Chronic nicotine exposure stimulates biliary growth and fibrosis in normal rats

Digestive and Liver Disease

Volumn 45, Issue 9, 2013, Pages 754-761

  Jensen, Kendal ^b   Afroze, Syeda ^b   Ueno, Yoshiyuki ^e   Rahal, Kinan ^c   Frenzel, Amber ^d   Sterling, Melanie ^d   Guerrier, Micheleine ^b   Nizamutdinov, Damir ^a,c   Dostal, David E ^a,c   Meng, Fanyin ^a,b,c   Glaser, Shannon S ^a,b,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b Scott ans White Digestive Disease Research Center (DDRC)   (United States)

^c TEXAS A M COLLEGE OF MEDICINE   (United States)

^d Undergraduate Research Program   (United States)

^e YAMAGATA UNIVERSITY   (Japan)

Author keywords

Biliary epithelia; Cholangiocytes; Fibrosis; Nicotinic receptors; Proliferation

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BUNGAROTOXIN RECEPTOR; CALCIUM ION; FIBRONECTIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NICOTINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LINE; CELL PROLIFERATION; CONTROLLED STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; INTRAHEPATIC BILE DUCT; LONG TERM EXPOSURE; MALE; NONHUMAN; OSMOTIC MINIPUMP; PRIMARY BILIARY CIRRHOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

BILIARY EPITHELIA; CHOLANGIOCYTES; FIBROSIS; NICOTINIC RECEPTORS; PROLIFERATION;

ACTINS; ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; BILE DUCTS; CELL PROLIFERATION; COLLAGEN; EPITHELIAL CELLS; FIBRONECTINS; LIVER; LIVER CIRRHOSIS; MAP KINASE SIGNALING SYSTEM; NICOTINE; NICOTINIC AGONISTS; RATS; RATS, INBRED F344; RNA, MESSENGER;

EID: 84882251664     PISSN: 15908658     EISSN: 18783562     Source Type: Journal    
DOI: 10.1016/j.dld.2013.02.023     Document Type: Article

References (71)

