IL-6 downregulates transcription of NTPDase2 via specific promoter elements

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 294, Issue 3, 2008, Pages

  Yu, Jin ^a   Lavoie, Élise G ^b   Sheung, Nina ^a   Tremblay, Jacques J ^b   Sévigny, Jean ^b   Dranoff, Jonathan A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

Bile duct epithelia; Biliary cirrhosis; Ecto adenosine triphosphatase; Interleukin 6; Nucleoside triphosphate diphosphohydrolase 2; P2Y

Indexed keywords

ALPHA ACTIN; GLYCOPROTEIN GP 130; INTERLEUKIN 6; MESSENGER RNA; NUCLEOSIDE DIPHOSPHATASE; NUCLEOSIDE TRIPHOSPHATE DIPHOSPHOHYDROLASE 2; RNA LIGASE; SMOOTH MUSCLE ACTIN; UNCLASSIFIED DRUG;

ARTICLE; BILE DUCT; BILIARY CIRRHOSIS; BILIARY TRACT FIBROSIS; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE TIME EFFECT RELATION; ENZYME BINDING; ENZYME REGULATION; GENE AMPLIFICATION; GENE MUTATION; GROWTH REGULATION; HUMAN; HUMAN CELL; LIVER CELL; MYOFIBROBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; TRANSCRIPTION REGULATION;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CLONING, MOLECULAR; CYTOKINE RECEPTOR GP130; DNA, COMPLEMENTARY; DOWN-REGULATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; INTERLEUKIN-6; LUCIFERASES; MALE; MICROSCOPY, CONFOCAL; MUTAGENESIS, SITE-DIRECTED; PROMOTER REGIONS (GENETICS); RATS; RATS, SPRAGUE-DAWLEY; RESPONSE ELEMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 41549104122     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00208.2007     Document Type: Article

References (58)

