Live free or die: Tales of homeless (cells) in cancer

American Journal of Pathology

Volumn 177, Issue 3, 2010, Pages 1044-1052

  Horbinski, Craig ^a   Mojesky, Colton ^a   Kyprianou, Natasha ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; FLICE INHIBITORY PROTEIN; INTEGRIN; PROTEIN P53;

ANOIKIS; APOPTOSIS; AUTOPHAGY; CANCER CELL; CELL ADHESION; CELL GROWTH; CELL SURVIVAL; EXTRACELLULAR MATRIX; HUMAN; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

EID: 77956538766     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.091270     Document Type: Review

References (87)

1. Frisch SM, Francis H: Disruption of epithelial cell-matrix interactions induces apoptosis. J Cell Biol 1994, 124:619-626
2. Mailleux AA, Overholtzer M, Schmelzle T, Bouillet P, Strasser A, Brugge JS: BIM regulates apoptosis during mammary ductal morphogenesis, and its absence reveals alternative cell death mechanisms. Dev Cell 2007, 12:221-234 (Pubitemid 46172902)
3. Debnath J, Mills KR, Collins NL, Reginato MJ, Muthuswamy SK, Brugge JS: The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 2002, 111:29-40
4. Eisenberg-Lerner A, Bialik S, Simon HU, Kimchi A: Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ 2009, 16:966-975
5. Hotchkiss RS, Strasser A, McDunn JE, Swanson PE: Cell death. N Engl J Med 2009, 361:1570-1583
6. Valmiki MG, Ramos JW: Death effector domain-containing proteins. Cell Mol Life Sci 2009, 66:814-830
7. Thome M, Schneider P, Hofmann K, Fickenscher H, Meinl E, Neipel F, Mattmann C, Burns K, Bodmer JL, Schroter M, Scaffidi C, Krammer PH, Peter ME, Tschopp J: Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 1997, 386:517-521 (Pubitemid 27164081)
8. Micheau O, Tschopp J: Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 2003, 114:181-190 (Pubitemid 36936912)
9. Hill MM, Adrain C, Martin SJ: Portrait of a killer: the mitochondrial apoptosome emerges from the shadows. Mol Interv 2003, 3:19-26
10. Tomita Y, Marchenko N, Erster S, Nemajerova A, Dehner A, Klein C, Pan H, Kessler H, Pancoska P, Moll UM: WT p53, but not tumor-derived mutants, bind to Bcl2 via the DNA binding domain and induce mitochondrial permeabilization. J Biol Chem 2006, 281:8600-8606 (Pubitemid 43847963)
11. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B: PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 2001, 7:673-682 (Pubitemid 32706358)
12. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ: Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001, 292:727-730 (Pubitemid 32385543)
13. Zong WX, Lindsten T, Ross AJ, MacGregor GR, Thompson CB: BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev 2001, 15:1481-1486 (Pubitemid 32552527)
14. Apel A, Zentgraf H, Buchler MW, Herr I: Autophagy-A double-edged sword in oncology. Int J Cancer 2009, 125:991-995
15. Levine B, Klionsky DJ: Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004, 6:463-477 (Pubitemid 38456176)
16. Mizushima N: The pleiotropic role of autophagy: from protein metabolism to bactericide. Cell Death Differ 2005, 12(Suppl 2):1535-1541 (Pubitemid 41553990)
17. Pattingre S, Espert L, Biard-Piechaczyk M, Codogno P: Regulation of macroautophagy by mTOR and Beclin 1 complexes. Biochimie 2008, 90:313-323 (Pubitemid 351181247)
18. Chiarugi P, Giannoni E: Anoikis: a necessary death program for anchorage- dependent cells. Biochem Pharmacol 2008, 76:1352-1364
19. Onder TT, Gupta PB, Mani SA, Yang J, Lander, ES, and Weinberg RA: Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 2008, 68:3645-3654
