Evaluation of ubiquitinated proteins by proteomics reveals the role of the ubiquitin proteasome system in the regulation of Grp75 and Grp78 chaperone proteins during intestinal inflammation

Proteomics

Volumn 13, Issue 22, 2013, Pages 3284-3292

  Bertrand, Julien ^a,b   Tennoune, Naouel ^a,b   Marion Letellier, Rachel ^a,b   Goichon, Alexis ^a,b   Chan, Philippe ^b,c   Mbodji, Khaly ^a,b   Vaudry, David ^a,b,c   Déchelotte, Pierre ^a,b,d   Coëffier, Moïse ^a,b,d  

^a UNIVERSITÉ DE ROUEN   (France)

^b UNIVERSITY OF ROUEN   (France)

^c Mont Saint Aignan   (France)

^d ROUEN UNIVERSITY HOSPITAL   (France)

Author keywords

Cell biology; HSPs; Inflammation; Intestine; Proteasome; Ubiquitin

Indexed keywords

CHAPERONE; GAMMA INTERFERON; GLUCOSE REGULATED PROTEIN 75; GLUCOSE REGULATED PROTEIN 78; HEAT SHOCK COGNATE PROTEIN 70; INTERLEUKIN 1BETA; INTERLEUKIN 8; PROTEASOME; TUMOR NECROSIS FACTOR ALPHA; UBIQUITIN; UBIQUITINATED PROTEIN; UNCLASSIFIED DRUG; GLUCOSE-REGULATED PROTEINS; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; MEMBRANE PROTEIN; MOLECULAR CHAPERONE GRP78; TRINITROBENZENESULFONIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; ELECTROSPRAY MASS SPECTROMETRY; IMMUNODETECTION; IMMUNOPRECIPITATION; IRRITABLE COLON; LIQUID CHROMATOGRAPHY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEOMICS; RAT; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS; UBIQUITINATION; ANIMAL; CHEMICALLY INDUCED; CHEMISTRY; COLON; HUMAN; INTESTINE MUCOSA; METABOLISM; PROCEDURES; TOXICITY; TUMOR CELL LINE; WISTAR RAT;

ANIMALS; CELL LINE, TUMOR; COLITIS; COLON; HEAT-SHOCK PROTEINS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; INTERLEUKIN-8; INTESTINAL MUCOSA; MALE; MEMBRANE PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOMICS; RATS; RATS, WISTAR; TRINITROBENZENESULFONIC ACID; UBIQUITIN; UBIQUITINATED PROTEINS;

EID: 84888033468     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201300082     Document Type: Article

References (44)

