Stabilization of HIF through inhibition of Cullin-2 neddylation is protective in mucosal inflammatory responses

FASEB Journal

Volumn 29, Issue 1, 2015, Pages 208-215

  Curtis, Valerie F ^a   Ehrentraut, Stefan F ^a   Campbell, Eric L ^a   Glover, Louise E ^a   Bayless, Amanda ^a   Kelly, Caleb J ^a   Kominsky, Douglas J ^a,b   Colgan, Sean P ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

Hypoxia; Inflammation; Intestinal epithelia

Indexed keywords

CULLIN; CULLIN 2; DEXTRAN SULFATE; HYPOXIA INDUCIBLE FACTOR; PEVONEDISTAT; UNCLASSIFIED DRUG; ((1S,2S,4R)-4-(4-((1S)-2,3-DIHYDRO-1H-INDEN-1-YLAMINO)-7H-PYRROLO(2,3-D)PYRIMIDIN-7-YL)-2-HYDROXYCYCLOPENTYL)METHYL SULPHAMATE; CUL2 PROTEIN, HUMAN; CYCLOPENTANE DERIVATIVE; HIF1A PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NEDD8 PROTEIN, HUMAN; PROTEINASE; PROTEINASE INHIBITOR; PYRIMIDINE DERIVATIVE; SENP8 PROTEIN, HUMAN; UBIQUITIN;

ANIMAL EXPERIMENT; ARTICLE; COLITIS; COLON LENGTH; CONTROLLED STUDY; DISEASE SEVERITY; DRUG MECHANISM; DRUG TARGETING; FEMALE; GENE TARGETING; HUMAN; HUMAN CELL; IC50; IN VITRO STUDY; IN VIVO STUDY; INTESTINE EPITHELIUM CELL; INTESTINE PARAMETERS; MOUSE; MUCOSA INFLAMMATION; NEDDYLATION; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; PROMOTER REGION; WEIGHT REDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL LINE; DISEASE MODEL; GENE SILENCING; GENETICS; HELA CELL LINE; INFLAMMATORY BOWEL DISEASES; INTESTINE MUCOSA; METABOLISM; PATHOLOGY; PROTEIN STABILITY;

MURINAE;

ANIMALS; CELL LINE; CULLIN PROTEINS; CYCLOPENTANES; DISEASE MODELS, ANIMAL; ENDOPEPTIDASES; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; METABOLIC NETWORKS AND PATHWAYS; MICE, INBRED C57BL; PROTEASE INHIBITORS; PROTEIN STABILITY; PYRIMIDINES; UBIQUITINS;

EID: 84937513949     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-259663     Document Type: Article

References (36)

