Endogenous Opioids Modulate the Growth of the Biliary Tree in the Course of Cholestasis

Gastroenterology

Volumn 130, Issue 6, 2006, Pages 1831-1847

  Marzioni, Marco ^a   Alpini, Gianfranco ^b,c   Saccomanno, Stefania ^a   de Minicis, Samuele ^a   Glaser, Shannon ^c   Francis, Heather ^c   Trozzi, Luciano ^a   Venter, Juliet ^c   Orlando, Fiorenza ^d   Fava, Giammarco ^a   Candelaresi, Cinzia ^a   Macarri, Giampiero ^a   Benedetti, Antonio ^a  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b DIVISION OF RESEARCH   (United States)

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

^d IRCCS   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR AGONIST; KAPPA OPIATE RECEPTOR; KAPPA OPIATE RECEPTOR AGONIST; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; NALOXONE; OPIATE RECEPTOR; PROTEIN KINASE B; PROTEIN KINASE C ALPHA;

ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHOLESTASIS; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; NEUROSECRETORY CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR INTRINSIC ACTIVITY; RECEPTOR SENSITIVITY; SIGNAL TRANSDUCTION;

EID: 33646336861     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2006.02.021     Document Type: Article

References (65)

1. Alpini G., Lenzi R., Sarkozi L., and Tavoloni N. Biliary physiology in rats with bile ductular cell hyperplasia. Evidence for a secretory function of proliferated bile ductules. J Clin Invest 81 (1988) 569-578
2. Lazaridis K.N., Strazzabosco M., and LaRusso N.F. The cholangiopathies. disorders of biliary epithelia. Gastroenterology 127 (2004) 1565-1577
3. Annual Report of the U. S. Organ Procurement and Transplantation Network and the Scientific Registry for Transplant Recipients: transplant data 1991-2000 (2001), Department of Health and Human Services, Health Resources and Services Administration, Office of Special Programs, Division of Transplantation, Rockville, MD
4. Glaser S., Benedetti A., Marucci L., Alvaro D., Baiocchi L., Kanno N., Caligiuri A., Phinizy J.L., Chowdury U., Papa E., LeSage G., and Alpini G. 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 32 (2000) 17-25
5. Kanno N., LeSage G., Glaser S., and Alpini G. Regulation of cholangiocyte bicarbonate secretion. Am J Physiol Gastrointest Liver Physiol 281 (2001) G612-G625
6. Gigliozzi A., Alpini G., Baroni G.S., Marucci L., Metalli V.D., Glaser S.S., Francis H., Mancino M.G., Ueno Y., Barbaro B., Benedetti A., Attili A.F., and Alvaro D. Nerve growth factor modulates the proliferative capacity of the intrahepatic biliary epithelium in experimental cholestasis. Gastroenterology 127 (2004) 1198-1209
7. LeSage G., Alvaro D., Benedetti A., Glaser S., Marucci L., Eisel W., Caligiuri A., Baiocchi L., Rodgers R., Phinizy J.L., Francis H., and Alpini G. Cholinergic system modulates growth, apoptosis and secretion of cholangiocytes from bile duct ligated rats. Gastroenterology 117 (1999) 191-199
8. LeSage G.D., Marucci L., Alvaro D., Glaser S., Benedetti A., Marzioni M., Patel T., Francis H., Phinizy J.L., and Alpini G. Insulin inhibits secretin-induced ductal secretion by activation of PKC alpha and inhibition of PKA activity. Hepatology 36 (2002) 641-651
9. LeSage G.D., Alvaro D., Glaser S., Francis H., Marucci L., Roskams T., Phinizy J.L., Marzioni M., Benedetti A., Taffetani S., Barbaro B., Fava G., Ueno Y., and Alpini G. Alpha-1 adrenergic receptor agonists modulate ductal secretion of BDL rats via Ca(2+)- and PKC-dependent stimulation of cAMP. Hepatology 40 (2004) 1116-1127
10. Tietz P.S., Alpini G., Pham L.D., and LaRusso N.F. Somatostatin inhibits secretin-induced ductal hypercholeresis and exocytosis by cholangiocytes. Am J Physiol 269 (1995) G110-G118
