Hepatocarcinogenesis following pancreatic islet transplantation in streptozotocin- and autoimmune-diabetic rats

Archives of Physiology and Biochemistry

Volumn 115, Issue 2, 2009, Pages 97-104

  Calvisi, Diego Francesco ^a   Evert, Matthias ^a   Dombrowski, Frank ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Foci of altered hepatocytes; Hepatocellular carcinoma; Hyperglycaemia; Insulin; Insulin like growth factors; Islet transplantation

Indexed keywords

ANIMALIA; RATTUS;

STREPTOZOCIN;

ANIMAL; ANIMAL MODEL; EXPERIMENTAL DIABETES MELLITUS; IMMUNOLOGY; INSULIN DEPENDENT DIABETES MELLITUS; LIVER TUMOR; METHODOLOGY; PANCREAS ISLET TRANSPLANTATION; PATHOLOGY; PRECANCER; RAT; REVIEW;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; ISLETS OF LANGERHANS TRANSPLANTATION; LIVER NEOPLASMS, EXPERIMENTAL; MODELS, ANIMAL; PRECANCEROUS CONDITIONS; RATS; STREPTOZOCIN;

EID: 68149126530     PISSN: 13813455     EISSN: 17444160     Source Type: Journal    
DOI: 10.1080/13813450902870457     Document Type: Review

References (71)

