The role of autophagy in cancer development and response to therapy (original) (raw)

• Klionsky, D. J. & Emr, S. D. Autophagy as a regulated pathway of cellular degradation. Science 290, 1717–1721 (2000). Comprehensive review of autophagic processes.
  Article CAS PubMed PubMed Central Google Scholar
• Levine, B. & Klionsky, D. J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6, 463–477 (2004). Comprehensive review of autophagy in eukaryotic development.
  Article CAS PubMed Google Scholar
• Meijer, A. J. & Codogno, P. Regulation and role of autophagy in mammalian cells. Int. J. Biochem. Cell Biol. 36, 2445–2462 (2004). Comprehensive review of the autophagic process in mammalian cells.
  Article CAS PubMed Google Scholar
• Larsen, K. E. & Sulzer, D. Autophagy in neurons: a review. Histol. Histopathol. 17, 897–908 (2002).
  CAS PubMed Google Scholar
• Nishino, I. Autophagic vacuolar myopathies. Curr. Neurol. Neurosci. Rep. 3, 64–69 (2003).
  Article PubMed Google Scholar
• Ogier-Denis, E. & Codogno, P. Autophagy: a barrier or an adaptive response to cancer. Biochim. Biophys. Acta 1603, 113–128 (2003).
  CAS PubMed Google Scholar
• Gozuacik, D. & Kimchi, A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23, 2891–2906 (2004). Reference 7, together with reference 6, provide comprehensive reviews of autophagy in cancer.
  Article CAS PubMed Google Scholar
• Gunn, J. M., Clark, M. G., Knowles, S. E., Hopgood, M. F. & Ballard, F. J. Reduced rates of proteolysis in transformed cells. Nature 266, 58–60 (1977).
  Article CAS PubMed Google Scholar
• Kisen, G. O. et al. Reduced autophagic activity in primary rat hepatocellular carcinoma and ascites hepatoma cells. Carcinogenesis 14, 2501–2505 (1993).
  Article CAS PubMed Google Scholar
• Kirkegaard, K., Taylor, M. P. & Jackson, W. T. Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nature Rev. Microbiol. 2, 301–314 (2004).
  Article CAS Google Scholar
• Otsuka, H. & Moskowitz, M. Differences in the rates of protein degradation in untransformed and transformed cell lines. Exp. Cell Res. 112, 127–35 (1978).
  Article CAS PubMed Google Scholar
• Schwarze, P. E. & Seglen, P. O. Reduced autophagic activity, improved protein balance and enhanced in vitro survival of hepatocytes isolated from carcinogen-treated rats. Exp. Cell Res. 157, 15–28 (1985).
  Article CAS PubMed Google Scholar
• Lee, H. K., Jones, R. T., Myers, R. A. & Marzella, L. Regulation of protein degradation in normal and transformed human bronchial epithelial cells in culture. Arch. Biochem. Biophys. 296, 271–278 (1992).
  Article CAS PubMed Google Scholar
• Liang, X. H. et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672–676 (1999). First demonstration of the relationship between autophagy-associated BECN1 and tumorigenicity in breast and other cancers.
  Article CAS PubMed Google Scholar
• Liang, X. H. et al. Protection against fatal Sindbis virus encephalitis by beclin, a novel BCL-2-interacting protein. J. Virol. 72, 8586–96 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Qu, X. et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J. Clin. Invest. 112, 1809–1820 (2003). First evidence of tumour development because of a deficiency of BECN1.
  Article CAS PubMed PubMed Central Google Scholar
• Yue, Z., Jin, S., Yang, C., Levine, A. J. & Heintz, N. beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl Acad. Sci. USA 100, 15077–15082 (2003). Reference 17, together with reference 16, provide the first demonstrations of the role of BECN1 as a tumour suppressor.
  Article CAS PubMed PubMed Central Google Scholar
• Cuervo, A. M. Autophagy: in sickness and in health. Trends Cell Biol. 14, 70–77 (2004).
