Differential expression of the activator protein 1 transcription factor regulates interleukin-1β induction of interleukin 6 in the developing enterocyte

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Cahill, Catherine M ^a   Zhu, Weishu ^a   Oziolor, Elias ^b   Yang, Yao Jong ^c   Tam, Bosco ^a   Rajanala, Susruthi ^a   Rogers, Jack T ^a   Walker, W Allan ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BAYLOR UNIVERSITY   (United States)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN C FOS; PROTEIN C JUN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR JUNB; IL6 PROTEIN, HUMAN; JUNB PROTEIN, HUMAN; STRESS ACTIVATED PROTEIN KINASE 1; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENZYME PHOSPHORYLATION; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; INTESTINE CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS REGULATION; ANIMAL; CELL LINE; CYTOLOGY; DNA RESPONSIVE ELEMENT; DRUG EFFECTS; EMBRYOLOGY; GENETICS; INTESTINE; METABOLISM; ORGAN CULTURE TECHNIQUE; PHOSPHORYLATION; PHYSIOLOGY; SCID MOUSE; SECRETION (PROCESS); SIGNAL TRANSDUCTION; XENOGRAFT;

ANIMALS; CELL LINE; ENTEROCYTES; HETEROGRAFTS; HUMANS; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTESTINES; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE, SCID; MITOGEN-ACTIVATED PROTEIN KINASE 8; NF-KAPPA B; ORGAN CULTURE TECHNIQUES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTORS;

EID: 84958162619     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0145184     Document Type: Article

References (50)