1. Glickman, M. H., Ciechanover, A., The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 2002, 82, 373-428.
2. Monaco, J. J., Nandi, D., The genetics of proteasomes and antigen processing. Annu. Rev. Genet. 1995, 29, 729-754.
3. Visekruna, A., Joeris, T., Seidel, D., Kroesen, A. et al., Proteasome-mediated degradation of IkappaBalpha and processing of p105 in Crohn disease and ulcerative colitis. J. Clin. Invest. 2006, 116, 3195-3203.
4. Xavier, R. J., Podolsky, D. K., Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007, 448, 427-434.
5. Bouma, G., Strober, W., The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 2003, 3, 521-533.
6. Drossman, D. A., Camilleri, M., Mayer, E. A., Whitehead, W. E., AGA technical review on irritable bowel syndrome. Gastroenterology 2002, 123, 2108-2131.
7. Thompson, W. G., Longstreth, G. F., Drossman, D. A., Heaton, K. W. et al., Functional bowel disorders and functional abdominal pain. Gut 1999, 45(Suppl 2), II43-II47.
8. Bertiaux-Vandaele, N., Youmba, S. B., Belmonte, L., Lecleire, S. et al., The expression and the cellular distribution of the tight junction proteins are altered in irritable bowel syndrome patients with differences according to the disease subtype. Am. J. Gastroenterol. 2011, 106, 2165-2173.
9. Tache, Y., Martinez, V., Wang, L., Million, M., CRF1 receptor signaling pathways are involved in stress-related alterations of colonic function and viscerosensitivity: implications for irritable bowel syndrome. Br. J. Pharmacol. 2004, 141, 1321-1330.
10. Leblond, J., Hubert-Buron, A., Bole-Feysot, C., Ducrotte, P. et al., Regulation of proteolysis by cytokines in the human intestinal epithelial cell line HCT-8: role of IFNgamma. Biochimie 2006, 88, 759-765.
11. Coeffier, M., Gloro, R., Boukhettala, N., Aziz, M. et al., Increased proteasome-mediated degradation of occludin in irritable bowel syndrome. Am. J. Gastroenterol. 2010, 105, 1181-1188.
12. Tsukamoto, S., Yokosawa, H., Targeting the proteasome pathway. Expert Opin. Ther. Targets 2009, 13, 605-621.
13. Inoue, S., Nakase, H., Matsuura, M., Mikami, S. et al., The effect of proteasome inhibitor MG132 on experimental inflammatory bowel disease. Clin. Exp. Immunol. 2009, 156, 172-182.
14. Lin, K. I., Baraban, J. M., Ratan, R. R., Inhibition versus induction of apoptosis by proteasome inhibitors depends on concentration. Cell Death Differ. 1998, 5, 577-583.
15. Meiners, S., Ludwig, A., Stangl, V., Stangl, K., Proteasome inhibitors: poisons and remedies. Med. Res. Rev. 2008, 28, 309-327.
16. Tilahun, A. Y., Theuer, J. E., Patel, R., David, C. S., Rajagopalan, G., Detrimental effect of the proteasome inhibitor, bortezomib in bacterial superantigen- and lipopolysaccharide-induced systemic inflammation. Mol. Ther. 2010, 18, 1143-1154.
17. Grande, E., Earl, J., Fuentes, R., Carrato, A., New targeted approaches against the ubiquitin-proteasome system in gastrointestinal malignancies. Expert Rev. Anticancer Ther. 2012, 12, 457-467.
18. Tan, M., Li, Y., Yang, R., Xi, N., Sun, Y., Inactivation of SAG E3 ubiquitin ligase blocks embryonic stem cell differentiation and sensitizes leukemia cells to retinoid acid. PloS One 2011, 6, e27726.
19. Marion, R., Coeffier, M., Leplingard, A., Favennec, L. et al., Cytokine-stimulated nitric oxide production and inducible NO-synthase mRNA level in human intestinal cells: lack of modulation by glutamine. Clin. Nutr. 2003, 22, 523-528.
20. O'Farrell, P. H., High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 1975, 250, 4007-4021.
21. Mbodji, K., Charpentier, C., Guerin, C., Querec, C. et al., Adjunct therapy of n-3 fatty acids to 5-ASA ameliorates inflammatory score and decreases NF-kappaB in rats with TNBS-induced colitis. J. Nutr. Biochem. 2012, 24, 700-705.
22. Ponferrada, A., Caso, J. R., Alou, L., Colon, A. et al., The role of PPARgamma on restoration of colonic homeostasis after experimental stress-induced inflammation and dysfunction. Gastroenterology 2007, 132, 1791-1803.
23. Li, J., Lee, B., Lee, A. S., Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J. Biol. Chem. 2006, 281, 7260-7270.
