Literature DB >> 20827720

Adenosine triphosphate release and purinergic (P2) receptor-mediated secretion in small and large mouse cholangiocytes.

Kangmee Woo1, Meghana Sathe, Charles Kresge, Victoria Esser, Yoshiyuki Ueno, Julie Venter, Shannon S Glaser, Gianfranco Alpini, Andrew P Feranchak.   

Abstract

UNLABELLED: Adenosine triphosphate (ATP) is released from cholangiocytes into bile and is a potent secretogogue by increasing intracellular Ca²(+) and stimulating fluid and electrolyte secretion via binding purinergic (P2) receptors on the apical membrane. Although morphological differences exist between small and large cholangiocytes (lining small and large bile ducts, respectively), the role of P2 signaling has not been previously evaluated along the intrahepatic biliary epithelium. The aim of these studies therefore was to characterize ATP release and P2-signaling pathways in small (MSC) and large (MLC) mouse cholangiocytes. The findings reveal that both MSCs and MLCs express P2 receptors, including P2X4 and P2Y2. Exposure to extracellular nucleotides (ATP, uridine triphosphate, or 2',3'-O-[4-benzoyl-benzoyl]-ATP) caused a rapid increase in intracellular Ca²(+) concentration and in transepithelial secretion (I(sc)) in both cell types, which was inhibited by the Cl(-) channel blockers 5-nitro-2-(-3-phenylpropylamino)-benzoic acid (NPPB) or niflumic acid. In response to mechanical stimulation (flow/shear or cell swelling secondary to hypotonic exposure), both MSCs and MLCs exhibited a significant increase in the rate of exocytosis, which was paralleled by an increase in ATP release. Mechanosensitive ATP release was two-fold greater in MSCs compared to MLCs. ATP release was significantly inhibited by disruption of vesicular trafficking by monensin in both cell types.
CONCLUSION: These findings suggest the existence of a P2 signaling axis along intrahepatic biliary ducts with the "upstream" MSCs releasing ATP, which can serve as a paracrine signaling molecule to "downstream" MLCs stimulating Ca²(+)-dependent secretion. Additionally, in MSCs, which do not express the cystic fibrosis transmembrane conductance regulator, Ca²(+)-activated Cl(-) efflux in response to extracellular nucleotides represents the first secretory pathway clearly identified in these cholangiocytes derived from the small intrahepatic ducts.

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Year:  2010        PMID: 20827720      PMCID: PMC2967625          DOI: 10.1002/hep.23883

Source DB:  PubMed          Journal:  Hepatology        ISSN: 0270-9139            Impact factor:   17.425


  28 in total

1.  The lipid products of phosphoinositide 3-kinase contribute to regulation of cholangiocyte ATP and chloride transport.

Authors:  A P Feranchak; R M Roman; R B Doctor; K D Salter; A Toker; J G Fitz
Journal:  J Biol Chem       Date:  1999-10-22       Impact factor: 5.157

2.  Regulation of biliary secretion through apical purinergic receptors in cultured rat cholangiocytes.

Authors:  T Schlenker; J M Romac; A I Sharara; R M Roman; S J Kim; N LaRusso; R A Liddle; J G Fitz
Journal:  Am J Physiol       Date:  1997-11

3.  Adenosine nucleotides in bile.

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Journal:  Am J Physiol       Date:  1996-02

Review 4.  Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides.

Authors:  G R Dubyak; C el-Moatassim
Journal:  Am J Physiol       Date:  1993-09

5.  Functional expression of the apical Na+-dependent bile acid transporter in large but not small rat cholangiocytes.

Authors:  G Alpini; S S Glaser; R Rodgers; J L Phinizy; W E Robertson; J Lasater; A Caligiuri; Z Tretjak; G D LeSage
Journal:  Gastroenterology       Date:  1997-11       Impact factor: 22.682

6.  Purinergic regulation of cholangiocyte secretion: identification of a novel role for P2X receptors.

Authors:  R Brian Doctor; Thomas Matzakos; Ryan McWilliams; Sylene Johnson; Andrew P Feranchak; J Gregory Fitz
Journal:  Am J Physiol Gastrointest Liver Physiol       Date:  2004-11-04       Impact factor: 4.052

7.  Immunohistochemical detection of chloride/bicarbonate anion exchangers in human liver.

Authors:  E Martínez-Ansó; J E Castillo; J Díez; J F Medina; J Prieto
Journal:  Hepatology       Date:  1994-06       Impact factor: 17.425

