Proteolytic activation of internalized cholera toxin within hepatic endosomes by cathepsin D

FEBS Journal

Volumn 272, Issue 17, 2005, Pages 4385-4397

  Merlen, Clémence ^a   Fayol Messaoudi, Domitille ^a   Fabrega, Sylvie ^a   Hage, Tatiana El ^a   Servin, Alain ^a   Authier, François ^a  

^a INSERM   (France)

Author keywords

Cathepsin D; Cholera toxin; Endocytosis; Hepatocyte; Proteolysis

Indexed keywords

ASPARTIC ACID; CATHEPSIN D; CHOLERA TOXIN; CHOLERA TOXIN A SUBUNIT; CHOLERA TOXIN B SUBUNIT; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PEPSTATIN; PROTEINASE; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL STRAIN CACO 2; CELL STRAIN HEPG2; CONTROLLED STUDY; CYTOTOXICITY; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; FLUORESCENCE; HUMAN; HUMAN CELL; HYDROLYSIS; IMMUNOPRECIPITATION; INTERNALIZATION; MALE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; RAT;

BOVINAE;

EID: 24644486090     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2005.04851.x     Document Type: Article

References (47)

1. Lencer WI (2001) Microbes and microbial Toxins: paradigms for microbial-mucosal toxins. V. Cholera: invasion of the intestinal epithelial barrier by a stably folded protein toxin. Am J Physiol 280, G781-G786.
2. Spangler BD (1992) Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol Rev 56, 622-647.
3. Lencer WI & Tsai B (2003) The intracellular voyage of cholera toxin: going retro. Trends Biochem Sci 28, 639-645.
4. Torgensen ML, Skretting G, Van Deurs B & Sandvig K (2001) Internalization of cholera toxin by different endocytic mechanisms. J Cell Sci 114, 3737-3747.
5. Shogomori H & Futerman AH (2001) Cholesterol depletion by methyl-beta-cyclodextrin blocks cholera toxin transport from endosomes to the Golgi apparatus in hippocampal neurons. J Neurochem 78, 991-999.
6. 125I- labeled cholera toxin taken up by rat liver in vivo. Eur J Biochem 163, 433-442.
7. Janicot M, Fouque F & Desbuquois B (1991) Activation of rat liver adenylate cyclase by cholera toxin requires toxin internalization and processing in endosomes. J Biol Chem 266, 12858-12865.
8. Sandvig K & Van Deurs B (2002) Membrane traffic exploited by protein toxins. Annu Rev Cell Dev Biol 18, 1-24.
9. Majoul I, Ferrari D & Soling HD (1997) Reduction of protein disulfide bonds in an oxidizing environment. The disulfide bridge of cholera toxin A-subunit is reduced in the endoplasmic reticulum. FEBS Lett 401, 104-108.
10. Schmitz A, Herrgen H, Winkeler A & Herzog V (2000) Cholera toxin is exported from microsomes by the Sec61p complex. J Cell Biol 148, 1203-1212.
11. Authier F, Mort JS, Bell AW, Posner BI & Bergeron JJM (1995) Proteolysis of glucagon within hepatic endosomes by membrane-associated cathepsins B and D. J Biol Chem 270, 15798-15807.
12. Authier F, Métioui M, Fabrega S, Kouach M & Briand G (2002) Endosomal proteolysis of internalized insulin at the C-terminal region of the B chain by cathepsin D. J Biol Chem 277, 9437-9446.
13. Authier F, Métioui M, Bell AW & Mort JS (1999) Negative regulation of epidermal growth factor signaling by selective proteolytic mechanisms in the endosome mediated by cathepsin B. J Biol Chem 274, 33723-33731.
14. Authier F, Danielsen GM, Kouach M, Briand G & Chauvet G (2001) Identification of insulin domains important for binding to and degradation by endosomal acidic insulinase. Endocrinology 142, 276-289.
15. 2+. Mol Endocrinol 1, 472-481.
16. Cuatrecasas P (1973) Interaction of Vibrio cholerae enterotoxin with cell membranes. Biochemistry 12, 3547-3558.
17. Cuatrecasas P (1973) Gangliosides and membrane receptors for cholera toxin. Biochemistry 12, 3558-3566.
18. Janicot M, Clot JP & Desbuquois B (1988) Interactions of cholera toxin with isolated hepatocytes. Biochem J 253, 735-743.
19. Montesano R, Roth J, Robert A & Orci L (1982) Non-coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature 296, 651-653.
20. Henley JR, Krueger EW, Oswald BJ & McNiven MA (1998) Dynamin-mediated internalization of caveolae. J Cell Biol 141, 85-99.
21. Calvo M, Tebar F, Lopez-Iglesias C & Enrich C (2001) Morphologic and functional characterization of caveolae in rat liver hepatocytes. Hepatology 33, 1259-1269.
22. Zeng L & Houslay MD (1995) Insulin and vasopressin elicit inhibition of cholera-toxin-stimulated adenylate cyclase activity in both hepatocytes and the P9 immortalized hepatocyte cell line through an action involving protein kinase C. Biochem J 312, 769-774.