1. Adami HO, Chow WH, Nyren O, Berne C, Linet MS, Ekbom A, Wolk A, McLaughlin JK, Fraumeni, JF. 1996. Excess risk of primary liver cancer in patients with diabetes mellitus. J Natl Cancer Inst 88:1472-1477
2. Adams LA, Lymp JF, St Sauver J, Sanderson SO, Lindor KD, Feldstein A, Angulo, P. 2005. The natural history of nonalcoholic fatty liver disease: a population-based cohort study. Gastroenterology 129:113-121
3. Adinolfi LE, Gambardella M, Andreana A, Tripodi MF, Utili R, Ruggiero, G. 2001. Steatosis accelerates the progression of liver damage of chronic hepatitis C patients and correlates with specific HCV genotype and visceral obesity. Hepatology 33:1358-1364
4. Baghdiguian S, Verrier B, Gerard C, Fantini, J. 1992. Insulin like growth factor I is an autocrine regulator of human colon cancer cell differentiation and growth. Cancer Lett 62:23-33.
5. Bannasch P, Zerban, H. 1990. Pathology of tumours in laboratory animals. Tumours of the rat. Tumours of the liver. IARC Sci Publ 99:199-240.
6. Bell RH, Hye WJ Jr, Miyai, K. 1984. Streptozotocin-induced liver tumors in the Syrian hamster. Carcinogenesis 5:1235-1238
7. Boissan M, Beurel E, Wendum D, Rey C, Lécluse Y, Housset C, Lacombe ML, Desbois-Mouthon, C. 2005. Overexpression of insulin receptor substrate-2 in human and murine hepatocellular carcinoma. Am J Pathol 167:869-877
8. Bretzel RG, Hering BJ, Federlin, KF. 1995. Islet cell transplantation in diabetes mellitus - from bench to bedside. Exp Clin Endocrinol Diabetes 103 Suppl 2:143-159
9. Breuhahn K, Schirmacher, P. 2008. Reactivation of the insulinlike growth factor-II signaling pathway in human hepatocellular carcinoma. World J Gastroenterol 14:1690-1698
10. Bruix J, Boix L, Sala M, Llovet, JM. 2004. Focus on hepatocellular carcinoma. Cancer Cell 5:215-219
11. Bucher ML, Swaffield, MN. 1975. Regulation of hepatic regeneration in rats by synergistic action of insulin and glucagon. Proc Natl Acad Sci USA 72:1157-1160
12. Bugianesi E, Leone N, Vanni E, Marchesini G, Brunello F, Carucci P, Musso A, De Paolis P, Capussotti L, Salizzoni M, et al. 2002. Expanding the natural history of nonalcoholicsteatohepatitis: from cryptogenic cirrhosis to hepatocellular carcinoma. Gastroenterology 123:134-140
13. Calvisi DF, Ladu S, Gorden A, Farina M, Conner EA, Lee JS, Factor VM, Thorgeirsson, SS. 2006. Ubiquitous activation of Ras and Jak/Stat pathways in human HCC. Gastroenterology 130:1117-1128
14. Calvisi DF, Pascale RM, Feo, F. 2007. Dissection of signal transduction pathways as a tool for the development of targeted therapies of hepatocellular carcinoma. Rev Recent Clin Trials 2:217-236
15. Cavin LG, Wang F, Factor VM, Kaur S, Venkatraman M, Thorgeirsson SS, Arsura M. 2005. Transforming growth factor-alpha inhibits the intrinsic pathway of c-Myc- induced apoptosis through activation of nuclear factorkappaB in murine hepatocellular carcinomas. Mol Cancer Res 3:403-412
16. Cariani E, Lasserre C, Seurin D, Hamelin B, Kemeny F, Franco D, Czech MP, Ullrich A, Brechot, C. 1988. Differential expression of insulin-like growth factor II mRNA in human primary liver cancers, benign liver tumors, and liver cirrhosis. Cancer Res 48:6844-6849
17. Chan JM, Stampfer MJ, Giovannucci E, Gann PH, Ma J, Wilkinson P, Hennekens CH, Pollak, M. 1998. Plasma insulin- like growth factor-I and prostate cancer risk: a prospective study. Science 279: 563-566
18. Christofori G, Naik P, Hanahan, D. 1994. A second signal supplied by insulin-like growth factor II in oncogene-induced tumorigenesis. Nature 369:414-418
19. Cotrim HP, Parana R, Braga E, Lyra, L. 2000. Nonalcoholic steatohepatitis and hepatocellular carcinoma: natural history? Am J Gastroenterol 5:3018-3019
20. Dombrowski F, Lehringer-Polzin M, Pfeifer, U. 1994. Hyperproliferative liver acini after intraportal islet transplantation in streptozotocin-induced diabetic rats. Lab Invest 71:688-699
21. Dombrowski F, Pfeifer, U. 1995. Hyperproliferative state of liver acini and pancreatic islets after intraportal transplantation of a small mass of islets of Langerhans in streptozotocin-induced diabetic rats. Exp Clin Endocrinol Diabetes 103 Suppl 2:112-117
22. Dombrowski F, Filsinger E, Bannasch P, Pfeifer, U. 1996. Altered liver acini induced in diabetic rats by portal vein islet isografts resemble preneoplastic hepatic foci in their enzymic pattern. Am J Pathol 148:1249-1256
23. Dombrowski F, Bannasch P, Pfeifer, U. 1997. Hepatocellular neoplasms induced by low-number pancreatic islet transplants in streptozotocin diabetic rats. Am J Pathol 150:1071-1087
