MUC1 oncoprotein promotes autophagy in a survival response to glucose deprivation

International Journal of Oncology

Volumn 34, Issue 6, 2009, Pages 1691-1699

  Yin, Li ^a,b   Kharbanda, Surender ^a,b   Kufe, Donald ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Department of Genus Oncology   (United States)

Author keywords

AMP activated protein kinase; ATG7; Autophagy; Glucose deprivation; LC3 II; MUC1; Oxidative stress

Indexed keywords

3 METHYLADENINE; ADENOSINE TRIPHOSPHATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LYSOSOME ENZYME; MUCIN 1; ONCOPROTEIN; PROTEIN ATG7; PROTEIN LC3 II; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; DEPLETION; DRUG MECHANISM; ENERGY DEPRIVATION; ENZYME ACTIVATION; GENE EXPRESSION; GENE SILENCING; GLUCOSE DEPRIVATION; GLUCOSE INTOLERANCE; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN METABOLISM;

ADENINE; ADENOSINE TRIPHOSPHATE; AMP-ACTIVATED PROTEIN KINASES; AUTOPHAGY; BLOTTING, WESTERN; CELL SURVIVAL; GLUCOSE; HCT116 CELLS; HUMANS; HYDROGEN PEROXIDE; MICROTUBULE-ASSOCIATED PROTEINS; MUCIN-1; NECROSIS; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; UBIQUITIN-ACTIVATING ENZYMES;

EID: 67649419014     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo_00000300     Document Type: Article

References (64)

