Inflammatory disease and cancer with a decrease in Kupffer cell numbers in Nucling-knockout mice

International Journal of Cancer

Volumn 126, Issue 5, 2010, Pages 1079-1094

  Sakai, Takashi ^a   Liu, Li ^a,b   Teng, Xichuan ^a,c   Ishimaru, Naozumi ^a   Mukai Sakai, Rika ^a   Tran, Nam Hoang ^a   Kim, Sun Mi ^a   Sano, Nobuya ^a,d   Hayashi, Yoshio ^a   Kaji, Ryuji ^a   Fukui, Kiyoshi ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c EASTERN LIAONING UNIVERSITY   (China)

^d Akashi Medical Center   (Japan)

Author keywords

Apoptosis; Hepatocellular carcinoma; Inflammation; Kupffer cell; NF B; Nucling; Tumorigenesis

Indexed keywords

GALECTIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NUCLING; PROTEIN DERIVATIVE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; CELL COUNT; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HEPATITIS; HYPERCHOLESTEROLEMIA; IMMUNE SYSTEM; KNOCKOUT MOUSE; KUPFFER CELL; LIVER; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER DYSFUNCTION; MALE; MOUSE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; WILD TYPE;

ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CARBON TETRACHLORIDE; CARCINOGENS; CARCINOMA, HEPATOCELLULAR; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLOW CYTOMETRY; HEPATITIS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; KUPFFER CELLS; LIVER NEOPLASMS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; NF-KAPPA B; PRECANCEROUS CONDITIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 74049095937     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.24789     Document Type: Article

References (72)

