PARP inhibitor ABT-888 affects response of MDA-MB-231 cells to doxorubicin treatment, targeting Snail expression

Oncotarget

Volumn 6, Issue 17, 2015, Pages 15008-15021

  Mariano, Germano ^a   Ricciardi, Maria Rosaria ^a   Trisciuoglio, Daniela ^b   Zampieri, Michele ^a,c   Ciccarone, Fabio ^a,c   Guastafierro, Tiziana ^a,c   Calabrese, Roberta ^a,c   Valentini, Elisabetta ^a   Tafuri, Agostino ^a   Del Bufalo, Donatella ^b   Caiafa, Paola ^a,c   Reale, Anna ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^c Pasteur Institute   (Italy)

Author keywords

Breast cancer; Chemoresistance; PARP inhibitors; Snail

Indexed keywords

ANTINEOPLASTIC ANTIBIOTIC; BENZIMIDAZOLE DERIVATIVE; DOXORUBICIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; ITPR1 PROTEIN, HUMAN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PARP1 PROTEIN, HUMAN; PROTEIN BINDING; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SNAIL; VELIPARIB;

APOPTOSIS; BREAST TUMOR; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MCF-7 CELL LINE; METABOLISM; PATHOLOGY; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; BENZIMIDAZOLES; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; DOXORUBICIN; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MCF-7 CELLS; POLY (ADP-RIBOSE) POLYMERASE-1; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; POLY(ADP-RIBOSE) POLYMERASES; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS;

EID: 84934270574     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3634     Document Type: Article

References (73)