1. Abbracchio MP, Burnstock G, Boeynaems JM, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA. International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58: 281-341, 2006.
2. 2+--ecto-ATPase in estrogen-induced and obstructive cholestasis in the rat. J Lab Clin Med 136: 125-137, 2000.
3. Alpini G, Ulrich CD 2nd, Phillips JO, Pham LD, Miller LJ, LaRusso NF. Upregulation of secretin receptor gene expression in rat cholangiocytes after bile duct ligation. Am J Physiol Gastrointest Liver Physiol 266: G922-G928, 1994.
4. Atkinson B, Dwyer K, Enjyoji K, Robson SC. Ecto-nucleotidases of the CD39/NTPDase family modulate platelet activation and thrombus formation: potential as therapeutic targets. Blood Cells Mol Dis 36: 217-222, 2006.
5. Boyd DC, Turner PC, Watkins NJ, Gerster T, Murphy S. Functional redundancy of promoter elements ensures efficient transcription of the human 7SK gene in vivo. J Mol Biol 253: 677-690, 1995.
6. Braun N, Sévigny J, Mishra SK, Robson SC, Barth SW, Gerstberger R, Hammer K, Zimmermann H. Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain. Eur J Neurosci 17: 1355-1364, 2003.
7. Braun N, Sévigny J, Robson SC, Hammer K, Hanani M, Zimmermann H. Association of the ecto-ATPase NTPDase2 with glial cells of the peripheral nervous system. Glia 45: 124-132, 2004.
8. Burnstock G. Purinergic signalling - an overview. Novartis Found Symp 276: 26-48; discussion 48-57, 275-281, 2006.
9. Chapdelaine P, Delahaye S, Gauthier E, Tremblay RR, Dube JY. A one-hour procedure for the preparation of genomic DNA from frozen tissues. Biotechniques 14: 163-164, 1993.
10. Dranoff JA, Kruglov E, Toure J, Braun N, Zimmermann H, Jain D, Knowles AF, Sévigny J. Ecto-nucleotidase NTPDase2 is selectively down-regulated in biliary cirrhosis. J Investig Med 52: 475-482, 2004.
11. Dranoff JA, Kruglov EA, Robson SC, Braun N, Zimmermann H, Sévigny J. The ecto-nucleoside triphosphate diphosphohydrolase NTPDase2/CD39L1 is expressed in a novel functional compartment within the liver. Hepatology 36: 1135-1144, 2002.
12. Dranoff JA, Masyuk AI, Kruglov EA, LaRusso NF, Nathanson MH. Polarized expression and function of P2Y ATP receptors in rat bile duct epithelia. Am J Physiol Gastrointest Liver Physiol 281: G1059-G1067, 2001.
13. Dranoff JA, Ogawa M, Kruglov EA, Gaca MD, Sévigny J, Robson SC, Wells RG. Expression of P2Y nucleotide receptors and ectonucleotidases in quiescent and activated rat hepatic stellate cells. Am J Physiol Gastrointest Liver Physiol 287: G417-G424, 2004.
14. Enjyoji K, Sévigny J, Lin Y, Frenette PS, Christie PD, Esch JS 2nd, Imai M, Edelberg JM, Rayburn H, Lech M, Beeler DL, Csizmadia E, Wagner DD, Robson SC, Rosenberg RD. Targeted disruption of cd39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation. Nat Med 5: 1010-1017, 1999.
15. Fausther M, Lecka J, Kukulski F, Levesque SA, Pelletier J, Zimmermann H, Dranoff JA, Sévigny J. Cloning, purification and identification of the liver canalicular ecto-ATPase as NTPDase8. Am J Physiol Gastrointest Liver Physiol 292: G785-G795, 2007.
16. Fey GH, Hattori M, Hocke G, Brechner T, Baffet G, Baumann M, Baumann H, Northemann W. Gene regulation by interleukin 6. Biochimie 73: 47-50, 1991.
17. Gao L, Dong L, Whitlock JP Jr. A novel response to dioxin. Induction of ecto-ATPase gene expression. J Biol Chem 273: 15358-15365, 1998.
18. Gever JR, Cockayne DA, Dillon MP, Burnstock G, Ford AP. Pharmacology of P2X channels. Pflügers Arch 452: 513-537, 2006.
19. Hocke GM, Barry D, Fey GH. Synergistic action of interleukin-6 and glucocorticoids is mediated by the interleukin-6 response element of the rat alpha 2 macroglobulin gene. Mol Cell Biol 12: 2282-2294, 1992.
20. Javahery R, Khachi A, Lo K, Zenzie-Gregory B, Smale ST. DNA sequence requirements for transcriptional initiator activity in mammalian cells. Mol Cell Biol 14: 116-127, 1994.