1. Sakai T, Liu L, Teng X, Mukai-Sakai R, Shimada H, Kaji R, Mitani T, Matsumoto M, Toida K, Ishimura K, Shishido Y, Mak TW, et al. Nucling recruits Apaf-1/pro-caspase-9 complex for the induction of stress-induced apoptosis. J Biol Chem2004;279:41131-40.
2. Liu L, Sakai T, Sano N, Fukui K. Nucling mediates apoptosis by inhibiting expression of galectin-3 through interference with nuclear factor kappaB signalling. Biochem J 2004;380:31-41.
3. Barondes SH, Cooper DN, Gitt MA, Lef.er H. Galectins. Structure and function of a large family of animal lectins. J Biol Chem 1994;269:20807-10.
4. Kasai K, Hirabayashi J. Galectins: a family of animal lectins that decipher glycocodes. J Biochem 1996;119:1-8.
5. Liu FT. Molecular biology of IgE-binding protein, IgE-binding factors, and IgE receptors. Crit Rev Immunol 1990;10:289-306.
6. van den Brule FA, Waltregny D, Liu FT, Castronovo V. Alteration of the cytoplasmic/nuclear expression pattern of galectin-3 correlates with prostate carcinoma progression. Int J Cancer 2000;89:361-7.
7. Yu F, Finley RL, Jr, Raz A, Kim HR. Galectin-3 translocates to the perinuclear membranes and inhibits cytochrome c release from the mitochondria. A role for synexin in galectin-3 translocation. J Biol Chem 2002;277:15819-27.
8. Yang RY, Hsu DK, Liu FT. Expression of galectin-3 modulates T-cell growth and apoptosis. Proc Natl Acad Sci U S A 1996;93:6737-42.
9. Liu L, Sakai T, Tran NH, Mukai-Sakai R, Kaji R, Fukui K. Nucling interacts with nuclear factor-kappaB, regulating its cellular distribution. FEBS J 2009;276:1459-70.
10. Hsu DK, Dowling CA, Jeng KC, Chen JT, Yang RY, Liu FT. Galectin-3 expression is induced in cirrhotic liver and hepatocellular carcinoma. Int J Cancer 1999;81:519-26.
11. Matsuda Y, Yamagiwa Y, Fukushima K, Ueno Y, Shimosegawa T. Expression of galectin-3 involved in prognosis of patients with hepatocellular carcinoma. Hepatol Res 2008;38:1098-111.
12. Peng W, Wang HY, Miyahara Y, Peng G, Wang RF. Tumor-associated galectin-3 modulates the function of tumor-reactive T cells. Cancer Res 2008;68:7228-36.
13. Zubieta MR, Furman D, Barrio M, Bravo AI, Domenichini E, Mordoh J. Galectin-3 expression correlates with apoptosis of tumor-associated lymphocytes in human melanoma biopsies. Am J Pathol 2006;168:1666-75.
14. Seki E, Brenner DA. The role of NFkappaB in hepatocarcinogenesis: promoter or suppressor? J Hepatol 2007;47:307-9.
15. Heuff G, van de Loosdrecht AA, Betjes MG, Beelen RH, Meijer S. Isolation and purification of large quantities of fresh human Kupffer cells, which are cytotoxic against colon carcinoma. Hepatology 1995;21:740-5.
16. Roh MS, Wang L, Oyedeji C, LeRoux ME, Curley SA, Pollock RE, Klostergaard J. Human Kupffer cells are cytotoxic against human colon adenocarcinoma. Surgery 1990;108:400-4; discussion 4-5.
17. Curley SA, Roh MS, Feig B, Oyedeji C, Kleinerman ES, Klostergaard J. Mechanisms of Kupffer cell cytotoxicity in vitro against the syngeneic murine colon adenocarcinoma line MCA26. J Leukoc Biol 1993;53:715-21.
18. Heuff G, Oldenburg HS, Boutkan H, Visser JJ, Beelen RH, Van Rooijen N, Dijkstra CD, Meyer S. Enhanced tumour growth in the rat liver after selective elimination of Kupffer cells. Cancer Immunol Immunother 1993;37:125-30.
19. Aono K, Isobe K, Nakashima I, Kondo S, Miyachi M, Nimura Y. Kupffer cells cytotoxicity against hepatoma cells is related to nitric oxide. Biochem Biophys Res Commun 1994;201:1175-81.
20. Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, Karin M. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 2007;317:121-4.
21. Sander LE, Trautwein C, Liedtke C. Is interleukin-6 a gender-specific risk factor for liver cancer? Hepatology 2007;46:1304-5.
22. Ramaiah SK, Rittling S. Pathophysiological role of osteopontin in hepatic inflammation, toxicity and cancer. Toxicol Sci 2007.
23. Ashare A, Monick MM, Nymon AB, Morrison JM, Noble M, Powers LS, Yarovinsky TO, Yahr TL, Hunninghake GW. Pseudomonas aeruginosa delays Kupffer cell death via stabilization of the X-chromosome-linked inhibitor of apoptosis protein. J Immunol 2007;179:505-13.
24. Peng Y, Gallagher SF, Haines K, Baksh K, Murr MM. Nuclear factor-kappaB mediates Kupffer cell apoptosis through transcriptional activation of Fas/FasL. J Surg Res 2006;130:58-65.
25. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, Kagnoff MF, Karin M. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004;118:285-96.
