Carrageenan inhibits insulin signaling through GRB10-mediated decrease in Tyr(P)-IRS1 and through inflammation-induced increase in Ser(P)307-IRS1

Journal of Biological Chemistry

Volumn 290, Issue 17, 2015, Pages 10764-10774

  Bhattacharyya, Sumit ^a,b   Feferman, Leo ^a,b   Tobacman, Joanne K ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b JESSE BROWN VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; PATHOLOGY; PHOSPHORYLATION; PROTEINS; SIGNALING;

AKT PHOSPHORYLATION; GROWTH FACTOR RECEPTORS; NEGATIVE REGULATORS; PROMOTER ACTIVITIES; REACTIVE OXYGEN SPECIES; RECEPTOR SUBSTRATES; TRANSCRIPTIONAL MECHANISMS; TYROSINE PHOSPHORYLATION;

INSULIN;

2 MORPHOLINO 8 PHENYLCHROMONE; ADAPTOR PROTEIN; CARRAGEENAN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 10; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; REACTIVE OXYGEN METABOLITE; SERINE; TEMPOL; TRANSCRIPTION FACTOR GATA 2; TYROSINE; GATA2 PROTEIN, HUMAN; GATA2 PROTEIN, MOUSE; GRB10 PROTEIN, HUMAN; GRB10 PROTEIN, MOUSE; INSULIN RECEPTOR SUBSTRATE; IRS1 PROTEIN, HUMAN; IRS1 PROTEIN, MOUSE; PROTEIN KINASE B; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HEPG2 CELL LINE; HUMAN; HUMAN CELL; INFLAMMATION; INSULIN RESPONSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; INSULIN RESISTANCE; MALE; METABOLISM; MOUSE; PHOSPHORYLATION; PROMOTER REGION; SIGNAL TRANSDUCTION; STATISTICAL MODEL;

MUS;

ANIMALS; CARRAGEENAN; GATA2 TRANSCRIPTION FACTOR; GENE EXPRESSION; GRB10 ADAPTOR PROTEIN; HEP G2 CELLS; HUMANS; INFLAMMATION; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; MALE; MICE; MICE, INBRED C57BL; MODELS, STATISTICAL; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; RNA, SMALL INTERFERING; SERINE; SIGNAL TRANSDUCTION; TYROSINE;

EID: 84928397780     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.630053     Document Type: Article

References (43)