20. Derksen, .W.B., Liu X, Saridin F, van der Guifden H, Zevenhoven J, Evers B, von Beijnum JR, Griffioen AW, Vink J, Krimpenfont P, Peterse J, Cardiff R, Berns A, and Jonkers J: Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 2006, 10:437-449 (Pubitemid 44693469)
21. Frisch SM, Vuori K, Ruoslathi E, Chan-Hui PY: Control of adhesion-dependent cell survival by focal adhesion kinase. J Cell Biol 1996, 134:793-799 (Pubitemid 26269148)
22. Demers MJ, Thibodeau S, Noel D, Fujita N, Tsuruo T, Gauthier R, Arguin M, Vachon PH: Intestinal epithelial cancer cell anoikis resistance: eGFR-mediated sustained activation of Src overrides Fak-dependent signaling to MEK/Erk and/or PI3-K/Akt-1. J Cell Biochem 2009, 107:639-654
23. Shain KH, Landowski TH, Dalton WS: Adhesion-mediated intracellular redistribution of c-Fas-associated death domain-like IL-1-converting enzyme-like inhibitory protein-long confers resistance to CD95-induced apoptosis in hematopoietic cancer cell lines. J Immunol 2002, 168:2544-2553
24. Orford K, Orford CC, Byers SW: Exogenous expression of β-catenin regulates contact inhibition, anchorage-independent growth, anoikis, and radiation-induced cell cycle arrest. J Cell Biol 1999, 146:855-868 (Pubitemid 29408910)
25. Laguigne LM, Samara RN, Wang W, El-Deiry WS, Corner G, Augenlicht L, Mishra L, Jessup JM: DR5 receptor mediates anoikis in human colorectal carcinoma cell lines Cancer Res 2008, 68:909-917
26. Scaffidi C, Schmitz I, Krammer PH, Peter ME: The role of c-FLIP in modulation of CD95-induced apoptosis. J Biol Chem 1999, 274:1541-1548 (Pubitemid 129507745)
27. Aoudjit F, Vuori K: Matrix attachment regulates Fas-induced apoptosis in endothelial cells: a role for c-flip and implications for anoikis. J Cell Biol 2001, 152:633-643 (Pubitemid 34280244)
28. Simpson CD, Anyiwe K, Schimmer AD: Anoikis resistance and tumor metastasis. Cancer Lett 2008, 272:177-185
29. Mawji IA, Simpson CD, Gronda M, Williams MA, Hurren R, Henderson CJ, Datti A, Wrana JL, Schimmer AD: A chemical screen identifies anisomycin as an anoikis sensitizer that functions by decreasing FLIP protein synthesis. Cancer Res 2007, 67:8307-8315 (Pubitemid 47395169)
30. Kurenova E, Xu, L-H, Yang X, Baldwin AS Jr, Craven RJ, Hanks SK, Liu, ZG, Cance WG: Focal adhesion kinase suppresses apoptosis by binding to the death domain of receptor-interacting protein. Mol Cell Biol 2004, 24:4361-4371 (Pubitemid 41071006)
31. Kamajaran P, Burnek J, Nunez G, Kaplla YL: Receptor-interacting protein shuttles between cell death and survival signaling pathways. Mol Biol Cell 2010, 3:481-488
32. Tsuji T, Ibaragi S, Hu GF: Epithelial-mesenchymal transition and cell cooperativity in metastasis. Cancer Res 2009, 69:7135-7139
33. Zhu ML, Kyprianou N: Role of androgens and the androgen receptor in epithelial-mesenchymal transition and invasion of prostate cancer cells. FASEB J 2010, 24:769-777
34. Rohwer N, Welzel M, Daskalow K, Pfander D, Wiedenmann B, Detjen K, Cramer T: Hypoxia-inducible factor 1αmediates anoikis resistance via suppression of α5 integrin. Cancer Res 2008, 68:10113-10120
35. Lee GY, Kenny PA, Lee EH, Bissell MJ: Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods 2007, 4:359-365 (Pubitemid 46766981)
36. Fournier MV, Fata JE, Martin KJ, Yaswen P, Bissell MJ: Interaction of E-cadherin and PTEN regulates morphogenesis and growth arrest in human mammary epithelial cells. Cancer Res 2009, 69:4545-4552
