Intestinal epithelial CD98 synthesis specifically modulates expression of colonic microRNAs during colitis

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 302, Issue 11, 2012, Pages

  Charania, Moiz A ^a   Ayyadurai, Saravanan ^a   Ingersoll, Sarah A ^a,b   Xiao, Bo ^a   Viennois, Emilie ^a   Yan, Yutao ^a,b   Laroui, Hamed ^a   Sitaraman, Shanthi V ^c   Merlin, Didier ^a,b  

^a GEORGIA STATE UNIVERSITY   (United States)

^b ATLANTA VA MEDICAL CENTER   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Epithelial cells; Inflammation

Indexed keywords

CD98 ANTIGEN; DEXTRAN SULFATE; MICRORNA; MICRORNA 132; MICRORNA 23A; MICRORNA 23B; RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COLITIS; CONTROLLED STUDY; DOWN REGULATION; INTESTINE EPITHELIUM CELL; LIVER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN;

ANIMALS; ANTIGENS, CD98; COLITIS; COLON; EPITHELIAL CELLS; INFLAMMATION; INTESTINAL MUCOSA; MICE; MICRORNAS;

EID: 84861858185     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00401.2011     Document Type: Article

References (46)

1. Akila P, Prashant V, Suma MN, Prashant SN, Chaitra TR. CD163 and its expanding functional repertoire. Clin Chim Acta 413: 669-674, 2012.
2. Amasheh S, Fromm M, Gunzel D. Claudins of intestine and nephron-a correlation of molecular tight junction structure and barrier function. Acta Physiol (Oxf) 201: 133-140, 2011.
3. Ambros V. The functions of animal microRNAs. Nature 431: 350-355, 2004.
4. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, function. Cell 116: 281-297, 2004.
5. Buechler C, Ritter M, Orso E, Langmann T, Klucken J, Schmitz G. Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro-and anti-inflammatory stimuli. J Leukoc Biol 67: 97-103, 2000.
6. Bueno MJ, Perez de Castro I, Malumbres M. Control of cell proliferation pathways by microRNAs. Cell Cycle 7: 3143-3148, 2008.
7. Bussey KJ, Kane D, Sunshine M, Narasimhan S, Nishizuka S, Reinhold WC, Zeeberg B, Ajay W, Weinstein JN. MatchMiner: a tool for batch navigation among gene and gene product identifiers. Genome Biol 4: R27, 2003.
8. Cantor JM, Ginsberg MH, Rose DM. Integrin-associated proteins as potential therapeutic targets. Immunol Rev 223: 236-251, 2008.
9. Dalal SR, Kwon JH. The role of microRNA in inflammatory bowel disease. Gastroenterol Hepatol (N Y) 6: 714-722, 2010.
10. Dalmasso G, Nguyen HT, Yan Y, Laroui H, Srinivasan S, Sitaraman SV, Merlin D. MicroRNAs determine human intestinal epithelial cell fate. Differentiation 80: 147-154, 2010.
11. Davis BN, Hata A. Regulation of microRNA biogenesis: a miRiad of mechanisms. Cell Commun Signal 7: 18, 2009.
12. Deves R, Boyd CA. Surface antigen CD98(4F2): not a single membrane protein, but a family of proteins with multiple functions. J Membr Biol 173: 165-177, 2000.
13. Fang K, Bruce M, Pattillo CB, Zhang S, Stone R, 2nd Clifford J, Kevil CG. Temporal genomewide expression profiling of DSS colitis reveals novel inflammatory and angiogenesis genes similar to ulcerative colitis. Physiol Genomics 43: 43-56, 2011.
14. Fenczik CA, Sethi T, Ramos JW, Hughes PE, Ginsberg MH. Complementation of dominant suppression implicates CD98 in integrin activation. Nature 390: 81-85, 1997.
15. Furuta K, Lichtenberger R, Helariutta Y. The role of mobile small RNA species during root growth and development. Curr Opin Cell Biol 24: 211-216, 2012.
16. Gordon JI. Intestinal epithelial differentiation: new insights from chimeric and transgenic mice. J Cell Biol 108: 1187-1194, 1989.
17. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. miRBase: tools for microRNA genomics. Nucleic Acids Res 36: D154-D158, 2008.
18. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91-105, 2007.
19. Henderson NC, Collis EA, Mackinnon AC, Simpson KJ, Haslett C, Zent R, Ginsberg M, Sethi T. CD98hc (SLC3A2) interaction with beta 1 integrins is required for transformation. J Biol Chem 279: 54731-54741, 2004.
20. Hering NA, Fromm M, Schulzke JD. Determinants of colonic barrier function in inflammatory bowel disease and potential therapeutics. J Physiol 590: 1035-1044, 2012.
21. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57, 2009.