24. Lee, A. S., The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem. Sci. 2001, 26, 504-510.
25. Hendershot, L. M., The ER function BiP is a master regulator of ER function. Mount Sinai J. Med. 2004, 71, 289-297.
26. Shkoda, A., Ruiz, P. A., Daniel, H., Kim, S. C. et al., Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology 2007, 132, 190-207.
27. Bogaert, S., De Vos, M., Olievier, K., Peeters, H. et al., Involvement of endoplasmic reticulum stress in inflammatory bowel disease: a different implication for colonic and ileal disease? PloS One 2011, 6, e25589.
28. Treton, X., Pedruzzi, E., Cazals-Hatem, D., Grodet, A. et al., Altered endoplasmic reticulum stress affects translation in inactive colon tissue from patients with ulcerative colitis. Gastroenterology 2011, 141, 1024-1035.
29. Lopitz-Otsoa, F., Rodriguez-Suarez, E., Aillet, F., Casado-Vela, J. et al., Integrative analysis of the ubiquitin proteome isolated using tandem ubiquitin binding entities (TUBEs). J. Proteomics 2012, 75, 2998-3014.
30. Wadhwa, R., Kaul, S. C., Ikawa, Y., Sugimoto, Y., Identification of a novel member of mouse hsp70 family. Its association with cellular mortal phenotype. J. Biol. Chem. 1993, 268, 6615-6621.
31. Wadhwa, R., Taira, K., Kaul, S. C., An Hsp70 family chaperone, mortalin/mthsp70/PBP74/Grp75: what, when, and where? Cell Stress Chaperones 2002, 7, 309-316.
32. Sitja-Bobadilla, A., Calduch-Giner, J., Saera-Vila, A., Palenzuela, O. et al., Chronic exposure to the parasite Enteromyxum leei (Myxozoa: Myxosporea) modulates the immune response and the expression of growth, redox and immune relevant genes in gilthead sea bream, Sparus aurata L. Fish Shellfish Immunol. 2008, 24, 610-619.
33. Dundas, S. R., Lawrie, L. C., Rooney, P. H., Murray, G. I., Mortalin is over-expressed by colorectal adenocarcinomas and correlates with poor survival. J. Pathol. 2005, 205, 74-81.
34. Lu, W. J., Lee, N. P., Kaul, S. C., Lan, F. et al., Mortalin-p53 interaction in cancer cells is stress dependent and constitutes a selective target for cancer therapy. Cell Death Differ. 2011, 18, 1046-1056.
35. Beckmann, R. P., Mizzen, L. E., Welch, W. J., Interaction of Hsp 70 with newly synthesized proteins: implications for protein folding and assembly. Science 1990, 248, 850-854.
36. Chirico, W. J., Waters, M. G., Blobel, G., 70K heat shock related proteins stimulate protein translocation into microsomes. Nature 1988, 332, 805-810.
37. Bercovich, B., Stancovski, I., Mayer, A., Blumenfeld, N. et al., Ubiquitin-dependent degradation of certain protein substrates in vitro requires the molecular chaperone Hsc70. J. Biol. Chem. 1997, 272, 9002-9010.
38. Esser, C., Scheffner, M., Hohfeld, J., The chaperone-associated ubiquitin ligase CHIP is able to target p53 for proteasomal degradation. J. Biol. Chem. 2005, 280, 27443-27448.
39. Kubota, H., Yamamoto, S., Itoh, E., Abe, Y. et al., Increased expression of co-chaperone HOP with HSP90 and HSC70 and complex formation in human colonic carcinoma. Cell Stress Chaperones 2010, 15, 1003-1011.
40. Bomsztyk, K., Denisenko, O., Ostrowski, J., hnRNP K: one protein multiple processes. BioEssays 2004, 26, 629-638.
41. Davison, E. J., Pennington, K., Hung, C. C., Peng, J. et al., Proteomic analysis of increased Parkin expression and its interactants provides evidence for a role in modulation of mitochondrial function. Proteomics 2009, 9, 4284-4297.
42. Noguchi, E., Homma, Y., Kang, X., Netea, M. G., Ma, X., A Crohn's disease-associated NOD2 mutation suppresses transcription of human IL10 by inhibiting activity of the nuclear ribonucleoprotein hnRNP-A1. Nat. Immunol. 2009, 10, 471-479.
43. Cooley, J., Takayama, T. K., Shapiro, S. D., Schechter, N. M., Remold-O'Donnell, E., The serpin MNEI inhibits elastase-like and chymotrypsin-like serine proteases through efficient reactions at two active sites. Biochemistry 2001, 40, 15762-15770.
44. Uchiyama, K., Naito, Y., Takagi, T., Mizushima, K. et al., Serpin B1 protects colonic epithelial cell via blockage of neutrophil elastase activity and its expression is enhanced in patients with ulcerative colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 302, G1163-G1170.