Inhibitors of Intravesicular Acidification Protect Against Shiga Toxin in a pH-Independent Manner

Traffic

Volumn 13, Issue 3, 2012, Pages 443-454

  Dyve Lingelem, Anne Berit ^a,b,c   Bergan, Jonas ^a,b,c   Sandvig, Kirsten ^a,b,c  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c UNIVERSITY OF OSLO   (Norway)

Author keywords

Bafilomycin A1; Chloroquine; Concanamycin A; Intracellular transport; Nigericin; Shiga toxin

Indexed keywords

ADENOSINE TRIPHOSPHATE; BAFILOMYCIN A1; CHLOROQUINE; CONCANAMYCIN A; EARLY ENDOSOME ANTIGEN 1; IONOPHORE; NIGERICIN; PROTON PUMP; SHIGA TOXIN;

ACIDIFICATION; ARTICLE; CELL FUNCTION; CYTOSOL; ENDOSOME; ENVIRONMENTAL FACTOR; ION TRANSPORT; MEMBRANE PERMEABILITY; MEMBRANE POTENTIAL; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; PROTON TRANSPORT; TOXIN ANALYSIS; TRANS GOLGI NETWORK;

ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE; CHLOROQUINE; ENDOPLASMIC RETICULUM; ENDOSOMES; ENZYME INHIBITORS; HYDROGEN-ION CONCENTRATION; MACROLIDES; NIGERICIN; SHIGA TOXIN;

EID: 84856779356     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01319.x     Document Type: Article

References (49)

