Midbody accumulation through evasion of autophagy contributes to cellular reprogramming and tumorigenicity

Nature Cell Biology

Volumn 13, Issue 10, 2011, Pages 1214-1223

  Kuo, Tse Chun ^a   Chen, Chun Ting ^a   Baron, Desiree ^a   Onder, Tamer T ^b,c,d   Loewer, Sabine ^b,c,d   Almeida, Sandra ^a   Weismann, Cara M ^a   Xu, Ping ^a   Houghton, Jean Marie ^a   Gao, Fen Biao ^a   Daley, George Q ^b,c,d,e   Doxsey, Stephen ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HARVARD STEM CELL INSTITUTE   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGIC RECEPTOR NBR1; CELL PROTEIN; CEP55 MIDBODY PROTEIN; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CANCER STEM CELL; CARCINOGENICITY; CELL DEGENERATION; CELL DIFFERENTIATION; CELL DIVISION; CELL ENCAPSULATION; CELL FUNCTION; CELL ORGANELLE; CENTROSOME; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MIDBODY; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL;

ANIMALS; AUTOPHAGY; CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; CELL LINE; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CENTROSOME; CHROMOSOMAL PROTEINS, NON-HISTONE; COCULTURE TECHNIQUES; EMBRYONIC STEM CELLS; HELA CELLS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; LYSOSOMES; MICE; NEOPLASTIC STEM CELLS; NUCLEAR PROTEINS; NUCLEAR REPROGRAMMING; ORGANELLES; PROTEINS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; TIME FACTORS; TRANSFECTION;

EID: 80053564250     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2332     Document Type: Article

References (70)

