Removal of the BH4 domain from Bcl-2 protein triggers an autophagic process that impairs tumor growth

Neoplasia (United States)

Volumn 15, Issue 3, 2013, Pages 315-327

  Trisciuoglio, Daniela ^a   de Luca, Teresa ^a   Desideri, Marianna ^a   Passeri, Daniela ^b   Gabellini, Chiara ^a   Scarpino, Stefania ^c   Liang, Chengyu ^d   Orlandi, Augusto ^b   Del Bufalo, Donatella ^a  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BECLIN 1; ENHANCED GREEN FLUORESCENT PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN P62;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BH4 DOMAIN; CARCINOGENICITY; CELL PROLIFERATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE DELETION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MELANOMA; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRUCTURAL HOMOLOGY; TUMOR GROWTH; TUMOR XENOGRAFT; WESTERN BLOTTING;

EID: 84874589230     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.121392     Document Type: Article

References (40)

1. Vairo G, Soos TJ, Upton TM, Zalvide J, DeCaprio JA, Ewen ME, Koff A, and Adams JM (2000). Bcl-2 retards cell cycle entry through p27Kip1, pRB relative p130, and altered E2F regulation. Mol Cell Biol 20, 4745-4753.
2. Furth PA, Bar-Peled U, Li M, Lewis A, Laucirica R, Jager R, Weiher H, and Russell RG (1999). Loss of anti-mitotic effects of Bcl-2 with retention of antiapoptotic activity during tumor progression in a mouse model. Oncogene 18, 6589-6596.
3. Huang DC, O'Reilly LA, Strasser A, and Cory S (1997). The anti-apoptosis function of Bcl-2 can be genetically separated from its inhibitory effect on cell cycle entry. EMBO J 16, 4628-4638.
4. Ricca A, Biroccio A, Del Bufalo D, Mackay AR, Santoni A, and Cippitelli M (2000). Bcl-2 over-expression enhances NF-κB activity and induces mmp-9 transcription in human MCF7ADR breast-cancer cells. Int J Cancer 86, 188-196.
5. Trisciuoglio D, Desideri M, Ciuffreda L, Mottolese M, Ribatti D, Vacca A, Del Rosso M, Marcocci L, Zupi G, and Del Bufalo D (2005). Bcl-2 overexpression in melanoma cells increases tumor progression-associated properties and in vivo tumor growth. J Cell Physiol 205, 414-421.
6. Biroccio A, Candiloro A, Mottolese M, Sapora O, Albini A, Zupi G, and Del Bufalo D (2000). Bcl-2 overexpression and hypoxia synergistically act to modulate vascular endothelial growth factor expression and in vivo angiogenesis in a breast carcinoma line. FASEB J 14, 652-660.
7. Del Bufalo D, Trisciuoglio D, Scarsella M, Zangemeister-Wittke U, and Zupi G (2003). Treatment of melanoma cells with a bcl-2/bcl-xL antisense oligonucleotide induces antiangiogenic activity. Oncogene 22, 8441-8447.
8. Giorgini S, Trisciuoglio D, Gabellini C, Desideri M, Castellini L, Colarossi C, Zangemeister-Wittke U, Zupi G, and Del Bufalo D (2007). Modulation of bcl-xL in tumor cells regulates angiogenesis through CXCL8 expression. Mol Cancer Res 5, 761-771.
9. Iervolino A, Trisciuoglio D, Ribatti D, Candiloro A, Biroccio A, Zupi G, and Del Bufalo D (2002). Bcl-2 overexpression in human melanoma cells increases angiogenesis through VEGF mRNA stabilization and HIF-1-mediated transcriptional activity. FASEB J 16, 1453-1455.
10. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, and Levine B (2005). Bcl-2 antiapoptotic proteins inhibit beclin 1-dependent autophagy. Cell 122, 927-939.
11. He C and Klionsky DJ (2009). Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43, 67-93.
12. Komatsu Mand Ichimura Y (2010). Physiological significance of selective degradation of p62 by autophagy. FEBS Lett 584, 1374-1378.
13. Edinger AL and Thompson CB (2003). Defective autophagy leads to cancer. Cancer Cell 4, 422-424.
14. Akar U, Chaves-Reyez A, Barria M, Tari A, Sanguino A, Kondo Y, Kondo S, Arun B, Lopez-Berestein G, and Ozpolat B (2008). Silencing of Bcl-2 expression by small interfering RNA induces autophagic cell death in MCF-7 breast cancer cells. Autophagy 4, 669-679.
15. Gao P, Bauvy C, Souquere S, Tonelli G, Liu L, Zhu Y, Qiao Z, Bakula D, Proikas-Cezanne T, Pierron G, et al. (2010). The Bcl-2 homology domain 3 mimetic gossypol induces both Beclin 1-dependent and Beclin 1-independent cytoprotective autophagy in cancer cells. J Biol Chem 285, 25570-25581.
16. Cheng EH, Kirsch DG, Clem RJ, Ravi R, Kastan MB, Bedi A, Ueno K, and Hardwick JM (1997). Conversion of bcl-2 to a bax-like death effector by caspases. Science 278, 1966-1968.
17. Trisciuoglio D, Gabellini C, Desideri M, Ragazzoni Y, De Luca T, Ziparo E, and Del Bufalo D (2011). Involvement of BH4 domain of bcl-2 in the regulation of HIF-1-mediated VEGF expression in hypoxic tumor cells. Cell Death Differ 18, 1024-1035.
18. Trisciuoglio D, Ragazzoni Y, Pelosi A, Desideri M, Carradori S, Gabellini C, Maresca G, Nescatelli R, Secci D, Bolasco A, et al. (2012). CPTH6, a thiazole derivative, induces histone hypoacetylation and apoptosis in human leukemia cells. Clin Cancer Res 18, 475-486.
