Liver pathology and hepatocarcinogenesis in a long-term mouse model of erythropoietic protoporphyria

Journal of Pathology

Volumn 199, Issue 2, 2003, Pages 191-200

  Libbrecht, Louis ^a   Meerman, Leo ^b   Kuipers, Folkert ^c   Roskams, Tania ^a   Desmet, Valeer ^a   Jansen, Peter ^c  

^a UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^b MEDICAL CENTER LEEUWARDEN   (Netherlands)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Erythropoietic protoporphyria; Ferrochelatase; Hepatocarcinogenesis; Histopathology; Immunohistochemistry; Liver; Mouse model; Protoporphyrin

Indexed keywords

FERROCHELATASE; HEME; PROTOPORPHYRIN;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT OBSTRUCTION; CANCER STAGING; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DYSPLASIA; ERYTHROPOIETIC PROTOPORPHYRIA; FATTY LIVER; FEMALE; HEME SYNTHESIS; HETEROZYGOSITY; HISTOPATHOLOGY; HOMOZYGOSITY; IMMUNOHISTOCHEMISTRY; LIVER CARCINOGENESIS; LIVER CARCINOMA; LIVER CELL DAMAGE; LIVER DISEASE; LIVER FIBROSIS; MALE; MOUSE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; STEM CELL;

ANIMALS; BILE DUCTS; DISEASE MODELS, ANIMAL; FEMALE; FERROCHELATASE; GENES; IMMUNOHISTOCHEMISTRY; LIVER; LIVER CIRRHOSIS; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; ORGAN SIZE; PORPHYRIA, HEPATOERYTHROPOIETIC; PRECANCEROUS CONDITIONS; PROTOPORPHYRINS;

EID: 0037314376     PISSN: 00223417     EISSN: None     Source Type: Journal    
DOI: 10.1002/path.1257     Document Type: Article

References (64)