  Article PubMed CAS Google Scholar
• Edinger, A. L. & Thompson, C. B. Defective autophagy leads to cancer. Cancer Cell 4, 422–424 (2003).
  Article CAS PubMed Google Scholar
• Ogier-Denis, E., Houri, J. J., Bauvy, C. & Codogno, P. Guanine nucleotide exchange on heterotrimeric GI3 protein controls autophagic sequestration in HT-29 cells. J. Biol. Chem. 271, 28593–28600 (1996).
  Article CAS PubMed Google Scholar
• Liang, X. H., Yu, J., Brown, K. & Levine, B. Beclin 1 contains a leucine-rich nuclear export signal that is required for its autophagy and tumor suppressor function. Cancer Res. 61, 3443–3449 (2001).
  CAS PubMed Google Scholar
• Proikas-Cezanne, T. et al. WIPI-1α (WIPI49), a member of the novel 7-bladed WIPI protein family, is aberrantly expressed in human cancer and is linked to starvation-induced autophagy. Oncogene 23, 9314–9325 (2004).
  Article CAS PubMed Google Scholar
• Susan, P. P. & Dunn, W. A. Jr. Starvation-induced lysosomal degradation of aldolase B requires glutamine 111 in a signal sequence for chaperone-mediated transport. J. Cell. Physiol. 187, 48–58 (2001).
  Article CAS PubMed Google Scholar
• Ito, H., Daido, S., Kanzawa, T., Kondo, S. & Kondo, Y. Radiation-induced autophagy is associated with LC3 and its inhibition sensitizes malignant glioma cells. Int. J. Oncol. 26, 1401–1410 (2005).
  CAS PubMed Google Scholar
• Furuta, S., Hidaka, E., Ogata, A., Yokota, S. & Kamata, T. RAS is involved in the negative control of autophagy through the class I PI3-kinase. Oncogene 23, 3898–3904 (2004).
  Article CAS PubMed Google Scholar
• Izuishi, K., Kato, K., Ogura, T., Kinoshita, T. & Esumi, H. Remarkable tolerance of tumor cells to nutrient deprivation: possible new biochemical target for cancer therapy. Cancer Res. 60, 6201–6207 (2000).
  CAS PubMed Google Scholar
• Clarke, P. G. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol (Berl). 181, 195–213 (1990). Renews interest in the role of autophagy during cell death.
  Article CAS PubMed Google Scholar
• Bursch, W. et al. Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy. Carcinogenesis 17, 1595–1607 (1996).
  Article CAS PubMed Google Scholar
• Scarlatti, F. et al. Ceramide-mediated macroautophagy involves inhibition of protein kinase B and up-regulation of Beclin 1. J. Biol. Chem. 279, 18384–18391 (2004).
  Article CAS PubMed Google Scholar
• Kanzawa, T. et al. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 11, 448–457 (2004). First investigation to find that inhibition of autophagy at different stages causes distinct outcomes.
  Article CAS PubMed Google Scholar
• Paglin, S. et al. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 61, 439–444 (2001). First investigation to show the feasibility of treating cancer cells by autophagy inhibition.
  CAS PubMed Google Scholar
• Yao, K. C. et al. Molecular response of human glioblastoma multiforme cells to ionizing radiation: cell cycle arrest, modulation of the expression of cyclin-dependent kinase inhibitors, and autophagy. J. Neurosurg. 98, 378–384 (2003).
  Article CAS PubMed Google Scholar
• Shao, Y., Gao, Z., Marks, P. A. & Jiang, X. Apoptotic and autophagic cell death induced by histone deacetylase inhibitors. Proc. Natl Acad. Sci. USA, 101, 18030–18035 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Komata, T. et al. Mild heat shock induces autophagic growth arrest, but not apoptosis in U251-MG and U87-MG human malignant glioma cells. J. Neurooncol. 68, 101–111 (2004).