1. LeSage G., Benedetti A., Glaser S., et al. Acute carbon tetrachloride feeding selectively damages large, but not small, cholangiocytes from normal rat liver. Hepatology 1999, 29:307-319.
2. 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.
3. Alpini G., Prall R.T., LaRusso N.F. The pathobiology of biliary epithelia. The liver; biology & pathobiology, vol. 4E 2001, 421-435. Lippincott Williams & Wilkins, Philadelphia, PA. I.M. Arias, J.L. Boyer, F.V. Chisari, N. Fausto, W. Jakoby, D. Schachter, D.A. Shafritz (Eds.).
4. Munshi M.K., Priester S., Gaudio E., et al. Regulation of biliary proliferation by neuroendocrine factors: implications for the pathogenesis of cholestatic liver diseases. American Journal of Pathology 2011, 178:472-484.
5. Alpini G., McGill J.M., Larusso N.F. The pathobiology of biliary epithelia. Hepatology 2002, 35:1256-1268.
6. Glaser S.S., Gaudio E., Miller T., et al. Cholangiocyte proliferation and liver fibrosis. Expert Reviews in Molecular Medicine 2009, 11:e7.
7. Glaser S., Francis H., DeMorrow S., et al. Heterogeneity of the intrahepatic biliary epithelium. World Journal of Gastroenterology 2006, 12:3523-3536.
8. Corpechot C., Gaouar F., Chretien Y., et al. Smoking as an independent risk factor of liver fibrosis in primary biliary cirrhosis. Journal of Hepatology 2012, 56:218-224.
9. Tsochatzis E., Papatheodoridis G.V., Manolakopoulos S., et al. Smoking is associated with steatosis and severe fibrosis in chronic hepatitis C but not B. Scandinavian Journal of Gastroenterology 2009, 44:752-759.
10. Zein C.O., Unalp A., Colvin R., et al. Smoking and severity of hepatic fibrosis in nonalcoholic fatty liver disease. Journal of Hepatology 2011, 54:753-759.
11. Tischendorf J.J., Meier P.N., Strassburg C.P., et al. Characterization and clinical course of hepatobiliary carcinoma in patients with primary sclerosing cholangitis. Scandinavian Journal of Gastroenterology 2006, 41:1227-1234.
12. Benowitz N.L. Drug therapy. Pharmacologic aspects of cigarette smoking and nicotine addition. New England Journal of Medicine 1988, 319:1318-1330.
13. Cahill K., Stead L.F., Lancaster T. Nicotine receptor partial agonists for smoking cessation. Cochrane Database of Systematic Reviews 2011, CD006103.
14. Hukkanen J., Jacob P., 3rd, Benowitz N.L. Metabolism and disposition kinetics of nicotine. Pharmacological Reviews 2005, 57:79-115.
15. Millar N.S., Harkness P.C. Assembly and trafficking of nicotinic acetylcholine receptors. Molecular Membrane Biology 2008, 25:279-292. (Review).
16. Wessler I., Kirkpatrick C.J. Acetylcholine beyond neurons: the non-neuronal cholinergic system in humans. British Journal of Pharmacology 2008, 154:1558-1571.
17. Egleton R.D., Brown K.C., Dasgupta P. Nicotinic acetylcholine receptors in cancer: multiple roles in proliferation and inhibition of apoptosis. Trends in Pharmacological Sciences 2008, 29:151-158.
18. Schuller H.M. Is cancer triggered by altered signalling of nicotinic acetylcholine receptors?. Nature Reviews Cancer 2009, 9:195-205.
19. Dasgupta P., Rastogi S., Pillai S., et al. Nicotine induces cell proliferation by beta-arrestin-mediated activation of Src and Rb-Raf-1 pathways. Journal of Clinical Investigation 2006, 116:2208-2217.
20. Zheng Y., Ritzenthaler J.D., Roman J., et al. Nicotine stimulates human lung cancer cell growth by inducing fibronectin expression. American Journal of Respiratory Cell and Molecular Biology 2007, 37:681-690.
21. Soeda J., Morgan M., McKee C., et al. Nicotine induces fibrogenic changes in human liver via nicotinic acetylcholine receptors expressed on hepatic stellate cells. Biochemical and Biophysical Research Communications 2012, 417:17-22.
22. Gotti C., Clementi F. Neuronal nicotinic receptors: from structure to pathology. Progress in Neurobiology 2004, 74:363-396.
23. Alvaro D., Alpini G., Jezequel A.M., et al. Role and mechanisms of action of acetylcholine in the regulation of rat cholangiocyte secretory functions. Journal of Clinical Investigation 1997, 100:1349-1362.
24. Lesage G., Alvaro D., Benedetti A., et al. Cholinergic system modulates growth, apoptosis, and secretion of cholangiocytes from bile duct-ligated rats. Gastroenterology 1999, 117:191-199.
25. Bodnar A.L., Cortes-Burgos L.A., Cook K.K., et al. Discovery and structure-activity relationship of quinuclidine benzamides as agonists of alpha7 nicotinic acetylcholine receptors. Journal of Medicinal Chemistry 2005, 48:905-908.