11. Marzioni M., Glaser S., Francis H., Marucci L., Benedetti A., Alvaro D., Taffetani S., Ueno Y., Roskams T., Phinizy J.L., Venter J., Fava G., LeSage G.D., and Alpini G. Autocrine/paracrine regulation of the growth of the biliary tree by the neuroendocrine hormone serotonin. Gastroenterology 128 (2005) 121-137
12. Roskams T., van den Oord J.J., De Vos R., and Desmet V.J. Neuroendocrine features of reactive bile ductules in cholestatic liver disease. Am J Pathol 137 (1990) 1019-1025
13. Glasel J.A. The effects of morphine on cell proliferation. Prog Drug Res 55 (2000) 33-80
14. Zagon I.S., Smith J.P., and McLaughlin P.J. Human pancreatic cancer cell proliferation in tissue culture is tonically inhibited by opioid growth factor. Int J Oncol 14 (1999) 577-584
15. Zagon I.S., Hytrek S.D., and McLaughlin P.J. Opioid growth factor tonically inhibits human colon cancer cell proliferation in tissue culture. Am J Physiol 271 (1996) R511-R518
16. Zagon I.S., Wu Y., and McLaughlin P.J. Opioid growth factor is present in human and mouse gastrointestinal tract and inhibits DNA synthesis. Am J Physiol 272 (1997) R1094-R1104
17. Simon E.J. Opioid receptors and endogenous opioid peptides. Med Res Rev 11 (1991) 357-374
18. Wollemann M., and Benyhe S. Non-opioid actions of opioid peptides. Life Sci 75 (2004) 257-270
19. Bergasa N.V., Liau S., Homel P., and Ghali V. Hepatic Met-enkephalin immunoreactivity is enhanced in primary biliary cirrhosis. Liver 22 (2002) 107-113
20. Bergasa N.V., Rothman R.B., Vergalla J., Xu H., Swain M.G., and Jones E.A. Central mu-opioid receptors are down-regulated in a rat model of cholestasis. J Hepatol 15 (1992) 220-224
21. Bergasa N.V., Vergalla J., Swain M.G., and Jones E.A. Hepatic concentrations of proenkephalin-derived opioids are increased in a rat model of cholestasis. Liver 16 (1996) 298-302
22. Swain M.G., Rothman R.B., Xu H., Vergalla J., Bergasa N.V., and Jones E.A. Endogenous opioids accumulate in plasma in a rat model of acute cholestasis. Gastroenterology 103 (1992) 630-635
23. Jones E.A., and Bergasa N.V. The pruritus of cholestasis. Hepatology 29 (1999) 1003-1006
24. Bergasa N.V., Sabol S.L., Young III W.S., Kleiner D.E., and Jones E.A. Cholestasis is associated with preproenkephalin mRNA expression in the adult rat liver. Am J Physiol 268 (1995) G346-G354
25. Bao L., Jin S.X., Zhang C., Wang L.H., Xu Z.Z., Zhang F.X., Wang L.C., Ning F.S., Cai H.J., Guan J.S., Xiao H.S., Xu Z.Q., He C., Hokfelt T., Zhou Z., and Zhang X. Activation of delta opioid receptors induces receptor insertion and neuropeptide secretion. Neuron 37 (2003) 121-133
26. Melone M., Brecha N.C., Sternini C., Evans C., and Conti F. Etorphine increases the number of mu-opioid receptor-positive cells in the cerebral cortex. Neuroscience 100 (2000) 439-443
27. Zhang N., Rogers T.J., Caterina M., and Oppenheim J.J. Proinflammatory chemokines, such as C-C chemokine ligand 3, desensitize mu-opioid receptors on dorsal root ganglia neurons. J Immunol 173 (2004) 594-599
28. Marzioni M., LeSage G., Glaser S., Patel T., Marienfeld C., Ueno Y., Francis H., Alvaro D., Phinizy J.L., Tadlock L., Benedetti A., Marucci L., Baiocchi L., and Alpini G. Taurocholate prevents the loss of intrahepatic bile ducts due to vagotomy in bile duct ligated rats. Am J Physiol 284 (2003) G837-G852
29. Qiao L., Yacoub A., Studer E., Gupta S., Pei X.Y., Grant S., Hylemon P.B., and Dent P. Inhibition of the MAPK and PI3K pathways enhances UDCA-induced apoptosis in primary rodent hepatocytes. Hepatology 35 (2002) 779-789
30. 2+ and AMPK both mediate stimulation of glucose transport by muscle contractions. Diabetes 53 (2004) 330-335
31. Tian Y., and Laychock S.G. Protein kinase C and calcium regulation of adenylyl cyclase in isolated rat pancreatic islets. Diabetes 50 (2001) 2505-2513