  Article PubMed Google Scholar
• Kanzawa, T., Kondo, Y., Ito, H., Kondo, S., and Germano, I. Induction of autophagic cell death in malignant glioma cells by arsenic trioxide. Cancer Res. 63, 2103–2108 (2003). Provides evidence that bafilomycin A 1 increases the antitumour effect of arsenic trioxide by inhibiting autophagy.
  CAS PubMed Google Scholar
• Kanzawa, T. et al. Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3. Oncogene 24, 980–991 (2005).
  Article CAS PubMed Google Scholar
• Opipari, A. W. Jr. et al. Resveratrol-induced autophagocytosis in ovarian cancer cells. Cancer Res. 64, 696–703 (2004).
  Article CAS PubMed Google Scholar
• Ellington, A. A., Berhow, M. & Singletary, K. W. Induction of macroautophagy in human colon cancer cells by soybean B-group triterpenoid saponins. Carcinogenesis 26, 159–167 (2005).
  Article CAS PubMed Google Scholar
• Takeuchi, H. et al. Augmentation of rapamycin-induced autophagy in malignant glioma cells by phosphatidylinositol 3-phosphate kinase/protein kinase B inhibitors. Cancer Res. 65, 3336–3346 (2005).
  Article CAS PubMed Google Scholar
• Blume-Jensen, P. & Hunter, T. Oncogenic kinase signalling. Nature 411, 355–365 (2001).
  Article CAS PubMed Google Scholar
• Vivanco, I. & Sawyers, C. L. The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nature Rev. Cancer 2, 489–501 (2002).
  Article CAS Google Scholar
• Shintani, T. & Klionsky, D. J. Autophagy in health and disease: a double-edged sword. Science 306, 990–995 (2004). Reviews a role of autophagy in health and disease.
  Article CAS PubMed PubMed Central Google Scholar
• Schmelzle, T. & Hall, M. N. TOR, a central controller of cell growth. Cell 103, 253–262 (2000). Reviews the function of TOR and mTOR as central regulators for cell growth.
  Article CAS PubMed Google Scholar
• Gingras, A. C., Raught, B. & Sonenberg, N. Regulation of translation initiation by FRAP/mTOR. Genes Dev. 15, 807–826 (2001). Review shows that mTOR is involved in the regulation of translation initiation.
  Article CAS PubMed Google Scholar
• Wang, C. W. & Klionsky, D. J. The molecular mechanism of autophagy. Mol. Med. 3–4, 65–76 (2003).
  Article Google Scholar
• Petiot, A., Ogier-Denis, E., Blommaart, E. F., Meijer, A. J. & Codogno, P. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275, 992–998 (2000).
  Article CAS PubMed Google Scholar
• Arico, S. et al. The tumor suppressor PTEN positively regulates macroautophagy by inhibiting the phosphatidylinositol 3-kinase/protein kinase B pathway. J. Biol. Chem. 276, 35243–35246 (2001).
  Article CAS PubMed Google Scholar
• Steck, P. A. et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nature Genet. 15, 356–362 (1997).
  Article CAS PubMed Google Scholar
• Kihara, A., Kabeya, Y., Ohsumi, Y. & Yoshimori, T. Beclin–phosphatidylinositol 3-kinase complex functions at the _trans_-Golgi network. EMBO Rep. 2, 330–335 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Brown, W. J., DeWald, D. B., Emr, S. D., Plutner, H. & Balch, W. E. Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells. J. Cell Biol. 130, 781–796 (1995).
  Article CAS PubMed Google Scholar
• Inbal, B., Bialik, S., Sabanay, I., Shani, G. & Kimchi, A. DAP kinase and DRP-1 mediate membrane blebbing and the formation of autophagic vesicles during programmed cell death. J. Cell Biol. 157, 455–468 (2002). Demonstrates the induction of autophagic cell death by DAPK and DRP1.