1. Meng D, Zhu W, Shi HN, Lu L, Wijendran V, XuWet al. (2015) Toll-like receptor-4 in human and mouse colonic epithelium is developmentally regulated: a possible role in necrotizing enterocolitis. Pediatr Res 77: 416-424. doi: 10.1038/pr.2014.207
2. Hackam DJ, Afrazi A, Good M, Sodhi CP (2013) Innate immune signaling in the pathogenesis of necrotizing enterocolitis. Clin Dev Immunol 2013: 475415. doi: 10.1155/2013/475415
3. Leaphart CL, Cavallo J, Gribar SC, Cetin S, Li J, Branca MF, et al. (2007) A critical role for TLR4 in the pathogenesis of necrotizing enterocolitis by modulating intestinal injury and repair. J Immunol 179: 4808-4820.
4. Chan KY, Leung FW, Lam HS, Tam YH, To KF, Cheung HM et al. Immunoregulatory protein profiles of necrotizing enterocolitis versus spontaneous intestinal perforation in preterm infants. PLoS One 7: e36977. doi: 10.1371/journal.pone.0036977
5. Neu J, Walker WA Necrotizing enterocolitis. N Engl J Med 364: 255-264. doi: 10.1056/ NEJMra1005408
6. Neu J, MihatschWRecent developments in necrotizing enterocolitis. JPEN J Parenter Enteral Nutr 36: 30S-35S. doi: 10.1177/0148607111422068
7. Nanthakumar NN, Fusunyan RD, Sanderson I, Walker WA (2000) Inflammation in the developing human intestine: A possible pathophysiologic contribution to necrotizing enterocolitis. Proc Natl Acad Sci U S A 97: 6043-6048.
8. Nanthakumar N, Meng D, Goldstein AM, Zhu W, Lu L, Uauy R et al. The mechanism of excessive intestinal inflammation in necrotizing enterocolitis: an immature innate immune response. PLoS One 6: e17776. doi: 10.1371/journal.pone.0017776
9. Harris MC, Costarino AT Jr., Sullivan JS, Dulkerian S, McCawley L, et al. (1994) Cytokine elevations in critically ill infants with sepsis and necrotizing enterocolitis. J Pediatr 124: 105-111.
10. Choo-Wing R, Nedrelow JH, Homer RJ, Elias JA, Bhandari V (2007) Developmental differences in the responses of IL-6 and IL-13 transgenic mice exposed to hyperoxia. Am J Physiol Lung Cell Mol Physiol 293: L142-150.
11. Wang L, Walia B, Evans J, Gewirtz AT, Merlin D, Sitaraman SV. (2003) IL-6 induces NF-kappa B activation in the intestinal epithelia. J Immunol 171: 3194-3201.
12. Jin X, Zimmers TA, Perez EA, Pierce RH, Zhang Z, Koniaris LGl. (2006) Paradoxical effects of shortand long-term interleukin-6 exposure on liver injury and repair. Hepatology 43: 474-484.
13. Vanden Berghe W, De Bosscher K, Boone E, Plaisance S, Haegeman G (1999) The nuclear factorkappaB engages CBP/p300 and histone acetyltransferase activity for transcriptional activation of the interleukin-6 gene promoter. J Biol Chem 274: 32091-32098.
14. Cahill CM, Rogers JT (2008) Interleukin (IL) 1beta induction of IL-6 is mediated by a novel phosphatidylinositol 3-kinase-dependent AKT/IkappaB kinase alpha pathway targeting activator protein-1. J Biol Chem 283: 25900-25912. doi: 10.1074/jbc.M707692200
15. Foletta VC, Segal DH, Cohen DR (1998) Transcriptional regulation in the immune system: all roads lead to AP-1. J Leukoc Biol 63: 139-152.
16. Karin M, Liu Z, Zandi E (1997) AP-1 function and regulation. Curr Opin Cell Biol 9: 240-246.
17. Kyriakis JM, Avruch J Mammalian MAPK signal transduction pathways activated by stress and inflammation: a 10-year update. Physiol Rev 92: 689-737. doi: 10.1152/physrev.00028.2011
18. Kyriakis JM, Avruch J (1996) Sounding the alarm: protein kinase cascades activated by stress and inflammation. J Biol Chem 271: 24313-24316.
19. Tanos T, Marinissen MJ, Leskow FC, Hochbaum D, Martinetto H, et al. (2005) Phosphorylation of c- Fos by members of the p38 MAPK family. Role in the AP-1 response to UV light. J Biol Chem 280: 18842-18852.
20. Wilkinson DG, Bhatt S, Ryseck RP, Bravo R (1989) Tissue-specific expression of c-jun and junB during organogenesis in the mouse. Development 106: 465-471.
21. Garaude J, Farras R, Bossis G, Charni S, Piechaczyk M, Hipskind RA et al. (2008) SUMOylation regulates the transcriptional activity of JunB in T lymphocytes. J Immunol 180: 5983-5990.
22. Pflegerl P, Vesely P, Hantusch B, Schlederer M, Zenz R, Janig E et al. (2009) Epidermal loss of JunB leads to a SLE phenotype due to hyper IL-6 signaling. Proc Natl Acad Sci U S A 106: 20423-20428. doi: 10.1073/pnas.0910371106
23. Eickelberg O, Pansky A, Mussmann R, Bihl M, Tamm M, Hildebrand P et al. (1999) Transforming growth factor-beta1 induces interleukin-6 expression via activating protein-1 consisting of JunD homodimers in primary human lung fibroblasts. J Biol Chem 274: 12933-12938.
24. Faggioli L, Costanzo C, Donadelli M, Palmieri M (2004) Activation of the Interleukin-6 promoter by a dominant negative mutant of c-Jun. Biochim Biophys Acta 1692: 17-24.
25. Savidge TC, Lowe DC, Walker WA (2001) Developmental regulation of intestinal epithelial hydrolase activity in human fetal jejunal xenografts maintained in severe-combined immunodeficient mice. Pediatr Res 50: 196-202.
26. Nanthakumar NN, Young C, Ko JS, Meng D, Chen J, Buie T et al. (2005) Glucocorticoid responsiveness in developing human intestine: possible role in prevention of necrotizing enterocolitis. Am J Physiol Gastrointest Liver Physiol 288: G85-92.