1. Rebucci M, Michiels C. Molecular aspects of cancer cell resistance to chemotherapy. Biochemical pharmacology. 2013; 85:1219-1226.
2. Videira M, Reis RL, Brito MA. Deconstructing breast cancer cell biology and the mechanisms of multidrug resistance. Biochimica et biophysica acta. 2014; 1846:312-325.
3. Chen DR, Lu DY, Lin HY, Yeh WL. Mesenchymal stem cell-induced doxorubicin resistance in triple negative breast cancer. BioMed research international. 2014; 2014:532161.
4. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelialmesenchymal transitions in development and disease. Cell. 2009; 139:871-890.
5. de Herreros AG, Peiro S, Nassour M, Savagner P. Snail family regulation and epithelial mesenchymal transitions in breast cancer progression. Journal of mammary gland biology and neoplasia. 2010; 15:135-147.
6. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nature reviews. 2007; 7:415-428.
7. Nieto MA. Epithelial-Mesenchymal Transitions in development and disease: old views and new perspectives. The International journal of developmental biology. 2009; 53:1541-1547.
8. Barrallo-Gimeno A, Nieto MA. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development (Cambridge, England). 2005; 132:3151-3161.
9. Olmeda D, Jorda M, Peinado H, Fabra A, Cano A. Snail silencing effectively suppresses tumour growth and invasiveness. Oncogene. 2007; 26:1862-1874.
10. Olmeda D, Montes A, Moreno-Bueno G, Flores JM, Portillo F, Cano A. Snai1 and Snai2 collaborate on tumor growth and metastasis properties of mouse skin carcinoma cell lines. Oncogene. 2008; 27:4690-4701.
11. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nature reviews. 2009; 9:265-273.
12. Yilmaz M, Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer metastasis reviews. 2009; 28:15-33.
13. Nieto MA. The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol. 2002; 3:155-166.
14. Kajita M, McClinic KN, Wade PA. Aberrant expression of the transcription factors snail and slug alters the response to genotoxic stress. Molecular and cellular biology. 2004; 24:7559-7566.
15. Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY, Bapat SA. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem cells (Dayton, Ohio). 2009; 27:2059-2068.
16. Moody SE, Perez D, Pan TC, Sarkisian CJ, Portocarrero CP, Sterner CJ, Notorfrancesco KL, Cardiff RD, Chodosh LA. The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer cell. 2005; 8:197-209.
17. Vega S, Morales AV, Ocana OH, Valdes F, Fabregat I, Nieto MA. Snail blocks the cell cycle and confers resistance to cell death. Genes & development. 2004; 18:1131-1143.
18. Roy HK, Iversen P, Hart J, Liu Y, Koetsier JL, Kim Y, Kunte DP, Madugula M, Backman V, Wali RK. Downregulation of SNAIL suppresses MIN mouse tumorigenesis: modulation of apoptosis, proliferation, and fractal dimension. Molecular cancer therapeutics. 2004; 3:1159-1165.
19. Poser I, Dominguez D, de Herreros AG, Varnai A, Buettner R, Bosserhoff AK. Loss of E-cadherin expression in melanoma cells involves up-regulation of the transcriptional repressor Snail. The Journal of biological chemistry. 2001; 276:24661-24666.
20. Wu Y, Zhou BP. Snail: More than EMT. Cell adhesion & migration. 2010; 4:199-203.
21. Escriva M, Peiro S, Herranz N, Villagrasa P, Dave N, Montserrat-Sentis B, Murray SA, Franci C, Gridley T, Virtanen I, Garcia de Herreros A. Repression of PTEN phosphatase by Snail1 transcriptional factor during gamma radiation-induced apoptosis. Molecular and cellular biology. 2008; 28:1528-1540.
22. Zheng H, Kang Y. Multilayer control of the EMT master regulators. Oncogene. 2013; 33:1755-1763.
23. Peiro S, Escriva M, Puig I, Barbera MJ, Dave N, Herranz N, Larriba MJ, Takkunen M, Franci C, Munoz A, Virtanen I, Baulida J, Garcia de Herreros A. Snail1 transcriptional repressor binds to its own promoter and controls its expression. Nucleic acids research. 2006; 34:2077-2084.
24. Rodriguez MI, Gonzalez-Flores A, Dantzer F, Collard J, de Herreros AG, Oliver FJ. Poly(ADP-ribose)-dependent regulation of Snail1 protein stability. Oncogene. 2011; 30:4365-4372.
25. Yang Z, Rayala S, Nguyen D, Vadlamudi RK, Chen S, Kumar R. Pak1 phosphorylation of snail, a master regulator of epithelial-to-mesenchyme transition, modulates snail's subcellular localization and functions. Cancer research. 2005; 65:3179-3184.
26. Wang Y, Shi J, Chai K, Ying X, Zhou BP. The Role of Snail in EMT and Tumorigenesis. Current cancer drug targets. 2013; 13:963-972.
27. McPhee TR, McDonald PC, Oloumi A, Dedhar S. Integrinlinked kinase regulates E-cadherin expression through PARP-1. Dev Dyn. 2008; 237:2737-2747.