26. Zhang Z.W., Vijayaraghavan S., Berg D.K. Neuronal acetylcholine receptors that bind alpha-bungarotoxin with high affinity function as ligand-gated ion channels. Neuron 1994, 12:167-177.
27. 2+-dependent PKC isoforms. Liver International 2003, 23:78-88.
28. 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.
29. Ohmura Y., Jutkiewicz E.M., Zhang A., et al. Dopamine D1/5 and D2/3 agonists differentially attenuate somatic signs of nicotine withdrawal in rats. Pharmacology Biochemistry and Behavior 2011, 99:552-556.
30. Malin D.H., Goyarzu P. Rodent models of nicotine withdrawal syndrome. Handbook of Experimental Pharmacology 2009, 401-434.
31. Hamilton K.R., Berger S.S., Perry M.E., et al. Behavioral effects of nicotine withdrawal in adult male and female rats. Pharmacology Biochemistry and Behavior 2009, 92:51-59.
32. Ohmura Y., Jutkiewicz E.M., Domino E.F. l-DOPA attenuates nicotine withdrawal-induced behaviors in rats. Pharmacology Biochemistry and Behavior 2011, 98:552-558.
33. Benowitz N.L., Kuyt F., Jacob P. Circadian blood nicotine concentrations during cigarette smoking. Clinical Pharmacology and Therapeutics 1982, 32:758-764.
34. LeSage M.G., Keyler D.E., Shoeman D., et al. Continuous nicotine infusion reduces nicotine self-administration in rats with 23-h/day access to nicotine. Pharmacology Biochemistry and Behavior 2002, 72:279-289.
35. Alpini G., Ulrich C., Roberts S., et al. Molecular and functional heterogeneity of cholangiocytes from rat liver after bile duct ligation. American Journal of Physiology. Gastrointestinal and Liver Physiology 1997, 272:G289-G297.
36. Alpini G., Phinizy J.L., Glaser S., et al. Development and characterization of secretin-stimulated secretion of cultured rat cholangiocytes. American Journal of Physiology. Gastrointestinal and Liver Physiology 2003, 284:G1066-G1073.
37. Glaser S., Rodgers R.E., Phinizy J.L., et al. Gastrin inhibits secretin-induced ductal secretion by interaction with specific receptors on rat cholangiocytes. American Journal of Pathology 1997, 273:G1061-G1070.
38. Glaser S., DeMorrow S., Francis H., et al. Progesterone stimulates the proliferation of female and male cholangiocytes via autocrine/paracrine mechanisms. American Journal of Physiology. Gastrointestinal and Liver Physiology 2008, 295:G124-G136.
39. Seguela P., Wadiche J., Dineley-Miller K., et al. Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium. Journal of Neuroscience 1993, 13:596-604.
40. Tso J.Y., Sun X.H., Kao T.H., et al. Isolation and characterization of rat and human glyceraldehyde-3-phosphate dehydrogenase cDNAs: genomic complexity and molecular evolution of the gene. Nucleic Acids Research 1985, 13:2485-2502.
41. Glaser S., Gaudio E., Renzi A., et al. Knockout of the neurokinin-1 receptor reduces cholangiocyte proliferation in bile duct-ligated mice. American Journal of Physiology. Gastrointestinal and Liver Physiology 2011, 301:G297-G305.
42. Glaser S., Wang M., Ueno Y., et al. Differential transcriptional characteristics of small and large biliary epithelial cells derived from small and large bile ducts. American Journal of Physiology. Gastrointestinal and Liver Physiology 2010, 299:G769-G777.
43. Glaser S., Alvaro D., Francis H., et al. Adrenergic receptor agonists prevent bile duct injury induced by adrenergic denervation by increased cAMP levels and activation of Akt. American Journal of Physiology. Gastrointestinal and Liver Physiology 2006, 290:G813-G826.
44. 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. Journal of Clinical Investigation 1988, 81:569-578.
45. 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. American Journal of Physiology. Gastrointestinal and Liver Physiology 2009, 297:G11-G26.
46. Leheup B.P., Federspiel S.J., Guerry-Force M.L., et al. Extracellular matrix biosynthesis by cultured fetal rat lung epithelial cells. I. Characterization of the clone and the major genetic types of collagen produced. Laboratory Investigation 1989, 60:791-807.
47. Hsu C.Y., Frankel F.R. Effect of estrogen on the expression of mRNAs of different actin isoforms in immature rat uterus, Cloning of alpha-smooth muscle actin message. Journal of Biological Chemistry 1987, 262:9594-9600.
48. Schneider C., Rasband W., Eliceiri K. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 2012, 9:671-675.