23. Millar DG & Hirst RT (2001) Cholera toxin and Escherichia coli enterotoxin B-subunits inhibit macrophage-mediated antigen processing and presentation: evidence for antigen persistence in non-acidic recycling endosomal compartments. Cell Microbiol 3, 311-329.
24. Villadangos JA, Bryant RA, Deussing J, Driessen C, Lennon-Dumenil AM, Riese RJ, Roth W, Saftig P, Shi GP, Chapman HA, Peters C & Ploegh HL (1999) Proteases involved in MHC class II antigen presentation. Immunol Rev 172, 109-120.
25. Diment S, Martin KJ & Stahl PD (1989) Cleavage of parathyroid hormone in macrophage endosomes illustrates a novel pathway for intracellular processing of proteins. J Biol Chem 264, 13403-13406.
26. Blum JS, Diaz R, Mayorga LS & Stahl PD (1993) Reconstitution of endosomal transport and proteolysis. In Subcellular Biochemistry (Bergeron, JJM & Harris, JR, eds), Vol. 19, pp. 69-93. Plenum Publishing Corp, New York, USA.
27. Grüninger-Leitch F, Berndt P, Langen H, Nelboeck P & Dobeli H (2000) Identification of beta-secretase-like activity using a mass spectrometry-based assay system. Nat Biotechnol 18, 66-70.
28. Fiani ML, Blum JS & Stahl PD (1993) Endosomal proteolysis precedes ricin A-chain toxicity in macrophages. Arch Biochem Biophys 307, 225-230.
29. Gordon VM, Kumpel KR, Arora N, Henderson MA & Leppla SH (1995) Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases. Infect Immun 63, 82-87.
30. Nakayama K, Watanabe T, Nakagawa T, Kim WS, Nagahama M, Hosaka M, Hatsuzawa K, Kondoh-Hashiba K & Murakami K (1992) Consensus sequence for precursor processing at mono-arginyl sites. Evidence for the involvement of a Kex2-like endoprotease in precursor cleavages at both dibasic and mono-arginyl sites. J Biol Chem 267, 16335-16340.
31. Chiron MF, Fryling CM & FitzGerald DJ (1994) Cleavage of pseudomonas exotoxin and diphtheria toxin by a furin-like enzyme prepared from beef liver. J Biol Chem 269, 18167-18176.
32. Lencer WI, Hirst TR & Holmes RK (1999) Membrane traffic and the cellular uptake of cholera toxin. Biochim Biophys Acta 1450, 177-190.
33. Lencer WI, Constable C, Moe S, Jobling MG, Webb HM, Ruston S, Madara JL, Hirst TR & Holmes RK (1995) Targeting of cholera toxin and Escherichia coli heat labile toxin in polarized epithelia: role of COOH-terminal KDEL. J Cell Biol 131, 951-962.
34. Klausner RD, Donaldson JG & Lippincott-Schwartz J (1992) Brefeldin A: insights into the control of membrane traffic and organelle structure. J Cell Biol 116, 1071-1080.
35. Orlandi PA (1997) Protein-disulfide isomerase-mediated reduction of the A subunit of cholera toxin in a human intestinal cell line. J Biol Chem 272, 4591-4599.
36. Hazes B & Read RJ (1997) Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry 36, 11051-11054.
37. Orlandi PA, Curran PK & Fishman PH (1993) Brefeldin A blocks the response of cultured cells to cholera toxin. Implications for intracellular trafficking in toxin action. J Biol Chem 268, 12010-12016.
38. Van Dyke RW (1997) Cholera and pertussis toxins increase acidification of endocytic vesicles without altering ion conductances. Am J Physiol 272, C1123-C1133.
39. Colombo MI, Mayorga LS, Casey PJ & Stahl PD (1992) Evidence of a role for heterotrimeric GTP-binding proteins in endosome fusion. Science 255, 1695-1697.
40. Van Dyke RW (2004) Heterotrimeric G protein subunits are located on rat liver endosomes. BMC Physiol 4, 1-16.
41. Haraguchi K & Rodbell M (1990) Isoproterenol stimulates shift of G proteins from plasma membrane to pinocytotic vesicles in rat adipocytes: a possible means of signal dissemination. Proc Natl Acad Sci USA 87, 1208-1212.
42. Cheng H & Farquhar MG (1976) Presence of adenylate cyclase activity in Golgi and other fractions from rat liver. I. Biochemical determination. J Cell Biol 70, 660-670.
43. Authier F, Desbuquois B & De Galle B (1992) Ligand-mediated internalization of glucagon receptors in intact rat liver. Endocrinology 131, 447-457.
44. Colombo MI, Mayorga LS, Nishimoto I, Ross EM & Stahl PD (1994) Gs regulation of endosome fusion suggests a role for signal transduction pathways in endocytosis. J Biol Chem 269, 14919-14923.
45. B27]insulin in rat liver in vivo. Biochem J 332, 421-430.
46. Lowry OH, Rosebrough NJ, Farr AL & Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265-275.
47. Laemmli U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.