37. Fung C, Lock R, Gao S, Salas E, Debnath J: Induction of autophagy during extracellular matrix detachment promotes cell survival. Mol Biol Cell 2008, 19:797-806 (Pubitemid 351481798)
38. Mills KR, Reginato M, Debnath J, Queenan B, Brugge JS: Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is required for induction of autophagy during lumen formation in vitro. Proc Natl Acad Sci USA 2004, 101:3438-3443 (Pubitemid 38338213)
39. Debnath J, Baehrecke EH, Kroemer G: Does autophagy contribute to cell death?. Autophagy 2005, 1:66-74
40. Sinha S, Levine B: The autophagy effector Beclin 1: a novel BH3-only protein, Oncogene 2008, 27(Suppl 1):S137-S148
41. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B: Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939 (Pubitemid 41345209)
42. L). Autophagy 2007, 3:374-376
43. Luo S, Rubinsztein DC: Apoptosis blocks Beclin 1-dependent autophagosome synthesis: an effect rescued by Bcl-xL. Cell Death Differ 2010, 17:268-277
44. Li AE, Ito H, Rovira II, Kim KS, Takeda K, Yu ZY, Ferrans VJ, Finkel T: A role for reactive oxygen species in endothelial cell anoikis. Circ Res 1999, 85:304-310 (Pubitemid 29398862)
45. Giannoni E, Buricchi F, Grimaldi G, Parri M, Cialdai F, Taddei ML, Raugei G, Ramponi G, Chiarugi P: Redox regulation of anoikis: reactive oxygen species as essential mediators of cell survival. Cell Death Differ 2008, 15:867-878 (Pubitemid 351524429)
46. Giannoni E, Fiaschi T, Ramponi G, Chiarugi P: Redox regulation of anoikis resistance of metastatic prostate cancer cells: key role for Src and EGFR-mediated pro-survival signals. Oncogene 2009, 28:2074-2086
47. Edick MJ, Tesfay L, Lamb LE, Knudsen BS, Miranti CK: Inhibition of integrin-mediated crosstalk with epidermal growth factor receptor/Erk or Src signaling pathways in autophagic prostate epithelial cells induces caspase-independent death. Mol Biol Cell 2007, 18:2481-2490 (Pubitemid 47025714)
48. Schafer ZT, Grassian AR, Song L, Jiang Z, Gerhart-Hines Z, Irie HY, Gao S, Puigserver P, Brugge JS: Antioxidant and oncogene rescue of metabolic defects caused by loss of matrix attachment. Nature 2009, 461:109-113
49. Reginato MJ, Mills KR, Paulus JK, Lynch DK, Sgroi DC, Debnath J, Muthuswamy SK, Brugge JS: Integrins and EGFR coordinately regulate the pro-apoptotic protein Bim to prevent anoikis. Nat Cell Biol 2003, 5:733-740 (Pubitemid 36986781)
50. Wang X, Lin G, Martins-Taylor K, Zeng H, Xu RH: Inhibition of caspase-mediated anoikis is critical for bFGF-sustained culture of human pluripotent stem cells. J Biol Chem 2009, 284:34054-34064
51. Neiva KG, Zhang Z, Miyazawa M, Warner KA, Karl E, Nor JE: Cross talk initiated by endothelial cells enhances migration and inhibits anoikis of squamous cell carcinoma cells through STAT3/Akt/ERK signaling. Neoplasia 2009, 11:583-593
52. Rul W, Zugasti O, Roux P, Peyssonnaux C, Eychene A, Franke TF, Lenormand P, Fort P, Hibner U: Activation of ERK, controlled by Rac1 and Cdc42 via Akt, is required for anoikis. Ann NY Acad Sci 2002, 973:145-148 (Pubitemid 36124995)
53. Ma L, Chen Z, Erdjument-Bromage H, Tempst P, Pandolfi PP: Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis. Cell 2005, 121:179-193 (Pubitemid 40546387)
54. Roux PP, Ballif BA, Anjum R, Gygi SP, Blenis J: Tumor-promoting phorbol esters and activated Ras inactivate the tuberous sclerosis tumor suppressor complex via p90 ribosomal S6 kinase. Proc Natl Acad Sci USA 2004, 101:13489-13494 (Pubitemid 39238430)
