Histamine stimulates the proliferation of small and large cholangiocytes by activation of both IP 3/Ca 2+ and cAMP-dependent signaling mechanisms

Laboratory Investigation

Volumn 92, Issue 2, 2012, Pages 282-294

  Francis, Heather L ^a   Demorrow, Sharon ^a   Franchitto, Antonio ^b,c   Venter, Julie K ^a   Mancinelli, Romina A ^b   White, Mellanie A ^a   Meng, Fanyin ^a   Ueno, Yoshiyuki ^d   Carpino, Guido ^e   Renzi, Anastasia ^a,b   Baker, Kimberly K ^a   Shine, Hannah E ^a   Francis, Taylor C ^a   Gaudio, Eugenio ^b   Alpini, Gianfranco D ^a   Onori, Paolo ^f  

^a SCOTT AND WHITE MEMORIAL HOSPITAL   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c Eleonora Lonillard Spencer Cenci Foundation   (Italy)

^d TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF ROME FORO ITALICO   (Italy)

^f UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

biliary epithelium; biogenic amines; cAMP; heterogeneity; IP 3; secretin receptor

Indexed keywords

CALCIUM ION; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; HISTAMINE; HISTAMINE H1 RECEPTOR; HISTAMINE H1 RECEPTOR AGONIST; HISTAMINE H2 RECEPTOR; HISTAMINE H2 RECEPTOR AGONIST; HISTAMINE H3 RECEPTOR; HISTAMINE H3 RECEPTOR AGONIST; HISTAMINE H4 RECEPTOR; HISTAMINE H4 RECEPTOR AGONIST; INOSITOL 1,4,5 TRISPHOSPHATE; PROTEIN KINASE C ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BILE DUCT; CELL PROLIFERATION; ENZYME PHOSPHORYLATION; HEPATOBILIARY SYSTEM; INTRAHEPATIC BILE DUCT; LIVER; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; BILE DUCTS; CALCIUM; CELL PROLIFERATION; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HISTAMINE; INOSITOL PHOSPHATES; MALE; PHOSPHORYLATION; PROTEIN KINASE C-ALPHA; RATS; RATS, INBRED F344; SIGNAL TRANSDUCTION;

EID: 84856428575     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2011.158     Document Type: Article

References (54)