8.  Cyclic AMP regulates bicarbonate secretion in cholangiocytes through release of ATP into bile.

Authors:  Noritaka Minagawa; Jun Nagata; Kazunori Shibao; Anatoliy I Masyuk; Dawidson A Gomes; Michele A Rodrigues; Gene Lesage; Yasutada Akiba; Jonathan D Kaunitz; Barbara E Ehrlich; Nicholas F Larusso; Michael H Nathanson
Journal:  Gastroenterology       Date:  2007-08-14       Impact factor: 22.682

9.  Bioluminescence detection of ATP release mechanisms in epithelia.

Authors:  A L Taylor; B A Kudlow; K L Marrs; D C Gruenert; W B Guggino; E M Schwiebert
Journal:  Am J Physiol       Date:  1998-11

10.  Morphological, molecular, and functional heterogeneity of cholangiocytes from normal rat liver.

Authors:  G Alpini; S Roberts; S M Kuntz; Y Ueno; S Gubba; P V Podila; G LeSage; N F LaRusso
Journal:  Gastroenterology       Date:  1996-05       Impact factor: 22.682

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  25 in total

1.  Role of purinergic P2X receptors in the control of liver homeostasis.

Authors:  Michel Fausther; Emmanuel Gonzales; Jonathan A Dranoff
Journal:  Wiley Interdiscip Rev Membr Transp Signal       Date:  2012-01-11

2.  Mechanosensor transient receptor potential vanilloid member 4 (TRPV4) regulates mouse cholangiocyte secretion and bile formation.

Authors:  Qin Li; Charles Kresge; Kristy Boggs; Julie Scott; Andrew Feranchak
Journal:  Am J Physiol Gastrointest Liver Physiol       Date:  2019-11-25       Impact factor: 4.052

3.  H19 promotes cholestatic liver fibrosis by preventing ZEB1-mediated inhibition of epithelial cell adhesion molecule.

Authors:  Yongfeng Song; Chune Liu; Xia Liu; Jocelyn Trottier; Michele Beaudoin; Li Zhang; Chad Pope; Guangyong Peng; Olivier Barbier; Xiaobo Zhong; Linheng Li; Li Wang
Journal:  Hepatology       Date:  2017-08-26       Impact factor: 17.425

Review 4.  Calcium signaling in the liver.

Authors:  Maria Jimena Amaya; Michael H Nathanson
Journal:  Compr Physiol       Date:  2013-01       Impact factor: 9.090

Review 5.  Physiology of cholangiocytes.

Authors:  James H Tabibian; Anatoliy I Masyuk; Tetyana V Masyuk; Steven P O'Hara; Nicholas F LaRusso
Journal:  Compr Physiol       Date:  2013-01       Impact factor: 9.090

6.  Coupled ATP and potassium efflux from intercalated cells.

Authors:  J David Holtzclaw; Ryan J Cornelius; Lori I Hatcher; Steven C Sansom
Journal:  Am J Physiol Renal Physiol       Date:  2011-03-30

7.  Regulation of purinergic signaling in biliary epithelial cells by exocytosis of SLC17A9-dependent ATP-enriched vesicles.

Authors:  Meghana N Sathe; Kangmee Woo; Charles Kresge; Abhijit Bugde; Kate Luby-Phelps; Matthew A Lewis; Andrew P Feranchak
Journal:  J Biol Chem       Date:  2011-05-25       Impact factor: 5.157

8.  Regulation of mechanosensitive biliary epithelial transport by the epithelial Na(+) channel.

Authors:  Qin Li; Charles Kresge; Abhijit Bugde; Michelle Lamphere; Jason Y Park; Andrew P Feranchak
Journal:  Hepatology       Date:  2015-12-14       Impact factor: 17.425

Review 9.  Calcium signaling and the secretory activity of bile duct epithelia.

Authors:  Maria Jimena Amaya; Michael H Nathanson
Journal:  Cell Calcium       Date:  2014-02-12       Impact factor: 6.817

Review 10.  Role of cholangiocytes in primary biliary cirrhosis.

Authors:  Ana Lleo; Luca Maroni; Shannon Glaser; Gianfranco Alpini; Marco Marzioni
Journal:  Semin Liver Dis       Date:  2014-07-24       Impact factor: 6.115

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