1. Bhattacharyya, S., O'Sullivan, I., Katyal, S., Unterman, T., and Tobacman, J. K. (2012) Exposure to the common food additive carrageenan leads to glucose intolerance, insulin resistance and inhibition of insulin signaling in HepG2 cells and C57BL/6J mice. Diabetologia 55, 194-203
2. Borthakur, A., Bhattacharyya, S., Dudeja, P. K., and Tobacman, J. K. (2007) Carrageenan induces interleukin-8 production through distinct Bcl10 pathway in normal human colonic epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 292, G829-G838
3. Bhattacharyya, S., Gill, R., Chen M.-L., Zhang, F., Linhardt, R. J., Dudeja, P. K., and Tobacman, J. K. (2008) Toll-like receptor 4 mediates induction of Bcl10-NFκB-IL-8 inflammatory pathway by carrageenan in human intestinal epithelial cells. J. Biol. Chem. 283, 10550-10558
4. Bhattacharyya, S., Dudeja, P. K., and Tobacman, J. K. (2008) Carrageenan-induced NFκB activation depends on distinct pathways mediated by reactive oxygen species and Hsp27 or by Bcl10. Biochim. Biophys. Acta 1780, 973-982
5. Bhattacharyya, S., Borthakur, A., Tyagi, S., Gill, R., Chen, M. L., Dudeja, P. K., and Tobacman, J. K. (2010) BCL10 is required for NFκB nuclear translocation by both canonical and non-canonical pathways and for NIK phosphorylation. J. Biol. Chem. 285, 522-530
6. Gao, Z., Hwang, D., Bataille, F., Lefevre, M., York, D., Quon, M. J., and Ye J. (2002) Serine phosphorylation of insulin receptor substrate 1 by inhibitor κB kinase complex. J. Biol. Chem. 277, 48115-48121
7. Nakamori, Y., Emoto, M., Fukuda, N., Taguchi, A., Okuya, S., Tajiri, M., Miyagishi, M., Taira, K., Wada, Y., and Tanizawa Y. (2006) Myosin motor Myo1c and its receptor NEMO/IKK-γ promote TNF-α-induced serine 307 phosphorylation of IRS-1. J. Cell Biol. 173, 665-671
8. Kanety, H., Feinstein, R., Papa, M. Z., Hemi, R., and Karasik A. (1995) Tumor necrosis factor α-induced phosphorylation of insulin receptor substrate-1 (IRS-1): possible mechanism for suppression of insulin-stimulated tyrosine phosphorylation of IRS-1. J. Biol. Chem. 270, 23780-23784
9. Huret, J. L., Ahmad, M., Arsaban, M., Bernheim, A., Cigna, J., Desangles, F., Guignard, J. C., Jacquemot-Perbal, M. C., Labarussias, M., Leberre, V., Malo, A., Morel-Pair, C., Mossafa, H., Potier, J. C., Texier, G., Viguio, F., Wan, Y. C., Senon, S., Zasadzinski, A., and Dessen, P. (2013) Atlas of genetics and cytogenetics in oncology and haematology in 2013. Nucleic Acids Res. 41, D920-D924
10. Depetris, R. S., Wu, J., and Hubbard, S. R. (2009) Structural and functional studies of the Ras-associating and pleckstrin-homology domains of Grb10 and Grb14. Nat. Struct. Mol. Biol. 16, 833-839
11. Dong, L. Q., Du, H., Porter, S. G., Kolakowski, L. F., Jr., Lee, A. V., Mandarino, L. J., Fan, J., Yee, D., Liu, F., and Mandarino J. (1997) Cloning, chromosome localization, expression, and characterization of an Src homology 2 and pleckstrin homology domain-containing insulin receptor binding protein hGrb10γ. J. Biol. Chem. 272, 29104-29112
12. Laviola, L., Giorgino, F., Chow, J. C., Baquero, J. A., Hansen, H., Ooi, J., Zhu, J., Riedel, H., and Smith, R. J. (1997) The adapter protein Grb10 associates preferentially with the insulin receptor as compared with the IGF-1 receptor in mouse fibroblasts. J. Clin. Invest. 99, 830-837
13. Hansen, H., Svensson, U., Zhu, J., Laviola, L., Giorgino, F., Wolf, G., Smith, R. J., and Riedel H. (1996) Interaction between the Grb10 SH2 domain and the insulin receptor carboxyl terminus. J. Biol. Chem. 271, 8882-8886
14. Wick, K. R., Werner, E. D., Langlais, P., Ramos, F. J., Dong, L. Q., Shoelson, S. E., and Liu F. (2003) Grb10 inhibits insulin-stimulated insulin receptor substrate (IRS)-phosphatidylinositol 3-kinase/Akt signaling pathway by disrupting the association of IRS-1/IRS-2 with the insulin receptor. J. Biol. Chem. 278, 8460-8467