1. Alpini G, Roberts S, Kuntz SM, et al. Morphological, molecular, and functional heterogeneity of cholangiocytes from normal rat liver. Gastroenterology 1996;110:1636-1643. (Pubitemid 26134100)
2. Glaser S, Gaudio E, Rao A, et al. Morphological and functional heterogeneity of the mouse intrahepatic biliary epithelium. Lab Invest 2009;89:456-469.
3. Alpini G, Lenzi R, Sarkozi L, et al. Biliary physiology in rats with bile ductular cell hyperplasia. Evidence for a secretory function of proliferated bile ductules. J Clin Invest 1988;81:569-578. (Pubitemid 18075253)
4. Nathanson MH, Boyer JL. Mechanisms and regulation of bile secretion. Hepatology 1991;14:551-566.
5. Kato A, Gores GJ, LaRusso NF. Secretin stimulates exocytosis in isolated bile duct epithelial cells by a cyclic AMP-mediated mechanism. J Biol Chem 1992;267:15523-15529.
6. Alpini G, Ulrich C, Roberts S, et al. Molecular and functional heterogeneity of cholangiocytes from rat liver after bile duct ligation. Am J Physiol Gastrointest Liver Physiol 1997;272:G289-G297.
7. Banales JM, Arenas F, Rodriguez-Ortigosa CM, et al. Bicarbonate-rich choleresis induced by secretin in normal rat is taurocholate-dependent and involves AE2 anion exchanger. Hepatology 2006;43:266-275.
8. Alpini G, Glaser S, Ueno Y, et al. Heterogeneity of the proliferative capacity of rat cholangiocytes after bile duct ligation. Am J Physiol Gastrointest Liver Physiol 1998;274:G767-G775.
9. LeSage G, Glaser S, Gubba S, et al. Regrowth of the rat biliary tree after 70% partial hepatectomy is coupled to increased secretin-induced ductal secretion. Gastroenterology 1996;111:1633-1644. (Pubitemid 26404229)
10. Alpini G, Prall RT, LaRusso NF. The pathobiology of biliary epithelia. The Liver; Biology & Pathobiology, 4 edn IM Arias, JL Boyer, FV Chisari et al (eds) 4 edn Philadelphia, PA
11. LeSage G, Glaser S, Marucci L, et al. Acute carbon tetrachloride feeding induces damage of large but not small cholangiocytes from BDL rat liver. Am J Physiol Gastrointest Liver Physiol 1999;276:G1289- G1301. (Pubitemid 29251929)
12. Alpini G, Ulrich CD, Phillips JO, et al. Upregulation of secretin receptor gene expression in rat cholangiocytes after bile duct ligation. Am J Physiol Gastrointest Liver Physiol 1994;266:G922-G928.
13. Francis H, Glaser S, Ueno Y, et al. cAMP stimulates the secretory and proliferative capacity of the rat intrahepatic biliary epithelium through changes in the PKA/Src/MEK/ERK1/2 pathway. J Hepatol 2004;41: 528-537. (Pubitemid 39297786)
14. Glaser S, Benedetti A, Marucci L, et al. Gastrin inhibits cholangiocyte growth in bile duct-ligated rats by interaction with cholecystokinin-B/Gastrin receptors via D-myo-inositol 1,4,5-triphosphate-, Ca(2+)-, and protein kinase C alpha-dependent mechanisms. Hepatology 2000;32:17-25. (Pubitemid 30432361)
15. Francis H, Glaser S, DeMorrow S, et al. Small mouse cholangiocytes proliferate in response to H1 histamine receptor stimulation by activation of the IP3/CaMK I/CREB pathway. Am J Physiol Cell Physiol 2008;295:C499-C513. (Pubitemid 352755782)
16. Francis H, Franchitto A, Ueno Y, et al. H3 histamine receptor agonist inhibits biliary growth of BDL rats by downregulation of the cAMP-dependent PKA/ERK1/2/ELK-1 pathway. Lab Invest 2007;87: 473-487. (Pubitemid 46633123)
17. Rosenthaler J, Guirard BM, Chang GW, et al. Purification and properties of histidine decarboxylase from Lactobacillus 30a. Proc Natl Acad Sci USA 1965;54:152-158.
18. Repka-Ramirez MS. New concepts of histamine receptors and actions. Curr Allergy Asthma Rep 2003;3:227-231. (Pubitemid 38899097)
19. Nguyen T, Shapiro DA, George SR, et al. Discovery of a novel member of the histamine receptor family. Mol Pharmacol 2001;59:427-433. (Pubitemid 32179919)