55. Wang J, Whiteman MW, Lian H, Wang G, Singh A, Huang D, Denmark T: A non-canonical MEK/ERK signaling pathway regulates autophagy via regulating Beclin 1. J Biol Chem 2009, 284:21412-21424
56. Horbinski C, Chu CT: Kinase signaling cascades in the mitochondrion: a matter of life or death. Free Radic Biol Med 2005, 38:2-11 (Pubitemid 39626903)
57. Kulich SM, Chu CT: Sustained extracellular signal-regulated kinase activation by 6-hydroxydopamine: implications for Parkinson's disease. J Neurochem 2001, 77:1058-1066 (Pubitemid 32467060)
58. Kulich SM, Horbinski C, Patel M, Chu CT: 6-Hydroxydopamine induces mitochondrial ERK activation. Free Radic Biol Med 2007, 43:372-383 (Pubitemid 46977632)
59. Cheng H, Liu P, Wang ZC, Zou L, Santiago S, Garbitt V, Gjoerup OV, Iglehart JD, Miron A, Richardson AL, Hahn WC, and Zhao JJ: SIK1 couples LKB1 to p53-depedent anoikis and suppresses metastasis. Sci Signal 2009, 2:35-40
60. Zhang Y, Lu H, Dazin P, Kapila Y: Squamous cell carcinoma cell aggregates escape suspension-induced, p53-mediated anoikis: fibronectin and integrin αv mediate survival signals through focal adhesion kinase. J Biol Chem 2004, 279:48342-48349 (Pubitemid 39540990)
61. Feng Z, Zhang H, Levine AJ, Jin S: The coordinate regulation of the p53 and mTOR pathways in cells. Proc Natl Acad Sci USA 2005, 102:8204-8209 (Pubitemid 40800067)
62. Tasdemir E, Maiuri MC, Galluzzi L, Vitale I, Djavaheri-Mergny M, D'Amelio M, Criollo A, Morselli E, Zhu C, Harper F, Nannmark U, Samara C, Pinton P, Vicencio JM, Carnuccio R, Moll UM, Madeo F, Paterlini-Brechot P, Rizzuto R, Szabadkai G, Pierron G, Blomgren K, Tavernarakis N, Codogno P, Cecconi F, Kroemer G: Regulation of autophagy by cytoplasmic p53. Nat Cell Biol 2008, 10:676-687
63. Bialik S, Kimchi A: The death-associated protein kinases: structure, function, and beyond. Annu Rev Biochem 2006, 75:189-210 (Pubitemid 44118031)
64. Chen CH, Wang WJ, Kuo JC, Tsai HC, Lin JR, Chang ZF, Chen RH: Bidirectional signals transduced by DAPK-ERK interaction promote the apoptotic effect of DAPK. EMBO J 2005, 24:294-304
65. Wang WJ, Kuo JC, Yao CC, Chen RH: DAP-kinase induces apoptosis by suppressing integrin activity and disrupting matrix survival signals. J Cell Biol 2002, 159:169-179
66. Gozuacik D, Bialik S, Raveh T, Mitou G, Shohat G, Sabanay H, Mizushima N, Yoshimori T, Kimchi A: DAP-kinase is a mediator of endoplasmic reticulum stress-induced caspase activation and autophagic cell death. Cell Death Differ 2008, 15:1875-1886
67. 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 2002, 157:455-468 (Pubitemid 34839809)
68. Zalckvar E, Berissi H, Eisenstein M, Kimchi A: Phosphorylation of Beclin 1 by DAP-kinase promotes autophagy by weakening its interactions with Bcl-2 and Bcl-XL. Autophagy 2009, 5:720-722
69. Zalckvar E, Berissi H, Mizrachy L, Idelchuk Y, Koren I, Eisenstein M, Sabanay H, Pinkas-Kramarski R, Kimchi A: DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO Rep 2009, 10:285-292
70. Stevens C, Lin Y, Harrison B, Burch L, Ridgway RA, Sansom O, Hupp T: Peptide combinatorial libraries identify TSC2 as a death-associated protein kinase (DAPK) death domain-binding protein and reveal a stimulatory role for DAPK in mTORC1 signaling. J Biol Chem 2009, 284:334-344