21. Jhandier MN, Kruglov EA, Lavoie É G, Sévigny J, Dranoff JA. Portal fibroblasts regulate the proliferation of bile duct epithelia via expression of NTPDase2. J Biol Chem 280: 22986-22992, 2005.
22. Kershenobich Stalnikowitz D, Weissbrod AB. Liver fibrosis and inflammation. A review. Ann Hepatol 2: 159-163, 2003.
23. Kittel A, Pelletier J, Bigonnesse F, Guckelberger O, Kordas K, Braun N, Robson SC, Sévigny J. Localization of nucleoside triphosphate diphosphohydrolase-1 (NTPDase1) and NTPDase2 in pancreas and salivary gland. J Histochem Cytochem 52: 861-871, 2004.
24. Knowles AF, Chiang WC. Enzymatic and transcriptional regulation of human ecto-ATPase/E-NTPDase 2. Arch Biochem Biophys 418: 217-227, 2003.
25. Knowles AF, Li C. Molecular cloning and characterization of expressed human ecto-nucleoside triphosphate diphosphohydrolase 8 (E-NTPDase 8) and its soluble extracellular domain. Biochemistry 45: 7323-7333, 2006.
26. Kruglov EA, Jain D, Dranoff JA. Isolation of primary rat liver fibroblasts. J Investig Med 50: 179-184, 2002.
27. Kruglov EA, Nathanson RA, Nguyen T, Dranoff JA. Secretion of MCP-1/CCL2 by bile duct epithelia induces myofibroblastic transdifferentiation of portal fibroblasts. Am J Physiol Gastrointest Liver Physiol 290: G765-G771, 2006.
28. Kukulski F, Levesque SA, Lavoie É G, Lecka J, Bigonesse F, Knowles AF, Robson TL, Sévigny J. Comparative hydrolysis of P2 receptor antagonists by NTPDases 1, 2, 3, and 8. Purinergic Signal 1: 193-204, 2005.
29. Lu Q, Porter LD, Cui X, Sanborn BM. Ecto-ATPase mRNA is regulated by FSH in Sertoli cells. J Androl 22: 289-301, 2001.
30. Marra F, DeFranco R, Grappone C, Milani S, Pastacaldi S, Pinzani M, Romanelli RG, Laffi G, Gentilini P. Increased expression of monocyte chemotactic protein-1 during active hepatic fibrogenesis: correlation with monocyte infiltration. Am J Pathol 152: 423-430, 1998.
31. Mishra SK, Braun N, Shukla V, Fullgrabe M, Schomerus C, Korf HW, Gachet C, Ikehara Y, Sévigny J, Robson SC, Zimmermann H. Extracellular nucleotide signaling in adult neural stem cells: synergism with growth factor-mediated cellular proliferation. Development 133: 675-684, 2006.
32. Muller C, Zielinski CC. Interleukin-6 production by peripheral blood monocytes in patients with chronic liver disease and acute viral hepatitis. J Hepatol 15: 372-377, 1992.
33. Napoli J, Bishop GA, McCaughan GW. Increased intrahepatic messenger RNA expression of interleukins 2, 6, and 8 in human cirrhosis. Gastroenterology 107: 789-798, 1994.
34. Park J, Gores GJ, Patel T. Lipopolysaccharide induces cholangiocyte proliferation via an interleukin-6-mediated activation of p44/p42 mitogen-activated protein kinase. Hepatology 29: 1037-1043, 1999.
35. Presnell SR, Zhang L, Ramilo CA, Chan HW, Lutz CT. Functional redundancy of transcription factor-binding sites in the killer cell Ig-like receptor (KIR) gene promoter. Int Immunol 18: 1221-1232, 2006.
36. Pugh BF, Tjian R. Mechanism of transcriptional activation by Sp1: evidence for coactivators. Cell 61: 1187-1197, 1990.
37. Reigada D, Lu W, Zhang X, Friedman C, Pendrak K, McGlinn A, Stone RA, Laties AM, Mitchell CH. Degradation of extracellular ATP by the retinal pigment epithelium. Am J Physiol Cell Physiol 289: C617-C624, 2005.
38. Robson SC, Sévigny J, Zimmermann H. The E-NTPDase family of ectonucleotidases: structure, function, relationships, and pathophysiological significance. Purinergic Signal 2: 409-430, 2006.
39. Robson SC, Wu Y, Sun X, Knosalla C, Dwyer K, Enjyoji K. Ectonucleotidases of CD39 family modulate vascular inflammation and thrombosis in transplantation. Semin Thromb Hemost 31: 217-233, 2005.
40. Scheller J, Rose-John S. Interleukin-6 and its receptor: from bench to bedside. Med Microbiol Immunol 195: 173-183, 2006.