  Article CAS PubMed PubMed Central Google Scholar
• Saeki, K. et al. BCL-2 down-regulation causes autophagy in a caspase-independent manner in human leukemic HL60 cells. Cell Death Differ. 7, 1263–1269 (2000).
  Article CAS PubMed Google Scholar
• Vande Velde, C. et al. BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol. Cell. Biol. 20, 5454–5468 (2000). Demonstrates the involvement of BNIP3 in autophagic cell death.
  Article CAS PubMed PubMed Central Google Scholar
• Yanagisawa, H., Miyashita, T., Nakano, Y. & Yamamoto, D. HSPIN1, a transmembrane protein interacting with BCL-2/BCL-XL, induces a caspase-independent autophagic cell death. Cell Death Differ., 10, 798–807 (2003).
  Article CAS PubMed Google Scholar
• Ogier-Denis, E., Pattingre, S., El Benna, J. & Codogno, P. ERK1/2-dependent phosphorylation of Gα-interacting protein stimulates its GTPase accelerating activity and autophagy in human colon cancer cells. J. Biol. Chem. 275, 39090–39095 (2000).
  Article CAS PubMed Google Scholar
• Inbal, B. et al. DAP kinase links the control of apoptosis to metastasis. Nature 390, 180–184 (1997).
  Article CAS PubMed Google Scholar
• Daido, S. et al. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res. 64, 4286–4293 (2004).
  Article CAS PubMed Google Scholar
• Shimizu, S. et al. Role of BCL-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nature Cell Biol. 6, 1221–1228 (2004).
  Article CAS PubMed Google Scholar
• Lum, J. J. et al. Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120, 237–248 (2005).
  Article CAS PubMed Google Scholar
• Su, B. & Karin, M. Mitogen-activated protein kinase cascades and regulation of gene expression. Curr. Opin. Immunol. 8, 402–411 (1996).
  Article CAS PubMed Google Scholar
• Hanahan, D. & Weinberg, R. A. The hallmarks of cancer. Cell 100, 57–70 (2000).
  Article CAS PubMed Google Scholar
• Alva, A. S., Gultekin, S. H. & Baehrecke, E. H. Autophagy in human tumors: cell survival or death? Cell Death Differ. 11, 1046–1048 (2004).
  Article CAS PubMed Google Scholar
• Bursch, W., Ellinger, A., Gerner, C., Frohwein, U. & Schulte-Hermann, R. Programmed cell death (PCD). Apoptosis, autophagic PCD, or others? Ann. NY Acad. Sci. 926, 1–12 (2000).
  Article CAS PubMed Google Scholar
• Bursch, W. et al. Autophagic and apoptotic types of programmed cell death exhibit different fates of cytoskeletal filaments. J. Cell Sci. 113, 1189–1198 (2000).
  Article CAS PubMed Google Scholar
• Bursch, W. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ. 8, 569–581 (2001).
  Article CAS PubMed Google Scholar
• Yu, L. et al. Regulation of an ATG7–Beclin 1 program of autophagic cell death by caspase-8. Science 304, 1500–1502 (2004). Demonstrates the direct interaction between autophagy and apoptosis.
  Article CAS PubMed Google Scholar
• Boya, P. et al. Inhibition of macroautophagy triggers apoptosis. Mol. Cell. Biol., 25, 1025–1040 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Bauvy, C., Gane, P., Arico, S., Codogno, P. & Ogier-Denis, E. Autophagy delays sulindac sulfide-induced apoptosis in the human intestinal colon cancer cell line HT-29. Exp. Cell Res. 268, 139–149 (2001).
  Article CAS PubMed Google Scholar
• Pelicano, H. et al. Inhibition of mitochondrial respiration: a novel strategy to enhance drug-induced apoptosis in human leukemia cells by a reactive oxygen species-mediated mechanism. J. Biol. Chem. 278, 37832–37839 (2003).
  Article CAS PubMed Google Scholar
• Piacentini, M., Evangelisti, C., Mastroberardino, P. G., Nardacci, R. & Kroemer, G. Does prothymosin-α act as molecular switch between apoptosis and autophagy? Cell Death Differ. 10, 937–939 (2003).