24. Dombrowski F, Jost CM, Manekeller S, Evert, M. 2005. Cocarcinogenic effects of islet hormones and N-nitrosomorpholine in hepatocarcinogenesis after intrahepatic transplantation of pancreatic islets in streptozotocin- diabetic rats. Cancer Res 65:7013-7022
25. Dombrowski F, Mathieu C, Evert, M. 2006. Hepatocellular neoplasms induced by low-number pancreatic islet transplants in autoimmune diabetic BB/Pfd rats. Cancer Res 66:1833-1843
26. Dong ZZ, Yao DF, Yao DB, Wu XH, Wu W, Qiu LW, Jiang DR, Zhu JH, Meng, XY. 2005. Expression and alteration of insulin- like growth factor II-messenger RNA in hepatoma tissues and peripheral blood of patients with hepatocellular carcinoma. World J Gastroenterol 11: 4655-4660
27. El Serag HB, Tran T, Everhart, JE. 2004. Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma. Gastroenterology 126:460-468
28. El-Serag HB, Hampel H, Javadi, F. 2006. The association between diabetes and hepatocellular carcinoma: a systematic review of epidemiologic evidence. Clin Gastroenterol Hepatol 4:369-380
29. El-Serag HB, Rudolph, KL. 2007. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132:2557-2576
30. Evert M, Schneider-Stock R, Dombrowski, F. 2003. Apolipoprotein A-IV mRNA overexpression in early preneoplastic hepatic foci induced by low-number pancreatic islet transplants in streptozotocin-diabetic rats. Pathol Res Pract 199:373-379
31. Evert M, Sun J, Pichler S, Slavova N, Schneider-Stock R, Dombrowski, F. 2004. Insulin receptor, insulin receptor substrate-1, Raf-1, and Mek-1 during hormonal hepatocarcinogenesis by intrahepatic pancreatic islet transplantation in diabetic rats. Cancer Res 64:8093-8100
32. Evert M, Schneider-Stock R, Dombrowski F. 2005. Overexpression of fatty acid synthase in chemically in hormonally induced hepatocarcinogenesis of the rat. Lab Invest 85:99-108.
33. Farazi PA, DePinho, RA. 2006. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat Rev Cancer 6:674-687
34. Favoni RE, de Cupis A, Ravera F, Cantoni C, Pirani P, Ardizzoni A, Noonan D, Biassoni, R. 1994. Expression and function of the insulin-like growth factor I system in human non-smallcell lung cancer and normal lung cell lines. Int J Cancer 56:858-866 (Pubitemid 24102754)
35. Fiore G, Fera G, Napoli N, Vella F, Schiraldi, O. 1996. Liver steatosis and chronic hepatitis C: a spurious association? Eur J Gastroenterol Hepatol 8:125-129
36. Gong Y, Cui L, Minuk, GY. 2000. The expression of insulin-like growth factor binding proteins in human hepatocellular carcinoma. Mol Cell Biochem 207:101-104
37. Griffith RC, Scharp DW, Hartman BK, Ballinger WF, Lacy, PE. 1977. A morphologic study of intrahepatic portal-vein islet isografts. Diabetes 26:201-214
38. Hessner MJ, Wang X, Meyer L, Geoffrey R, Jia S, Fuller J, Lernmark A, Ghosh, S. 2004. Involvement of Eotaxin, eosinophils, and pancreatic predisposition in development of type 1 diabetes mellitus in the biobreeding rat. J Immunol 173:6992-7002.
39. Huynh H, Chow PK, Ooi LL, Soo, KC. 2002. A possible role for insulin-like growth factor-binding protein-3 autocrine/ paracrine loops in controlling hepatocellular carcinoma cell proliferation. Cell Growth Differ 13: 115-122
40. Kamei T, Callery MP, Ricordi C, Lacy PE, Flye, MW. 1989. Reduction of liver atrophy by intraportal syngeneic pancreatic islet transplantation before portacaval shunt. Transplantation 48:870-872
41. Kemp CB, Knight MJ, Scharp DW, Ballinger WF, Lacy, PE. 1973. Effect of transplantation site on the results of pancreatic islet isografts in diabetic rats. Diabetologia 9:486-491
42. Lambert S, Collette J, Gillis J, Franchimont P, Desaive C, Gol- Winkler, R. 1991. Tumor IGF-II content in a patient with a colon adenocarcinoma correlates with abnormal expression of the gene. Int J Cancer 48:826-830
43. Li X, Cui H, Sandstedt B, Nordlinder H, Larsson E, Ekstrom, TJ. 1996. Expression levels of the insulin-like growth factor-II gene (IGF2) in the human liver: developmental relationships of the four promoters. J Endocrinol 149:117-124 (Pubitemid 26132836)
44. Li X, Nong Z, Ekstrom C, Larsson E, Nordlinder H, Hofmann WJ, Trautwein C, Odenthal M, Dienes HP, Ekstrom TJ, et al. 1997. Disrupted IGF2 promoter control by silencing of promoter P1 in human hepatocellular carcinoma. Cancer Res 57:2048-2054
45. Llovet JM, Burroughs A, Bruix, J. 2003. Hepatocellular carcinoma. Lancet 362:1907-1917
46. Lund P, Schubert D, Niketeghad F, Schirmacher, P. 2004. Autocrine inhibition of chemotherapy response in human liver tumor cells by insulin-like growth factor-II. Cancer Lett 206: 85-89
47. Malaisse WJ, Courtois P, Scott, FW. 2004. Insulin-dependent diabetes and gut dysfunction: The BB rat model. Horm Metab Res 36:585-594