20. Molina-Hernandez A, Velasco I. Histamine induces neural stem cell proliferation and neuronal differentiation by activation of distinct histamine receptors. J Neurochem 2008;106:706-717.
21. Medina VA, Rivera ES. Histamine receptors and cancer pharmacology. Br J Pharmacol 2010;161:755-767.
22. Dickenson JM. Stimulation of protein kinase B and p70 S6 kinase by the histamine H1 receptor in DDT1MF-2 smooth muscle cells. Br J Pharmacol 2002;135:1967-1976. (Pubitemid 34478309)
23. Mitsuhashi M, Mitsuhashi T, Payan D. Multiple signaling pathways of histamine H2 receptors (Identification of an H2 receptor-dependent Ca2+ mobilization pathway in human HL-60 promyelocytic leukemia cells). J Biol Chem 1989;264:18356-18362. (Pubitemid 19277576)
24. Schultheiss G, Hennig B, Schunack W, et al. Histamine-induced ion secretion across rat distal colon: involvement of histamine H1 and H2 receptors. Eur J Pharmacol 2006;546:161-170. (Pubitemid 44331843)
25. Karavodin L, Jensen R, Sarno M, et al. Toxicology and toxicokinetics of acute and subchronic administration of histamine dihydrochloride in rats. Drug Chem Toxicol 2003;26:35-49. (Pubitemid 36287832)
26. Farzin D, Asghari L, Nowrouzi M. Rodent antinociception following acute treatment with different histamine receptor agonists and antagonists. Pharmacol Biochem Behav 2002;72:751-760. (Pubitemid 34450874)
27. Coruzzi G, Gambarelli E, Bertaccini G, et al. Cardiovascular effects of the novel histamine H2 receptor agonist amthamine: interaction with the adrenergic system. Naunyn Schmiedebergs Arch Pharmacol 1996;353:417-422. (Pubitemid 26106418)
28. Gantner F, Sakai K, Tusche MW, et al. Histamine h(4) and h(2) receptors control histamine-induced interleukin-16 release from human CD8(+) T cells. J Pharmacol Exp Ther 2002;303:300-307.
29. Ishii M, Vroman B, LaRusso NF. Isolation and morphologic characterization of bile duct epithelial cells from normal rat liver. Gastroenterology 1989;97:1236-1247. (Pubitemid 19258709)
30. Rutenburg AM, Kim H, Fischbein JW, et al. Histochemical and ultrastructural demonstration of γ-glutamyl transpeptidase activity. J Histochem Cytochem 1969;17:517-526.
31. Alpini G, Phinizy JL, Glaser S, et al. Development and characterization of secretin-stimulated secretion of cultured rat cholangiocytes. Am J Physiol Gastrointest Liver Physiol 2003;284:G1066-G1073. (Pubitemid 36597350)
32. Wadugu BA, Ng C, Bartley BL, et al. DNA interstrand cross-linking activity of (1-Chloroethenyl)oxirane, a metabolite of beta-chloroprene. Chem Res Toxicol 2010;23:235-239.
33. Mancinelli R, Onori P, Gaudio E, et al. Follicle-stimulating hormone increases cholangiocyte proliferation by an autocrine mechanism via cAMP-dependent phosphorylation of ERK1/2 and Elk-1. Am J Physiol Gastrointest Liver Physiol 2009;297:G11-G26.
34. Mancinelli R, Franchitto A, Gaudio E, et al. After damage of large bile ducts by gamma-aminobutyric acid, small ducts replenish the biliary tree by amplification of calcium-dependent signaling and de novo acquisition of large cholangiocyte phenotypes. Am J Pathol 2010;176:1790-1800.
35. Mancinelli R, Onori P, Gaudio E, et al. Taurocholate feeding to bile duct ligated rats prevents caffeic acid-induced bile duct damage by changes in cholangiocyte VEGF expression. Exp Biol Med (Maywood) 2009;234:462-474.
36. Ghosh AK, Hirasawa N, Ohuchi K. Enhancement by histamine of vascular endothelial growth factor production in granulation tissue via H(2) receptors. Br J Pharmacol 2001;134:1419-1428. (Pubitemid 33131892)
