Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene

Journal of Clinical Investigation

Volumn 112, Issue 12, 2003, Pages 1809-1820

  Qu, Xueping ^a   Yu, Jie ^a   Bhagat, Govind ^a   Furuya, Norihiko ^a   Hibshoosh, Hanina ^a   Troxel, Andrea ^a   Rosen, Jeffrey ^b   Eskelinen, Eeva Liisa ^c   Mizushima, Noboru ^d,e   Ohsumi, Yoshinori ^d   Cattoretti, Giorgio ^a,f   Levine, Beth ^a,g  

^a Department of Medicine   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF KIEL   (Germany)

^d NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^f Columbia Univ Coll of Phys/Surgs ^*  (United States)

^g New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BECLIN 1 GENE; BREAST CANCER; CARCINOGENESIS; CELL CYCLE; CELL GROWTH; CELL PROLIFERATION; GENE MAPPING; HEPATITIS B VIRUS; LIVER CANCER; LUNG CANCER; LYMPHOMA; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; OVARY CANCER; PATHOGENESIS; PRIORITY JOURNAL; PROSTATE CANCER; TUMOR SUPPRESSOR GENE; VIRUS CARCINOGENESIS;

EID: 9144240441     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI20039     Document Type: Article

References (72)

1. Spataro, V., Norbury, C., and Harris, A.L. 1998. The ubiquitin-proteasome pathway in cancer. Br. J. Cancer. 77:448-455.
2. Elliott, P.J., and Ross, J.S. 2001. The proteasome: a new target For novel drug therapies. Am. J. Clin. Pathol. 116:637-646.
3. Richardson, P. 2003. Clinical update: proreasome inhibitors in hematologic malignancies. Cancer Treat. Rev. 29(Suppl. 1):33-39.
4. Lenz, H.J. 2003. Clinical update: proteasome inhibitors in solid rumors. Cancer Treat. Rev. 29(Suppl. 1):41-48.
5. Bursch, W., et al. 1996. Active cell death induced by the anti-estrogens tamoxifen and ICI 164 34 in human mammary carcinoma cells (MC7-7) in culture: the role of autophagy. Carcinogenesis. 17:1595-1607.
6. Noda, T., and Ohsumi, Y. 1998. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 273:3963-3966.
7. Dunn, W.A.J. 1994. Autophagy and related mechanisms of lysosome-mediated protein degradation. Trends Cell Biol. 4:139-143.
8. Klionsky, D.J., and Emr, S.D. 2000. Autophagy as a regulated pathway of cellular degradation. Science. 290:1717-1721.
9. Klionsky, D.J. 2003. Autophagy Landes Bioscience. Georgetown, Texas, USA. 307 pp.
10. Gunn, J.M., Clark, M.G., Knowles, S.E., Hopgood, M.F., and Ballard, F.J. 1977. Reduced rates of proteolysis in transformed cells. Nature. 266:58-60.
11. Otsuka, H., and Moskowitz, M. 1978. Differences in the rates of protein degradation in untransformed and transformed cell lines. Exp. Cell Res. 112:127-135.
12. Knecht, E., Hernandez-Yago, J., and Grisolia, S. 1984. Regulation of lysosomal autophagy in transformed and non-transformed mouse fibroblasts under several growth conditions. Exp. Cell Res. 154:224-232.
13. Kopitz J., Kisen, G.O., Gordon, P.B., Bohley, P., and Seglen, P.O. 1990. Nonselective autophagy of cytosolic enzymes by isolated rat hepatocytes. J. Cell Biol. 111:941-953.
14. Kisen, G.O., et al. 1993. Reduced autophagic activity in primary rat hepatocellular carcinoma and ascites hepatoma cells. Carcinogenesis. 14:2501-2505.
15. Tsukada, M., and Ohsumi, Y. 1993. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333:169-174.
16. Thumm, M., et al. 1994. Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett. 349:275-280.
17. Liang, X.H., et al. 1998. Protection against fatal Sindbis virus encephalitis by Beclin, a novel Bcl-2-interacting protein. J. Virol. 72:8586-8596.
18. Kametaka, S., Okano, T., Ohsumi, M., and Ohsumi, Y. 1998. Apg14p and Apg6/Vps30p form a protein complex essential For autophagy in the yeast, Saccharomyces cerevisiae. J. Biol. Chem. 273:22284-22291.
19. Liang, X.H., et al. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 402:672-676.
20. Kihara, A., Kabeya, Y., Ohsumi, Y., and Yoshimori, T. 2001. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2:330-335.
21. Russell, S.E., Hickey, G.I., Lowry, W.S., White, P., and Atkinson, R.J. 1990. Allele loss from chromosome 17 in ovarian cancer. Oncogene. 5:1581-1583.
