Interferon-inducible transmembrane proteins of the innate immune response act as membrane organizers by influencing clathrin and v-ATPase localization and function

Innate Immunity

Volumn 18, Issue 6, 2012, Pages 834-845

  Wee, Yin Shen ^a   Roundy, Kirstin M ^a   Weis, Janis J ^a   Weis, John H ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Endocytosis; interferon; membrane; mouse knockout; phagocytosis; virus

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BETA INTERFERON; CLATHRIN; INTERFERON INDUCIBLE TRANSMEMBRANE PROTEIN; MEMBRANE PROTEIN; PROTON PUMP; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVITY; ENZYME LOCALIZATION; IMMUNOPRECIPITATION; INNATE IMMUNITY; MOUSE; NONHUMAN; PHAGOCYTOSIS; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; CELL MEMBRANE; CELLS, CULTURED; CLATHRIN; ENDOCYTOSIS; ENDOSOMES; IMMUNITY, INNATE; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTEIN BINDING; PROTEIN TRANSPORT; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84866916975     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425912443392     Document Type: Article

References (50)

1. Lange UC, Saitou M, Western PS, Barton SC, Surani MA. The fragilis interferon-inducible gene family of transmembrane proteins is associated with germ cell specification in mice. BMC Dev Biol. 2003 ; 3: 1-1
2. Lewin AR, Reid LE, McMahon M, Stark GR, Kerr IM. Molecular analysis of a human interferon-inducible gene family. Eur J Biochem. 1991 ; 199: 417-423
3. Moffatt P, Gaumond MH, Salois P, Sellin K, Bessette MC, Godin E, et al. Bril: a novel bone-specific modulator of mineralization. J Bone Miner Res. 2008 ; 23: 1497-1508
4. Ackrill AM, Reid LE, Gilbert CS, Gewert DR, Porter AC, Lewin AR, et al. Differential response of the human 6-16 and 9-27 genes to alpha and gamma interferons. Nucleic Acids Res. 1991 ; 19: 591-598
5. Jaffe EA, Armellino D, Lam G, Cordon-Cardo C, Murray HW, Evans RL. IFN-gamma and IFN-alpha induce the expression and synthesis of Leu 13 antigen by cultured human endothelial cells. J Immunol. 1989 ; 143: 3961-3966
6. Chen YX, Welte K, Gebhard DH, Evans RL. Induction of T cell aggregation by antibody to a 16kd human leukocyte surface antigen. J Immunol. 1984 ; 133: 2496-2501
7. Evans SS, Collea RP, Leasure JA, Lee DB. IFN-alpha induces homotypic adhesion and Leu-13 expression in human B lymphoid cells. J Immunol. 1993 ; 150: 736-747
8. Frey M, Appenheimer MM, Evans SS. Tyrosine kinase-dependent regulation of L-selectin expression through the Leu-13 signal transduction molecule: evidence for a protein kinase C-independent mechanism of L-selectin shedding. J Immunol. 1997 ; 158: 5424-5434
9. Yang G, Xu Y, Chen X, Hu G. IFITM1 plays an essential role in the antiproliferative action of interferon-gamma. Oncogene. 2007 ; 26: 594-603
10. Xu Y, Yang G, Hu G. Binding of IFITM1 enhances the inhibiting effect of caveolin-1 on ERK activation. Acta Biochim Biophys Sin (Shanghai). 2009 ; 41: 488-494
11. Takahashi S, Doss C, Levy S, Levy R. TAPA-1, the target of an antiproliferative antibody, is associated on the cell surface with the Leu-13 antigen. J Immunol. 1990 ; 145: 2207-2213
12. Bradbury LE, Kansas GS, Levy S, Evans RL, Tedder TF. The CD19/CD21 signal transducing complex of human B lymphocytes includes the target of antiproliferative antibody-1 and Leu-13 molecules. J Immunol. 1992 ; 149: 2841-2850
13. Seo GS, Lee JK, Yu JI, Yun KJ, Chae SC, Choi SC. Identification of the polymorphisms in IFITM3 gene and their association in a Korean population with ulcerative colitis. Exp Mol Med. 2010 ; 42: 99-104