1. Jovic M, Sharma M, Rahajeng J, Caplan S. The early endosome: a busy sorting station for proteins at the crossroads. Histol Histopathol 2010;25:99-112.
2. van Weert AW, Dunn KW, Gueze HJ, Maxfield FR, Stoorvogel W. Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J Cell Biol 1995;130:821-834.
3. Reaves B, Banting G. Vacuolar ATPase inactivation blocks recycling to the trans-Golgi network from the plasma membrane. FEBS Lett 1994;345:61-66.
4. Mellman I, Fuchs R, Helenius A. Acidification of the endocytic and exocytic pathways. Annu Rev Biochem 1986;55:663-700.
5. Gruenberg J, van der Goot FG. Mechanisms of pathogen entry through the endosomal compartments. Nat Rev Mol Cell Biol 2006;7:495-504.
6. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol 2007;8:917-929.
7. Fuchs R, Schmid S, Mellman I. A possible role for Na+, K+-ATPase in regulating ATP-dependent endosome acidification. Proc Natl Acad Sci U S A 1989;86:539-543.
8. Eiklid K, Olsnes S. Entry of Shigella dysenteriae toxin into HeLa cells. Infect Immun 1983;42:771-777.
9. Keusch GT, Jacewicz M. Primary amines and chloroquine inhibit cytotoxic responses to Shigella toxin and permit late antibody rescue of toxin treated cells. Biochem Biophys Res Commun 1984;121:69-76.
10. Sandvig K, Brown JE. Ionic requirements for entry of Shiga toxin from Shigella dysenteriae 1 into cells. Infect Immun 1987;55:298-303.
11. Sandvig K, Torgersen ML, Engedal N, Skotland T, Iversen T-G. Protein toxins from plants and bacteria: probes for intracellular transport and tools in medicine. FEBS Lett 2010;584:2626-2634.
12. Bowman EJ, Siebers A, Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A 1988;85:7972-7976.
13. Dröse S, Bindseil KU, Bowman EJ, Siebers A, Zeeck A, Altendorf K. Inhibitory effect of modified bafilomycins and concanamycins on P- and V-type adenosinetriphosphatases. Biochemistry 1993;32:3902-3906.
14. Bowman BJ, Bowman EJ. Mutations in subunit C of the vacuolar ATPase confer resistance to bafilomycin and identify a conserved antibiotic binding site. J Biol Chem 2002;277:3965-3972.
15. Huss M, Ingenhorst G, König S, Gassel M, Dröse S, Zeeck A, Altendorf K, Wieczorek H. Concanamycin A, the specific inhibitor of V-ATPases, binds to the V(o) subunit c. J Biol Chem 2002;277:40544-40548.
16. Schapiro FB, Lingwood C, Furuya W, Grinstein S. pH-independent retrograde targeting of glycolipids to the Golgi complex. Am J Physiol 1998;274:C319-C332.
17. Mallard F, Antony C, Tenza D, Salamero J, Goud B, Johannes L. Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of shiga toxin B-fragment transport. J Cell Biol 1998;143:973-990.
18. Chiron MF, Fryling CM, FitzGerald DJ. Cleavage of pseudomonas exotoxin and diphtheria toxin by a furin-like enzyme prepared from beef liver. J Biol Chem 1994;269:18167-18176.
19. Garred O, van Deurs B, Sandvig K. Furin-induced cleavage and activation of Shiga toxin. J Biol Chem 1995;270:10817-10821.
20. Torgersen ML, Wälchli S, Grimmer S, Skånland SS, Sandvig K. Protein kinase Cdelta is activated by Shiga toxin and regulates its transport. J Biol Chem 2007;282:16317-16328.
21. Lauvrak SU, Torgersen ML, Sandvig K. Efficient endosome-to-Golgi transport of Shiga toxin is dependent on dynamin and clathrin. J Cell Sci 2004;117:2321-2331.
22. Mallard F, Tang BL, Galli T, Tenza D, Saint-Pol A, Yue X, Antony C, Hong W, Goud B, Johannes L. Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J Cell Biol 2002;156:653-664.
23. '. Traffic 2006;7:663-672.
24. Wälchli S, Skånland SS, Gregers TF, Lauvrak SU, Torgersen ML, Ying M, Kuroda S, Maturana A, Sandvig K. The mitogen-activated protein kinase p38 links Shiga toxin-dependent signaling and trafficking. Mol Biol Cell 2008;19:95-104.
25. Dyve AB, Bergan J, Utskarpen A, Sandvig K. Sorting nexin 8 regulates endosome-to-Golgi transport. Biochem Biophys Res Commun 2009;390:109-114.
26. Yoshida T, Chen C, Zhang M, Wu HC. Increased cytotoxicity of ricin in a putative Golgi-defective mutant of Chinese hamster ovary cell. Exp Cell Res 1990;190:11-16.
27. Thompson WL, Scovill JP, Pace JG. Drugs that show protective effects from ricin toxicity in in vitro protein synthesis assays. Nat Toxins 1995;3:369-377.
28. Grøndahl F, Tveit H, Prydz K. Neutralization of endomembrane compartments in epithelial MDCK cells affects proteoglycan synthesis in the apical secretory pathway. Biochem J 2009;418:517-528.