22. Eccles, D.M., et al. 1992. Early loss of heterozygosity on 17q in ovarian cancer. Oncogene. 7:2069-2072.
23. Cliby, W., et al. 1993. Human epithelial ovarian cancer allelotype. Cancer Res. 53:2393-2398.
24. Tangir, J., et al. 1996. A 400 kb novel deletion unit centromeric to the BRCA1 gene in sporadic epithetial ovarian cancer. Oncogene. 12:735-740.
25. Futreal, P.A., et al. 1992. Detection of frequent allelic loss on proximal chromosome 17q in sporadic breast carcinoma using microsatellite length polymorphisms. Cancer Res. 52:2624-2627.
26. Saito, H., et al. 1993. Detailed deletion mapping of chromosome 17q in ovarian and breast cancers: 2-cM region on 17q21.3 often and commonly deleted in tumors. Cancer Res. 53:3382-3385.
27. Gao, X., et al. 1995. Loss of heterozygosity of the BRCA1 and other loci on chromosome 17q in human prostate cancer. Cancer Res. 55:1002-1005.
28. Knudson, A.G.J. 1971. Mutation and cancer: statistical study of retinoblastoma. Proc. Natl. Acad. Sci. U. S. A. 68:820-823.
29. Aita, V.M., et al. 1999. Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics. 59:59-65.
30. Liang, X.H., Yu, J., Brown, K., and Levine, B. 2001. Beclin 1 contains a leucine-rich nuclear export signal that is required for its autophagy and tumor suppressor function. Cancer Res. 61:3443-3449.
31. Furuya, N., Liang, X.H., and Levine, B. 2003. Autophagy and cancer. In Autophagy. D.J. Klionsky, editor. Landes Bioscience. Georgetown, Texas, USA. 244-253.
32. Mouse Tumor Biology Database. http://tumor.informatics.jax.org/FMPro?-db=Source&-format=strain_search. html&-view.
33. Chisari, F.V., et al. 1989. Molecular pathogenesis of hepatocellular carcinoma in hepatitis B virus transgenic mice. Cell. 59:1145-1156.
34. Morse, H.C., et al. 2002. Bethesda proposals for classification of lymphoid neoplasms in mice. Blood. 100:246-258.
35. Bessler, M., et al. 2002. Glycosylphosphatidylinositol-linked proteins are required for maintenance of a normal peripheral lymphoid compartment but not for lymphocyte development. Eur. J. Immunol. 32:2607-2616
36. Shyamala, G., Yang, X., Silberstein, G., Barcellos-Hoff, M.H., and Dale, E. 1998. Transgenic mice carrying an imbalance in the native ratio of A to B forms of progesterone receptor exhibit developmental abnormalities in mammary glands. Proc Natl. Acad. Sci. U. S. A. 95:696-701.
37. Cardiff, R.D., et al. 2000. The mammary pathology of genetically engineered mice: the consensus report and recommendations from the Annapolis meeting. Oncogene. 19:968-988.
38. Rose, M.L., Birbeck, M.S., Wallis, V.J., Forrester, J.A., and Davies, A.J. 1980. Peanut lectin binding properties of germinal centres of mouse lymphoid tissues. Nature. 284:364-366.
39. Flano, E, Kim, I.-J., Woodland, D.L., and Blackman, M.A. 2002. γ-Herpesvirus latency is preferentially maintained in splenic germinal center and memory B cells. J. Exp. Med 196:1363-1372.
40. Talloczy, Z., et al. 2002. Regulation of starvation- and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 99:190-195.
41. Weibel, E.R. 1969. Stereological principles for morphometry in electron microscopic cytology. Int. Rev. Cytol. 26:235-302.
42. Ikeda, K., et al. 1995. Gene structure and expression of human thyroid transcription factor-1 in respiratory epithelial cells. J. Biol. Chem. 270:8108-8114.
43. Kitamura, H., Kameda, Y., Ito, T., and Hayashi, H. 1999. Atypical adenomatous hyerplasia of the lung. Implications for the pathogenesis of peripheral lung adenocarcinoma. Am. J. Clin. Pathol. 111:610-622.
44. Dalla-Favera, R., et al. 1999. Molecular pathogenesis of B cell malignancy: the role of BCL-6. Curr. Top. Microbiol. Immunol. 246:257-263.
45. Malek, S.N., Dordai, D.I., Reim, J., Dintzis, H., and Desiderio, S. 1998. Malignant transformation of early lymphoid progenitors in mice expressing an activated Blk tryosine kinase. Proc. Natl. Acad. Sci. U. S. A. 95:7351-7356.
46. Jolly, C.J., Klix, N., and Neuberger, M.S. 1997. Rapid methods for the analysis of immunoglobulin gene hypermutation: application to transgenic and gene targered mice. Nucleic Acids Res. 25:1913-1919.