14. Zucchi I, Montagna C, Susani L, Vezzoni P, Dulbecco R. The rat gene homologous to the human gene 9-27 is involved in the development of the mammary gland. Proc Natl Acad Sci USA. 1998 ; 95: 1079-1084
15. Zucchi I, Prinetti A, Scotti M, Valsecchi V, Valaperta R, Mento E, et al. Association of rat8 with Fyn protein kinase via lipid rafts is required for rat mammary cell differentiation in vitro. Proc Natl Acad Sci USA. 2004 ; 101: 1880-1885
16. Tanaka SS, Nagamatsu G, Tokitake Y, Kasa M, Tam PP, Matsui Y. Regulation of expression of mouse interferon-induced transmembrane protein like gene-3, Ifitm3 (mil-1, fragilis), in germ cells. Dev Dyn. 2004 ; 230: 651-659
17. Tanaka SS, Yamaguchi YL, Tsoi B, Lickert H, Tam PP. IFITM/Mil/fragilis family proteins IFITM1 and IFITM3 play distinct roles in mouse primordial germ cell homing and repulsion. Dev Cell. 2005 ; 9: 745-756
18. Lange UC, Adams DJ, Lee C, Barton S, Schneider R, Bradley A, Surani MA. Normal germ line establishment in mice carrying a deletion of the Ifitm/Fragilis gene family cluster. Mol Cell Biol. 2008 ; 28: 4688-4696
19. Smith RA, Young J, Weis JJ, Weis JH. Expression of the mouse fragilis gene products in immune cells and association with receptor signaling complexes. Genes Immun. 2006 ; 7: 113-121
20. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, Feeley EM, et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell. 2009 ; 139: 1243-1254
21. Jiang D, Weidner JM, Qing M, Pan XB, Guo H, Xu C, et al. Identification of five interferon-induced cellular proteins that inhibit west nile virus and dengue virus infections. J Virol. 2010 ; 84: 8332-8341
22. Huang IC, Bailey CC, Weyer JL, Radoshitzky SR, Becker MM, Chiang JJ, et al. Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus. PLoS Pathog. 2011 ; 7: e1001258 - e1001258
23. Weidner JM, Jiang D, Pan XB, Chang J, Block TM, Guo JT. Interferon-induced cell membrane proteins, IFITM3 and tetherin, inhibit vesicular stomatitis virus infection via distinct mechanisms. J Virol. 2010 ; 84: 12646-12657
24. Lu J, Pan Q, Rong L, Liu SL, Liang C. The IFITM proteins inhibit HIV-1 infection. J Virol. 2011 ; 85: 2126-2137
25. Feeley EM, Sims JS, John SP, Chin CR, Pertel T, Chen LM, et al. IFITM3 inhibits influenza A virus infection by preventing cytosolic entry. PLoS Pathog. 2011 ; 7: e1002337 - e1002337
26. Mercer J, Schelhaas M, Helenius A. Virus entry by endocytosis. Annu Rev Biochem. 2010 ; 79: 803-833
27. Tanaka SS, Matsui Y. Developmentally regulated expression of mil-1 and mil-2, mouse interferon-induced transmembrane protein like genes, during formation and differentiation of primordial germ cells. Mech Dev. 2002 ; 119 (Suppl. 1). S261 - S267
28. Imai T, Yoshie O. C33 antigen and M38 antigen recognized by monoclonal antibodies inhibitory to syncytium formation by human T cell leukemia virus type 1 are both members of the transmembrane 4 superfamily and associate with each other and with CD4 or CD8 in T cells. J Immunol. 1993 ; 151: 6470-6481
29. Hanagata N, Li X. Osteoblast-enriched membrane protein IFITM5 regulates the association of CD9 with an FKBP11-CD81-FPRP complex and stimulates expression of interferon-induced genes. Biochem Biophys Res Commun. 2011 ; 409: 378-384
30. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, et al. Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci USA. 2005 ; 102: 2760-2765