1. Xavier, R. J., and Podolsky, D. K. (2007) Unravelling the pathogenesis of inflammatory bowel disease. Nature 448, 427-434
2. Ehrentraut, S. F., and Colgan, S. P. (2012) Implications of protein post-translational modifications in IBD. Inflamm. Bowel Dis. 18, 1378-1388
3. Xirodimas, D. P. (2008) Novel substrates and functions for the ubiquitin-like molecule NEDD8. Biochem. Soc. Trans. 36, 802-806
4. Mikus, P., and Zundel, W. (2005) COPing with hypoxia. Semin. Cell Dev. Biol. 16, 462-473
5. Read, M. A., Brownell, J. E., Gladysheva, T. B., Hottelet, M., Parent, L. A., Coggins, M. B., Pierce, J. W., Podust, V. N., Luo, R. S., Chau, V., and Palombella, V. J. (2000) Nedd8 modification of cul-1 activates SCF(beta(TrCP))-dependent ubiquitination of IkappaBalpha. Mol. Cell. Biol. 20, 2326-2333
6. Liakopoulos, D., Büsgen, T., Brychzy, A., Jentsch, S., and Pause, A. (1999) Conjugation of the ubiquitin-like protein NEDD8 to cullin-2 is linked to von Hippel-Lindau tumor suppressor function. Proc. Natl. Acad. Sci. USA 96, 5510-5515
7. Wada, H., Yeh, E. T., and Kamitani, T. (1999) Identification of NEDD8-conjugation site in human cullin-2. Biochem. Biophys. Res. Commun. 257, 100-105
8. Amir, R. E., Iwai, K., and Ciechanover, A. (2002) The NEDD8 pathway is essential for SCF(beta-TrCP)-mediated ubiquitination and processing of the NF-kappa B precursor p105. J. Biol. Chem. 277, 23253-23259
9. Collier-Hyams, L. S., Sloane, V., Batten, B. C., and Neish, A. S. (2005) Cutting edge: bacterial modulation of epithelial signaling via changes in neddylation of cullin-1. J. Immunol. 175, 4194-4198
10. Kumar, A., Wu, H., Collier-Hyams, L. S., Kwon, Y. M., Hanson, J. M., and Neish, A. S. (2009) The bacterial fermentation product butyrate influences epithelial signaling via reactive oxygen species-mediated changes in cullin-1 neddylation. J. Immunol. 182, 538-546
11. Khoury, J., Ibla, J. C., Neish, A. S., and Colgan, S. P. (2007) Antiinflammatory adaptation to hypoxia through adenosine-mediated cullin-1 deneddylation. J. Clin. Invest. 117, 703-711
12. Maxwell, P. H., Wiesener, M. S., Chang, G. W., Clifford, S. C., Vaux, E. C., Cockman, M. E., Wykoff, C. C., Pugh, C. W., Maher, E. R., and Ratcliffe, P. J. (1999) The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 399, 271-275
13. Sufan, R. I., and Ohh, M. (2006) Role of the NEDD8 modification of Cul2 in the sequential activation of ECV complex. Neoplasia 8, 956-963
14. Colgan, S. P., and Taylor, C. T. (2010) Hypoxia: an alarm signal during intestinal inflammation. Nat. Rev. Gastroenterol. Hepatol. 7, 281-287
15. MacManus, C. F., Campbell, E. L., Keely, S., Burgess, A., Kominsky, D. J., and Colgan, S. P. (2011) Anti-inflammatory actions of adrenomedullin through fine tuning of HIF stabilization. FASEB J. 25, 1856-1864
16. Mendoza, H. M., Shen, L. N., Botting, C., Lewis, A., Chen, J., Ink, B., and Hay, R. T. (2003) NEDP1, a highly conserved cysteine protease that deNEDDylates Cullins. J. Biol. Chem. 278, 25637-25643
17. Gan-Erdene, T., Nagamalleswari, K., Yin, L., Wu, K., Pan, Z. Q., and Wilkinson, K. D. (2003) Identification and characterization of DEN1, a deneddylase of the ULP family. J. Biol. Chem. 278, 28892-28900
18. Wu, K., Yamoah, K., Dolios, G., Gan-Erdene, T., Tan, P., Chen, A., Lee, C. G., Wei, N., Wilkinson, K. D., Wang, R., and Pan, Z. Q. (2003) DEN1 is a dual function protease capable of processing the C terminus of Nedd8 and deconjugating hyper-neddylated CUL1. J. Biol. Chem. 278, 28882-28891