27. Nanthakumar NN, Klopcic CE, Fernandez I, Walker WA (2003) Normal and glucocorticoid-induced development of the human small intestinal xenograft. Am J Physiol Regul Integr Comp Physiol 285: R162-170.
28. Rautava S, Lu L, Nanthakumar NN, Dubert-Ferrandon A, Walker WA TGF-beta2 induces maturation of immature human intestinal epithelial cells and inhibits inflammatory cytokine responses induced via the NF-kappaB pathway. J Pediatr Gastroenterol Nutr 54: 630-638. doi: 10.1097/MPG. 0b013e31823e7c29
29. Rautava S, Nanthakumar NN, Dubert-Ferrandon A, Lu L, Rautava J, Walker WA. Breast milk-transforming growth factor-beta(2) specifically attenuates IL-1beta-induced inflammatory responses in the immature human intestine via an SMAD6- and ERK-dependent mechanism. Neonatology 99: 192-201. doi: 10.1159/000314109
30. Ganguli K, Meng D, Rautava S, Lu L, Walker WA, Nanthakumar N. Probiotics prevent necrotizing enterocolitis by modulating enterocyte genes that regulate innate immune-mediated inflammation. Am J Physiol Gastrointest Liver Physiol 304: G132-141. doi: 10.1152/ajpgi.00142.2012
31. Sanderson IR, Ezzell RM, Kedinger M, Erlanger M, Xu ZX, Pringault E et al. (1996) Human fetal enterocytes in vitro: modulation of the phenotype by extracellular matrix. Proc Natl Acad Sci U S A 93: 7717-7722.
32. Moyer MP, Manzano LA, Merriman RL, Stauffer JS, Tanzer LR (1996) NCM460, a normal human colon mucosal epithelial cell line. In Vitro Cell Dev Biol Anim 32: 315-317.
33. Savidge TC, Morey AL, Ferguson DJ, Fleming KA, Shmakov AN, Phillips A. D (1995) Human intestinal development in a severe-combined immunodeficient xenograft model. Differentiation 58: 361-371.
34. Okamoto S, Mukaida N, Yasumoto K, Rice N, Ishikawa Y, Horiguchi H. et al. (1994) The interleukin-8 AP-1 and kappa B-like sites are genetic end targets of FK506-sensitive pathway accompanied by calcium mobilization. J Biol Chem 269: 8582-8589.
35. Kyriakis JM, Avruch J (1996) Protein kinase cascades activated by stress and inflammatory cytokines. Bioessays 18: 567-577.
36. Vanden Berghe W, Vermeulen L, De Wilde G, De Bosscher K, Boone E, Haegeman G. (2000) Signal transduction by tumor necrosis factor and gene regulation of the inflammatory cytokine interleukin-6. Biochem Pharmacol 60: 1185-1195.
37. Fujioka S, Niu J, Schmidt C, Sclabas GM, Peng B, Uwagawa T. et al. (2004) NF-kappaB and AP-1 connection: mechanism of NF-kappaB-dependent regulation of AP-1 activity. Mol Cell Biol 24: 7806-7819.
38. Gomard T, Michaud HA, Tempe D, Thiolon K, Pelegrin M, Piechaczyk M. An NF-kappaB-dependent role for JunB in the induction of proinflammatory cytokines in LPS-activated bone marrow-derived dendritic cells. PLoS One 5: e9585. doi: 10.1371/journal.pone.0009585
39. Xiao W, Hodge DR, Wang L, Yang X, Zhang X, FarrarWL. (2004) NF-kappaB activates IL-6 expression through cooperation with c-Jun and IL6-AP1 site, but is independent of its IL6-NFkappaB regulatory site in autocrine human multiple myeloma cells. Cancer Biol Ther 3: 1007-1017.
40. Schreiber M, Kolbus A, Piu F, Szabowski A, Mohle-Steinlein U, Tian J. (1999) Control of cell cycle progression by c-Jun is p53 dependent. Genes Dev 13: 607-619.
41. Ding Q, Dong Z, Evers BM (1999) Enterocyte-like differentiation of the Caco-2 intestinal cell line is associated with increases in AP-1 protein binding. Life Sci 64: 175-182.
42. Sanderson IR, Walker WA (1995) Establishment of a human fetal small intestinal epithelial cell line. Int Arch Allergy Immunol 107: 396-397.
43. Smart DE, Vincent KJ, Arthur MJ, Eickelberg O, Castellazzi M, Mann J. et al. (2001) JunD regulates transcription of the tissue inhibitor of metalloproteinases-1 and interleukin-6 genes in activated hepatic stellate cells. J Biol Chem 276: 24414-24421.
44. Lamb JA, Ventura JJ, Hess P, Flavell RA, Davis RJ (2003) JunD mediates survival signaling by the JNK signal transduction pathway. Mol Cell 11: 1479-1489.
45. Lu C, Ren W, Su XM, Chen JQ, Wu SH, Zhou GP (2009) EGF-recruited JunD/c-fos complexes activate CD2AP gene promoter and suppress apoptosis in renal tubular epithelial cells. Gene 433: 56-64. doi: 10.1016/j.gene.2008.11.015
46. Marden JJ, Zhang Y, Oakley FD, Zhou W, Luo M, Jia HP et al. (2008) JunD protects the liver from ischemia/ reperfusion injury by dampening AP-1 transcriptional activation. J Biol Chem 283: 6687-6695. doi: 10.1074/jbc.M705606200
47. Grondin B, Lefrancois M, Tremblay M, Saint-Denis M, Haman A, Waga K et al. (2007) c-Jun homodimers can function as a context-specific coactivator. Mol Cell Biol 27: 2919-2933.
48. Kallunki T, Deng T, Hibi M, Karin M (1996) c-Jun can recruit JNK to phosphorylate dimerization partners via specific docking interactions. Cell 87: 929-939.
49. Chiu R, Angel P, Karin M (1989) Jun-B differs in its biological properties from, and is a negative regulator of, c-Jun. Cell 59: 979-986.
50. Luther J, Driessler F, Megges M, Hess A, Herbort B, Mandic V et al. Elevated Fra-1 expression causes severe lipodystrophy. J Cell Sci 124: 1465-1476. doi: 10.1242/jcs.079855.