41. Schreiber E, Matthias P, Muller MM, Schaffner W. Rapid detection of octamer binding proteins with "mini-extracts," prepared from a small number of cells. Nucleic Acids Res 17: 6419, 1989.
42. 2+- changes NTPDase and ecto-5′-nucleotidase activities in central nervous system of zebrafish (Danio rerio). Toxicology 226: 229-237, 2006.
43. Sévigny J, Robson SC, Waelkens E, Csizmadia E, Smith RN, Lemmens R. Identification and characterization of a novel hepatic canalicular ATP diphosphohydrolase. J Biol Chem 275: 5640-5647, 2000.
44. Sévigny J, Sundberg C, Braun N, Guckelberger O, Csizmadia E, Qawi I, Imai M, Zimmermann H, Robson SC. Differential catalytic properties and vascular topography of murine nucleoside triphosphate diphosphohydrolase 1 (NTPDase1) and NTPDase2 have implications for thromboregulation. Blood 99: 2801-2809, 2002.
45. Strazzabosco M, Spirli C, Okolicsanyi L. Pathophysiology of the intrahepatic biliary epithelium. J Gastroenterol Hepatol 15: 244-253, 2000.
46. Taga T. IL6 signalling through IL6 receptor and receptor-associated signal transducer, gp130. Res Immunol 143: 737-739, 1992.
47. Terada R, Yamamoto K, Hakoda T, Shimada N, Okano N, Baba N, Ninomiya Y, Gershwin ME, Shiratori Y. Stromal cell-derived factor-1 from biliary epithelial cells recruits CXCR4-positive cells: implications for inflammatory liver diseases. Lab Invest 83: 665-672, 2003.
48. Thevananther S, Sun H, Li D, Arjunan V, Awad SS, Wyllie S, Zimmerman TL, Goss JA, Karpen SJ. Extracellular ATP activates c-jun N-terminal kinase signaling and cell cycle progression in hepatocytes. Hepatology 39: 393-402, 2004.
49. Tsukamoto H. Cytokine regulation of hepatic stellate cells in liver fibrosis. Alcohol Clin Exp Res 23: 911-916, 1999.
50. Viger RS, Mertineit C, Trasler JM, Nemer M. Transcription factor GATA-4 is expressed in a sexually dimorphic pattern during mouse gonadal development and is a potent activator of the Mullerian inhibiting substance promoter. Development 125: 2665-2675, 1998.
51. Volonte C, Amadio S, D'Ambrosi N, Colpi M, Burnstock G. P2 receptor web: complexity and fine-tuning. Pharmacol Ther 112: 264-280, 2006.
52. Wang Y, Roman R, Lidofsky SD, Fitz JG. Autocrine signaling through ATP release represents a novel mechanism for cell volume regulation. Proc Natl Acad Sci USA 93: 12020-12025, 1996.
53. Wu Y, Sun X, Kaczmarek E, Dwyer KM, Bianchi E, Usheva A, Robson SC. RanBPM associates with CD39 and modulates ecto-nucleotidase activity. Biochem J 396: 23-30, 2006.
54. Xu B, Broome U, Ericzon BG, Sumitran-Holgersson S. High frequency of autoantibodies in patients with primary sclerosing cholangitis that bind biliary epithelial cells and induce expression of CD44 and production of interleukin 6. Gut 51: 120-127, 2002.
55. Yang C, Bolotin E, Jiang T, Sladek FM, Martinez E. Prevalence of the initiator over the TATA box in human and yeast genes and identification of DNA motifs enriched in human TATA-less core promoters. Gene 389: 52-65, 2007.
56. Yasoshima M, Kono N, Sugawara H, Katayanagi K, Harada K, Nakanuma Y. Increased expression of interleukin-6 and tumor necrosis factor-alpha in pathologic biliary epithelial cells: in situ and culture study. Lab Invest 78: 89-100, 1998.
57. Yokoyama T, Komori A, Nakamura M, Takii Y, Kamihira T, Shimoda S, Mori T, Fujiwara S, Koyabu M, Taniguchi K, Fujioka H, Migita K, Yatsuhashi H, Ishibashi H. Human intrahepatic biliary epithelial cells function in innate immunity by producing IL-6 and IL-8 via the TLR4-NF-kappaB and -MAPK signaling pathways. Liver Int 26: 467-476, 2006.
58. Zhang Z, Fuentes NL, Fuller GM. Characterization of the IL-6 responsive elements in the gamma fibrinogen gene promoter. J Biol Chem 270: 24287-24291, 1995.