47. Blommaart, E.F., Luiken, J.J., and Meijer, A.J. 1997. Autophagic proteolysis: control and specificity. Histochem. J. 29:365-385.
48. Hu, J.-F., et al. 1997. Repression of hepatitis B virus (HBV) transgene and HBV-induced liver injury by low protein diet. Oncogene. 15:2795-2801.
49. Kojiro, M. 2000. Premalignant lesions of hepatocellular carcinoma: pathologic viewpoint. J. Hepatobiliary Pancreat. Surg. 7:535-541.
50. Terasaki, S., Kaneko, S., Kobayashi, K., Nonomura, A., and Nakanuma, Y. 1998. Histological features predicting malignant transformation of nonmalignant hepatocellular nodules: a prospective study. Gastroenterology. 115:1216-1222.
51. Libbrecht, L., Craninx, M., Nevens, F., Desmet, V., and Roskams, T. 2001. Predictive value of liver cell dysplasia for development of heparocellular carcinoma in patients with non-cirrhotic and cirrhotic chronic viral hepatitis. Htstopathology. 39:66-73.
52. Melendez, A., et al. 2003. Autophagy genes are essential for dauer development and lifespan extension in C elegans. Science. 301:1387-1391.
53. Seaman, M.N., Marcusson, E.G., Cereghino, J.L., and Emr, S.D. 1997. Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of the VPS29, VPS30, and VPS35 gene products. J. Cell Biol. 137:79-92.
54. Kihara, A., Noda, T., Ishihara, N., and Ohsumi, Y. 2001. Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol. 152:519-530.
55. Kirisako, T., et al. 1999. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147:435-446.
56. Huang, W.-P., Scott, S.V., Kim, J., and Klionsky, D.J. 2000. The itinerary of a vesicle component, Aut7p/CvtSp, terminates in the yeast vacuole vis the autophagy/cvt pathways. J. Biol. Chem. 275:5845-5851.
57. Kabeya, Y., et al. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19:5720-5728.
58. Suzuki, K., et al. 2001. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 20:5971-5981.
59. Kim, J., Huang, W.P., Stromhaug, P.E., and Klionsky, D.J. 2002. Convergence of multiple autophagy and cytoplasm to vacuole targeting components to a perivacuolar membrane compartment prior to de novo vesicle formation. J. Biol. Chem. 277:763-773.
60. kip1 is haplo-insufficient for tumour suppression. Nature. 396:177-180.
61. Petiot, A., Ogier-Denis, E., Blommaart, E.F., Meijer, A.J., and Codogno, P. 2000. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol Chem. 275:992-998.
62. Arico, S., et al. 2001. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J. Biol. Chem. 276:35243-35246.
63. Cutler, N.S., Heitman, J., and Cardenas, M.E. 1999. TOR kinase homologs function in a signal transduction pathway that is conserved from yeast to mammals. Mol. Cell. Endocrinol. 155:135-142.
64. +/- mice. Proc. Natl. Acad. Sci. U. S. A. 98:10320-10325.
65. Huang, S., and Houghton, PJ. 2002. Inhibitors of mammalian target of rapamycin as novel antitumor agents: from bench to clinic. Curr. Opin. Investig. Drugs. 3:295-304.
66. Elit, L. 2002. CCI-779 Wyeth. Curr. Opin. Investig. Drugs. 3:1249-1253.
67. Tanaka, K., and Ichihara, A. 1978. Effect of the growth state on protein turnover in two lines of cultured BHK cells. J. Cell. Physiol. 93:407-416.
68. Hendil, K.B. 1977. Intracellular protein degradation in growing, in density-inhibited, and in serum-restricted fibroblast cultures. J. Cell. Physiol. 92:353-364.
69. Amenta, J.S., Sargus, M.J., Venkatesan, S., and Shinozuka, H. 1978. Role of the vacuolar apparatus in augmented protein degradation in cultured fibroblasts. J. Cell. Physiol. 94:77-86.
70. Amenta, J.S., Sargus, M.J., and Brocher, S.C. 1980. Protein synthesis and degradation in growth regulation in rat embryo fibroblasts: role of fast turnover and slow-turnover protein. J. Cell. Physiol. 105:51-61.
71. Ogier-Denis, E., and Codogno, P. 2003. Autophagy: a barrier or an adaptive response to cancer? Biochim. Biophys. Acta. 1603:113-128.
72. Watanabe, S., et al. 1983. Morphologic studies of the liver cell dysplasia. Cancer. 51:2197-2205.