28. Chu S, Xu H, Ferro TJ, Rivera PX. Poly(ADP-ribose) polymerase-1 regulates vimentin expression in lung cancer cells. American journal of physiology. 2007; 293:L1127-1134.
29. Lonn P, van der Heide LP, Dahl M, Hellman U, Heldin CH, Moustakas A. PARP-1 attenuates Smad-mediated transcription. Molecular cell. 2010; 40:521-532.
30. Pu H, Horbinski C, Hensley PJ, Matuszak EA, Atkinson T, Kyprianou N. PARP-1 regulates epithelial-mesenchymal transition (EMT) in prostate tumorigenesis. Carcinogenesis. 2014; 35:2592-2601.
31. Rodriguez MI, Peralta-Leal A, O'Valle F, Rodriguez-Vargas JM, Gonzalez-Flores A, Majuelos-Melguizo J, Lopez L, Serrano S, de Herreros AG, Rodriguez-Manzaneque JC, Fernandez R, Del Moral RG, de Almodovar JM, Oliver FJ. PARP-1 regulates metastatic melanoma through modulation of vimentin-induced malignant transformation. PLoS genetics. 2013; 9:e1003531.
32. D'Amours D, Desnoyers S, D'Silva I, Poirier GG. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. The Biochemical journal. 1999; 342:249-268.
33. Krishnakumar R, Kraus WL. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Molecular cell. 2010; 39:8-24.
34. Ryu KW, Kim DS, Kraus WL. New Facets in the Regulation of Gene Expression by ADP-Ribosylation and Poly(ADP-ribose) Polymerases. Chemical reviews. 2015.
35. Kraus WL. Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Current opinion in cell biology. 2008; 20:294-302.
36. Reale A, Matteis GD, Galleazzi G, Zampieri M, Caiafa P. Modulation of DNMT1 activity by ADP-ribose polymers. Oncogene. 2005; 24:13-19.
37. Tulin A, Chinenov Y, Spradling A. Regulation of chromatin structure and gene activity by poly(ADP-ribose) polymerases. Current topics in developmental biology. 2003; 56:55-83.
38. Zampieri M, Passananti C, Calabrese R, Perilli M, Corbi N, De Cave F, Guastafierro T, Bacalini MG, Reale A, Amicosante G, Calabrese L, Zlatanova J, Caiafa P. Parp1 localizes within the Dnmt1 promoter and protects its unmethylated state by its enzymatic activity. PloS one. 2009; 4:e4717.
39. Zardo G, Reale A, De Matteis G, Buontempo S, Caiafa P. A role for poly(ADP-ribosyl)ation in DNA methylation. Biochemistry and cell biology = Biochimie et biologie cellulaire. 2003; 81:197-208.
40. Bacalini MG, Di Lonardo D, Catizone A, Ciccarone F, Bruno T, Zampieri M, Guastafierro T, Calabrese R, Fanciulli M, Passananti C, Caiafa P, Reale A. Poly(ADPribosyl) ation affects stabilization of Che-1 protein in response to DNA damage. DNA repair. 2011; 10:380-389.
41. Schreiber V, Dantzer F, Ame JC, de Murcia G. Poly(ADPribose): novel functions for an old molecule. Nat Rev Mol Cell Biol. 2006; 7:517-528.
42. Aredia F, Scovassi AI. Poly(ADP-ribose): A signaling molecule in different paradigms of cell death. Biochemical pharmacology. 2014.
43. Burkle A, Virag L. Poly(ADP-ribose): PARadigms and PARadoxes. Molecular aspects of medicine. 2012; 34:1046-1065.
44. Chevanne M, Zampieri M, Caldini R, Rizzo A, Ciccarone F, Catizone A, D'Angelo C, Guastafierro T, Biroccio A, Reale A, Zupi G, Caiafa P. Inhibition of PARP activity by PJ-34 leads to growth impairment and cell death associated with aberrant mitotic pattern and nucleolar actin accumulation in M14 melanoma cell line. Journal of cellular physiology. 2010; 222:401-410.
45. Masutani M, Fujimori H. Poly(ADP-ribosyl)ation in carcinogenesis. Molecular aspects of medicine. 2013; 34:1202-1216.
46. Weaver AN, Yang ES. Beyond DNA Repair: Additional Functions of PARP-1 in Cancer. Frontiers in oncology. 2013; 3:290.
47. Audeh MW, Carmichael J, Penson RT, Friedlander M, Powell B, Bell-McGuinn KM, Scott C, Weitzel JN, Oaknin A, Loman N, Lu K, Schmutzler RK, Matulonis U, Wickens M, Tutt A. Oral poly(ADP-ribose) polymerase inhibitor olaparib in patients with BRCA1 or BRCA2 mutations and recurrent ovarian cancer: a proof-of-concept trial. Lancet. 2003; 376:245-251.
48. Benafif S, Hall M. An update on PARP inhibitors for the treatment of cancer. OncoTargets and therapy. 2015; 8:519-528.
49. Ibrahim YH, Garcia-Garcia C, Serra V, He L, Torres-Lockhart K, Prat A, Anton P, Cozar P, Guzman M, Grueso J, Rodriguez O, Calvo MT, Aura C, Diez O, Rubio IT, Perez J, et al. PI3K inhibition impairs BRCA1/2 expression and sensitizes BRCA-proficient triple-negative breast cancer to PARP inhibition. Cancer discovery. 2012; 2:1036-1047.
50. Kummar S, Ji J, Morgan R, Lenz HJ, Puhalla SL, Belani CP, Gandara DR, Allen D, Kiesel B, Beumer JH, Newman EM, Rubinstein L, Chen A, Zhang Y, Wang L, Kinders RJ, et al. A phase I study of veliparib in combination with metronomic cyclophosphamide in adults with refractory solid tumors and lymphomas. Clin Cancer Res. 2003; 18:1726-1734.