26. Maeda S, Kamata H, Luo JL, Leffert H, Karin M. IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 2005;121:977-90.
27. Pikarsky E, Porat RM, Stein I, Abramovitch R, Amit S, Kasem S, Gutkovich-Pyest E, Urieli-Shoval S, Galun E, Ben-Neriah Y. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 2004;431:461-6.
28. Laboratory TJ. Jax Bulletin No. 4 2000; http://jaxmice.jax.org/html/ nomenclature/hybrid.pdf.
29. Sakai T, Furukawa T, Iwanari H, Oka C, Nakano T, Kawaichi M, Honjo T. Loss of immunostaining of the RBP-J kappa transcription factor upon F9 cell differentiation induced by retinoic acid. J Biochem 1995;118:621-8.
30. Block TM, Mehta AS, Fimmel CJ, Jordan R. Molecular viral oncology of hepatocellular carcinoma. Oncogene 2003;22:5093-107.
31. Frith CH, Ward JM. A morphologic classification of proliferative and neoplastic hepatic lesions in mice. J Environ Pathol Toxicol 1979;3:329-51.
32. Andres D, Sanchez-Reus I, Bautista M, Cascales M. Depletion of Kupffer cell function by gadolinium chloride attenuates thioacetamide-induced hepatotoxicity. Expression of metallothionein and HSP70. Biochem Pharmacol 2003;66:917-26.
33. Edwards MJ, Keller BJ, Kauffman FC, Thurman RG. The involvement of Kupffer cells in carbon tetrachloride toxicity. Toxicol Appl Pharmacol 1993;119:275-9.
34. Muriel P, Escobar Y. Kupffer cells are responsible for liver cirrhosis induced by carbon tetrachloride. J Appl Toxicol 2003;23:103-8.
35. Rivera CA, Bradford BU, Hunt KJ, Adachi Y, Schrum LW, Koop DR, Burchardt ER, Rippe RA, Thurman RG. Attenuation of CCl(4)-induced hepatic fibrosis by GdCl(3) treatment or dietary glycine. Am J Physiol Gastrointest Liver Physiol 2001;281:G200-7.
36. Titos E, Claria J, Planaguma A, Lopez-Parra M, Gonzalez-Periz A, Gaya J, Miquel R, Arroyo V, Rodes J. Inhibition of 5-lipoxygenase-activating protein abrogates experimental liver injury: role of Kupffer cells. J Leukoc Biol 2005;78:871-8.
37. Chen F, Castranova V. Nuclear factorkappaB, an unappreciated tumor suppressor. Cancer Res 2007;67:11093-8.
38. Xu L, Zhu J, Hu X, Zhu H, Kim HT, LaBaer J, Goldberg A, Yuan J. c-IAP1 cooperates with Myc by acting as a ubiquitin ligase for Mad1. Mol Cell 2007;28:914-22.
39. Ulleras E, Karlberg M, Moller Westerberg C, Alfredsson J, Gerondakis S, Strasser A, Nilsson G. NFAT but not NF-kappaB is critical for transcriptional induction of the prosurvival gene A1 after IgE receptor activation in mast cells. Blood 2008;111:3081-9.
40. Papa S, Zazzeroni F, Bubici C, Jayawardena S, Alvarez K, Matsuda S, Nguyen DU, Pham CG, Nelsbach AH, Melis T, De Smaele E, Tang WJ, et al. Gadd45 beta mediates the NF-kappa B suppression of JNK signalling by targeting MKK7/JNKK2. Nat Cell Biol 2004;6:146-53.
41. Takei Y, Kawano S, Nishimura Y, Goto M, Nagai H, Chen SS, Omae A, Fusamoto H, Kamada T, Ikeda K, Kawada N, Kaneda K. Apoptosis: A new mechanism of endothelial and Kupffer cell killing. J Gastroenterology and Hepatology 2008;10:S65-S7.
42. Ding WX, Yin XM. Dissection of the multiple mechanisms of TNF-alpha-induced apoptosis in liver injury. J Cell Mol Med 2004;8:445-54.
43. Wajant H, Pfizenmaier K, Scheurich P. Tumor necrosis factor signaling. Cell Death Differ 2003;10:45-65.
44. Flanagan DL, Jennings CD, Bryson JS. Th1 cytokines and NK cells participate in the development of murine syngeneic graft-versus-host disease. J Immunol 1999;163:1170-7.
45. Flotte TJ, Springer TA, Thorbecke GJ. Dendritic cell and macrophage staining by monoclonal antibodies in tissue sections and epidermal sheets. Am J Pathol 1983;111:112-24.
46. Kim H, Lee J, Hyun JW, Park JW, Joo HG, Shin T. Expression and immunohistochemical localization of galectin-3 in various mouse tissues. Cell Biol Int 2007;31:655-62.
47. Chung EJ, Sung YK, Farooq M, Kim Y, Im S, Tak WY, Hwang YJ, Kim YI, Han HS, Kim JC, Kim MK. Gene expression profile analysis in human hepatocellular carcinoma by cDNA microarray. Mol Cells 2002;14:382-7.
48. Haines DC, Chattopadhyay S, Ward JM. Pathology of aging B6;129 mice. Toxicol Pathol 2001;29:653-61.
49. Ward J, Anver M, Mahler J, Devor-Henneman D. Pathology of mice commonly used in genetic engineering (C57BL/6, 129, B6,129 and FVB/N). In: Ward J, Mahler J, Maronpot R, Sundberg J, eds. Pathology of genetically engineered mice ames. Iowa: Iowa State University Press, 2000. 161-79.