  Article CAS PubMed Google Scholar
• Yamamoto, A. et al. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct. Funct. 23, 33–42 (1998).
  Article CAS PubMed Google Scholar
• Cheney, I. W. et al. Suppression of tumorigenicity of glioblastoma cells by adenovirus-mediated MMAC1/PTEN gene transfer. Cancer Res. 58, 2331–2334 (1998).
  CAS PubMed Google Scholar
• Davies, M. A. et al. Adenoviral-mediated expression of MMAC/PTEN inhibits proliferation and metastasis of human prostate cancer cells. Clin. Cancer Res. 8, 1904–1914 (2002).
  CAS PubMed Google Scholar
• Chan, S. Targeting the mammalian target of rapamycin (mTOR): a new approach to treating cancer. Br. J. Cancer 91, 1420–1424 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Eshleman, J. S. et al. Inhibition of the mammalian target of rapamycin sensitizes U87 xenografts to fractionated radiation therapy. Cancer Res. 62, 7291–7297 (2002).
  CAS PubMed Google Scholar
• Mondesire, W. H. et al. Targeting mammalian target of rapamycin synergistically enhances chemotherapy-induced cytotoxicity in breast cancer cells. Clin. Cancer Res. 10, 7031–7042 (2004).
  Article CAS PubMed Google Scholar
• Stephan, S. et al. Effect of rapamycin alone and in combination with antiangiogenesis therapy in an orthotopic model of human pancreatic cancer. Clin. Cancer Res. 10, 6993–7000 (2004).
  Article CAS PubMed Google Scholar
• Kim, J. & Klionsky, D. J. Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Ann. Rev. Biochem. 69, 303–342 (2000).
  Article CAS PubMed Google Scholar
• Kabeya, Y. et al. LC3, a mammalian homologue of yeast APG8P, is localized in autophagosome membranes after processing. EMBO J. 19, 5720–5728 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Mizushima, N. et al. Dissection of autophagosome formation using APG5-deficient mouse embryonic stem cells. J. Cell Biol. 152, 657–668 (2001). First demonstration of the de novo synthesis of the autophagosome membrane.
  Article CAS PubMed PubMed Central Google Scholar
• Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T. & Ohsumi, Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 15, 1101–1111 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Dunn, W. A. Jr. Studies on the mechanisms of autophagy: formation of the autophagic vacuole. J. Cell Biol. 110, 1923–1933 (1990).
  Article PubMed Google Scholar
• Yokota, S., Himeno, M., Roth, J., Brada, D. & Kato, K. Formation of autophagosomes during degradation of excess peroxisomes induced by di-(2-ethylhexyl)phthalate treatment. II. Immunocytochemical analysis of early and late autophagosomes. Eur. J. Cell Biol. 62, 372–383 (1993).
  CAS PubMed Google Scholar
• Stromhaug, P. E., Berg, T. O., Fengsrud, M. & Seglen, P. O. Purification and characterization of autophagosomes from rat hepatocytes. Biochem. J. 335, 217–224 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Noda, T., Suzuki, K. & Ohsumi, Y. Yeast autophagosomes: de novo formation of a membrane structure. Trends Cell Biol. 12, 231–25 (2002).
  Article CAS PubMed Google Scholar
• Reunanen, H., Marttinen, M. & Hirsimaki, P. Effects of griseofulvin and nocodazole on the accumulation of autophagic vacuoles in Ehrlich ascites tumor cells. Exp. Mol. Pathol. 48, 97–102 (1988).
  Article CAS PubMed Google Scholar
• Punnonen, E. L. & Reunanen, H. Effects of vinblastine, leucine, and histidine, and 3-methyladenine on autophagy in Ehrlich ascites cells. Exp. Mol. Pathol. 52, 87–97 (1990).
  Article CAS PubMed Google Scholar