32. Demetris A., Lunz J., Subbotin V., Wu T., Nozaki I., Contrucci S., and Yin X. Participation of cytokines and growth factors in biliary epithelial proliferation and mito-inhibition during ductular reactions. In: Alpini G., Alvaro D., Marzioni M., LeSage G., and LaRusso N. (Eds). The pathobiology of biliary epithelia (2004), Landes Biosciences, Georgetown, TX 167-191
33. Svegliati-Baroni G., Ridolfi F., Hannivoort R., Saccomanno S., Homan M., De Minicis S., Jansen P.L., Candelaresi C., Benedetti A., and Moshage H. Bile acids induce hepatic stellate cell proliferation via activation of the epidermal growth factor receptor. Gastroenterology 128 (2005) 1042-1055
34. Liu B.H., Mo P., and Zhang S.B. Effects of mu and kappa opioid receptor agonists and antagonists on contraction of isolated colon strips of rats with cathartic colon. World J Gastroenterol 10 (2004) 1672-1674
35. Maga G., and Hubscher U. Proliferating cell nuclear antigen (PCNA). a dancer with many partners. J Cell Sci 116 (2003) 3051-3060
36. Dolbeare F. Bromodeoxyuridine: a diagnostic tool in biology and medicine, part III. Proliferation in normal, injured and diseased tissue, growth factors, differentiation, DNA replication sites and in situ hybridization. Histochem J 28 (1996) 531-575
37. Chen C., and Pollack G.M. Extensive biliary excretion of the model opioid peptide [D-PEN2,5] enkephalin in rats. Pharm Res 14 (1997) 345-350
38. Devoino L.V., Cheido M.A., and Al'perina E.L. Involvement of the nucleus accumbens in stimulation of the immune response in rats after activation of opioid mu receptors with DAGO. Neurosci Behav Physiol 32 (2002) 529-532
39. Gallate J.E., Mallet P.E., and McGregor I.S. Combined low dose treatment with opioid and cannabinoid receptor antagonists synergistically reduces the motivation to consume alcohol in rats. Psychopharmacology (Berl) 173 (2004) 210-216
40. Ishii M., Vroman B., and LaRusso N.F. Isolation and morphological characterization of bile duct epithelial cells from normal rat liver. Gastroenterology 97 (1989) 1236-1247
41. Alpini G., Ulrich C., Roberts S., Phillips J.O., Ueno Y., Podila P.V., Colegio O., LeSage G.D., Miller L.J., and LaRusso N.F. Molecular and functional heterogeneity of cholangiocytes from rat liver after bile duct ligation. Am J Physiol 272 (1997) G289-G297
42. LeSage G.D., Benedetti A., Glaser S., Marucci L., Tretjak Z., Caligiuri A., Rodgers R., Phinizy J.L., Baiocchi L., Francis H., Lasater J., Ugili L., and Alpini G. Acute carbon tetrachloride feeding selectively damages large, but not small, cholangiocytes from normal rat liver. Hepatology 29 (1999) 307-319
43. Suenaga T., Morinobu S., Kawano K., Sawada T., and Yamawaki S. Influence of immobilization stress on the levels of CaMKII and phospho-CaMKII in the rat hippocampus. Int J Neuropsychopharmacol 7 (2004) 299-309
44. Watanabe H., Shimizu T., Nishihira J., Abe R., Nakayama T., Taniguchi M., Sabe H., Ishibashi T., and Shimizu H. Ultraviolet A-induced production of matrix metalloproteinase-1 is mediated by macrophage migration inhibitory factor (MIF) in human dermal fibroblasts. J Biol Chem 279 (2004) 1676-1683
45. Thornton J.R., and Losowsky M.S. Opioid peptides and primary biliary cirrhosis. BMJ 297 (1988) 1501-1504
46. Bisignani G.J., McLaughlin P.J., Ordille S.D., Beltz M.S., Jarowenko M.V., and Zagon I.S. Human renal cell cancer proliferation in tissue culture is tonically inhibited by opioid growth factor. J Urol 162 (1999) 2186-2191
47. Marzioni M., Glaser S.S., Francis H., Phinizy J.L., LeSage G., and Alpini G. Functional heterogeneity of cholangiocytes. Semin Liver Dis 22 (2002) 227-240
48. Andreeva V., Prudovsky I., and Thomas M. Stimulation of quiescent cells by individual polypeptide growth factors is limited to one cell cycle. Eur J Cell Biol 83 (2004) 327-335
