The critical role of membrane cholesterol in Salmonella-induced autophagy in intestinal epithelial cells

International Journal of Molecular Sciences

Volumn 15, Issue 7, 2014, Pages 12558-12572

  Huang, Fu Chen ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

Autophagy; Cholesterol; Intestine epithelia; Salmonella

Indexed keywords

BECLIN 1; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CHOLESTEROL; APOPTOSIS REGULATORY PROTEIN; ATG16L1 PROTEIN, HUMAN; BECN1 PROTEIN, HUMAN; BETA CYCLODEXTRIN DERIVATIVE; CARRIER PROTEIN; LIGHT CHAIN 3, HUMAN; MEMBRANE PROTEIN; METHYL-BETA-CYCLODEXTRIN; MICROTUBULE ASSOCIATED PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NOD2 PROTEIN, HUMAN;

ARTICLE; AUTOPHAGY; CELL FRACTIONATION; CELL MEMBRANE; CELL VIABILITY; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; INTESTINE EPITHELIUM CELL; MICROSCOPY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA; SIGNAL TRANSDUCTION; WESTERN BLOTTING; CACO 2 CELL LINE; DRUG EFFECTS; GENETICS; INTESTINE CELL; METABOLISM; MICROBIOLOGY; PATHOGENICITY;

APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; BETA-CYCLODEXTRINS; CACO-2 CELLS; CARRIER PROTEINS; CELL MEMBRANE; CHOLESTEROL; ENTEROCYTES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; NOD2 SIGNALING ADAPTOR PROTEIN; SALMONELLA;

EID: 84904439333     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms150712558     Document Type: Article

References (42)