1. Semenza GL: Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732, 2003.
2. Harris AL: Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer 2: 38-47, 2002.
3. Dang CV and Semenza GL: Oncogenic alterations of metabolism. Trends Biochem Sci 24: 68-72, 1999.
4. Seagroves TN, Ryan HE, Lu H, et al: Transcription factor HIF-1 is a necessary mediator of the pasteur effect in mammalian cells. Mol Cell Biol 21: 3436-3444, 2001.
5. Helmlinger G, Yuan F, Dellian M and Jain RK: Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med 3: 177-182, 1997.
6. + transport in the interstitial fluid. Novartis Found Symp 240: 46-62; discussion 62-67, 152-153, 2001.
7. Secomb TW, Hsu R, Braun RD, Ross JR, Gross JF and Dewhirst MW: Theoretical simulation of oxygen transport to tumors by three-dimensional networks of microvessels. Adv Exp Med Biol 454: 629-634, 1998.
8. Jelluma N, Yang X, Stokoe D, Evan GI, Dansen TB and Haas-Kogan DA: Glucose withdrawal induces oxidative stress followed by apoptosis in glioblastoma cells but not in normal human astrocytes. Mol Cancer Res 4: 319-330, 2006.
9. 2 mediate glucose deprivation-induced stress in human cancer cells. J Biol Chem 280: 4254-4263, 2005.
10. Xu RH, Pelicano H, Zhou Y, et al: Inhibition of glycolysis in cancer cells: a novel strategy to overcome drug resistance associated with mitochondrial respiratory defect and hypoxia. Cancer Res 65: 613-621, 2005.
11. Buzzai M, Bauer DE, Jones RG, et al: The glucose dependence of Akt-transformed cells can be reversed by pharmacologic activation of fatty acid beta-oxidation. Oncogene 24: 4165-4173, 2005.
12. Laderoute KR, Amin K, Calaoagan JM, et al: 5′-AMP-activated protein kinase (AMPK) is induced by low-oxygen and glucose deprivation conditions found in solid-tumor microenvironments. Mol Cell Biol 26: 5336-5347, 2006.
13. Eguchi Y, Shimizu S and Tsujimoto Y: Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res 57: 1835-1840, 1997.
14. Leist M, Single B, Castoldi AF, Kuhnle S and Nicotera P: Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 185: 1481-1486, 1997.
15. Klionsky DJ and Emr SD: Autophagy as a regulated pathway of cellular degradation. Science 290: 1717-1721, 2000.
16. Kim E, Sohn S, Kwon H, et al: Sodium selenite induces superoxide-mediated mitochondrial damage and subsequent autophagic cell death in malignant glioma cells. Cancer Res 67: 6314-6324, 2007.
17. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L and Elazar Z: Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 3: 371-373, 2007.
18. Gao M, Yeh P, Lu Y, et al: OSU-03012, a novel celecoxib derivative, induces reactive oxygen species-related autophagy in hepatocellular carcinoma. Cancer Res 68: 9348-9357, 2008.
19. Kiffin R, Bandyopadhyay U and Cuervo AM: Oxidative stress and autophagy. Antioxid Redox Signal 8: 152-162, 2006.
20. Kondo Y, Kanzawa T, Sawaya R and Kondo S: The role of autophagy in cancer development and response to therapy. Nat Rev Cancer 5: 726-734, 2005.
21. Hahn-Windgassen A, Nogueira V, Chen CC, Skeen JE, Sonenberg N and Hay N: Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. J Biol Chem 280: 32081-32089, 2005.
22. Meley D, Bauvy C, Houben-Weerts JH, et al: AMP-activated protein kinase and the regulation of autophagic proteolysis. J Biol Chem 281: 34870-34879, 2006.
23. Wang Z, Wilson WA, Fujino MA and Roach PJ: Antagonistic controls of autophagy and glycogen accumulation by Snf1p, the yeast homolog of AMP-activated protein kinase, and the cyclin-dependent kinase Pho85p. Mol Cell Biol 21: 5742-5752, 2001.
24. Vande Velde C, Cizeau J, Dubik D, et al: BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol Cell Biol 20: 5454-5468, 2000.
25. Saeki K, Yuo A, Okuma E, 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.
26. Yanagisawa H, Miyashita T, Nakano Y and 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.
27. Yue Z, Jin S, Yang C, Levine AJ and 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.
28. Qu X, Yu J, Bhagat G, et al: Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 112: 1809-1820, 2003.
29. Degenhardt K, Mathew R, Beaudoin B, et al: Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10: 51-64, 2006.
30. Kufe D, Inghirami G, Abe M, Hayes D, Justi-Wheeler H and Schlom J: Differential reactivity of a novel monoclonal antibody (DF3) with human malignant versus benign breast tumors. Hybridoma 3: 223-232, 1984.
31. Gendler S, Taylor-Papadimitriou J, Duhig T, Rothbard J and Burchell JA: A highly immunogenic region of a human polymorphic epithelial mucin expressed by carcinomas is made up of tandem repeats. J Biol Chem 263: 12820-12823, 1988.
32. Siddiqui J, Abe M, Hayes D, Shani E, Yunis E and Kufe D: Isolation and sequencing of a cDNA coding for the human DF3 breast carcinoma-associated antigen. Proc Natl Acad Sci USA 85: 2320-2323, 1988.
33. Merlo G, Siddiqui J, Cropp C, et al: DF3 tumor-associated antigen gene is located in a region on chromosome 1q frequently altered in primary human breast cancer. Cancer Res 49: 6966-6971, 1989.