19. Martens S, Parvanova I, Zerrahn J, Griffiths G, Schell G, Reichmann G, and Howard JC (2005). Disruption of toxoplasma gondii parasitophorous vacuoles by the mouse p47-resistance GTPases. PLoS Pathog 1, e24.
20. Del Bufalo D, Trisciuoglio D, Biroccio A, Marcocci L, Buglioni S, Candiloro A, Scarsella M, Leonetti C, and Zupi G (2001). Bcl-2 overexpression decreases BCNU sensitivity of a human glioblastoma line through enhancement of catalase activity. J Cell Biochem 83, 473-483.
21. Del Bufalo D, Rizzo A, Trisciuoglio D, Cardinali G, Torrisi MR, Zangemeister-Wittke U, Zupi G, and Biroccio A (2005). Involvement of hTERT in apoptosis induced by interference with Bcl-2 expression and function. Cell Death Differ 12, 1429-1438.
22. Trisciuoglio D, Gabellini C, Desideri M, Ziparo E, Zupi G, and Del Bufalo D (2010). Bcl-2 regulates HIF-1α protein stabilization in hypoxic melanoma cells via the molecular chaperone HSP90. PLoS One 5, e11772.
23. Marcellini M, De Luca N, Riccioni T, Ciucci A, Orecchia A, Lacal PM, Ruffini F, Pesce M, Cianfarani F, Zambruno G, et al. (2006). Increased melanoma growth and metastasis spreading in mice overexpressing placenta growth factor. Am J Pathol 169, 643-654.
24. Ciuffreda L, Di Sanza C, Cesta Incani U, Eramo A, Desideri M, Biagioni F, Passeri D, Falcone I, Sette G, Bergamo P, et al. (2012). The mitogen-activated protein kinase (MAPK) cascade controls phosphatase and tensin homolog (PTEN) expression through multiple mechanisms. J Mol Med (Berl) 90, 667-679.
25. Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, and Levine B (1999). Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 402, 672-676.
26. Saeki K, Yuo A, Okuma E, Yazaki Y, Susin SA, Kroemer G, and Takaku F (2000). Bcl-2 down-regulation causes autophagy in a caspase-independent manner in human leukemic HL60 cells. Cell Death Differ 7, 1263-1269.
27. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, and Tsien RY (2002). A monomeric red fluorescent protein. Proc Natl Acad Sci USA 99, 7877-7882.
28. Chen Q, Gong B, and Almasan A (2000). Distinct stages of cytochrome c release from mitochondria: evidence for a feedback amplification loop linking caspase activation to mitochondrial dysfunction in genotoxic stress induced apoptosis. Cell Death Differ 7, 227-233.
29. Oh S, Xiaofei E, Ni D, Pirooz SD, Lee JY, Lee D, Zhao Z, Lee S, Lee H, Ku B, et al. (2011). Downregulation of autophagy by Bcl-2 promotes MCF7 breast cancer cell growth independent of its inhibition of apoptosis. Cell Death Differ 18, 452-464.
30. Hirotani M, Zhang Y, Fujita N, Naito M, and Tsuruo T (1999). NH2-terminal BH4 domain of Bcl-2 is functional for heterodimerization with bax and inhibition of apoptosis. J Biol Chem 274, 20415-20420.
31. Zhang Z, Lapolla SM, Annis MG, Truscott M, Roberts GJ, Miao Y, Shao Y, Tan C, Peng J, Johnson AE, et al. (2004). Bcl-2 homodimerization involves two distinct binding surfaces, a topographic arrangement that provides an effective mechanism for Bcl-2 to capture activated bax. J Biol Chem 279, 43920-43928.
32. Cheng EH, Levine B, Boise LH, Thompson CB, and Hardwick JM (1996). Bax-independent inhibition of apoptosis by Bcl-XL. Nature 379, 554-556.
33. Erlich S, Mizrachy L, Segev O, Lindenboim L, Zmira O, Adi-Harel S, Hirsch JA, Stein R, and Pinkas-Kramarski R (2007). Differential interactions between Beclin 1 and Bcl-2 family members. Autophagy 3, 561-568.
34. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, Tasdemir E, Pierron G, Troulinaki K, Tavernarakis N, et al. (2007). Functional and physical interaction between Bcl-XL and a BH3-like domain in Beclin-1. EMBO J 26, 2527-2539.
35. Wei Y, Pattingre S, Sinha S, Bassik M, and Levine B (2008). JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell 30, 678-688.
36. Zhang J and Ney PA (2009). Role of BNIP3 and NIX in cell death, autophagy, and mitophagy. Cell Death Differ 16, 939-946.
37. Zalckvar E, Berissi H, Eisenstein M, and Kimchi A (2009). Phosphorylation of Beclin 1 by DAP-kinase promotes autophagy by weakening its interactions with Bcl-2 and Bcl-XL. Autophagy 5, 720-722.
38. Hallin U, Kondo E, Ozaki Y, Hagberg H, Shibasaki F, and Blomgren K (2006). Bcl-2 phosphorylation in the BH4 domain precedes caspase-3 activation and cell death after neonatal cerebral hypoxic-ischemic injury. Neurobiol Dis 21, 478-486.
39. Wang S, Wang Z, Boise L, Dent P, and Grant S (1999). Loss of the bcl-2 phosphorylation loop domain increases resistance of human leukemia cells (U937) to paclitaxel-mediated mitochondrial dysfunction and apoptosis. Biochem Biophys Res Commun 259, 67-72.
40. Pathan N, Aime-Sempe C, Kitada S, Basu A, Haldar S, and Reed JC (2001). Microtubule-targeting drugs induce bcl-2 phosphorylation and association with Pin1. Neoplasia 3, 550-559.