49. Knapp P.E., Maderspach K., and Hauser K.F. Endogenous opioid system in developing normal and jimpy oligodendrocytes. mu and kappa opioid receptors mediate differential mitogenic and growth responses. Glia 22 (1998) 189-201
50. Leslie F.M., Chen Y., and Winzer-Serhan U.H. Opioid receptor and peptide mRNA expression in proliferative zones of fetal rat central nervous system. Can J Physiol Pharmacol 76 (1998) 284-293
51. Wang H., Cuzon V.C., and Pickel V.M. Ultrastructural localization of delta-opioid receptors in the rat caudate-putamen nucleus during postnatal development. relation to synaptogenesis. J Comp Neurol 467 (2003) 343-353
52. Hauser K.F., Houdi A.A., Turbek C.S., Elde R.P., and Maxson III W. Opioids intrinsically inhibit the genesis of mouse cerebellar granule neuron precursors in vitro. differential impact of mu and delta receptor activation on proliferation and neurite elongation. Eur J Neurosci 12 (2000) 1281-1293
53. Nelson C.J., Schneider G.M., and Lysle D.T. Involvement of central mu- but not delta- or kappa-opioid receptors in immunomodulation. Brain Behav Immun 14 (2000) 170-184
54. Belcheva M.M., Szucs M., Wang D., Sadee W., and Coscia C.J. mu-Opioid receptor-mediated ERK activation involves calmodulin-dependent epidermal growth factor receptor transactivation. J Biol Chem 276 (2001) 33847-33853
55. Opanashuk L.A., and Hauser K.F. Opposing actions of the EGF family and opioids. heparin binding-epidermal growth factor (HB-EGF) protects mouse cerebellar neuroblasts against the antiproliferative effect of morphine. Brain Res 804 (1998) 87-94
56. Marra F., Arrighi M.C., Fazi M., Caligiuri A., Pinzani M., Romanelli R.G., Efsen E., Laffi G., and Gentilini P. Extracellular signal-regulated kinase activation differentially regulates platelet-derived growth factor's actions in hepatic stellate cells, and is induced by in vivo liver injury in the rat. Hepatology 30 (1999) 951-958
57. Hirata K., Dufour J.F., Shibao K., Knickelbein R., O'Neill A.F., Bode H.P., Cassio D., St-Pierre M.V., LaRusso N.F., Leite M.F., and Nathanson M.H. Regulation of Ca(2+) signaling in rat bile duct epithelia by inositol 1,4,5-trisphosphate receptor isoforms. Hepatology 36 (2002) 284-296
58. 2+ signaling in rat bile duct epithelia. Am J Physiol 271 (1996) G86-G96
59. Shibao K., Hirata K., Robert M.E., and Nathanson M.H. Loss of inositol 1,4,5-trisphosphate receptors from bile duct epithelia is a common event in cholestasis. Gastroenterology 125 (2003) 1175-1187
60. Alpini G., Baiocchi L., Glaser S., Ueno Y., Marzioni M., Francis H., Phinizy J.L., Angelico M., and LeSage G. Ursodeoxycholate and tauroursodeoxycholate inhibit cholangiocyte proliferation and secretion of bile duct ligated rats through activation of PKC alpha. Hepatology 35 (2002) 1041-1052
61. 2+ mobilization and astroglial development. morphine inhibits DNA synthesis and stimulates cellular hypertrophy through a Ca(2+)-dependent mechanism. Brain Res 720 (1996) 191-203
62. Tanowitz M., and von Zastrow M. A novel endocytic recycling signal that distinguishes the membrane trafficking of naturally occurring opioid receptors. J Biol Chem 278 (2003) 45978-45986
63. Benedetti A., Di Sario A., Casini A., Ridolfi F., Bendia E., Pigini P., Tonnini C., D'Ambrosio L., Feliciangeli G., Macarri G., and Svegliati-Baroni G. Inhibition of the NA(+)/H(+) exchanger reduces rat hepatic stellate cell activity and liver fibrosis. an in vitro and in vivo study. Gastroenterology 120 (2001) 545-556
64. + exchange inhibition by cariporide reduces liver fibrosis in the rat. Hepatology 37 (2003) 256-266
65. Jule Y., Clerc N., Niel J.P., and Condamin M. [Met]- and [Leu]enkephalin-like immunoreactive cell bodies and nerve fibres in the coeliac ganglion of the cat. Neuroscience 18 (1986) 487-498