48. Marrero JA, Fontana RJ, Su GL, Conjeevaram HS, Emick DM, Lok, AS. 2002. NAFLD may be a common underlying liver disease in patients with hepatocellular carcinoma in the United States, Hepatology 36:1349-1354
49. Martin DC, Fowlkes JL, Babic B, Khokha, R. 1999. Insulin-like growth factor II signaling in neoplastic proliferation is blocked by transgenic expression of the metalloproteinase inhibitor TIMP-1. J Cell Biol 146:881-892
50. Mathieu C, Kuttler B, Waer M, Bouillon R, Hahn, HJ. 1994. Spontaneous reestablishment of self-tolerance in BB/Pfd rats. Transplantation 58:349-354
51. Nakafusa Y, Goss JA, Roland CR, Lacy PE, Flye, MW. 1992. Beneficial effect of intraportal syngeneic pancreatic islet transplantation after portacaval shunt in rats. Transplant Proc 24:2916.
52. Nussbaum T, Samarin J, Ehemann V, Bissinger M, Ryschich E, Khamidjanov A, Yu X, Gretz N, Schirmacher P, Breuhahn K. 2008. Autocrine insulin-like growth factor-II stimulation of tumor cell migration is a progression step in human hepatocarcinogenesis. Hepatology 48:146-156
53. Oka Y, Rozek LM, Czech MP. 1985. Direct demonstration of rapid insulin-like growth factor II Receptor internalization and recycling in rat adipocytes. Insulin stimulates 125I-insulinlike growth factor II degradation by modulating the IGF-II receptor recycling process. J Biol Chem 260: 9435-9442
54. Pfeifer U. 1978. Inhibition by insulin of the formation of autophagic vacuoles in rat liver. A morphometric approach to the kinetics of intracellular degradation by autophagy. J Cell Biol 78:152-167
55. Pipeleers-Marichal MA, Pipeleers DG, Cutler J, Lacy PE, Kipnis, DM. 1976. Metabolic and morphologic studies in intraportal- islet-transplanted rats. Diabetes 25:1041-1051
56. Ratziu V, Giral P, Charlotte F, Bruckert E, Thibault V, Theodorou I, Khalil L, Turpin G, Opolon P, Poynard, T. 2000. Liver fibrosis in overweight patients. Gastroenterology 118:1117-1123
57. Reed GB, Grisham, JW. 1975. Insulin and hydrocortisone effects on viability and glycogen stores of postnatal rat liver organ culture. Lab Invest 33:298-304.
58. Reeve AE, Eccles MR, Wilkins RJ, Bell GI, Millow, LJ. 1985. Expression of insulin-like growth factor-II transcripts in Wilms' tumour. Nature 317:258-260
59. Regimbeau JM, Colombat M, Mognol P, Durand F, Abdalla E, Degott C, Degos F, Farges O, Belghiti, J. 2004. Obesity and diabetes as a risk factor for hepatocellular carcinoma. Liver Transpl 10:S69-73.
60. Robertson, RP. 2004. Islet transplantation as a treatment for diabetes - a work in progress. N Engl J Med 350:694-705.
61. Santoni-Rugiu E, Jensen MR, Thorgeirsson, SS. 1998. Disruption of the pRb/E2F pathway and inhibition of apoptosis are major oncogenic events in liver constitutively expressing c-myc and transforming growth factor alpha. Cancer Res 58:123-134
62. Scharf JG, Ramadori G, Dombrowski, F. 2000. Analysis of the IGF axis in preneoplastic hepatic foci and hepatocellular neoplasms developing after low-number pancreatic islet transplantation into the livers of streptozotocin diabetic rats. Lab Invest 80:1399-1411
63. Starzl TE, Watanabe K, Porter KA, Putnam CW. 1976. Effects of insulin, glucagon, and insuling/glucagon infusions on liver morphology and cell division after complete portacaval shunt in dogs. Lancet 1:821-825
64. Sutherland DE, Gores PF, Hering BJ, Wahoff D, McKeehen DA, Gruessner, RW. 1996. Islet transplantation: an update. Diabetes Metab Rev 12:137-150
65. Tang SH, Yang DH, Huang W, Zhou HK, Lu XH, Ye, G. 2006. Hypomethylated P4 promoter induces expression of the insulin-like growth factor-II gene in hepatocellular carcinoma in a Chinese population. Clin Cancer Res 12:4171-4177
66. Thorgeirsson SS, Grisham, JW. 2002. Molecular pathogenesis of human hepatocellular carcinoma. Nat Genet 31:339-346
67. Toropainen E, Lipponen P, Syrjanen, K. 1995. Expression of insulin-like growth factor I (IGF-I) in female breast cancer as related to established prognostic factors and long-term prognosis. Eur J Cancer 31A:1443-1448
68. Vu TH, Hoffman, AR. 1994. Promoter-specific imprinting of the human insulin-like growth factor-II gene. Nature 371:714-717
69. Westin J, Nordlinder H, Lagging M, Norkrans G, Wejstal, R. 2002. Steatosis accelerates fibrosis development over time in hepatitis C virus genotype 3 infected patients. J Hepatol 37:837-842
70. Wideroff L, Gridley G, Mellemkjaer L, Chow WH, Linet M, Keehn S, Borch-Johnsen K, Olsen JH. 1997. Cancer incidence in a population-based cohort of patients hospitalized with diabetes mellitus in Denmark. J Natl Cancer Inst 89:1360-1365
71. Zen Y, Katayanagi K, Tsuneyama K, Harada K, Araki I, Nakanuma, Y. 2001. Hepatocellular carcinoma arising in non-alcoholic steatohepatitis. Pathol Int 51:127-131