1. Eggert, U. S., Mitchison, T. J. & Field, C. M. Animal cytokinesis: from parts list to mechanisms. Annu. Rev. Biochem. 75, 543-66 (2006). (Pubitemid 44118043)
2. Neumüller, R. A. & Knoblich, J. A. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 23, 2675-2699 (2009).
3. Doxsey, S., McCollum, D. & Theurkauf, W. Centrosomes in cellular regulation. Annu. Rev. Cell Dev. Biol. 21, 411-434 (2005). (Pubitemid 41740641)
4. Yamashita, Y. M., Mahowald, A. P., Perlin, J. R. & Fuller, M. T. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315, 518-521 (2007). (Pubitemid 46175756)
5. Wang, X. et al. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461, 947-955 (2009).
6. Yamashita, Y. M., Jones, D. L. & Fuller, M. T. Orientation of asymmetric stem cell division by the APC tumor suppressor and centrosome. Science 301, 1547-1550 (2003). (Pubitemid 37128549)
7. Barr, F. A. & Gruneberg, U. Cytokinesis: placing and making the final cut. Cell 131, 847-860 (2007). (Pubitemid 350138092)
8. Mullins, J. M. & Biesele, J. J. Terminal phase of cytokinesis in D-98s cells. J. Cell Biol. 73, 672-684 (1977). (Pubitemid 8115201)
9. Gromley, et al. Centriolin anchoring of exocyst and SNARE complexes at the midbody is required for secretory-vesicle-mediated abscission. Cell 123, 75-87 (2005). (Pubitemid 41414530)
10. Steigemann, P. et al. Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 136, 473-484 (2009).
11. Goss, J. W. & Toomre, D. K. Both daughter cells traffic and exocytose membrane at the cleavage furrow during mammalian cytokinesis. J. Cell Biol. 181, 1047-1054 (2008). (Pubitemid 351915480)
12. Pohl, C. & Jentsch, S. Midbody ring disposal by autophagy is a post-abscission event of cytokinesis. Nat. Cell Biol. 11, 65-70 (2009).
13. Marzesco, A. M. et al. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J. Cell Sci. 118, 2849-2858 (2005).
14. Dubreuil, V. et al. Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1. J. Cell. Biol. 176, 483-495 (2007).
15. Mizushima, N., Levine, B., Cuervo, A. M. & Klionsky, D. J. Autophagy fights disease through cellular self-digestion. Nature 451, 1069-1075 (2008). (Pubitemid 351317450)
16. Mizushima, N. & Klionsky, D. Protein turnover via autophagy: implications for metabolism. Annu. Rev. Nutr. 27, 19-40 (2007). (Pubitemid 351373346)
17. Yorimitsu, T. & Klionsky, D. J. Eating the endoplasmic reticulum: quality control by autophagy. Trends Cell Biol. 17, 279-285 (2007). (Pubitemid 46829849)
18. Levine, B. & Kroemer, G. Autophagy in the pathogenesis of disease. Cell 132, 27-42 (2008).
19. Kuma, A. et al. The role of autophagy during the early neonatal starvation period. Nature 432, 1032-1036 (2004). (Pubitemid 40052234)
20. Fimia, G. M. et al. Ambra1 regulates autophagy and development of the nervous system. Nature 447, 1121-1125 (2007).
21. Tsukamoto, S. et al. Autophagy is essential for preimplantation development of mouse embryos. Science 321, 117-120 (2008). (Pubitemid 351956245)
22. Cecconi, F. & Levine, B. The role of autophagy in mammalian development: cell makeover rather than cell death. Dev. Cell 15, 344-357 (2008).
23. Hara, T. et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885-889 (2006).
24. Komatsu, M. et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169, 425-434 (2005). (Pubitemid 40686693)
25. Rujano, M. A. et al. Polarised asymmetric inheritance of accumulated protein damage in higher eukaryotes. PLoS Biol. 4, 2325-2335 (2006). (Pubitemid 44917621)
26. Johnston, J. A., Illing, M. E. & Kopito, R. R. Cytoplasmic dynein/dynactin mediates the assembly of aggresomes. Cell. Motil. Cytoskeleton 53, 26-38 (2002). (Pubitemid 34984442)
27. Anderson, C. T. & Stearns, T. Centriole age underlies asynchronous primary cilium growth in mammalian cells. Curr. Biol. 19, 1498-1502 (2009).
28. Piel, M., Meyer, P., Khodjakov, A., Rieder, C. L. & Bornens, M. The respective contributions of the mother and daughter centrioles to centrosome activity and behavior in vertebrate cells. J. Cell Biol. 149, 317-330 (2000).
29. Oatley, J. M. & Brinster, R. L. Regulation of spermatogonial stem cell self-renewal in mammals. Annu. Rev. Cell Dev. Biol. 24, 263-286 (2008).
30. Barroca, V. et al. Mouse differentiating spermatogonia can generate germinal stem cells in vivo. Nat. Cell Biol. 11, 190-196 (2009).
31. Bilgüvar, K. et al. Whole-exome sequencing identifies recessive WDR62 mutations in severe brain malformations. Nature 467, 207-210 (2010).
32. Morris, R. J. et al. Capturing and profiling adult hair follicle stem cells. Nat. Biotechnol. 22, 411-417 (2004). (Pubitemid 38451371)
33. Conboy, M. J., Cerletti, M., Wagers, A. J. & Conboy, I. M. Immuno-analysis and FACS sorting of adult musclefiber-associated stem/precursor cells. Methods Mol. Biol. 621, 165-173 (2010).
34. Park, I. H. et al. Reprogramming of human somatic cells to pluripotency with de-ned factors. Nature 451, 141-146 (2008).
35. Chan, E. M. et al. Live cell imaging distinguishes bonaflde human iPS cells from partially reprogrammed cells. Nat. Biotechnol. 27, 1033-1037 (2009).