1. Kappas A, Sassa S, Galbraith RA, Nordmann Y. The porphyrias. In The Metabolic and Molecular Bases of Inherited Disease, Scriver CR, Beaudet AL, Sly WS, Valle E (eds). McGraw Hill: New York, 1995; 2103-2159.
2. Cox TM. Erythropoietic protoporphyria. J Inherit Metab Dis 1997; 20: 258-269.
3. Schneider-Yin X, Gouya L, Meier-Weinand A, Deybach JC, Minder EI. New insights into the pathogenesis of erythropoietic protoporphyria and their impact on patient care. Eur J Pediatr 2000; 159: 719-725.
4. Schneider-Yin X, Gouya L, Dorsey M, Rufenacht U, Deybach JC, Ferreira GC. Mutations in the iron-sulfur cluster ligands of the human ferrochelatase lead to erythropoietic protoporphyria. Blood 2000; 96: 1545-1549.
5. Plosch T, Bloks VW, Baller JFW, et al. Mdr P-glycoproteins are not essential for biliary excretion of the hydrophobic heme precursor protoporphyrin in a griseofulvin-induced mouse model of erythropoietic protoporphyria. Hepatology 2002; 35: 299-306.
6. Todd DJ. Erythropoietic porphyria. Br J Dermatol 1994; 131: 751-766.
7. Bloomer JR. The liver in protoporphyria. Hepatology 1988; 8: 402-407.
8. Meerman L. Erythropoietic protoporphyria. An overview with emphasis on the liver. Scand J Gastroenterol Suppl 2000; 232(Suppl): 79-85.
9. Klatskin G, Bloomer JR. Birefringence of hepatic pigment deposits in erythropoietic protoporphyria. Gastroenterology 1974; 67: 294-302.
10. Bloomer JR, Enriquez R. Evidence that hepatic crystalline deposits in a patient with protoporphyria are composed of protoporphyrin. Gastroenterology 1982; 82: 569-572.
11. Meerman L, Koopen NR, Bloks V, et al. Biliary fibrosis associated with altered bile composition in a mouse model of erythropoietic protoporphyria. Gastroenterology 1999; 117: 696-705.
12. Tutois S, Montagutelli X, Da Silva V, et al. Erythropoietic protoporphyria in the house mouse. A recessive inherited ferrochelatase deficiency with anemia, photosensitivity, and liver disease. J Clin Invest 1991; 88: 1730-1736.
13. Boulechfar S, Lamoril J, Montagutelli X, et al. Ferrochelatase structural mutant (Fechm1Pas) in the house mouse. Genomics 1993; 16: 645-648.
14. Bancroft JD, Cook HC. Manual of Histological Techniques. Churchill Livingstone: Edinburgh, 1984.
15. Clotman F, Lannoy VJ, Reber M, et al. The onecut transcription factor HNF-6 is required for normal development of the biliary tract. Development 2002; 129: 1819-1828.
16. Knodell RG, Ishak KG, Black WC, et al. Formulation and application of a numerical scoring system for assessing histological activity in asymptomatic chronic active hepatitis. Hepatology 1981; 1: 431-435.
17. Nakanuma Y, Hoso M, Sanzen T, Sasaki M. Microstructure and development of the normal and pathologic biliary tract in humans, including blood supply. Microsc Res Tech 1997; 38: 552-570.
18. Sell S. Comparison of liver progenitor cells in human atypical ductular reactions with those seen in experimental models of liver injury. Hepatology 1998; 27: 317-331.
19. Anthony PP, Vogel CL, Barker LF. Liver cell dysplasia: a premalignant condition. J Clin Pathol 1973; 26: 217-223.
20. Watanabe S, Okita K, Harada T, et al. Morphologic studies of the liver cell dysplasia. Cancer 1983; 51: 2197-2205.
21. Altavilla G, Caputo A, Lanfredi M, Piola C, Barbanti-Brodano G, Corallini A. Enhancement of chemical hepatocarcinogenesis by the HIV-1 tat gene. Am J Pathol 2000; 157: 1081-1089.
22. International Working Party. Terminology of nodular hepatocellular lesions. Hepatology 1995; 22: 983-993.
23. Oikawa H, Masuda T, Sato SI, et al. Changes in lymph vessels and portal veins in the portal tract of patients with idiopathic portal hypertension: a morphometric study. Hepatology 1998; 27: 1607-1610.
24. Lee RG, Tsamandas AC, Demetris AJ. Large cell change (liver cell dysplasia) and hepatocellular carcinoma in cirrhosis: matched case-control study, pathological analysis, and pathogenetic hypothesis. Hepatology 1997; 26: 1415-1422.
25. Bruguera M, Esquerda JE, Mascaro JM, Pinol J. Erythropoietic protoporphyria. A light, electron, and polarization microscopical study of the liver in three patients. Arch Pathol Lab Med 1976; 100: 587-589.
26. Wells MM, Golitz LE, Bender BJ. Erythropoietic protoporphyria with hepatic cirrhosis. Arch Dermatol 1980; 116: 429-432.
27. MacDonald DM, Germain D, Perrot H. The histopathology and ultrastructure of liver disease in erythropoietic protoporphyria. Br J Dermatol 1981; 104: 7-17.
28. Thompson RP, Molland EA, Nicholson DC, Gray CH. 'Erythropoietic' protoporphyria and cirrhosis in sisters. Gut 1973; 14: 934-938.
29. Bloomer JR, Phillips MJ, Davidson DL, Klatskin G. Hepatic disease in erythropoietic protoporphyria. Am J Med 1975; 58: 869-882.
30. Singer JA, Plaut AG, Kaplan MM. Hepatic failure and death from erythropoietic protoporphyria. Gastroenterology 1978; 74: 588-591.
31. Komatsu H, Ishii K, Imamura K, et al. A case of erythropoietic protoporphyria with liver cirrhosis suggesting a therapeutic value of supplementation with alpha-tocopherol. Hepatol Res 2000; 18: 298-309.
32. Bloks VW, Plosch T, van Goor H, et al. Hyperlipidemia and atherosclerosis associated with liver disease in ferrochelatase-deficient mice. J Lipid Res 2001; 42: 41-50.