51. Lord CJ, Ashworth A. Targeted therapy for cancer using PARP inhibitors. Current opinion in pharmacology. 2008; 8:363-369.
52. Yap TA, Sandhu SK, Carden CP, de Bono JS. Poly(ADPribose) polymerase (PARP) inhibitors: Exploiting a synthetic lethal strategy in the clinic. CA: a cancer journal for clinicians. 2011; 61:31-49.
53. Chuang HC, Kapuriya N, Kulp SK, Chen CS, Shapiro CL. Differential anti-proliferative activities of poly(ADP-ribose) polymerase (PARP) inhibitors in triple-negative breast cancer cells. Breast cancer research and treatment. 2012; 134:649-659.
54. Mason KA, Valdecanas D, Hunter NR, Milas L. INO-1001, a novel inhibitor of poly(ADP-ribose) polymerase, enhances tumor response to doxorubicin. Investigational new drugs. 2008; 26:1-5.
55. Munoz-Gamez JA, Martin-Oliva D, Aguilar-Quesada R, Canuelo A, Nunez MI, Valenzuela MT, Ruiz de Almodovar JM, De Murcia G, Oliver FJ. PARP inhibition sensitizes p53-deficient breast cancer cells to doxorubicin-induced apoptosis. The Biochemical journal. 2005; 386:119-125.
56. Gewirtz DA. A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochemical pharmacology. 1999; 57:727-741.
57. Gatti L, Zunino F. Overview of tumor cell chemoresistance mechanisms. Methods in molecular medicine. 2005; 111:127-148.
58. Reiss KA, Herman JM, Zahurak M, Brade A, Dawson LA, Scardina A, Joffe C, Petito E, Hacker-Prietz A, Kinders RJ, Wang L, Chen A, Temkin S, Horiba N, Siu LL, Azad NS. A Phase I study of veliparib (ABT-888) in combination with low-dose fractionated whole abdominal radiation therapy in patients with advanced solid malignancies and peritoneal carcinomatosis. Clin Cancer Res. 2015; 21:68-76.
59. Krukenberg KA, Jiang R, Steen JA, Mitchison TJ. Basal activity of a PARP1-NuA4 complex varies dramatically across cancer cell lines. Cell reports. 2014; 8:1808-1818.
60. Tan C, Costello P, Sanghera J, Dominguez D, Baulida J, de Herreros AG, Dedhar S. Inhibition of integrin linked kinase (ILK) suppresses beta-catenin-Lef/Tcf-dependent transcription and expression of the E-cadherin repressor, snail, in APC-/-human colon carcinoma cells. Oncogene. 2001; 20:133-140.
61. Julien S, Puig I, Caretti E, Bonaventure J, Nelles L, van Roy F, Dargemont C, de Herreros AG, Bellacosa A, Larue L. Activation of NF-kappaB by Akt upregulates Snail expression and induces epithelium mesenchyme transition. Oncogene. 2007; 26:7445-7456.
62. Palmer MB, Majumder P, Green MR, Wade PA, Boss JM. A 3' enhancer controls snail expression in melanoma cells. Cancer research. 2007; 67:6113-6120.
63. Krishnakumar R, Kraus WL. PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Molecular cell. 2010; 39:736-749.
64. Chalhoub N, Baker SJ. PTEN and the PI3-kinase pathway in cancer. Annual review of pathology. 2009; 4:127-150.
65. Boohaker RJ, Cui X, Stackhouse M, Xu B. ATM-mediated Snail Serine 100 phosphorylation regulates cellular radiosensitivity. Radiother Oncol. 2013; 108:403-408.
66. Sun M, Guo X, Qian X, Wang H, Yang C, Brinkman KL, Serrano-Gonzalez M, Jope RS, Zhou B, Engler DA, Zhan M, Wong ST, Fu L, Xu B. Activation of the ATMSnail pathway promotes breast cancer metastasis. Journal of molecular cell biology. 2012; 4:304-315.
67. Dhasarathy A, Kajita M, Wade PA. The transcription factor snail mediates epithelial to mesenchymal transitions by repression of estrogen receptor-alpha. Molecular endocrinology Baltimore, Md. 2007; 21:2907-2918.
68. Yook JI, Li XY, Ota I, Fearon ER, Weiss SJ. Wntdependent regulation of the E-cadherin repressor snail. The Journal of biological chemistry. 2005; 280:11740-11748.
69. Pavri R, Lewis B, Kim TK, Dilworth FJ, Erdjument-Bromage H, Tempst P, de Murcia G, Evans R, Chambon P, Reinberg D. PARP-1 determines specificity in a retinoid signaling pathway via direct modulation of mediator. Molecular cell. 2005; 18:83-96.
70. Lin Y, Kang T, Zhou BP. Doxorubicin enhances Snail/LSD1-mediated PTEN suppression in a PARP1-dependent manner. Cell cycle Georgetown, Tex. 2014; 13:1708-1716.
71. Shah GM, Robu M, Purohit NK, Rajawat J, Tentori L, Graziani G. PARP Inhibitors in Cancer Therapy: Magic Bullets but Moving Targets. Frontiers in oncology. 2013; 3:279.
72. Ricciardi MR, Petrucci MT, Gregorj C, Ariola C, Lemoli RM, Fogli M, Mauro FR, Cerretti R, Foa R, Mandelli F, Tafuri A. Reduced susceptibility to apoptosis correlates with kinetic quiescence in disease progression of chronic lymphocytic leukaemia. British journal of haematology. 2001; 113:391-399.
73. Zampieri M, Guastafierro T, Calabrese R, Ciccarone F, Bacalini MG, Reale A, Perilli M, Passananti C, Caiafa P. ADP-ribose polymers localized on Ctcf-Parp1-Dnmt1 complex prevent methylation of Ctcf target sites. The Biochemical journal. 2012; 441:645-652.