Role for Hedgehog signaling in hepatic stellate cell activation and viability

Laboratory Investigation

Volumn 85, Issue 11, 2005, Pages 1368-1380

  Sicklick, Jason K ^a,b   Li, Yin Xiong ^a   Choi, Steve S ^a   Qi, Yi ^a   Chen, Wei ^a   Bustamante, Marcia ^c   Huang, Jiawen ^a   Zdanowicz, Marzena ^a   Camp, Terese ^a   Torbenson, Michael S ^b   Rojkind, Marcos ^c   Diehl, Anna Mae ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cirrhosis; Cyclopamine; Liver; Myofibroblast; Neuroendocrine cells; Patched

Indexed keywords

BETA GALACTOSIDASE; CYCLOPAMINE; LIGAND; LUCIFERASE; NEUTRALIZING ANTIBODY; PROTEIN INHIBITOR; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL FATE; CELL ISOLATION; CELL LINE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPOTHESIS; LIVER CELL; LIVER INJURY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; STELLATE CELL;

ANIMALS; ANTIBODIES; APOPTOSIS; BETA-GALACTOSIDASE; CELL SURVIVAL; CELLS, CULTURED; CLONE CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENES, REPORTER; HEDGEHOG PROTEINS; HEPATOCYTES; HUMANS; LIGANDS; LUCIFERASES; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; VERATRUM ALKALOIDS;

EID: 27144554034     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.3700349     Document Type: Article

References (72)

1. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005;115:209-218.
2. Fallowfield JA, Iredale JP. Targeted treatments for cirrhosis. Expert Opin Ther Targets 2004;8:423-435.
3. Sato M, Suzuki S, Senoo H. Hepatic stellate cells: unique characteristics in cell biology and phenotype. Cell Struct Funct 2003;28:105-112.
4. Magness ST, Bataller R, Yang L, et al. A dual reporter gene transgenic mouse demonstrates heterogeneity in hepatic fibrogenic cell populations. Hepatology 2004;40:1151-1159.
5. Friedman SL. Stellate cells: a moving target in hepatic fibrogenesis. Hepatology 2004;40:1041-1043.
6. Niki T, Pekny M, Hellemans K, et al. Class VI intermediate filament protein nestin is induced during activation of rat hepatic stellate cells. Hepatology 1999;29:520-527.
7. Roskams T, Cassiman D, De Vos R, et al. Neuroregulation of the neuroendocrine compartment of the liver. Anat Rec A Discov Mol Cell Evol Biol 2004;280:910-923.
8. Oben JA, Roskams T, Yang S, et al. Hepatic fibrogenesis requires sympathetic neurotransmitters. Gut 2004;53:438-445.
9. Oben JA, Diehl AM. Sympathetic nervous system regulation of liver repair. Anat Rec A Discov Mol Cell Evol Biol 2004;280:874-883.
10. Oben JA, Yang S, Lin H, et al. Acetylcholine promotes the proliferation and collagen gene expression of myofibroblastic hepatic stellate cells. Biochem Biophys Res Commun 2003;300:172-177.
11. Oben JA, Yang S, Lin H, et al. Norepinephrine and neuropeptide Y promote proliferation and collagen gene expression of hepatic myofibroblastic stellate cells. Biochem Biophys Res Commun 2003;302:685-690.
12. Bataller R, Sancho-Bru P, Gines P, et al. Activated human hepatic stellate cells express the renin-angiotensin system and synthesize angiotensin II. Gastroenterology 2003;125:117-125.
13. Reynaert H, Rombouts K, Vandermonde A, et al. Expression of somatostatin receptors in normal and cirrhotic human liver and in hepatocellular carcinoma. Gut 2004;53:1180-1189.
14. Potter JJ, Womack L, Mezey E, et al. Transdifferentiation of rat hepatic stellate cells results in leptin expression. Biochem Biophys Res Commun 1998;244:178-182.
15. Fu M, Lui VC, Sham MH, et al. Sonic hedgehog regulates the proliferation, differentiation, and migration of enteric neural crest cells in gut. J Cell Biol 2004;166:673-684.
16. Taipale J, Beachy PA. The Hedgehog and Wnt signalling pathways in cancer. Nature 2001;411:349-354.
17. Rafuse VF, Soundararajan P, Leopold C, et al. Neuroprotective properties of cultured neural progenitor cells are associated with the production of sonic hedgehog. Neuroscience 2005;131:899-916.
18. van den Brink GR, Bleuming SA, Hardwick JC, et al. Indian Hedgehog is an antagonist of Wnt signaling in colonic epithelial cell differentiation. Nat Genet 2004;36:277-282.
19. Madison BB, Braunstein K, Kuizon E, et al. Epithelial hedgehog signals pattern the intestinal crypt-villus axis. Development 2005;132:279-289.
20. Nielsen CM, Williams J, van den Brink GR, et al. Hh pathway expression in human gut tissues and in inflammatory gut diseases. Lab Invest 2004;84:1631-1642.
21. Goodrich LV, Milenkovic L, Higgins KM, et al. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 1997;277:1109-1113.
22. Chen JK, Taipale J, Cooper MK, et al. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev 2002;16:2743-2748.
23. Xu L, Hui AY, Albanis E, et al. Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis. Gut 2005;54:142-151.
24. Greenwel P, Schwartz M, Rosas M, et al. Characterization of fat-storing cell lines derived from normal and CCl4-cirrhotic livers. Differences in the production of interleukin-6. Lab Invest 1991;65:644-653.
25. Watkins DN, Berman DM, Burkholder SG, et al. Hedgehog signalling within airway epithelial progenitors and in small-cell lung cancer. Nature 2003;422:313-317.
26. Ramm GA. Isolation and culture of rat hepatic stellate cells. J Gastroenterol Hepatol 1998;13:846-851.
27. Friedman SL, Rockey DC, McGuire RF, et al. Isolated hepatic lipocytes and Kupffer cells from normal human liver: morphological and functional characteristics in primary culture. Hepatology 1992;15:234-243.
28. Oben JA, Roskams T, Yang S, et al. Norepinephrine induces hepatic fibrogenesis in leptin deficient ob/ob mice. Biochem Biophys Res Commun 2003;308:284-292.
29. Reeves HL, Friedman SL. Activation of hepatic stellate cells - a key issue in liver fibrosis. Front Biosci 2002;7:d808-d826.
30. She H, Xiong S, Hazra S, et al. Adipogenic transcriptional regulation of hepatic stellate cells. J Biol Chem 2005;280:4959-4967.
31. Armendariz-Borunda J, Greenwel P, Rojkind M. Kupffer cells from CC1(4)-treated rat livers induce skin fibroblast and liver fat-storing cell proliferation in culture. Matrix 1989;9:150-158.
32. Lee JS, Kang Decker N, Chatterjee S, et al. Mechanisms of nitric oxide interplay with Rho GTPase family members in modulation of actin membrane dynamics in pericytes and fibroblasts. Am J Pathol 2005;166:1861-1870.
33. Ericson J, Morton S, Kawakami A, et al. Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 1996;87:661-673.
34. Berman DM, Karhadkar SS, Maitra A, et al. Widespread requirement for Hedgehog ligand stimulation in growth of digestive tract tumours. Nature 2003;425:846-851.
35. Skalli O, Ropraz P, Trzeciak A, et al. A monoclonal antibody against alpha-smooth muscle actin: a new probe for smooth muscle differentiation. J Cell Biol 1986;103:2787-2796.
36. Castellano B, Gonzalez B, Jensen MB, et al. A double staining technique for simultaneous demonstration of astrocytes and microglia in brain sections and astroglial cell cultures. J Histochem Cytochem 1991;39:561-568.
37. Itano N, Atsumi F, Sawai T, et al. Abnormal accumulation of hyaluronan matrix diminishes contact inhibition of cell growth and promotes cell migration. Proc Natl Acad Sci USA 2002;99:3609-3614.
38. Sudarshan S, Holman DH, Hyer ML, et al. In vitro efficacy of Fas ligand gene therapy for the treatment of bladder cancer. Cancer Gene Ther 2005;12:12-18.