49. Khalil A.A., Jameson M.J., Broaddus W.C., Lin P.S., Chung T.D., et al. Nicotine enhances proliferation, migration, and radioresistance of human malignant glioma cells through EGFR activation. Brain Tumor Pathology 2012, [Epub ahead of print].
50. Maggi L., Sher E., Cherubini E. Regulation of GABA release by nicotinic acetylcholine receptors in the neonatal rat hippocampus. Journal of Physiology 2001, 536:89-100.
51. 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.
52. Lien Y.C., Wang W., Kuo L.J., et al. Nicotine promotes cell migration through alpha7 nicotinic acetylcholine receptor in gastric cancer cells. Annals of Surgical Oncology 2011, 18:2671-2679.
53. Wei P.L., Kuo L.J., Huang M.T., et al. Nicotine enhances colon cancer cell migration by induction of fibronectin. Annals of Surgical Oncology 2011, 18:1782-1790.
54. Cucina A., Dinicola S., Coluccia P., et al. Nicotine stimulates proliferation and inhibits apoptosis in colon cancer cell lines through activation of survival pathways. Journal of Surgical Research 2012, 178:233-241.
55. Momi N., Ponnusamy M.P., Kaur S., et al. Nicotine/cigarette smoke promotes metastasis of pancreatic cancer through alpha7nAChR-mediated MUC4 upregulation. Oncogene 2012, (May). [Epub ahead of print]. 10.1038/onc.2012.163.
56. 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. Journal of Hepatology 2004, 41:528-537.
57. Chowdhury P., Hosotani R., Rayford P.L. Weight loss and altered circulating GI peptide levels of rats exposed chronically to nicotine. Pharmacology Biochemistry and Behavior 1989, 33:591-594.
58. Frankham P., Cabanac M. Nicotine lowers the body-weight set-point in male rats. Appetite 2003, 41:1-5.
59. Arany I., Reed D.K., Grifoni S.C., et al. A novel U-STAT3-dependent mechanism mediates the deleterious effects of chronic nicotine exposure on renal injury. American Journal of Physiology. Renal Physiology 2012, 302:F722-F729.
60. Frazier K., Williams S., Kothapalli D., et al. Stimulation of fibroblast cell growth, matrix production, and granulation tissue formation by connective tissue growth factor. Journal of Investigative Dermatology 1996, 107:404-411.
61. Cory A.H., Owen T.C., Barltrop J.A., et al. Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Communications 1991, 3:207-212.
62. Dajas-Bailador F., Wonnacott S. Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends in Pharmacological Sciences 2004, 25:317-324.
63. Pillai S., Chellappan S. alpha7 nicotinic acetylcholine receptor subunit in angiogenesis and epithelial to mesenchymal transition. Current Drug Targets 2012, 13:671-679.
64. Schuller H.M., Al-Wadei H.A. Neurotransmitter receptors as central regulators of pancreatic cancer. Future Oncology 2010, 6:221-228.
65. Rezonzew G., Chumley P., Feng W., et al. Nicotine exposure and the progression of chronic kidney disease: role of the alpha7-nicotinic acetylcholine receptor. American Journal of Physiology. Renal Physiology 2012, 303:F304-F312.
66. Strohschneider T., Oberhoff M., Hanke H., et al. Effect of chronic nicotine delivery on the proliferation rate of endothelial and smooth muscle cells in experimentally induced vascular wall plaques. The Clinical Investigator 1994, 72:908-912.
67. Renzi A., Glaser S., DeMorrow S., et al. Melatonin inhibits cholangiocyte hyperplasia in cholestatic rats by interaction with MT1 but not MT2 melatonin receptors. American Journal of Physiology. Gastrointestinal and Liver Physiology 2011, 301:G634-G643.
68. Kurtul N., Cil M.Y., Bakan E. The effects of alcohol and smoking on serum, saliva, and urine sialic acid levels. Saudi Medical Journal 2004, 25:1839-1844.
69. Breitling L.P., Arndt V., Drath C., et al. Liver enzymes: interaction analysis of smoking with alcohol consumption or BMI, comparing AST and ALT to gamma-GT. PLoS ONE 2011, 6:e27951.
70. Krebs M., Sakurai R., Torday J.S., et al. Evidence for in vivo nicotine-induced alveolar interstitial fibroblast-to-myofibroblast transdifferentiation. Experimental Lung Research 2010, 36:390-398.
71. Chernyavsky A.I., Arredondo J., Qian J., et al. Coupling of ionic events to protein kinase signaling cascades upon activation of alpha7 nicotinic receptor: cooperative regulation of alpha2-integrin expression and Rho kinase activity. Journal of Biological Chemistry 2009, 284:22140-22148.