A TRP channel senses lysosome neutralization by pathogens to trigger their expulsion

Cell

Volumn 161, Issue 6, 2015, Pages 1306-1319

  Miao, Yuxuan ^a   Li, Guojie ^a   Zhang, Xiaoli ^c   Xu, Haoxing ^c   Abraham, Soman N ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUCOLIPIN TRANSIENT RECEPTOR POTENTIAL CHANNEL 3; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3; UNCLASSIFIED DRUG; MCOLN3 PROTEIN, MOUSE; TRANSIENT RECEPTOR POTENTIAL CATION CHANNEL, SUBFAMILY C, MEMBER 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL C;

ARTICLE; AUTOPHAGY; BACTERIAL CLEARANCE; BLADDER EPITHELIUM; CELL PH; CONTROLLED STUDY; DEGRADATION; EPITHELIUM CELL; EXOCYTOSIS; HUMAN; HUMAN CELL; LYSOSOME; PRIORITY JOURNAL; UROPATHOGENIC ESCHERICHIA COLI; ANIMAL; BLADDER; ENZYMOLOGY; ESCHERICHIA COLI INFECTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUSE; PATHOLOGY; PHYSIOLOGY; URINARY TRACT INFECTION;

VERTEBRATA;

ANIMALS; AUTOPHAGY; ESCHERICHIA COLI INFECTIONS; EXOCYTOSIS; LYSOSOMES; MICE; TRANSIENT RECEPTOR POTENTIAL CHANNELS; TRPC CATION CHANNELS; URINARY BLADDER; URINARY TRACT INFECTIONS; UROPATHOGENIC ESCHERICHIA COLI;

EID: 84930413971     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.05.009     Document Type: Article

References (36)