33. Rank JM, Carithers R, Bloomer J. Evidence of neurological dysfunction in end-stage protoporphyric liver disease. Hepatology 1993; 18: 1404-1409.
34. Lock G, Holstege A, Mueller AR, et al. Liver failure in erythropoietic protoporphyria associated with choledocholithiasis and severe post-transplantation polyneuropathy. Liver 1996; 16: 211-217.
35. Williams M, van der Zee J, van Steveninck J. Toxic dark effects of protoporphyrin on the cytochrome P-450 system in rat liver microsomes. Biochem J 1992; 288: 155-159.
36. Koningsberger JC, Van Asbeck BS, Van Hattum J, et al. The effect of porphyrins on cellular redox systems: a study on the dark effect of porphyrins on phagocytes. Eur J Clin Invest 1993; 23: 716-723.
37. Williams M, Krootjes BB, van Steveninck J, van der Zee J. The pro- and antioxidant properties of protoporphyrin IX. Biochim Biophys Acta 1994; 1211: 310-316.
38. Koningsberger JC, Rademakers LH, van Hattum J, et al. Exogenous protoporphyrin inhibits Hep G2 cell proliferation, increases the intracellular hydrogen peroxide concentration and causes ultrastructural alterations. J Hepatol 1995; 22: 57-65.
39. Barnes HD, Hurworth E, Millar JH. Erythropoietic porphyrin hepatitis. J Clin Pathol 1968; 21: 157-159.
40. Scott AJ, Ansford AJ, Webster BH, Stringer HC. Erythropoietic protoporphyria with features of a sideroblastic anaemia terminating in liver failure. Am J Med 1973; 54: 251-259.
41. Denk H, Stumptner C, Zatloukal K. Mallory bodies revisited. J Hepatol 2000; 32: 689-702.
42. Matilla A, Molland EA. A light and electron microscopic study of the liver in case of erythrohepatic protoporphyria and in griseofulvin-induced porphyria in mice. J Clin Pathol 1974; 27: 698-709.
43. Gschnait F, Konrad K, Honigsmann H, Denk H, Wolff K. Mouse model for protoporphyria. I. The liver and hepatic protoporphyrin crystals. J Invest Dermatol 1975; 65: 290-299.
44. Hoosner SB, Beasly VR, Lovell RA, Carmichael WW, Haschek WM. Toxicity of microcystin LR, a cyclic hepatopeptide hepatoxin from microcystic aeruginosa, to rats and mice. Vet Pathol 1989; 26: 246-252.
45. Nakanuma Y, Hoso M, Sasaki M, et al. Histopathology of the liver in non-cirrhotic portal hypertension of unknown aetiology. Histopathology 1996; 28: 195-204.
46. Donaldson EM, McCall AJ, Magnus IA, Simpson JR, Caldwell RA, Hargreaves T. Erythropoietic protoporphyria: two deaths from hepatic cirrhosis. Br J Dermatol 1971; 84: 14-24.
47. Alison M, Sarraf C. Hepatic stem cells. J Hepatol 1998; 29: 676-682.
48. Petersen BE. Hepatic 'stem' cells: coming full circle. Blood Cells Mol Dis 2001; 27: 590-600.
49. Fontanellas A, Mazurier F, Landry M, et al. Reversion of hepatobiliary alterations by bone marrow transplantation in a murine model of erythropoietic protoporphyria. Hepatology 2000; 32: 73-81.
50. Kirimlioglu H, Dvorchick I, Ruppert K, et al. Hepatocellular carcinomas in native livers from patients treated with orthotopic liver transplantation: biologic and therapeutic implications. Hepatology 2001; 34: 502-510.
51. Le Bail B, Bernard PH, Carles J, Balabaud C, Bioulac-Sage P. Prevalence of liver cell dysplasia and association with HCC in a series of 100 cirrhotic liver explants. J Hepatol 1997; 27: 835-842.
52. Marchio A, Terris B, Meddeb M, et al. Chromosomal abnormalities in liver cell dysplasia detected by comparative genomic hybridisation. J Clin Pathol 2001; 54: 270-274.
53. Santoni-Rugiu E, Thorgeirsson SS. Transgenic animals as models for hepatocarcinogenesis. In Liver Growth and Repair, Strain AJ, Diehl AM (eds). Chapman & Hall: London, 1998; 100-142.
54. Libbrecht L, Desmet V, Van Damme B, Roskams T. The immunohistochemical phenotype of dysplastic foci in human liver: correlation with putative progenitor cells. J Hepatol 2000; 33: 76-84.
55. Sell S. Heterogeneity and plasticity of hepatocyte lineage cells. Hepatology 2001; 33: 738-750.
56. Libbrecht L, De Vos R, Cassiman D, Desmet V, Aerts R, Roskams T. Hepatic progenitor cells in hepatocellular adenomas. Am J Surg Pathol 2001; 25: 1388-1396.
57. Terasaki S, Kaneko S, Kobayashi K, Nonomura A, Nakanuma Y. Histological features predicting malignant transformation of nonmalignant hepatocellular nodules: a prospective study. Gastroenterology 1998; 115: 1216-1222.
58. Maggioni M, Coggi G, Cassani B, et al. Molecular changes in hepatocellular dysplastic nodules on microdissected liver biopsies. Hepatology 2000; 32: 942-946.
59. Bjorkhem L, Teclebrhan H, Kesen E, Olsson JM, Eriksson LC, Bjornstedt M. Increased levels of cytosolic thioredoxin reductase activity and mRNA in rat liver nodules. J Hepatol 2001; 35: 259-264.
60. Cochrane CG. Cellular injury by oxidants. Am J Med 1991; 91: 23S-30S.
61. 2-generating peroxisomal urate oxidase. Cancer Res 1996; 56: 4846-4852.
62. Weston-Hurst E, Paget GE. Protoporphyrin, cirrhosis and hepatomata in the livers of mice given griseofulvin. Br J Dermatol 1963; 75: 105-112.
63. Denk H, Gschnait F, Wolff K. Hepatocellar hyalin (Mallory bodies) in long term griseofulvin-treated mice: a new experimental model for the study of hyalin formation. Lab Invest 1975; 32: 773-776.
64. Fracanzani AL, Taioli E, Sampietro M, et al. Liver cancer risk is increased in patients with porphyria cutanea tarda in comparison to matched control patients with chronic liver disease. J Hepatol 2001; 35: 498-503.