31. Johannes L, Lamaze C. Clathrin-dependent or not: is it still the question?. Traffic. 2002 ; 3: 443-451
32. Levy S, Shoham T. The tetraspanin web modulates immune-signalling complexes. Nat Rev Immunol. 2005 ; 5: 136-148
33. Forgac M. Structure, mechanism and regulation of the clathrin-coated vesicle and yeast vacuolar H(+)-ATPases. J Exp Biol. 2000 ; 203: 71-80
34. Sun-Wada GH, Tabata H, Kawamura N, Aoyama M, Wada Y. Direct recruitment of H+-ATPase from lysosomes for phagosomal acidification. J Cell Sci. 2009 ; 122: 2504-2513
35. Lafourcade C, Sobo K, Kieffer-Jaquinod S, Garin J, van der Goot FG. Regulation of the V-ATPase along the endocytic pathway occurs through reversible subunit association and membrane localization. PLoS One. 2008 ; 3: e2758 - e2758
36. Drory O, Nelson N. The emerging structure of vacuolar ATPases. Physiology (Bethesda). 2006 ; 21: 317-325
37. Cherukuri A, Carter RH, Brooks S, Bornmann W, Finn R, Dowd CS, Pierce SK. B cell signaling is regulated by induced palmitoylation of CD81. J Biol Chem. 2004 ; 279: 31973-31982
38. Yount JS, Moltedo B, Yang YY, Charron G, Moran TM, Lopez CB, Hang HC. Palmitoylome profiling reveals S-palmitoylation-dependent antiviral activity of IFITM3. Nat Chem Biol. 2010 ; 6: 610-614
39. Karlas A, Machuy N, Shin Y, Pleissner KP, Artarini A, Heuer D, et al. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature. 2010 ; 463: 818-822
40. Konig R, Stertz S, Zhou Y, Inoue A, Hoffmann HH, Bhattacharyya S, et al. Human host factors required for influenza virus replication. Nature. 2010 ; 463: 813-817
41. Hanagata N, Li X, Morita H, Takemura T, Li J, Minowa T. Characterization of the osteoblast-specific transmembrane protein IFITM5 and analysis of IFITM5-deficient mice. J Bone Miner Metab. 2011 ; 29: 279-290
42. Kartner N, Yao Y, Li K, Crasto GJ, Datti A, Manolson MF. Inhibition of osteoclast bone resorption by disrupting vacuolar H+-ATPase a3-B2 subunit interaction. J Biol Chem. 2010 ; 285: 37476-37490
43. Perez-Sayans M, Somoza-Martin JM, Barros-Angueira F, Rey JM, Garcia-Garcia A. V-ATPase inhibitors and implication in cancer treatment. Cancer Treat Rev. 2009 ; 35: 707-713
44. Lee JA, Sinkovits RS, Mock D, Rab EL, Cai J, Yang P, et al. Components of the antigen processing and presentation pathway revealed by gene expression microarray analysis following B cell antigen receptor (BCR) stimulation. BMC Bioinformatics. 2006 ; 7: 237-237
45. Wang E, Michl J, Pfeffer LM, Silverstein SC, Tamm I. Interferon suppresses pinocytosis but stimulates phagocytosis in mouse peritoneal macrophages: related changes in cytoskeletal organization. J Cell Biol. 1984 ; 98: 1328-1341
46. Myers M, Forgac M. The coated vesicle vacuolar (H+)-ATPase associates with and is phosphorylated by the 50-kDa polypeptide of the clathrin assembly protein AP-2. J Biol Chem. 1993 ; 268: 9184-9186
47. Liu Q, Feng Y, Forgac M. Activity and in vitro reassembly of the coated vesicle (H+)-ATPase requires the 50-kDa subunit of the clathrin assembly complex AP-2. J Biol Chem. 1994 ; 269: 31592-31597
48. Traub LM. Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J Cell Biol. 2003 ; 163: 203-208
49. Wilde A, Beattie EC, Lem L, Riethof DA, Liu SH, Mobley WC, et al. EGF receptor signaling stimulates SRC kinase phosphorylation of clathrin, influencing clathrin redistribution and EGF uptake. Cell. 1999 ; 96: 677-687
50. Wilde A, Brodsky FM. In vivo phosphorylation of adaptors regulates their interaction with clathrin. J Cell Biol. 1996 ; 135: 635-645