Autophagy-related protein Vps34 controls the homeostasis and function of antigen cross-presenting CD8α+ dendritic cells

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

Volumn 114, Issue 31, 2017, Pages E6371-E6380

  Parekh, Vrajesh V ^a,e   Pabbisetty, Sudheer K ^a   Wu, Lan ^a   Sebzda, Eric ^a   Martinez, Jennifer ^b   Zhang, Jianhua ^c,d   Van Kaer, Luc ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c University of Alabama at Birmingham   (United States)

^d BIRMINGHAM VA MEDICAL CENTER   (United States)

^e PFIZER INC   (United States)

Author keywords

Antigen presentation; Cross presentation; Dendritic cells; MHC class I; Vps34

Indexed keywords

AUTOPHAGY RELATED PROTEIN; CD103 ANTIGEN; CD11B ANTIGEN; CD8 ANTIGEN; GLYCOPROTEIN P 15095; IMMUNOGLOBULIN; INTERLEUKIN 10; INTERLEUKIN 6; LIGHT CHAIN 3; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MUCIN 4; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN; TIM 4 RECEPTOR; TOLL LIKE RECEPTOR; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; CD8ALPHA ANTIGEN; CYTOKINE; HLA ANTIGEN CLASS 1; MEMBRANE PROTEIN; TIM-4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; APOPTOSIS; ARTICLE; AUTOPHAGY; CADAVER; CELL FUNCTION; CLINICAL ASSESSMENT; CONTROLLED STUDY; CROSS PRESENTATION; CYTOKINE PRODUCTION; DENDRITIC CELL; GENETIC ASSOCIATION; LUNG METASTASIS; MELANOMA CELL; MOUSE; NONHUMAN; PHAGOCYTOSIS; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; REGULATORY MECHANISM; T LYMPHOCYTE; ANIMAL; BIOSYNTHESIS; CD8+ T LYMPHOCYTE; CELL CULTURE; ENDOCYTOSIS; EXPERIMENTAL MELANOMA; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; ANTIGEN PRESENTATION; AUTOPHAGY; AUTOPHAGY-RELATED PROTEINS; CD8 ANTIGENS; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CLASS III PHOSPHATIDYLINOSITOL 3-KINASES; CROSS-PRIMING; CYTOKINES; DENDRITIC CELLS; ENDOCYTOSIS; HISTOCOMPATIBILITY ANTIGENS CLASS I; MELANOMA, EXPERIMENTAL; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; PHAGOCYTOSIS;

EID: 85026645019     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1706504114     Document Type: Article

References (48)