1. Abraham, S.N., Sun, D., Dale, J.B., and Beachey, E.H. (1988). Conservation of the D-mannose-Adhesion protein among type 1 fimbriated members of the family Enterobacteriaceae. Nature 336, 682-684.
2. Akira, S., Uematsu, S., and Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell 124, 783-801.
3. Baietti, M.F., Zhang, Z., Mortier, E., Melchior, A., Degeest, G., Geeraerts, A., Ivarsson, Y., Depoortere, F., Coomans, C., Vermeiren, E., et al. (2012). Syndecan- syntenin-ALIX regulates the biogenesis of exosomes. Nat. Cell Biol. 14, 677-685.
4. Bishop, B.L., Duncan, M.J., Song, J., Li, G., Zaas, D., and Abraham, S.N. (2007). Cyclic AMP-regulated exocytosis of Escherichia coli from infected bladder epithelial cells. Nat. Med. 13, 625-630.
5. Clapham, D.E. (2003). TRP channels as cellular sensors. Nature 426, 517-524.
6. Dong, X.P., Cheng, X., Mills, E., Delling, M., Wang, F., Kurz, T., and Xu, H. (2008). The type IV mucolipidosis-Associated protein TRPML1 is an endolysosomal iron release channel. Nature 455, 992-996.
7. Fader, C.M., Sánchez, D.G., Mestre, M.B., and Colombo, M.I. (2009). TIVAMP/ VAMP7 and VAMP3/cellubrevin: Two v-SNARE proteins involved in specific steps of the autophagy/multivesicular body pathways. Biochim. Biophys. Acta 1793, 1901-1916.
8. Filimonenko, M., Stuffers, S., Raiborg, C., Yamamoto, A., Malerød, L., Fisher, E.M., Isaacs, A., Brech, A., Stenmark, H., and Simonsen, A. (2007). Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J. Cell Biol. 179, 485-500.
9. Fujita, N., Hayashi-Nishino, M., Fukumoto, H., Omori, H., Yamamoto, A., Noda, T., and Yoshimori, T. (2008). An Atg4B mutant hampers the lipidation of LC3 paralogues and causes defects in autophagosome closure. Mol. Biol. Cell 19, 4651-4659.
10. Goren, M.B. (1977). Phagocyte lysosomes: Interactions with infectious agents, phagosomes, and experimental perturbations in function. Annu. Rev. Microbiol. 31, 507-533.
11. Grimm, C., Jörs, S., Saldanha, S.A., Obukhov, A.G., Pan, B., Oshima, K., Cuajungco, M.P., Chase, P., Hodder, P., and Heller, S. (2010). Small molecule activators of TRPML3. Chem. Biol. 17, 135-148.
12. Hagedorn, M., Rohde, K.H., Russell, D.G., and Soldati, T. (2009). Infection by tubercular mycobacteria is spread by nonlytic ejection from their amoeba hosts. Science 323, 1729-1733.
13. Haller, T., Dietl, P., Deetjen, P., and Völkl, H. (1996). The lysosomal compartment as intracellular calcium store in MDCK cells: A possible involvement in InsP3-mediated Ca2+ release. Cell Calcium 19, 157-165.
14. Jahn, R., and Südhof, T.C. (1999). Membrane fusion and exocytosis. Annu. Rev. Biochem. 68, 863-911.
15. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. (2000). LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728.
16. Kim, H.J., Li, Q., Tjon-Kon-Sang, S., So, I., Kiselyov, K., Soyombo, A.A., and Muallem, S. (2008). A novel mode of TRPML3 regulation by extracytosolic pH absent in the varitint-waddler phenotype. EMBO J. 27, 1197-1205.
17. Klionsky, D.J., Abdalla, F.C., Abeliovich, H., Abraham, R.T., Acevedo-Arozena, A., Adeli, K., Agholme, L., Agnello, M., Agostinis, P., Aguirre-Ghiso, J.A., et al. (2012). Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8, 445-544.
18. Kobayashi, T., Vischer, U.M., Rosnoblet, C., Lebrand, C., Lindsay, M., Parton, R.G., Kruithof, E.K., and Gruenberg, J. (2000). The tetraspanin CD63/lamp3 cycles between endocytic and secretory compartments in human endothelial cells. Mol. Biol. Cell 11, 1829-1843.
19. Lee, J.A., Liu, L., and Gao, F.B. (2009). Autophagy defects contribute to neurodegeneration induced by dysfunctional ESCRT-III. Autophagy 5, 1070-1072.
20. Levine, B., Mizushima, N., and Virgin, H.W. (2011). Autophagy in immunity and inflammation. Nature 469, 323-335.
21. Lönnbro, P., Nordenfelt, P., and Tapper, H. (2008). Isolation of bacteriacontaining phagosomes by magnetic selection. BMC Cell Biol. 9, 35.
22. Menashe, O., Kaganskaya, E., Baasov, T., and Yaron, S. (2008). Aminoglycosides affect intracellular Salmonella enterica serovars typhimurium and virchow. Antimicrob. Agents Chemother. 52, 920-926.
23. Reddy, A., Caler, E.V., and Andrews, N.W. (2001). Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes. Cell 106, 157-169.
24. Samie, M., Wang, X., Zhang, X., Goschka, A., Li, X., Cheng, X., Gregg, E., Azar, M., Zhuo, Y., Garrity, A.G., et al. (2013). A TRP channel in the lysosome regulates large particle phagocytosis via focal exocytosis. Dev. Cell 26, 511-524.
25. Savina, A., Furlán, M., Vidal, M., and Colombo, M.I. (2003). Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J. Biol. Chem. 278, 20083-20090.
26. Shen, D., Wang, X., Li, X., Zhang, X., Yao, Z., Dibble, S., Dong, X.P., Yu, T., Lieberman, A.P., Showalter, H.D., and Xu, H. (2012). Lipid storage disorders block lysosomal trafficking by inhibiting a TRP channel and lysosomal calcium release. Nat. Commun. 3, 731.
27. Shoji-Kawata, S., Sumpter, R., Leveno, M., Campbell, G.R., Zou, Z., Kinch, L., Wilkins, A.D., Sun, Q., Pallauf, K., MacDuff, D., et al. (2013). Identification of a candidate therapeutic autophagy-inducing peptide. Nature 494, 201-206.
28. Simons, M., and Raposo, G. (2009). Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575-581.
29. Song, J., Bishop, B.L., Li, G., Grady, R., Stapleton, A., and Abraham, S.N. (2009). TLR4-mediated expulsion of bacteria from infected bladder epithelial cells. Proc. Natl. Acad. Sci. USA 106, 14966-14971.
30. Sturgill-Koszycki, S., Schlesinger, P.H., Chakraborty, P., Haddix, P.L., Collins, H.L., Fok, A.K., Allen, R.D., Gluck, S.L., Heuser, J., and Russell, D.G. (1994). Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 263, 678-681.
31. Théry, C., Zitvogel, L., and Amigorena, S. (2002). Exosomes: Composition, biogenesis and function. Nat. Rev. Immunol. 2, 569-579.
32. Thery, C., Amigorena, S., Raposo, G., and Clayton, A. (2006). Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Chapter 3, Unit 3.22.
33. Vance, R.E., Isberg, R.R., and Portnoy, D.A. (2009). Patterns of pathogenesis: Discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6, 10-21.
34. Vanlandingham, P.A., and Ceresa, B.P. (2009). Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J. Biol. Chem. 284, 12110-12124.
35. Vidal, M., Mangeat, P., and Hoekstra, D. (1997). Aggregation reroutes molecules from a recycling to a vesicle-mediated secretion pathway during reticulocyte maturation. J. Cell Sci. 110, 1867-1877.
36. Xu, H., and Ren, D. (2015). Lysosomal physiology. Annu. Rev. Physiol. 77, 57-80.