71. Li H, Ray G, Yoo BH, Erdogan M, Rosen KV: Down-regulation of death-associated protein kinase-2 is required for β-catenin-induced anoikis resistance of malignant epithelial cells. J Biol Chem 2009, 284:2012-2022
72. Sasnauskiene A, Kadziauskas J, Vezelyte N, Jonusiene V, Kirveliene V: Apoptosis, autophagy and cell cycle arrest following photodamage to mitochondrial interior. Apoptosis 2009, 14:276-286
73. Rodríguez-Hernández A, Cordero MD, Salviati L, Artuch R, Pineda M, Briones P, Gomez Izquierdo L, Cotan D, Navas P, Sanchez-Alcazar JA: Coenzyme Q deficiency triggers mitochondria degradation by mitophagy. Autophagy 2009, 5:19-32
74. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B: Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999, 402:672-676 (Pubitemid 129516338)
75. Qu X, Yu J, Bhagat G, Furuya N, Hibshoosh H, Troxel A, Rosen J, Eskelinen EL, Mizushima N, Ohsumi Y, Cattoretti G, Levine B: Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 2003, 112:1809-1820 (Pubitemid 38063704)
76. 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 USA 2003, 100: 15077-15082 (Pubitemid 37518019)
77. Mathew R, Karp CM, Beaudoin B, Vuong N, Chen G, Chen HY, Bray K, Reddy A, Bhanot G, Gelinas C, Dipaola RS, Karantza-Wadsworth V, White E: Autophagy suppresses tumorigenesis through elimination of p62. Cell 2009, 137:1062-1075
78. Mathew R, Kongara S, Beaudoin B, Karp CM, Bray K, Degenhardt K, Chen G, Jin S, White E: Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev 2007, 21:1367-1381 (Pubitemid 46871040)
79. Moscat J, Diaz-Meco MT: p62 at the crossroads of autophagy, apoptosis, and cancer. Cell 2009, 137:1001-1004
80. Yoo BH, Wu X, Li Y, Haniff M, Sasazuki T, Shirasawa S, Eskelinen EL, Rosen KV: Oncogenic ras-induced downregulation of autophagy mediator Beclin-1 is required for malignant transformation of intestinal epithelial cells. J Biol Chem 2010, 285:5438-5449
81. Carew JS, Medina EC, Esquivel JA 2nd, Mahalingam D, Swords R, Kelly K, Zhang H, Huang P, Mita AC, Mita MM, Giles FJ, Nawrocki ST: Autophagy inhibition enhances vorinostat-induced apoptosis via ubiquitinated protein accumulation. J Cell Mol Med 2009, doi: 10.1111/j.1582- 4934.2009.00832.x
82. Bijnsdorp IV, Peters GJ, Temmink OH, Fukushima M, Kruyt FA: Differential activation of cell death and autophagy results in an increased cytotoxic potential for trifluorothymidine compared to 5-fluorouracil in colon cancer cells. Int J Cancer 2010, 126:2457-2468
83. Lomonaco SL, Finniss S, Xiang C, Decarvalho A, Umansky F, Kalkanis SN, Mikkelsen T, Brodie C: The induction of autophagy by gamma-radiation contributes to the radioresistance of glioma stem cells. Int J Cancer 2009, 125:717-722
84. Yoo BH, Wu X, Derouet M, Haniff M, Eskelinen EL, Rosen K: Hypoxia-induced downregulation of autophagy mediator beclin 1 reduces the susceptibility of malignant intestinal epithelial cells to hypoxia-dependent apoptosis. Autophagy 2009, 5:1166-1179
85. Kiyono K, Suzuki HI, Matsuyama H, Morishita Y, Komuro A, Kano MR, Sugimoto K, Miyazono K: Autophagy Is activated by TGF-β and potentiates TGF-β-mediated growth inhibition in human hepatocellular carcinoma cells. Cancer Res 2009, 69:8844-8852
86. Sun Y, Zhang J, Peng ZL: Beclin1 induces autophagy and its potential contributions to sensitizes SiHa cells to carboplatin therapy. Int J Gynecol Cancer 2009, 19:772-776
87. Sakamoto S, McCann RO, Dhir, R. and Kyprianou N: Talin1 promotes tumor invasion and metastasis via focal adhesion signaling and anoikis resistance. Cancer Res 2010, 70:1885-1895