39. Takao T, Kumagai C, Hisakawa N, et al. Effect of 17beta-estradiol on tumor necrosis factor-alpha-induced cytotoxicity in the human peripheral T lymphocytes. J Endocrinol 2005;184:191-197.
40. Merchant M, Vajdos FF, Ultsch M, et al. Suppressor of fused regulates Gli activity through a dual binding mechanism. Mol Cell Biol 2004;24:8627-8641.
41. Murota H, Hamasaki Y, Nakashima T, et al. Disruption of tumor necrosis factor receptor p55 impairs collagen turnover in experimentally induced sclerodermic skin fibroblasts. Arthritis Rheum 2003;48:1117-1125.
42. Katayam M, Yoshida K, Ishimori H, et al. Patched and smoothened mRNA expression in human astrocytic tumors inversely correlates with histological malignancy. J Neurooncol 2002;59:107-115.
43. Hung CJ, Ginzinger DG, Zarnegar R, et al. Expression of vascular endothelial growth factor-C in benign and malignant thyroid tumors. J Clin Endocrinol Metab 2003;88:3694-3699.
44. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001;25:402-408.
45. Pepinsky RB, Shapiro RI, Wang S, et al. Long-acting forms of Sonic hedgehog with improved pharmacokinetic and pharmacodynamic properties are efficacious in a nerve injury model. J Pharm Sci 2002;91:371-387.
46. Geerts A, Greenwel P, Cunningham M, et al. Identification of connective tissue gene transcripts in freshly isolated parenchymal, endothelial, Kupffer and fat-storing cells by northern hybridization analysis. J Hepatol 1993;19:148-158.
47. Knittel T, Aurisch S, Neubauer K, et al. Cell-type-specific expression of neural cell adhesion molecule (N-CAM) in Ito cells of rat liver. Up-regulation during in vitro activation and in hepatic tissue repair. Am J Pathol 1996;149:449-462.
48. Friedman SL, Wei S, Blaner WS. Retinol release by activated rat hepatic lipocytes: regulation by Kupffer cell-conditioned medium and PDGF. Am J Physiol 1993;264:G947-G952.
49. Greenwel P, Rubin J, Schwartz M, et al. Liver fat-storing cell clones obtained from a CCl4-cirrhotic rat are heterogeneous with regard to proliferation, expression of extracellular matrix components, interleukin-6, and connexin 43. Lab Invest 1993;69:210-216.
50. Rojkind M, Novikoff PM, Greenwel P, et al. Characterization and functional studies on rat liver fat-storing cell line and freshly isolated hepatocyte coculture system. Am J Pathol 1995;146:1508-1520.
51. Inagaki Y, Truter S, Greenwel P, et al. Regulation of the alpha 2(1) collagen gene transcription in fat-storing cells derived from a cirrhotic liver. Hepatology 1995;22:573-579.
52. Friedman SL. Hepatic stellate cells. Prog Liver Dis 1996;14:101-130.
53. Taipale J, Chen JK, Cooper MK, et al. Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 2000;406:1005-1009.
54. Weaver M, Batts L, Hogan BL. Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Dev Biol 2003;258:169-184.
55. Linsenmayer TF, Hendrix MJ, Little CD. Production and characterization of a monoclonal antibody to chicken type I collagen. Proc Natl Acad Sci USA 1979;76:3703-3707.
56. Koyama E, Leatherman JL, Noji S, et al. Early chick limb cartilaginous elements possess polarizing activity and express hedgehog-related morphogenetic factors. Dev Dyn 1996;207:344-354.
57. Hooper JE, Scott MP. Communicating with hedgehogs. Nat Rev Mol Cell Biol 2005;6:306-317.
58. Tas S, Avci O. Rapid clearance of psoriatic skin lesions induced by topical cyclopamine. A preliminary proof of concept study. Dermatology 2004;209:126-131.
59. Xie J, Murone M, Luoh SM, et al. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 1998;391:90-92.
60. Karhadkar SS, Bova GS, Abdallah N, et al. Hedgehog signalling in prostate regeneration, neoplasia and metastasis. Nature 2004;431:707-712.
61. Shackel NA, McGuinness PH, Abbott CA, et al. Identification of novel molecules and pathogenic pathways in primary biliary cirrhosis: cDNA array analysis of intrahepatic differential gene expression. Gut 2001;49:565-576.
62. Shackel NA, McGuinness PH, Abbott CA, et al. Insights into the pathobiology of hepatitis C virus-associated cirrhosis: analysis of intrahepatic differential gene expression. Am J Pathol 2002;160:641-654.
63. Shackel NA, McGuinness PH, Abbott CA, et al. Novel differential gene expression in human cirrhosis detected by suppression subtractive hybridization. Hepatology 2003;38:577-588.
64. Koch CA, Chrousos GP, Chandra R, et al. Two-hit model for tumorigenesis of nevoid basal cell carcinoma (Gorlin) syndrome-associated hepatic mesenchymal tumor. Am J Med Genet 2002;109:74-76.
65. Sicklick JK, Jayaraman A, Kannangai R, et al. Hedgehog signaling correlates with hepatocellular carcinoma progression. J Clin Oncol 2005;23:9610 (abstract 30554).
66. Zhu J, Wu J, Frizell E, et al. Rapamycin inhibits hepatic stellate cell proliferation in vitro and limits fibrogenesis in an in vivo model of liver fibrosis. Gastroenterology 1999;117:1198-1204.
67. Shegogue D, Trojanowska M. Mammalian target of rapamycin positively regulates collagen type I production via a phosphatidylinositol 3-kinase-independent pathway. J Biol Chem 2004;279:23166-23175.
68. Louro ID, McKie-Bell P, Gosnell H, et al. The zinc finger protein GLI induces cellular sensitivity to the mTOR inhibitor rapamycin. Cell Growth Differ 1999;10:503-516.
69. Kim A, DiCarlo J, Cohen C, et al. Are keloids really 'gli-loids'?: high-level expression of gli-1 oncogene in keloids. J Am Acad Dermatol 2001;45:707-711.
70. Rombouts K, Kisanga E, Hellemans K, et al. Effect of HMG-CoA reductase inhibitors on proliferation and protein synthesis by rat hepatic stellate cells. J Hepatol 2003;38:564-572.
71. Porter JA, Young KE, Beachy PA. Cholesterol modification of hedgehog signaling proteins in animal development. Science 1996;274:255-259.
72. Balabaud C, Bioulac-Sage P, Desmouliere A. The role of hepatic stellate cells in liver regeneration. J Hepatol 2004;40:1023-1026.