Autophagy enhanced by microtubule- and mitochondrion-associated MAP1S suppresses genome instability and hepatocarcinogenesis

Cancer Research

Volumn 71, Issue 24, 2011, Pages 7537-7546

  Xie, Rui ^a   Wang, Fen ^a   McKeehan, Wallace L ^a   Liu, Leyuan ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIETHYLNITROSAMINE; MICROTUBULE PROTEIN; MITOCHONDRIAL PROTEIN; PROTEIN MAP1S; UNCLASSIFIED DRUG;

AGGRESOME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BIOACCUMULATION; CANCER GENETICS; CANCER GROWTH; CELL ORGANELLE; CONTROLLED STUDY; DISEASE ACTIVITY; DOUBLE STRANDED DNA BREAK; GENOMIC INSTABILITY; LIVER CARCINOGENESIS; LIVER CARCINOMA; MALE; METABOLIC STRESS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION;

ALKYLATING AGENTS; ANIMALS; AUTOPHAGY; CELL TRANSFORMATION, NEOPLASTIC; DIETHYLNITROSAMINE; DNA BREAKS, DOUBLE-STRANDED; FEMALE; GENOMIC INSTABILITY; IMMUNOBLOTTING; LIVER; LIVER NEOPLASMS; MALE; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS;

EID: 84255200364     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-2170     Document Type: Article

References (42)