36. Zwaka, T. P. & Thomson, J. A. Homologous recombination in human embryonic stem cells. Nat. Biotechnol. 21, 319-321 (2003). (Pubitemid 36314818)
37. Visvader, J. E. & Lindeman, G. J. Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer 8, 755-768 (2008).
38. O'Brien, C. A., Pollett, A., Gallinger, S. & Dick, J. E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445, 106-110 (2007). (Pubitemid 46067310)
39. Pece, S. et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140, 62-73 (2010).
40. Pardal, R., Clarke, M. F. & Morrison, S. J. Applying the principles of stem-cell biology to cancer. Nat. Rev. Cancer 3, 895-902 (2003). (Pubitemid 37500174)
41. Salic, A. & Mitchison, T. J. A chemical method for fast and sensitive detection of DNA synthesis in vivo. Proc. Natl Acad. Sci. USA 105, 2415-2420 (2008). (Pubitemid 351520528)
42. Lorenz, H., Hailey, D. W. & Lippincott-Schwartz, J. Fluorescence protease protection of GFP chimeras to reveal protein topology and subcellular localization. Nat. Methods 3, 205-210 (2006).
43. Eskelinen, E. L., Tanaka, Y. & Saftig, P. At the acidic edge: emerging functions for lysosomal membrane proteins. Trends Cell Biol. 13, 137-145 (2003). (Pubitemid 36293786)
44. Klionsky, D. J. et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-175 (2008). (Pubitemid 351231180)
45. Liang, X. H. et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676 (1999). (Pubitemid 129516338)
46. Sato, K. et al. Autophagy is activated in colorectal cancer cells and contributes to the tolerance to nutrient deprivation. Cancer Res. 67, 9677-9684 (2007). (Pubitemid 47621214)
47. Sarkar, S. et al. A rational mechanism for combination treatment of Huntington's disease using lithium and rapamycin. Hum. Mol. Genet. 17, 170-178 (2008).
48. Sarkar, S. et al. Lithium induces autophagy by inhibiting inositol monophosphatase. J. Cell Biol. 170, 1101-1111 (2005). (Pubitemid 41362642)
49. Mizushima, N. & Yoshimori, T. How to interpret LC3 immunoblotting. Autophagy 3, 542-545 (2007). (Pubitemid 350060049)
50. Bjorkoy, G. et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171, 603-614 (2005). (Pubitemid 41668720)
51. Komatsu, M. et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131, 1149-1163 (2007). (Pubitemid 350235021)
52. Pankiv, S. et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282, 24131-24145 (2007). (Pubitemid 47328003)
53. Kirkin, V. et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol. Cell 27, 505-516 (2009).
54. Waters, S. et al. Interactions with LC3 and polyubiquitin chains link nbr1 to autophagic protein turnover. FEBS Lett. 583, 1846-1852 (2009).
55. Yu, J. et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920 (2007).
56. Engelmann, K., Shen, H. & Finn, O. J. MCF7 side population cells with characteristics of cancer stem/progenitor cells express the tumor antigen MUC1. Cancer Res. 68, 2419-2426 (2008). (Pubitemid 351521817)
57. Zhang, Y. et al. SEPA-1 mediates the specific recognition and degradation of P granule components by autophagy in C. elegans. Cell 136, 308-321 (2009).
58. Strome, S. Specication of the germ line. WormBook 28, 1-10 (2005).
59. Fuchs, E. The tortoise and the hair: slow-cycling cells in the stem cell race. Cell 137, 811-819 (2009).
60. Lamark, T. et al. Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J. Biol. Chem. 278, 34568-34581 (2003). (Pubitemid 37553306)
61. Majeski, A. E. & Dice, J. F. Mechanisms of chaperone-mediated autophagy. Int. J. Biochem. Cell Biol. 36, 2435-2444 (2004). (Pubitemid 39119757)
62. Kaushik, et al. Constitutive activation of chaperone-mediated autophagy in cells with impaired macroautophagy. Mol. Biol. Cell 19, 2179-2192 (2008).
63. Nedelsky, N. et al. Autophagy and the ubiquitin-proteasome system: collaborators in neuroprotection. Biochim. Biophys. Acta. 1782, 691-699 (2008).
64. Xu, P. & Davis, R. J. c-Jun NH2-terminal kinase is required for lineagespecific differentiation but not stem cell self-renewal. Mol. Cell Biol. 30, 1329-1340 (2010).
65. Greenbaum, M. P., Ma, L. & Matzuk, M. M. Conversion of midbodies into germ cell intercellular bridges. Dev. Biol. 305, 389-396 (2007). (Pubitemid 46686608)
66. Mitchison, T., Evans, L., Schulze, E. & Kirschner, M. Sites of microtubule assembly and disassembly in the mitotic spindle. Cell 45, 515-527 (1986). (Pubitemid 16014974)
67. Yu, L. et al. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304, 1500-1502 (2004). (Pubitemid 38720930)
68. Loewer, S. et al. Large intergenic non-coding RNA-RoR modulates reprogramming of human induced pluripotent stem cells. Nat. Genet. 42, 1113-1117 (2010).
69. Yu, J. et al. Human induced pluripotent stem cells free of vector and transgene sequences. Science 324, 797-801 (2009).
70. Sachdev, S., Bu, Y. & Gelman, I. H. Paxillin-Y118 phosphorylation contributes to the control of Src-induced anchorage-independent growth by FAK and adhesion. BMC Cancer 12, 9-12 (2009).