1. Deretic, V. Autophagy in immunity and cell-autonomous defense against intracellular microbes. Immunol. Rev. 2011, 240, 92-104.
2. Moreau, K.; Rubinsztein, D. C. The plasma membrane as a control center for autophagy. Autophagy 2012, 8, 861-863.
3. Ravikumar, B.; Moreau, K.; Jahreiss, L.; Puri, C.; Rubinsztein, D. C. Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat. Cell Biol. 2010, 12, 747-757.
4. Knaevelsrud, H.; Simonsen, A. Lipids in autophagy: Constituents, signaling molecules and cargo with relevance to disease. Biochim. Biophys. Acta 2012, 1821, 1133-1145.
5. Huang, F. C. Plasma membrane cholesterol plays a critical role in the Salmonella-induced anti-inflammatory response in intestinal epithelial cells. Cell. Immunol. 2011, 271, 480-487.
6. Huang, F. C.; Li, Q.; Cherayil, B. J. A phosphatidyl-inositol-3-kinase-dependent anti-inflammatory pathway activated by Salmonella in epithelial cells. FEMS Microbiol. Lett. 2005, 243, 265-270.
7. Birmingham, C. L.; Brumell, J. H. Autophagy recognizes intracellular Salmonella enterica serovar Typhimurium in damaged vacuoles. Autophagy 2006, 2, 156-158.
8. Noda, T.; Kageyama, S.; Fujita, N.; Yoshimori, T. Three-axis model for Atg recruitment in autophagy against Salmonella. Int. J. Cell Biol. 2012, 2012, 389562.
9. Ellington, A. A.; Berhow, M. A.; Singletary, K. W. Inhibition of Akt signaling and enhanced ERK1/2 activity are involved in induction of macroautophagy by triterpenoid B-group soyasaponins in colon cancer cells. Carcinogenesis 2006, 27, 298-306.
10. Ogier-Denis, E.; Pattingre, S.; El Benna, J.; Codogno, P. Erk1/2-dependent phosphorylation of Galpha-interacting protein stimulates its GTPase accelerating activity and autophagy in human colon cancer cells. J. Biol. Chem. 2000, 275, 39090-39095.
11. Travassos, L. H.; Carneiro, L. A.; Ramjeet, M.; Hussey, S.; Kim, Y. G.; Magalhaes, J. G.; Yuan, L.; Soares, F.; Chea, E.; Le Bourhis, L.; et al. NOD1 and NOD2 direct autophagy by recruiting ATG16L1 to the plasma membrane at the site of bacterial entry. Nat. Immunol. 2010, 11, 55-62.
12. Cooney, R.; Baker, J.; Brain, O.; Danis, B.; Pichulik, T.; Allan, P.; Ferguson, D. J.; Campbell, B. J.; Jewell, D.; Simmons, A. NOD2 stimulation induces autophagy in dendritic cells influencing bacterial handling and antigen presentation. Nat. Med. 2010, 16, 90-97.
13. Lapaquette, P.; Darfeuille-Michaud, A. Abnormalities in the handling of intracellular bacteria in Crohn's disease. J. Clin. Gastroenterol. 2010, 44, S26-S29.
14. Kuballa, P.; Huett, A.; Rioux, J. D.; Daly, M. J.; Xavier, R. J. Impaired autophagy of an intracellular pathogen induced by a Crohn's disease associated ATG16L1 variant. PLoS One 2008, 3, e3391.
15. Homer, C. R.; Richmond, A. L.; Rebert, N. A.; Achkar, J. P.; McDonald, C. ATG16L1 and NOD2 interact in an autophagy-dependent antibacterial pathway implicated in Crohn's disease pathogenesis. Gastroenterology 2010, 139, 1630-1641.
16. Messer, J. S.; Murphy, S. F.; Logsdon, M. F.; Lodolce, J. P.; Grimm, W. A.; Bartulis, S. J.; Vogel, T. P.; Burn, M.; Boone, D. L. The Crohn's disease: Associated ATG16L1 variant and Salmonella invasion. BMJ Open 2014, doi: 10. 1136/bmjopen-2013-002790.
17. Billmann-Born, S.; Lipinski, S.; Bock, J.; Till, A.; Rosenstiel, P.; Schreiber, S. The complex interplay of NOD-like receptors and the autophagy machinery in the pathophysiology of Crohn disease. Eur. J. Cell Biol. 2011, 90, 593-602.
18. Arico, S.; Petiot, A.; Bauvy, C.; Dubbelhuis, P. F.; Meijer, A. J.; Codogno, P.; Ogier-Denis, E. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J. Biol. Chem. 2001, 276, 35243-35246.
19. Scarlatti, F.; Bauvy, C.; Ventruti, A.; Sala, G.; Cluzeaud, F.; Vandewalle, A.; Ghidoni, R.; Codogno, P. Ceramide-mediated macroautophagy involves inhibition of protein kinase B and up-regulation of Beclin 1. J. Biol. Chem. 2004, 279, 18384-18391.
20. Wang, J.; Whiteman, M. W.; Lian, H.; Wang, G.; Singh, A.; Huang, D.; Denmark, T. A non-canonical MEK/ERK signaling pathway regulates autophagy via regulating Beclin 1. J. Biol. Chem. 2009, 284, 21412-21424.
21. Liu, Y.; Yang, Y.; Ye, Y. C.; Shi, Q. F.; Chai, K.; Tashiro, S.; Onodera, S.; Ikejima, T. Activation of ERK-p53 and ERK-mediated phosphorylation of Bcl-2 are involved in autophagic cell death induced by the c-Met inhibitor SU11274 in human lung cancer A549 cells. J. Pharmacol. Sci. 2012, 118, 423-432.