29. Ohkuma S, Poole B. Cytoplasmic vacuolation of mouse peritoneal macrophages and the uptake into lysosomes of weakly basic substances. J Cell Biol 1981;90:656-664.
30. Umeda A, Fujita H, Kuronita T, Hirosako K, Himeno M, Tanaka Y. Distribution and trafficking of MPR300 is normal in cells with cholesterol accumulated in late endocytic compartments: evidence for early endosome-to-TGN trafficking of MPR300. J Lipid Res 2003;44:1821-1832.
31. Hurtado-Lorenzo A, Skinner M, El Annan J, Futai M, Sun-Wada G-H, Bourgoin S, Casanova J, Wildeman A, Bechoua S, Ausiello DA, Brown D, Marshansky V. V-ATPase interacts with ARNO and Arf6 in early endosomes and regulates the protein degradative pathway. Nat Cell Biol 2006;8:124-136.
32. Toyomura T, Murata Y, Yamamoto A, Oka T, Sun-Wada G-H, Wada Y, Futai M. From lysosomes to the plasma membrane. J Biol Chem 2003;278:22023-22030.
33. Moreau D, Kumar P, Wang SC, Chaumet A, Chew SY, Chevalley H, Bard F. Genome-wide RNAi screens identify genes required for Ricin and PE intoxications. Dev Cell 2011;21:231-244.
34. Peters C, Bayer MJ, Bühler S, Andersen JS, Mann M, Mayer A. Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature 2001;409:581-588.
35. Bayer MJ, Reese C, Buhler S, Peters C, Mayer A. Vacuole membrane fusion: V0 functions after trans-SNARE pairing and is coupled to the Ca2+-releasing channel. J Cell Biol 2003;162:211-222.
36. Hammond TG, Goda FO, Navar GL, Campbell WC, Majewski RR, Galvan DL, Pontillon F, Kaysen JH, Goodwin TJ, Paddock SW, Verroust PJ. Membrane potential mediates H(+)-ATPase dependence of "degradative pathway" endosomal fusion. J Membr Biol 1998;162:157-167.
37. Małecki J, Wiedłocha A, Wesche J, Olsnes S. Vesicle transmembrane potential is required for translocation to the cytosol of externally added FGF-1. EMBO J 2002;21:4480-4490.
38. Gibert M, Marvaud JC, Pereira Y, Hale ML, Stiles BG, Boquet P, Lamaze C, Popoff MR. Differential requirement for the translocation of clostridial binary toxins: iota toxin requires a membrane potential gradient. FEBS Lett 2007;581:1287-1296.
39. van der Poel S, Wolthoorn J, van den Heuvel D, Egmond M, Groux-Degroote S, Neumann S, Gerritsen H, van Meer G, Sprong H. Hyperacidification of trans-Golgi network and endo/lysosomes in melanocytes by glucosylceramide-dependent V-ATPase activity. Traffic 2011;12:1634-1647.
40. Morgan AJ, Platt FM, Lloyd-Evans E, Galione A. Molecular mechanisms of endolysosomal Ca2+ signalling in health and disease. Biochem J 2011;439:349-374.
41. Hazes B, Read RJ. Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry 1997;36:11051-11054.
42. Rodríguez-Menchaca AA, Navarro-Polanco RA, Ferrer-Villada T, Rupp J, Sachse FB, Tristani-Firouzi M, Sánchez-Chapula JA. The molecular basis of chloroquine block of the inward rectifier Kir2.1 channel. Proc Natl Acad Sci U S A 2008;105:1364-1368.
43. Bachmeyer C, Benz R, Barth H, Aktories K, Gilbert M, Popoff MR. Interaction of Clostridium botulinum C2 toxin with lipid bilayer membranes and Vero cells: inhibition of channel function by chloroquine and related compounds in vitro and intoxification in vivo. FASEB J 2001;15:1658-1660.
44. Schlitzer M. Malaria chemotherapeutics part I: history of antimalarial drug development, currently used therapeutics, and drugs in clinical development. ChemMedChem 2007;2:944-986.
45. Solomon VR, Lee H. Chloroquine and its analogs: a new promise of an old drug for effective and safe cancer therapies. Eur J Pharmacol 2009;625:220-233.
46. Kim JH, Johannes L, Goud B, Antony C, Lingwood CA, Daneman R, Grinstein S. Noninvasive measurement of the pH of the endoplasmic reticulum at rest and during calcium release. Proc Natl Acad Sci U S A 1998;95:2997-3002.
47. Lauvrak SU, Wälchli S, Iversen T-G, Slagsvold HH, Torgersen ML, Spilsberg B, Sandvig K. Shiga toxin regulates its entry in a Syk-dependent manner. Mol Biol Cell 2006;17:1096-1109.
48. Rapak A, Falnes PO, Olsnes S. Retrograde transport of mutant ricin to the endoplasmic reticulum with subsequent translocation to cytosol. Proc Natl Acad Sci U S A 1997;94:3783-3788.
49. Su GF, Brahmbhatt HN, Wehland J, Rohde M, Timmis KN. Construction of stable LamB-Shiga toxin B subunit hybrids: analysis of expression in Salmonella typhimurium aroA strains and stimulation of B subunit-specific mucosal and serum antibody responses. Infect Immun 1992;60:3345-3359.