19. Ehrentraut, S. F., Kominsky, D. J., Glover, L. E., Campbell, E. L., Kelly, C. J., Bowers, B. E., Bayless, A. J., and Colgan, S. P. (2013) Central role for endothelial human deneddylase-1/SENP8 in finetuning the vascular inflammatory response. J. Immunol. 190, 392-400
20. Soucy, T. A., Smith, P. G., Milhollen, M. A., Berger, A. J., Gavin, J. M., Adhikari, S., Brownell, J. E., Burke, K. E., Cardin, D. P., Critchley, S., Cullis, C. A., Doucette, A., Garnsey, J. J., Gaulin, J. L., Gershman, R. E., Lublinsky, A. R., McDonald, A., Mizutani, H., Narayanan, U., Olhava, E. J., Peluso, S., Rezaei, M., Sintchak, M. D., Talreja, T., Thomas, M. P., Traore, T., Vyskocil, S., Weatherhead, G. S., Yu, J., Zhang, J., Dick, L. R., Claiborne, C. F., Rolfe, M., Bolen, J. B., and Langston, S. P. (2009) An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature 458, 732-736
21. Boh, B. K., Smith, P. G., and Hagen, T. (2011) Neddylation-induced conformational control regulates cullin RING ligase activity in vivo. J. Mol. Biol. 409, 136-145
22. Brownell, J. E., Sintchak, M. D., Gavin, J. M., Liao, H., Bruzzese, F. J., Bump, N. J., Soucy, T. A., Milhollen, M. A., Yang, X., Burkhardt, A. L., Ma, J., Loke, H. K., Lingaraj, T., Wu, D., Hamman, K. B., Spelman, J. J., Cullins, C. A., Langston, S. P., Vyskocil, S., Sells, T. B., Mallender, W. D., Visiers, I., Li, P., Claiborne, C. F., Rolfe, M., Bolen, J. B., and Dick, L. R. (2010) Substrate-assisted inhibition of ubiquitin-like protein-activating enzymes: the NEDD8 E1 inhibitor MLN4924 forms a NEDD8-AMP mimetic in situ. Mol. Cell 37, 102-111
23. Sheta, E. A., Trout, H., Gildea, J. J., Harding, M. A., and Theodorescu, D. (2001) Cell density mediated pericellular hypoxia leads to induction of HIF-1alpha via nitric oxide and Ras/MAP kinase mediated signaling pathways. Oncogene 20, 7624-7634
24. Furuta, G. T., Turner, J. R., Taylor, C. T., Hershberg, R. M., Comerford, K., Narravula, S., Podolsky, D. K., and Colgan, S. P. (2001) Hypoxia-inducible factor 1-dependent induction of intestinal trefoil factor protects barrier function during hypoxia. J. Exp. Med. 193, 1027-1034
25. Dieleman, L. A., Palmen, M. J., Akol, H., Bloemena, E., Peña, A. S., Meuwissen, S. G., and Van Rees, E. P. (1998) Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines. Clin. Exp. Immunol. 114, 385-391
26. Glover, L. E., Bowers, B. E., Saeedi, B., Ehrentraut, S. F., Campbell, E. L., Bayless, A. J., Dobrinskikh, E., Kendrick, A. A., Kelly, C. J., Burgess, A., Miller, L., Kominsky, D. J., Jedlicka, P., and Colgan, S. P. (2013) Control of creatine metabolism by HIF is an endogenous mechanism of barrier regulation in colitis. Proc. Natl. Acad. Sci. USA 110, 19820-19825
27. Hou, Y., Wang, L., Yi, D., Ding, B., Chen, X., Wang, Q., Zhu, H., Liu, Y., Yin, Y., Gong, J., and Wu, G. (2014) Dietary supplementation with tributyrin alleviates intestinal injury in piglets challenged with intrarectal administration of acetic acid. Br. J. Nutr. 111, 1748-1758
28. Leonel, A. J., Teixeira, L. G., Oliveira, R. P., Santiago, A. F., Batista, N. V., Ferreira, T. R., Santos, R. C., Cardoso, V. N., Cara, D. C., Faria, A. M., and Alvarez-Leite, J. (2013) Antioxidative and immunomodulatory effects of tributyrin supplementation on experimental colitis. Br. J. Nutr. 109, 1396-1407
29. Kamura, T., Maenaka, K., Kotoshiba, S., Matsumoto, M., Kohda, D., Conaway, R. C., Conaway, J. W., and Nakayama, K. I. (2004) VHL-box and SOCS-box domains determine binding specificity for Cul2-Rbx1 and Cul5-Rbx2 modules of ubiquitin ligases. Genes Dev. 18, 3055-3065
30. Colgan, S. P., and Taylor, C. T. (2010) Hypoxia: an alarm signal during intestinal inflammation. Nat. Rev. Gastroenterol. Hepatol. 7, 281-287