1. Vyas JM, Van der Veen AG, Ploegh HL (2008) The known unknowns of antigen processing and presentation. Nat Rev Immunol 8:607–618.
2. Cresswell P, Ackerman AL, Giodini A, Peaper DR, Wearsch PA (2005) Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunol Rev 207: 145–157.
3. Bevan MJ (2006) Cross-priming. Nat Immunol 7:363–365.
4. Romao S, Gannage M, Münz C (2013) Checking the garbage bin for problems in the house, or how autophagy assists in antigen presentation to the immune system. Semin Cancer Biol 23:391–396.
5. Yang Z, Klionsky DJ (2010) Mammalian autophagy: Core molecular machinery and signaling regulation. Curr Opin Cell Biol 22:124–131.
6. Mizushima N (2007) Autophagy: Process and function. Genes Dev 21:2861–2873.
7. Yorimitsu T, Klionsky DJ (2005) Autophagy: Molecular machinery for self-eating. Cell Death Differ 12:1542–1552.
8. Nikoletopoulou V, Papandreou ME, Tavernarakis N (2015) Autophagy in the physiology and pathology of the central nervous system. Cell Death Differ 22:398–407.
9. Funderburk SF, Wang QJ, Yue Z (2010) The Beclin 1-VPS34 complex–At the crossroads of autophagy and beyond. Trends Cell Biol 20:355–362.
10. Backer JM (2008) The regulation and function of class III PI3Ks: Novel roles for Vps34. Biochem J 410:1–17.
11. Parekh VV, et al. (2013) Impaired autophagy, defective T cell homeostasis, and a wasting syndrome in mice with a T cell-specific deletion of Vps34. J Immunol 190: 5086–5101.
12. Willinger T, Flavell RA (2012) Canonical autophagy dependent on the class III phosphoinositide-3 kinase Vps34 is required for naive T-cell homeostasis. Proc Natl Acad Sci USA 109:8670–8675.
13. Jaber N, et al. (2012) Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function. Proc Natl Acad Sci USA 109:2003–2008.
14. Zhou X, et al. (2010) Deletion of PIK3C3/Vps34 in sensory neurons causes rapid neu-rodegeneration by disrupting the endosomal but not the autophagic pathway. Proc Natl Acad Sci USA 107:9424–9429.
15. Kihara A, Noda T, Ishihara N, Ohsumi Y (2001) Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharo-myces cerevisiae. J Cell Biol 152:519–530.
16. Edelson BT, et al. (2010) Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J Exp Med 207:823–836.
17. Sung SS, et al. (2006) A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J Immunol 176:2161–2172.
18. Naik SH, et al. (2005) Cutting edge: Generation of splenic CD8+ and CD8- dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J Immunol 174:6592–6597.
19. Pittini Á, Casaravilla C, Allen JE, Díaz Á (2016) Pharmacological inhibition of PI3K class III enhances the production of pro- and anti-inflammatory cytokines in dendritic cells stimulated by TLR agonists. Int Immunopharmacol 36:213–217.
20. den Haan JM, Lehar SM, Bevan MJ (2000) CD8(+) but not CD8(-) dendritic cells cross-prime cytotoxic T cells in vivo. J Exp Med 192:1685–1696.
21. Ravichandran KS, Lorenz U (2007) Engulfment of apoptotic cells: Signals for a good meal. Nat Rev Immunol 7:964–974.
22. Miyanishi M, et al. (2007) Identification of Tim4 as a phosphatidylserine receptor. Nature 450:435–439.
23. Smyth Templeton NE (2015) Gene Therapy and Cell Therapy (CRC, Boca Raton, FL).
24. Shen Z, Reznikoff G, Dranoff G, Rock KL (1997) Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules. J Immunol 158:2723–2730.
25. Boyle KB, Randow F (2015) Rubicon swaps autophagy for LAP. Nat Cell Biol 17: 843–845.
26. Martinez J, et al. (2015) Molecular characterization of LC3-associated phagocytosis reveals distinct roles for Rubicon, NOX2 and autophagy proteins. Nat Cell Biol 17:893–906.
27. Hildner K, et al. (2008) Batf3 deficiency reveals a critical role for CD8alpha+ dendritic cells in cytotoxic T cell immunity. Science 322:1097–1100.
28. Headley MB, et al. (2016) Visualization of immediate immune responses to pioneer metastatic cells in the lung. Nature 531:513–517.
29. Ostrand-Rosenberg S, Sinha P (2009) Myeloid-derived suppressor cells: Linking inflammation and cancer. J Immunol 182:4499–4506.
30. Backer JM (2016) The intricate regulation and complex functions of the class III phosphoinositide 3-kinase Vps34. Biochem J 473:2251–2271.
31. Mehta P, Henault J, Kolbeck R, Sanjuan MA (2014) Noncanonical autophagy: One small step for LC3, one giant leap for immunity. Curr Opin Immunol 26:69–75.
32. Münz C (2015) Of LAP, CUPS, and DRibbles - unconventional use of autophagy proteins for MHC restricted antigen presentation. Front Immunol 6:200.
33. Sanjuan MA, et al. (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450:1253–1257.
34. Martinez J, et al. (2011) Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells. Proc Natl Acad Sci USA 108:17396–17401.
35. Roche PA, Furuta K (2015) The ins and outs of MHC class II-mediated antigen processing and presentation. Nat Rev Immunol 15:203–216.
36. Schmid D, Pypaert M, Münz C (2007) Antigen-loading compartments for major his-tocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity 26:79–92.
37. Choi AM, Ryter SW, Levine B (2013) Autophagy in human health and disease. N Engl J Med 368:1845–1846.
38. Ronan B, et al. (2014) A highly potent and selective Vps34 inhibitor alters vesicle trafficking and autophagy. Nat Chem Biol 10:1013–1019.
39. Van Kaer L, Ashton-Rickardt PG, Ploegh HL, Tonegawa S (1992) TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-8+ T cells. Cell 71:1205–1214.
40. Lee HK, et al. (2010) In vivo requirement for Atg5 in antigen presentation by dendritic cells. Immunity 32:227–239.
41. Lutz MB, et al. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223:77–92.
42. Yan J, et al. (2006) In vivo role of ER-associated peptidase activity in tailoring peptides for presentation by MHC class Ia and class Ib molecules. J Exp Med 203:647–659.
43. Brasel K, De Smedt T, Smith JL, Maliszewski CR (2000) Generation of murine dendritic cells from flt3-ligand-supplemented bone marrow cultures. Blood 96:3029–3039.
44. Lorenzi S, et al. (2011) Type I IFNs control antigen retention and survival of CD8α(+) dendritic cells after uptake of tumor apoptotic cells leading to cross-priming. J Immunol 186:5142–5150.
45. Moore MW, Carbone FR, Bevan MJ (1988) Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 54:777–785.
46. Lewis MD, et al. (2015) A reproducible method for the expansion of mouse CD8+ T lymphocytes. J Immunol Methods 417:134–138.
47. Van Kaer L, et al. (2014) CD8αα+ innate-type lymphocytes in the intestinal epithelium mediate mucosal immunity. Immunity 41:451–464.
48. Parekh VV, et al. (2005) Glycolipid antigen induces long-term natural killer T cell anergy in mice. J Clin Invest 115:2572–2583.