37. Medina V, Croci M, Crescenti E, et al. The role of histamine in human mammary carcinogenesis: H3 and H4 receptors as potential therapeutic targets for breast cancer treatment. Cancer Biol Ther 2008;7:28-35. (Pubitemid 351590448)
38. Gaudio E, Barbaro B, Alvaro D, et al. Vascular endothelial growth factor stimulates rat cholangiocyte proliferation via an autocrine mechanism. Gastroenterology 2006;130:1270-1282.
39. LeSage G, Marucci L, Alvaro D, et al. Insulin inhibits secretin-induced ductal secretion by activation of PKC alpha and inhibition of PKA activity. Hepatology 2002;36:641-651. (Pubitemid 34977174)
40. Alpini G, Kanno N, Phinizy JL, et al. Tauroursodeoxycholate inhibits human cholangiocarcinoma growth via Ca2+-, PKC-, and MAPKdependent pathways. Am J Physiol Gastrointest Liver Physiol 2004;286:G973-G982. (Pubitemid 38715660)
41. Alpini G, Ueno Y, Glaser S, et al. Bile acid feeding increased proliferative activity and apical bile acid transporter expression in both small and large rat cholangiocytes. Hepatology 2001;34:868-876. (Pubitemid 33032020)
42. Kanno N, Glaser S, Chowdhury U, et al. Gastrin inhibits cholangiocarcinoma growth through increased apoptosis by activation of Ca2+-dependent protein kinase C-alpha. J Hepatol 2001;34:284-291. (Pubitemid 32176451)
43. LeSage G, Alvaro D, Glaser S, et al. Alpha-1 adrenergic receptor agonists modulate ductal secretion of BDL rats via Ca(2+)- and PKCdependent stimulation of cAMP. Hepatology 2004;40:1116-1127. (Pubitemid 39425567)
44. Marzioni M, Francis H, Benedetti A, et al. Ca2+-dependent cytoprotective effects of ursodeoxycholic and tauroursodeoxycholic acid on the biliary epithelium in a rat model of cholestasis and loss of bile ducts. Am J Pathol 2006;168:398-409. (Pubitemid 43271139)
45. Francis H, Onori P, Gaudio E, et al. H3 histamine receptor-mediated activation of protein kinase Calpha inhibits the growth of cholangiocarcinoma in vitro and in vivo. Mol Cancer Res 2009;7:1704-1713.
46. Mine T, Kojima I, Ogata E. Mechanism of glycogenolytic action of histamine in rat hepatocytes. Am J Physiol Gastrointest Liver Physiol 1991;261:G1000-G1004.
47. Garcia-Sainz JA, Macias-Silva M, Olivares-Reyes A, et al. Histamine activates phosphorylase and inositol phosphate production in guinea pig hepatocytes. Eur J Pharmacol 1992;227:325-331.
48. Alpini G, Franchitto A, DeMorrow S, et al. Activation of alpha(1) - adrenergic receptors stimulate the growth of small mouse cholangiocytes via calcium-dependent activation of nuclear factor of activated T cells 2 and specificity protein 1. Hepatology 2011;53: 628-639.
49. Strazzabosco M, Fiorotto R, Melero S, et al. Differentially expressed adenylyl cyclase isoforms mediate secretory functions in cholangiocyte subpopulation. Hepatology 2009;50:244-252.
50. Alpini G, Baiocchi L, Glaser S, et al. Ursodeoxycholate and tauroursodeoxycholate inhibit cholangiocyte growth and secretion of BDL rats through activation of PKC alpha. Hepatology 2002;35: 1041-1052. (Pubitemid 34454001)
51. Sharma GD, Ottino P, Bazan NG, et al. Epidermal and hepatocyte growth factors, but not keratinocyte growth factor, modulate protein kinase Calpha translocation to the plasma membrane through 15(S)- hydroxyeicosatetraenoic acid synthesis. J Biol Chem 2005;280:7917-7924. (Pubitemid 40349689)
52. Aziz MH, Manoharan HT, Sand JM, et al. Protein kinase Cepsilon interacts with Stat3 and regulates its activation that is essential for the development of skin cancer. Mol Carcinog 2007;46:646-653. (Pubitemid 47255182)
53. Francis H, Meininger CJ. A review of mast cells and liver disease: what have we learned? Dig Liver Dis 2010 42 529-536.
54. Quist RG, Ton-Nu HT, Lillienau J, et al. Activation of mast cells by bile acids. Gastroenterology 1991;101:446-456.