50. Tarone RE, Chu KC, Ward JM. Variability in the rates of some common naturally occurring tumors in Fischer 344 rats and (C57BL/6N x C3H/HeN)F1 (B6C3F1) mice. J Natl Cancer Inst 1981;66:1175-81.
51. Giannitrapani L, Soresi M, La Spada E, Cervello M, D' Alessandro N, Montalto G. Sex hormones and risk of liver tumor. Ann NY Acad Sci 2006;1089:228-36.
52. Dumic J, Lauc G, Flogel M. Expression of galectin-3 in cells exposed to stress-roles of jun and NF-kappaB. Cell Physiol Biochem 2000;10:149-58.
53. Zhu W, Sano H, Nagai R, Fukuhara K, Miyazaki A, Horiuchi S. The role of galectin-3 in endocytosis of advanced glycation end products and modified low density lipoproteins. Biochem Biophys Res Commun 2001;280:1183-8.
54. Mocellin S, Rossi CR, Pilati P, Nitti D. Tumor necrosis factor, cancer and anticancer therapy. Cytokine Growth Factor Rev 2005;16:35-53.
55. Szlosarek PW, Grimshaw MJ, Kulbe H, Wilson JL, Wilbanks GD, Burke F, Balkwill FR. Expression and regulation of tumor necrosis factor alpha in normal and malignant ovarian epithelium. Mol Cancer Ther 2006;5:382-90.
56. Morsi MI, Hussein AE, Mostafa M, El-Abd E, El-Moneim NA. Evaluation of tumour necrosis factor-alpha, soluble P-selectin, gamma-glutamyl transferase, glutathione S-transferase-pi and alpha-fetoprotein in patients with hepatocellular carcinoma before and during chemotherapy. Br J Biomed Sci 2006;63:74-8.
57. Wang YY, Lo GH, Lai KH, Cheng JS, Lin CK, Hsu PI. Increased serum concentrations of tumor necrosis factor-alpha are associated with disease progression and malnutrition in hepatocellular carcinoma. J Chin Med Assoc 2003;66:593-8.
58. Jeng JE, Tsai JF, Chuang LY, Ho MS, Lin ZY, Hsieh MY, Chen SC, Chuang WL, Wang LY, Yu ML, Dai CY, Chang JG. Tumor necrosis factor-alpha 308.2 polymorphism is associated with advanced hepatic fibrosis and higher risk for hepatocellular carcinoma. Neoplasia 2007;9:987-92.
59. Kroeger KM, Carville KS, Abraham LJ. The -308 tumor necrosis factor-alpha promoter polymorphism effects transcription. Mol Immunol 1997;34:391-9.
60. Wilson AG, di Giovine FS, Blakemore AI, Duff GW. Single base polymorphism in the human tumour necrosis factor alpha (TNF alpha) gene detectable by NcoI restriction of PCR product. Hum Mol Genet 1992;1:353.
61. Kitaichi N, Kotake S, Morohashi T, Onoe K, Ohno S, Taylor AW. Diminution of experimental autoimmune uveoretinitis (EAU) in mice depleted of NK cells. J Leukoc Biol 2002;72:1117-21.
62. Reichlin A, Yokoyama WM. Natural killer cell proliferation induced by anti-NK1.1 and IL-2. Immunol Cell Biol 1998;76:143-52.
63. Kucharczak J, Simmons MJ, Fan Y, Gelinas C. To be, or not to be: NF-kappaB is the answer-role of Rel/NF-kappaB in the regulation of apoptosis. Oncogene 2003;22:8961-82.
64. Kan Z, Ivancev K, Lunderquist A, McCuskey PA, McCuskey RS, Wallace S. In vivo microscopy of hepatic metastases: dynamic observation of tumor cell invasion and interaction with Kupffer cells. Hepatology 1995;21:487-94.
65. Roberts RA, Ganey PE, Ju C, Kamendulis LM, Rusyn I, Klaunig JE. Role of the Kupffer cell in mediating hepatic toxicity and carcinogenesis. Toxicol Sci 2006.
66. de Rijke YB, van Berkel TJ. Rat liver Kupffer and endothelial cells express different binding proteins for modified low density lipoproteins. Kupffer cells express a 95-kDa membrane protein as a specific binding site for oxidized low density lipoproteins. J Biol Chem 1994;269:824-7.
67. Buhman KF, Accad M, Farese RV. Mammalian acyl-CoA:cholesterol acyltransferases. Biochim Biophys Acta 2000;1529:142-54.
68. Chang TY, Chang CC, Cheng D. Acyl-coenzyme A:cholesterol acyltransferase. Annu Rev Biochem 1997;66:613-38.
69. Chang TY, Chang CC, Lin S, Yu C, Li BL, Miyazaki A. Roles of acyl-coenzyme A:cholesterol acyltransferase-1 and -2. Curr Opin Lipidol 2001;12:289-96.
70. Rudel LL, Lee RG, Cockman TL. Acyl coenzyme A:cholesterol acyltransferase types 1 and 2: structure and function in atherosclerosis. Curr Opin Lipidol 2001;12:121-7.
71. Lee RG, Willingham MC, Davis MA, Skinner KA, Rudel LL. Differential expression of ACAT1 and ACAT2 among cells within liver, intestine, kidney, and adrenal of nonhuman primates. J Lipid Res 2000;41:1991-2001.
72. Hoekstra M, Out R, Kruijt JK, Van Eck M, Van Berkel TJ. Diet induced regulation of genes involved in cholesterol metabolism in rat liver parenchymal and Kupffer cells. J Hepatol 2005;42:400-7.