22. Kang, R.; Zeh, H. J.; Lotze, M. T.; Tang, D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011, 18, 571-580.
23. Huang, F. C. Regulation of Salmonella flagellin-induced interleukin-8 in intestinal epithelial cells by muramyl dipeptide. Cell Immunol. 2012, 278, 1-9.
24. Cheng, J.; Ohsaki, Y.; Tauchi-Sato, K.; Fujita, A.; Fujimoto, T. Cholesterol depletion induces autophagy. Biochem. Biophys. Res. Commun. 2006, 351, 246-252.
25. Benjamin, J. L.; Sumpter, R., Jr.; Levine, B.; Hooper, L. V. Intestinal epithelial autophagy is essential for host defense against invasive bacteria. Cell Host Microbe 2013, 13, 723-734.
26. Shi, C. S.; Kehrl, J. H. MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages. J. Biol. Chem. 2008, 283, 33175-33182.
27. Codogno, P.; Mehrpour, M.; Proikas-Cezanne, T. Canonical and non-canonical autophagy: Variations on a common theme of self-eating? Nat. Rev. Mol. Cell Biol. 2012, 13, 7-12.
28. Gelman, A. E.; LaRosa, D. F.; Zhang, J.; Walsh, P. T.; Choi, Y.; Sunyer, J. O.; Turka, L. A. The adaptor molecule MyD88 activates PI-3 kinase signaling in CD4+ T cells and enables CpG oligodeoxynucleotide-mediated costimulation. Immunity 2006, 25, 783-793.
29. Smith, K. A.; Maizels, R. M. Defeating sepsis by misleading MyD88. Nat. Immunol. 2011, 12, 284-286.
30. Conway, K. L.; Kuballa, P.; Song, J. H.; Patel, K. K.; Castoreno, A. B.; Yilmaz, O. H.; Jijon, H. B.; Zhang, M.; Aldrich, L. N.; Villablanca, E. J.; et al. Atg16l1 is required for autophagy in intestinal epithelial cells and protection of mice from Salmonella infection. Gastroenterology 2013, 145, 1347-1357.
31. De Chastellier, C.; Thilo, L. Cholesterol depletion in Mycobacterium avium-infected macrophages overcomes the block in phagosome maturation and leads to the reversible sequestration of viable mycobacteria in phagolysosome-derived autophagic vacuoles. Cell. Microbiol. 2006, 8, 242-256.
32. Kumar, Y.; Valdivia, R. H. Leading a sheltered life: Intracellular pathogens and maintenance of vacuolar compartments. Cell Host Microbe 2009, 5, 593-601.
33. Birmingham, C. L.; Smith, A. C.; Bakowski, M. A.; Yoshimori, T.; Brumell, J. H. Autophagy controls Salmonella infection in response to damage to the Salmonella-containing vacuole. J. Biol. Chem. 2006, 281, 11374-11383.
34. Jia, K.; Thomas, C.; Akbar, M.; Sun, Q.; Adams-Huet, B.; Gilpin, C.; Levine, B. Autophagy genes protect against Salmonella typhimurium infection and mediate insulin signaling-regulated pathogen resistance. Proc. Natl. Acad. Sci. USA 2009, 106, 14564-14569.
35. Garcia Rodriguez, L. A.; Ruigomez, A.; Panes, J. Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology 2006, 130, 1588-1594.
36. Rioux, J. D.; Xavier, R. J.; Taylor, K. D.; Silverberg, M. S.; Goyette, P.; Huett, A.; Green, T.; Kuballa, P.; Barmada, M. M.; Datta, L. W.; et al. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat. Genet. 2007, 39, 596-604.
37. Knodler, L. A.; Finlay, B. B.; Steele-Mortimer, O. The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J. Biol. Chem. 2005, 280, 9058-9064.
38. Knodler, L. A.; Winfree, S.; Drecktrah, D.; Ireland, R.; Steele-Mortimer, O. Ubiquitination of the bacterial inositol phosphatase, SopB, regulates its biological activity at the plasma membrane. Cell. Microbiol. 2009, 11, 1652-1670.
39. Huang, F. C. Upregulation of Salmonella-induced IL-6 production in Caco-2 cells by PJ-34, PARP-1 inhibitor: Involvement of PI3K, p38 MAPK, ERK, JNK, and NF-κB. Mediators Inflamm. 2009, 2009, 103890.
40. Huang, F. C.; Werne, A.; Li, Q.; Galyov, E. E.; Walker, W. A.; Cherayil, B. J. Cooperative interactions between flagellin and SopE2 in the epithelial interleukin-8 response to Salmonella enterica serovar typhimurium infection. Infect. Immun. 2004, 72, 5052-5062.
41. Christian, A. E.; Haynes, M. P.; Phillips, M. C.; Rothblat, G. H. Use of cyclodextrins for manipulating cellular cholesterol content. J. Lipid Res. 1997, 38, 2264-2272.
42. Scheid, M. P.; Marignani, P. A.; Woodgett, J. R. Multiple phosphoinositide 3-kinase-dependent steps in activation of protein kinase B. Mol. Cell. Biol. 2002, 22, 6247-6260.