15. Dufresne, A. M., and Smith, R. J. (2005) The adapter protein GRB10 is an endogenous negative regulator of insulin-like growth factor signaling. Endocrinology 146, 4399-4409
16. Wang, L., Balas, B., Christ-Roberts, C. Y., Kim, R. Y., Ramos, F. J., Kikani, C. K., Li, C., Deng, C., Reyna, S., Musi, N., Dong, L. Q., DeFronzo, R. A., and Liu F. (2007) Peripheral disruption of the Grb10 gene enhances insulin signaling and sensitivity in vivo. Mol. Cell. Biol. 27, 6497-6505
17. Rampersaud, E., Damcott, C. M., Fu, M., Shen, H., McArdle, P., Shi, X., Shelton, J., Yin, J., Chang, Y. P., Ott, S. H., Zhang, L., Zhao, Y., Mitchell, B. D., O'Connell, J., and Shuldiner, A. R. (2007) Identification of novel candidate genes for type 2 diabetes from a genome-wide association scan in the old order Amish. Diabetes 56, 3053-3062
18. Di Paola, R., Wojcik, J., Succurro, E., Marucci, A., Chandalia, M., Padovano, L., Powers, C., Merla, G., Abate, N., Sesti, G., Doria, A., and Trischitta V. (2010) GRB10 gene and type 2 diabetes in whites. J. Intern. Med. 267, 132-133
19. Di Paola, R., Ciociola, E., Boonyasrisawat, W., Nolan, D., Duffy, J., Miscio, G., Cisternino, C., Fini, G., Tassi, V., Doria, A., and Trischitta V. (2006) Association of hGrb10 genetic variations with type 2 diabetes in Caucasian subjects. Diabetes Care 29, 1181-1183
20. Yamamoto, Y., Ishino, F., Kaneko-Ishino, T., Shiura, H., Uchio-Yamada, K., Matsuda, J., Suzuki, O., and Sato K. (2008) Type 2 diabetes mellitus in a non-obese mouse model induced by Meg/Grb10. Exp. Anim. 57, 385-395
21. Charalambous, M., Smith, F. M., Bennett, W. R., Crew, T. E., Mackenzie, F., and Ward A. (2003) Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proc. Natl. Acad. Sci. U.S.A. 100, 8292-8297
22. Shiura, H., Miyoshi, N., Konishi, A., Wakisaka-Saito, N., Suzuki, R., Muguruma, K., Kohda, T., Wakana, S., Yokoyama, M., Ishino, F., and Kaneko-Ishino T. (2005) Meg1/Grb10 overexpression causes postnatal growth retardation and insulin resistance via negative modulation of the IGF1R and IR cascades. Biochem. Biophys. Res. Commun. 329, 909-916
23. Prokopenko, I., Poon, W., Mägi, R., Prasad, B. R., Salehi, S. A., Almgren, P., Osmark, P., Bouatia-Naji, N., Wierup, N., Fall, T., Stančáková, A., Barker, A., Lagou, V., Osmond, C., Xie, W., Lahti, J., Jackson, A. U., Cheng, Y. C., Liu, J., O'Connell, J. R., Blomstedt, P. A., Fadista, J., Alkayyali, S., Dayeh, T., Ahlqvist, E., Taneera, J., Lecoeur, C., Kumar, A., Hansson, O., Hansson, K., Voight, B. F., Kang, H. M., Levy-Marchal, C., Vatin, V., Palotie, A., Syvänen, A. C., Mari, A., Weedon, M. N., Loos, R. J., Ong, K. K., Nilsson, P., Isomaa, B., Tuomi, T., Wareham, N. J., Stumvoll, M., Widen, E., Lakka, T. A., Langenberg, C., Tönjes, A., Rauramaa, R., Kuusisto, J., Frayling, T. M., Froguel, P., Walker, M., Eriksson, J. G., Ling, C., Kovacs, P., Ingelsson, E., McCarthy, M. I., Shuldiner, A. R., Silver, K. D., Laakso, M., Groop, L., and Lyssenko, V. A. (2014) Central Role for GRB10 in regulation of islet function in man. PLoS Genet. 10, e1004235
24. Monk, D., Arnaud, P., Frost, J., Hills, F. A., Stanier, P., Feil, R., and Moore, G. E. (2009) Reciprocal imprinting of human GRB10 in placental trophoblast and brain: evolutionary conservation of reversed allelic expression. Hum. Mol. Genet. 18, 3066-3074
25. Garfield, A. S., Cowley, M., Smith, F. M., Moorwood, K., Stewart-Cox, J. E., Gilroy, K., Baker, S., Xia, J., Dalley, J. W., Hurst, L. D., Wilkinson, L. S., Isles, A. R., and Ward A. (2011) Distinct physiological and behavioral functions for parental alleles of imprinted Grb10. Nature 469, 534-538
26. Macher, B. A., and Galili U. (2008) The Gal-α-1,3-Gal-β-1,4-GlcNAc-R (α-Gal) epitope: a carbohydrate of unique evolution and clinical relevance. Biochim. Biophys. Acta 1780, 75-88