34. Li Y, Liu D, Chen D, Kharbanda S and Kufe D: Human DF3/MUC1 carcinoma-associated protein functions as an oncogene. Oncogene 22: 6107-6110, 2003.
35. Ren J, Agata N, Chen D, et al: Human MUC1 carcinoma-associated protein confers resistance to genotoxic anti-cancer agents. Cancer Cell 5: 163-175, 2004.
36. Wei X, Xu H and Kufe D: Human MUC1 oncoprotein regulates p53-responsive gene transcription in the genotoxic stress response. Cancer Cell 7: 167-178, 2005.
37. Ren J, Bharti A, Raina D, Chen W, Ahmad R and Kufe D: MUC1 oncoprotein is targeted to mitochondria by heregulin-induced activation of c-Src and the molecular chaperone HSP90. Oncogene 25: 20-31, 2006.
38. Leng Y, Cao C, Ren J, et al: Nuclear import of the MUC1-C oncoprotein is mediated by nucleoporin Nup62. J Biol Chem 282: 19321-19330, 2007.
39. Li Y, Bharti A, Chen D, Gong J and Kufe D: Interaction of glycogen synthase kinase 3β with the DF3/MUC1 carcinoma-associated antigen and β-catenin. Mol Cell Biol 18: 7216-7224, 1998.
40. Li Y, Kuwahara H, Ren J, Wen G and Kufe D: The c-Src tyrosine kinase regulates signaling of the human DF3/MUC1 carcinoma-associated antigen with GSK3β and β-catenin. J Biol Chem 276: 6061-6064, 2001.
41. Ren J, Li Y and Kufe D: Protein kinase Cδ regulates function of the DF3/MUC1 carcinoma antigen in β-catenin signaling. J Biol Chem 277: 17616-17622, 2002.
42. Raina D, Ahmad R, Kumar S, et al: MUC1 oncoprotein blocks nuclear targeting of c-Abl in the apoptotic response to DNA damage. EMBO J 25: 3774-3783, 2006.
43. Yamamoto M, Bharti A, Li Y and Kufe D: Interaction of the DF3/MUC1 breast carcinoma-associated antigen and β-catenin in cell adhesion. J Biol Chem 272: 12492-12494, 1997.
44. Huang L, Chen D, Liu D, Yin L, Kharbanda S and Kufe D: MUC1 oncoprotein blocks GSK3β-mediated phosphorylation and degradation of β-catenin. Cancer Res 65: 10413-10422, 2005.
45. Ahmad R, Raina D, Trivedi V, et al: MUC1 oncoprotein activates the IκB kinase β complex and constitutive NF-κβ signaling. Nat Cell Biol 9: 1419-1427, 2007.
46. Yin L and Kufe D: Human MUC1 carcinoma antigen regulates intracellular oxidant levels and the apoptotic response to oxidative stress. J Biol Chem 278: 35458-35464, 2003.
47. Yin L, Huang L and Kufe D: MUC1 oncoprotein activates the FOXO3a transcription factor in a survival response to oxidative stress. J Biol Chem 279: 45721-45727, 2004.
48. Huang L, Ren J, Chen D, Li Y, Kharbanda S and Kufe D: MUC1 cytoplasmic domain coactivates Wnt target gene transcription and confers transformation. Cancer Biol Ther 2: 702-706, 2003.
49. Li Y, Ren J, Yu W-H, et al: The EGF receptor regulates interaction of the human DF3/MUC1 carcinoma antigen with c-Src and β-catenin. J Biol Chem 276: 35239-35242, 2001.
50. Ben-Ezra J, Johnson DA, Rossi J, Cook N and Wu A: Effect of fixation on the amplification of nucleic acids from paraffin-embedded material by the polymerase chain reaction. J Histochem Cytochem 39: 351-354, 1991.
51. Mizushima N, Ohsumi Y and Yoshimori T: Autophagosome formation in mammalian cells. Cell Struct Funct 27: 421-429, 2002.
52. Yu L, Alva A, Su H, et al: Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304: 1500-1502, 2004.
53. Kabeya Y, Mizushima N, Ueno T, et al: LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720-5728, 2000.
54. Asanuma K, Tanida I, Shirato I, et al: MAP-LC3, a promising autophagosomal marker, is processed during the differentiation and recovery of podocytes from PAN nephrosis. FASEB J 17: 1165-1167, 2003.
55. Schmid D, Pypaert M and Munz C: Antigen-loading compartments for major histocompatibility complex class II molecules continuously receive input from autophagosomes. Immunity 26: 79-92, 2007.
56. Tanida I, Minematsu-Ikeguchi N, Ueno T and Kominami E: Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1: 84-91, 2005.
57. Zhou G, Myers R, Li Y, et al: Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 108: 1167-1174, 2001.
58. Edinger AL and Thompson CB: Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 16: 663-669, 2004.
59. Nicotera P, Leist M and Ferrando-May E: Intracellular ATP, a switch in the decision between apoptosis and necrosis. Toxicol Lett 102-103: 139-142, 1998.
60. Blackburn RV, Spitz DR, Liu X, et al: Metabolic oxidative stress activates signal transduction and gene expression during glucose deprivation in human tumor cells. Free Radic Biol Med 26: 419-430, 1999.
61. Lee YJ, Galoforo SS, Berns CM, et al: Glucose deprivation-induced cytotoxicity and alterations in mitogen-activated protein kinase activation are mediated by oxidative stress in multidrug-resistant human breast carcinoma cells. J Biol Chem 273: 5294-5299, 1998.
62. Kiffin R, Christian C, Knecht E and Cuervo AM: Activation of chaperone-mediated autophagy during oxidative stress. Mol Biol Cell 15: 4829-4840, 2004.
63. Yu L, Wan F, Dutta S, et al: Autophagic programmed cell death by selective catalase degradation. Proc Natl Acad Sci USA 103: 4952-4957, 2006.
64. Vermeer PD, Einwalter LA, Moninger TO, et al: Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature 422: 322-326, 2003.