22. Kawabe H, Nakanishi H, Asada M, Fukuhara A, Morimoto K, Takeuchi M, Takai Y. Pilt, a novel peripheral membrane protein at tight junctions in epithelial cells. J Biol Chem 276: 48350-48355, 2001.
23. Kosaka N, Iguchi H, Yoshioka Y, Hagiwara K, Takeshita F, Ochiya T. Competitive interactions of cancer cells and normal cells via secretory microRNAs. J Biol Chem 287: 1397-1405, 2012.
24. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285: 17442-17452, 2010.
25. Kowal K, Silver R, Slawinska E, Bielecki M, Chyczewski L, Kowal-Bielecka O. CD163 and its role in inflammation. Folia Histochem Cytobiol 49: 365-374, 2011.
26. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N. Combinatorial microRNA target predictions. Nat Genet 37: 495-500, 2005.
27. Kucharzik T, Lugering A, Yan Y, Driss A, Charrier L, Sitaraman S, Merlin D. Activation of epithelial CD98 glycoprotein perpetuates colonic inflammation. Lab Invest 85: 932-941, 2005.
28. Lasky LA. How integrins are activated. Nature 390: 15; 17, 1997.
29. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20, 2005.
30. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 115: 787-798, 2003.
31. Liu S, Russo PA, Baldassano RN, Sullivan KE. CD68 expression is markedly different in Crohn's disease and the colitis associated with chronic granulomatous disease. Inflamm Bowel Dis 15: 1213-1217, 2009.
32. Merlin D, Sitaraman S, Liu X, Eastburn K, Sun J, Kucharzik T, Lewis B, Madara JL. CD98-mediated links between amino acid transport and beta 1 integrin distribution in polarized columnar epithelia. J Biol Chem 276: 39282-39289, 2001.
33. Nguyen HT, Dalmasso G, Torkvist L, Halfvarson J, Yan Y, Laroui H, Shmerling D, Tallone T, D'Amato M, Sitaraman SV, Merlin D. CD98 expression modulates intestinal homeostasis, inflammation, and colitisassociated cancer in mice. J Clin Invest 121: 1733-1747, 2011.
34. Nguyen HT, Dalmasso G, Yan Y, Laroui H, Dahan S, Mayer L, Sitaraman SV, Merlin D. MicroRNA-7 modulates CD98 expression during intestinal epithelial cell differentiation. J Biol Chem 285: 1479-1489, 2010.
35. Nguyen HT, Dalmasso G, Yan Y, Obertone TS, Sitaraman SV, Merlin D. Ecto-phosphorylation of CD98 regulates cell-cell interactions. PLoS One 3: e3895, 2008.
36. Pekow JR, Kwon JH. MicroRNAs in inflammatory bowel disease. Inflamm Bowel Dis 18: 187-193, 2012.
37. Schaer DJ, Boretti FS, Hongegger A, Poehler D, Linnscheid P, Staege H, Muller C, Schoedon G, Schaffner A. Molecular cloning and characterization of the mouse CD163 homologue, a highly glucocorticoidinducible member of the scavenger receptor cysteine-rich family. Immunogenetics 53: 170-177, 2001.
38. Schulzke JD, Ploeger S, Amasheh M, Fromm A, Zeissig S, Troeger H, Richter J, Bojarski C, Schumann M, Fromm M. Epithelial tight junctions in intestinal inflammation. Ann NY Acad Sci 1165: 294-300, 2009.
39. Taganov KD, Boldin MP, Baltimore D. MicroRNAs and immunity: tiny players in a big field. Immunity 26: 133-137, 2007.
40. Vo N, Klein ME, Varlamova O, Keller DM, Yamamoto T, Goodman RH, Impey S. A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc Natl Acad Sci USA 102: 16426-16431, 2005.
41. Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11: 228-234, 2009.
42. Wu F, Zhang S, Dassopoulos T, Harris ML, Bayless TM, Meltzer SJ, Brant SR, Kwon JH. Identification of microRNAs associated with ileal and colonic Crohn's disease. Inflamm Bowel Dis 16: 1729-1738, 2010.
43. Wu F, Zikusoka M, Trindade A, Dassopoulos T, Harris ML, Bayless TM, Brant SR, Chakravarti S, Kwon JH. MicroRNAs are differentially expressed in ulcerative colitis and alter expression of macrophage inflammatory peptide-2 alpha. Gastroenterology 135: 1624-1635 e1624, 2008.
44. Yan Y, Dalmasso G, Sitaraman S, Merlin D. Characterization of the human intestinal CD98 promoter and its regulation by interferon-. Am J Physiol Gastrointest Liver Physiol 292: G535-G545, 2007.
45. Yan Y, Vasudevan S, Nguyen HT, Merlin D. Intestinal epithelial CD98: an oligomeric and multifunctional protein. Biochim Biophys Acta 1780: 1087-1092, 2008.
46. Zwadlo G, Voegeli R, Osthoff KS, Sorg C. A monoclonal antibody to a novel differentiation antigen on human macrophages associated with the downregulatory phase of the inflammatory process. Exp Cell Biol 55: 295-304, 1987.