27. Tanemura, M., Yin, D., Chong, A. S., and Galili U. (2000) Differential immune responses to α-gal epitopes on xenografts and allografts: implications for accommodation in xenotransplantation. J. Clin. Invest. 105, 301-310
28. Galili U. (2005) The α-gal epitope and the anti-Gal antibody in xenotransplantation and in cancer immunotherapy. Immunol. Cell Biol. 83, 674-686
29. Bhattacharyya, S., Liu, H., Zhang, Z., Jam, M., Dudeja, P. K., Michel, G., Linhardt, R. J., and Tobacman, J. K. (2010) Carrageenan-induced innate immune response is modified by enzymes that hydrolyze distinct galactosidic bonds. J. Nutr. Biochem. 21, 906-913
30. Shi, H., Kokoeva, M. V., Inouye, K., Tzameli, I., Yin, H., and Flier, J. S. (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116, 3015-3025
31. Song, M. J., Kim, K. H., Yoon, J. M., and Kim, J. B. (2006) Activation of Toll-like receptor 4 is associated with insulin resistance in adipocytes. Biochem. Biophys. Res. Commun. 346, 739-745
32. Mohammad, M. K., Morran, M., Slotterbeck, B., Leaman, D. W., Sun, Y., Grafenstein, H., Hong, S. C., and McInerney, M. F. (2006) Dysregulated Toll-like receptor expression and signaling in bone marrow-derived macrophages at the onset of diabetes in the non-obese diabetic mouse. Int. Immunol. 18, 1101-1113
33. Bhattacharyya, S., Pant, N., Dudeja, P. K., and Tobacman, J. K. (2007) Development, evaluation, and application of a highly sensitive microtiter plate ELISA for human BCL10 protein. J. Immunoassay Immunochem. 28, 173-188
34. Vlahos, C. J., Matter, W. F., Hui, K. Y., and Brown, R. F. (1994) A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J. Biol. Chem. 269, 5241-5248
35. Ballou, L. M., Selinger, E. S., Choi, J. Y., Drueckhammer, D. G., and Lin RZ (2007) Inhibition of mammalian target of rapamycin signaling by 2-(morpholin-1-yl)pyrimidol[2,1-α]isoquinolin-4-one. J. Biol. Chem. 282, 24463-24470
36. Bhattacharyya, S., Feferman, L., and Tobacman, J. K. (2014) Arylsulfatase B regulates versican expression by galectin-3 and AP-1 mediated transcriptional effects. Oncogene 33, 5467-5476
37. Heinemeyer, T., Wingender, E., Reuter, I., Hermjakob, H., Kel, A. E., Kel, O. V., Ignatieva, E. V., Ananko, E. A., Podkolodnaya, O. A., Kolpakov, F. A., Podkolodny, N. L., and Kolchanov, N. A. (1998) Databases on transcriptional regulation: TRANSFAC, TRRD, and COMPEL. Nucleic Acids Res. 26, 362-367
38. Menghini R., Marchetti, V., Cardellini, M., Hribal, M. L., Mauriello, A., Lauro, D., Sbraccia, P., Lauro, R., and Federici M. (2005) Phosphorylation of GATA2 by Akt increases adipose tissue differentiation and reduces atherosclerosis, adipose tissue-related inflammation: a novel pathway linking obesity to atherosclerosis. Circulation 111, 1946-1953
39. Hançer, N. J., Qiu, W., Cherella, C., Li, Y., Copps, K. D., and White, M. F. (2014) Insulin and metabolic stress stimulate multisite serine/threonine phosphorylation of insulin receptor substrate 1 and inhibit tyrosine phosphorylation. J. Biol. Chem. 289, 12467-12484
40. Boura-Halfon, S., and Zick Y. (2009) Phosphorylation of IRS proteins, insulin action, and insulin resistance. Am. J. Physiol. Endocrinol. Metab. 296, E581-E591
41. Samuel, V. T., and Shulman, G. I. (2012) Mechanisms for insulin resistance: common threads and missing links. Cell 148, 852-871
42. Copps, K. D., and White, M. F. (2012) Regulation of insulin sensitivity by serine/threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia 55, 2565-2582
43. Towatari, M., May, G. E., Marais, R., Perkins, G. R., Marshall, C. J., Cowley, S., and Enver T. (1995) Regulation of GATA2 phosphorylation by mitogen-activated protein kinase and interleukin-3. J. Biol. Chem. 270, 4101-4107