1. Liu L, Xie R, Nguyen S, Ye M, McKeehan WL. Robust autophagy/mitophagy persists during mitosis. Cell Cycle 2009;8:1616-20.
2. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008;451:1069-75. (Pubitemid 351317450)
3. Kroemer G, Jaattela M. Lysosomes and autophagy in cell death control. Nat Rev Cancer 2005;5:886-97. (Pubitemid 41746033)
4. Desagher S, Martinou JC. Mitochondria as the central control point of apoptosis. Trends Cell Biol 2000;10:369-77. (Pubitemid 30612469)
5. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, et al. Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005;25:1025-40. (Pubitemid 40165810)
6. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 2003;112:1809-20. (Pubitemid 38063704)
7. Mathew R, Karp CM, Beaudoin B, Vuong N, Chen G, Chen HY, et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 2009;137:1062-75.
8. Mathew R, Kongara S, Beaudoin B, Karp CM, Bray K, Degenhardt K, et al. Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev 2007;21:1367-81. (Pubitemid 46871040)
9. Marino G, Salvador-Montoliu N, Fueyo A, Knecht E, Mizushima N, Lopez-Otin C. Tissue-specific autophagy alterations and increased tumorigenesis in mice deficient in Atg4C/autophagin-3. J Biol Chem 2007;282:18573-83. (Pubitemid 47100226)
10. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci U S A 2003;100:15077-82. (Pubitemid 37518019)
11. Takahashi Y, Coppola D, Matsushita N, Cualing HD, Sun M, Sato Y, et al. Bif-1 interacts with Beclin 1 through UVRAG and regulates autophagy and tumorigenesis. Nat Cell Biol 2007;9:1142-51. (Pubitemid 47500490)
12. Liu L, Amy V, Liu G, McKeehan WL. Novel complex integrating mitochondria and the microtubular cytoskeleton with chromosome remodeling and tumor suppressor RASSF1 deduced by in silico homology analysis, interaction cloning in yeast, and colocalization in cultured cells. In Vitro Cell Dev Biol Anim 2002;38:582-94. (Pubitemid 36666244)
13. Liu L, McKeehan WL. Sequence analysis of LRPPRC and its SEC1 domain interaction partners suggest roles in cytoskeletal organization, vesicular trafficking, nucleocytosolic shuttling and chromosome activity. Genomics 2002;79:124-36. (Pubitemid 34112074)
14. Liu L, Vo A, Liu G, McKeehan WL. Distinct structural domains within C19ORF5 support association with stabilized microtubules and mitochondrial aggregation and genome destruction. Cancer Res 2005;65:4191-201. (Pubitemid 40775657)
15. Liu L, Xie R, Yang C, McKeehan WL. Dual function microtubule- and mitochondria-associated proteins mediate mitotic cell death. Cell Oncol 2009;31:393-405.
16. Xie R, Nguyen S, McKeehan K, Wang F, McKeehan WL, Liu L. Microtubule-associated Protein 1S (MAP1S) bridges autophagic components with microtubules and mitochondria to affect autophagosomal biogenesis and degradation. J Biol Chem 2011;286:10367-77.
17. Davison EJ, Pennington K, Hung CC, Peng J, Rafiq R, Ostareck-Lederer A, et al. Proteomic analysis of increased Parkin expression and its interactants provides evidence for a role in modulation of mitochondrial function. Proteomics 2009;9:4284-97.
18. Huang X, Yang C, Jin C, Luo Y, Wang F, McKeehan WL. Resident hepatocyte fibroblast growth factor receptor 4 limits hepatocarcinogenesis. Mol Carcinog 2009;48:553-62.
19. Huang X, Yu C, Jin C, Kobayashi M, Bowles CA, Wang F, et al. Ectopic activity of fibroblast growth factor receptor 1 in hepatocytes accelerates hepatocarcinogenesis by driving proliferation and vascular endothelial growth factor-induced angiogenesis. Cancer Res 2006;66:1481-90. (Pubitemid 43259929)
20. Mitchell C, Willenbring H. A reproducible and well-tolerated method for 2/3 partial hepatectomy in mice. Nat Protoc 2008;3:1167-70.
21. Ho YF, Guenthner TM. Isolation of liver nuclei that retain functional trans-membrane transport. J Pharmacol Toxicol Methods 1997;38:163-8. (Pubitemid 28121353)
22. Liu L, Trimarchi JR, Smith PJ, Keefe DL. Mitochondrial dysfunction leads to telomere attrition and genomic instability. Aging Cell 2002;1:40-6.
23. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 2000;10:886-95. (Pubitemid 30647617)
24. McClintock B. The fusion of broken ends of chromosomes following nuclear fusion. Proc Natl Acad Sci U S A 1942;28:458-63.
25. Storchova Z, Pellman D. From polyploidy to aneuploidy, genome instability and cancer. Nat Rev Mol Cell Biol 2004;5:45-54. (Pubitemid 38089840)
26. Geigl JB, Obenauf AC, Schwarzbraun T, Speicher MR. Defining 'chromosomal instability'. Trends Genet 2008;24:64-9.
27. Boveri T. Zur frage der entstehung maligner tumoren. Jena, Germany: Gustav Fischer Verlag; 1914.
28. Duesberg P, Rasnick D. Aneuploidy, the somatic mutation that makes cancer a species of its own. Cell Motil Cytoskeleton 2000;47:81-107.
29. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999;402:672-6. (Pubitemid 129516338)
30. Takamura A, Komatsu M, Hara T, Sakamoto A, Kishi C, Waguri S, et al. Autophagy-deficient mice develop multiple liver tumors. Genes Dev 2011;25:795-800.
31. Zatloukal K, French SW, Stumptner C, Strnad P, Harada M, Toivola DM, et al. From Mallory to Mallory-Denk bodies: what, how and why? Exp Cell Res 2007;313:2033-49. (Pubitemid 46842981)
32. Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 2007;131:1149-63. (Pubitemid 350235021)
33. Marietta C, Thompson LH, Lamerdin JE, Brooks PJ. Acetaldehyde stimulates FANCD2 monoubiquitination, H2AX phosphorylation, and BRCA1 phosphorylation in human cells in vitro: implications for alcohol-related carcinogenesis. Mutat Res 2009;664:77-83.
34. Mishra PK, Raghuram GV, Panwar H, Jain D, Pandey H, Maudar KK. Mitochondrial oxidative stress elicits chromosomal instability after exposure to isocyanates in human kidney epithelial cells. Free Radic Res 2009;43:718-28.
35. D'Angiolella V, Santarpia C, Grieco D. Oxidative stress overrides the spindle checkpoint. Cell Cycle 2007;6:576-9. (Pubitemid 46440431)
36. Li M, Fang X, Baker DJ, Guo L, Gao X, Wei Z, et al. The ATM-p53 pathway suppresses aneuploidy-induced tumorigenesis. Proc Natl Acad Sci U S A 2010;107:14188-93.
37. Gisselsson D, Pettersson L, Hoglund M, Heidenblad M, Gorunova L, Wiegant J, et al. Chromosomal breakage-fusion-bridge events cause genetic intratumor heterogeneity. Proc Natl Acad Sci U S A 2000;97:5357-62. (Pubitemid 30313723)
38. Burma S, Chen BP, Chen DJ. Role of non-homologous end joining (NHEJ) in maintaining genomic integrity. DNA Repair (Amst) 2006;5:1042-8. (Pubitemid 44291616)
39. Weaver BA, Cleveland DW. Decoding the links between mitosis, cancer, and chemotherapy: the mitotic checkpoint, adaptation, and cell death. Cancer Cell 2005;8:7-12. (Pubitemid 40991810)
40. Mitelman F, Johansson B, Mertens F. The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer 2007;7:233-45. (Pubitemid 46480968)
41. Yamada K, Yamamiya I, Utsumi H. In vivo detection of free radicals induced by diethylnitrosamine in rat liver tissue. Free Radic Biol Med 2006;40:2040-6. (Pubitemid 43728859)
42. Limoli CL, Giedzinski E, Morgan WF, Swarts SG, Jones GD, Hyun W. Persistent oxidative stress in chromosomally unstable cells. Cancer Res 2003;63:3107-11. (Pubitemid 36735860)