)

Author keywords

Inflammation; Major histocompatibility complex; Microtubules; Phagocytosis; Toll like receptors

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; ACTIN; HLA ANTIGEN CLASS 2; LIPOPOLYSACCHARIDE; PEPTIDE; TLR4 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; CELL MATURATION; CELL MEMBRANE; CELL STIMULATION; COMPLEX FORMATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; INTRACELLULAR TRANSPORT; LYSOSOME; MALE; MICROTUBULE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHAGOLYSOSOME; PHAGOSOME; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; IMMUNOLOGY; METABOLISM;

ACTINS; ANIMALS; ANTIGEN PRESENTATION; DENDRITIC CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS II; LIPOPOLYSACCHARIDES; LYSOSOMES; MICE, INBRED C57BL; MICROTUBULES; MYELOID DIFFERENTIATION FACTOR 88; PEPTIDES; PHAGOSOMES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS;

EID: 84908584320     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1412998111     Document Type: Article

References (41)

1. Fairn GD, Grinstein S (2012) How nascent phagosomes mature to become phagolysosomes. Trends Immunol 33(8):397-405.
2. Kagan JC, Iwasaki A (2012) Phagosome as the organelle linking innate and adaptive immunity. Traffic 13(8):1053-1061.
3. Mantegazza AR, Magalhaes JG, Amigorena S, Marks MS (2013) Presentation of phagocytosed antigens by MHC class I and II. Traffic 14(2):135-152.
4. Watts C, West MA, Zaru R (2010) TLR signalling regulated antigen presentation in dendritic cells. Curr Opin Immunol 22(1):124-130.
5. Boes M, et al. (2002) T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 418(6901):983-988.
6. Boes M, et al. (2003) T cells induce extended class II MHC compartments in dendritic cells in a Toll-like receptor-dependent manner. J Immunol 171(8):4081-4088.
7. Chow A, Toomre D, Garrett W, Mellman I (2002) Dendritic cell maturation triggers retrograde MHC class II transport from lysosomes to the plasma membrane. Nature 418(6901):988-994.
8. Barton GM, Kagan JC (2009) A cell biological view of Toll-like receptor function: Regulation through compartmentalization. Nat Rev Immunol 9(8):535-542.
9. Takeda K, Akira S (2004) TLR signaling pathways. Semin Immunol 16(1):3-9.
10. Husebye H, et al. (2010) The Rab11a GTPase controls Toll-like receptor 4-induced activation of interferon regulatory factor-3 on phagosomes. Immunity 33(4):583-596.
11. Mantegazza AR, et al. (2012) Adaptor protein-3 in dendritic cells facilitates phagosomal Toll-like receptor signaling and antigen presentation to CD4(+) T cells. Immunity 36(5):782-794.
12. Underhill DM, et al. (1999) The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401(6755):811-815.
13. Wolf AJ, et al. (2011) Phagosomal degradation increases TLR access to bacterial ligands and enhances macrophage sensitivity to bacteria. J Immunol 187(11): 6002-6010.
14. Blander JM, Medzhitov R (2004) Regulation of phagosome maturation by signals from Toll-like receptors. Science 304(5673):1014-1018.
15. Blander JM, Medzhitov R (2006) Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 440(7085):808-812.
16. Hoffmann E, et al. (2012) Autonomous phagosomal degradation and antigen presentation in dendritic cells. Proc Natl Acad Sci USA 109(36):14556-14561.
17. Blander JM (2007) Coupling Toll-like receptor signaling with phagocytosis: Potentiation of antigen presentation. Trends Immunol 28(1):19-25.
18. Kleijmeer M, et al. (2001) Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J Cell Biol 155(1):53-63.
19. Pierre P, et al. (1997) Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 388(6644):787-792.
20. Turley SJ, et al. (2000) Transport of peptide-MHC class II complexes in developing dendritic cells. Science 288(5465):522-527.
21. Harrison RE, Bucci C, Vieira OV, Schroer TA, Grinstein S (2003) Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: Role of Rab7 and RILP. Mol Cell Biol 23(18):6494-6506.
22. Chen D, et al. (2010) Retromer is required for apoptotic cell clearance by phagocytic receptor recycling. Science 327(5970):1261-1264.
23. Damiani MT, Colombo MI (2003) Microfilaments and microtubules regulate recycling from phagosomes. Exp Cell Res 289(1):152-161.
24. Jancic C, et al. (2007) Rab27a regulates phagosomal pH and NADPH oxidase recruitment to dendritic cell phagosomes. Nat Cell Biol 9(4):367-378.
25. Dunne A, et al. (2010) IRAK1 and IRAK4 promote phosphorylation, ubiquitination, and degradation of MyD88 adaptor-like (Mal). J Biol Chem 285(24):18276-18282.
26. Clark K, Plater L, Peggie M, Cohen P (2009) Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IkappaB kinase epsilon: A distinct upstream kinase mediates Ser-172 phosphorylation and activation. J Biol Chem 284(21):14136-14146.
27. Florey O, Overholtzer M (2012) Autophagy proteins in macroendocytic engulfment. Trends Cell Biol 22(7):374-380.
28. Sanjuan MA, et al. (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450(7173):1253-1257.
29. Klionsky DJ, et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8(4):445-544.
30. Lee HK, et al. (2010) In vivo requirement for Atg5 in antigen presentation by dendritic cells. Immunity 32(2):227-239.
31. Hollenbeck PJ, Swanson JA (1990) Radial extension of macrophage tubular lysosomes supported by kinesin. Nature 346(6287):864-866.
32. Mrakovic A, Kay JG, Furuya W, Brumell JH, Botelho RJ (2012) Rab7 and Arl8 GTPases are necessary for lysosome tubulation in macrophages. Traffic 13(12):1667-1679.
33. Blocker A, Griffiths G, Olivo JC, Hyman AA, Severin FF (1998) A role for microtubule dynamics in phagosome movement. J Cell Sci 111(Pt 3):303-312.
34. Desjardins M, Huber LA, Parton RG, Griffiths G (1994) Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J Cell Biol 124(5):677-688.
35. Rudensky AYu, Rath S, Preston-Hurlburt P, Murphy DB, Janeway CA, Jr (1991) On the complexity of self. Nature 353(6345):660-662.
36. Axelrod D (1981) Cell-substrate contacts illuminated by total internal reflection fluorescence. J Cell Biol 89(1):141-145.
37. Duclos S, Corsini R, Desjardins M (2003) Remodeling of endosomes during lysosome biogenesis involves "kiss and run" fusion events regulated by rab5. J Cell Sci 116(Pt 5): 907-918.
38. Wubbolts R, et al. (1996) Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J Cell Biol 135(3):611-622.
39. Underhill DM, Goodridge HS (2012) Information processing during phagocytosis. Nat Rev Immunol 12(7):492-502.
40. Harding CV, Geuze HJ (1992) Class II MHC molecules are present in macrophage lysosomes and phagolysosomes that function in the phagocytic processing of Listeria monocytogenes for presentation to T cells. J Cell Biol 119(3):531-542.
41. Racoosin EL, Swanson JA (1993) Macropinosome maturation and fusion with tubular lysosomes in macrophages. J Cell Biol 121(5):1011-1020.