31. Glover, L. E., and Colgan, S. P. (2011) Hypoxia and metabolic factors that influence inflammatory bowel disease pathogenesis. Gastroenterology 140, 1748-1755
32. Keely, S., Campbell, E. L., Baird, A. W., Hansbro, P. M., Shalwitz, R. A., Kotsakis, A., McNamee, E. N., Eltzschig, H. K., Kominsky, D. J., and Colgan, S. P. (2014) Contribution of epithelial innate immunity to systemic protection afforded by prolyl hydroxylase inhibition in murine colitis. Mucosal Immunol. 7, 114-123
33. Colgan, S. P., and Eltzschig, H. K. (2012) Adenosine and hypoxia-inducible factor signaling in intestinal injury and recovery. Annu. Rev. Physiol. 74, 153-175
34. Franke, A., McGovern, D. P., Barrett, J. C., Wang, K., Radford-Smith, G. L., Ahmad, T., Lees, C. W., Balschun, T., Lee, J., Roberts, R., Anderson, C. A., Bis, J. C., Bumpstead, S., Ellinghaus, D., Festen, E. M., Georges, M., Green, T., Haritunians, T., Jostins, L., Latiano, A., Matthew, C. G., Montgomery, G. W., Prescott, N. J., Raychaudhuri, S., Rotter, J. I., Schumm, P., Sharma, Y., Simms, L. A., Taylor, K. D., Whiteman, D., Wijmenga, C., Baldassano, R. N., Barclay, M., Bayless, T. M., Brand, S., Brüning, C., Cohen, A., Colombel, J. F., Cottone, M., Stronati, L., Denson, T., De Vos, M., D'Inca, R., Dubinsky, M., Edwards, C., Florin, T., Franchimont, D., Gearry, R., Glas, J., Van Gossum, A., Guthery, S. L., Halfvarson, J., Verspaget, H. W., Hugot, J. P., Karban, A., Laukens, D., Lawrance, I., Lemann, M., Levine, A., Libioulle, C., Louis, E., Mowat, C., Newman, W., Panés, J., Phillips, A., Proctor, D. D., Regueiro, M., Russell, R., Rutgeerts, P., Sanderson, J., Sans, M., Seibold, F., Steinhart, A. H., Stokkers, P. C., Torkvist, L., Kullak-Ublick, G., Wilson, D., Walters, T., Targan, S. R., Brant, S. R., Rioux, J. D., D'Amato, M., Weersma, R. K., Kugathasan, S., Griffiths, A. M., Mansfield, J. C., Vermeire, S., Dueer, R. H., Silverberg, M. S., Satsangi, J., Schreiber, S., Cho, J. H., Annese, V., Hakonarson, H., Daly, M. J., and Parkes, M. (2010) Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat. Genet. 42, 1118-1125
35. McGovern, D. P., Gardet, A., Törkvist, L., Goyette, P., Essers, J., Taylor, K. D., Neale, B. M., Ong, R. T., Lagacé, C., Li, C., Green, T., Stevens, C. R., Beauchamp, C., Fleshner, P. R., Carlson, M., D'Amato, M., Halfvarson, J., Hibberd, M. L., Lordal, M., Padyukov, L., Andriulli, A., Colombo, E., Latiano, A., Palmieri, O., Bernard, E. J., Deslandres, C., Hommes, D. W., de Jong, D. J., Stokkers, P. C., Weersma, R. K., Sharma, Y., Silverberg, M. S., Cho, J. H., Wu, J., Roeder, K., Brant, S. R., Schumm, L. P., Duerr, R. H., Dubinsky, M. C., Glazer, N. L., Haritunians, T., Ippoliti, A., Melmed, G. Y., Siscovick, D. S., Vasiliauskas, E. A., Targan, S. R., Annese, V., Wijmenga, C., Pettersson, S., Rotter, J. I., Xavier, R. J., Daly, M. J., Rioux, J. D., and Seielstad, M. (2010) Genome-wide association identifies multiple ulcerative colitis susceptibility loci. Nat. Genet. 42, 332-337
36. Rivas, M. A., Beaudoin, M., Gardet, A., Stevens, C., Sharma, Y., Zhang, C. K., Boucher, G., Ripke, S., Ellinghaus, D., Burtt, N., Fennell, T., Kirby, A., Latiano, A., Goyette, P., Green, T., Halfvarson, J., Haritunians, T., Korn, J. M., Kuruvilla, F., Lagace, C., Neale, B., Lo, K. S., Schumm, P., Torkvist, L., Dubinsky, M. C., Brant, S. R., Silverberg, M. S., Duerr, R. H., Altshuler, D., Gabriel, S., Lettre, G., Franke, A., D'Amato, M., McGovern, D. P., Cho, J. H., Rioux, J. D., Xavier, R. J., and Daly, M. J. (2011) Deep resequencing of GWAS loci identifies independent rare variants associated with inflammatory bowel disease. Nat. Genet. 43, 1066-1073