Pyrrolo[3′,2′:6,7]cyclohepta[1,2-b]pyridines with potent photo-antiproliferative activity

European Journal of Medicinal Chemistry

Volumn 128, Issue , 2017, Pages 300-318

  Spanò, Virginia ^a   Giallombardo, Daniele ^a   Cilibrasi, Vincenzo ^a   Parrino, Barbara ^a   Carbone, Anna ^a   Montalbano, Alessandra ^a   Frasson, Ilaria ^b   Salvador, Alessia ^b   Richter, Sara N ^b   Doria, Filippo ^c   Freccero, Mauro ^c   Cascioferro, Stella ^a   Diana, Patrizia ^a   Cirrincione, Girolamo ^a   Barraja, Paola ^a  

^a UNIVERSITY OF PALERMO   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c UNIVERSITY OF PAVIA   (Italy)

Author keywords

Photo antiproliferative activity; Photosensitizing agents; Phototoxicity; Pyrrolo 3 ,2 :6,7 cyclohepta 1,2 b pyridine 9(1H) ones; Reactive oxygen species

Indexed keywords

1 (2 METHOXYBENZYL) 4,5,6,7 TETRAHYDROCYCLOHEPTA[B]PYRROL 8(1H) ONE; 1 (2 METHOXYBENZYL) 8 (PHENYLSULFONYL) 4,5,6,10 TETRAHYDROPYRROLO [3',2':6,7] CYCLOHEPTA[1,2 B]PYRIDIN 9(1H) ONE; 1 (3 METHOXYBENZYL) 4,5,6,7 TETRAHYDROCYCLOHEPTA[B]PYRROL 8(1H) ONE; 1 (3 METHOXYBENZYL) 8 (PHENYLSULFONYL) 4,5,6,10 TETRAHYDROPYRROLO [3',2':6,7] CYCLOHEPTA[1,2 B]PYRIDIN 9(1H) ONE; 1 (4 METHOXYBENZYL) 4,5,6,7 TETRAHYDROCYCLOHEPTA[B]PYRROL 8(1H) ONE; 1 (4 METHOXYBENZYL) 8 (PHENYLSULFONYL) 4,5,6,10 TETRAHYDROPYRROLO [3',2':6,7] CYCLOHEPTA[1,2 B]PYRIDIN 9(1H) ONE; 1 (PHENYLSULFONYL) 4,5,6,7 TETRAHYDROCYCLOHEPTA[B]PYRROL 8(1H) ONE; 1 BENZYL 4,5,6,7 TETRAHYDROCYCLOHEPTA[B]PYRROL 8(1H) ONE; 1 BENZYL 7 [(DIMETHYLAMINO)METHYLIDENE] 4,5,6,7 TETRAHYDROCYCLOHEPTA[B]PYRROL 8(1H) ONE; 1 BENZYL 8 (PHENYLSULFONYL) 4,5,6,10 TETRAHYDROPYRROLO [3',2':6,7] CYCLOHEPTA[1,2 B]PYRIDIN 9(1H) ONE; 1 METHYL 4,5,6,7 TETRAHYDROCYCLOHEPTA[B]PYRROL 8(1H) ONE; 1 METHYL 8 (PHENYLSULFONYL) 4,5,6,10 TETRAHYDROPYRROLO [3',2':6,7] CYCLOHEPTA[1,2 B]PYRIDIN 9(1H) ONE; 5 OXO 5 [1 (PHENYLSULFONYL) 1H PYRROL 3 YL] PENTANOIC ACID; 5 [1 (PHENYLSULFONYL) 1H PYRROL 3 YL] PENTANOIC ACID; 7 [(DIMETHYLAMINO)METHYLIDENE] 1 (2 METHOXYBENZYL) 4,5,6,7 TETRAHYDROCYCLOHEPTA [B]PYRROL 8(1H) ONE; 7 [(DIMETHYLAMINO)METHYLIDENE] 1 (3 METHOXYBENZYL) 4,5,6,7 TETRAHYDROCYCLOHEPTA [B]PYRROL 8(1H) ONE; 7 [(DIMETHYLAMINO)METHYLIDENE] 1 (4 METHOXYBENZYL) 4,5,6,7 TETRAHYDROCYCLOHEPTA [B]PYRROL 8(1H) ONE; 7 [(DIMETHYLAMINO)METHYLIDENE] 1 METHYL 4,5,6,7 TETRAHYDROCYCLOHEPTA[B]PYRROL 8(1H) ONE; ANTINEOPLASTIC AGENT; ETHYL 1 (2 METHOXYBENZYL) 8 OXO 1,4,5,6,7,8 HEXAHYDROCYCLOHEPTA[B]PYRROLE 2 CARBOXYLATE; ETHYL 1 (3 METHOXYBENZYL) 8 OXO 1,4,5,6,7,8 HEXAHYDROCYCLOHEPTA[B] PYRROLE 2 CARBOXYLATE; ETHYL 1 (3 METHOXYBENZYL) 9 OXO 8 (PHENYLSULFONYL) 1,4,5,6,9,10 HEXAHYDROPYRROLO [3',2':6,7]CYCLOHEPTA[1,2 B]PYRIDINE 2 CARBOXYLATE; ETHYL 1 BENZYL 7 [2 CYANO 2 (PHENYLSULFONYL)ETHENYL] 8 (DIMETHYLAMINO) 1,4,5,6 TETRAHYDROCYCLOHEPTA[B] PYRROLE 2 CARBOXYLATE; ETHYL 1 METHYL 9 OXO 8 (PHENYLSULFONYL) 1,4,5,6,9,10 HEXAHYDROPYRROLO[3',2':6,7] CYCLOHEPTA[1,2 B]PYRIDINE 2 CARBOXYLATE; ETHYL 7 [(DIMETHYLAMINO)METHYLIDENE] 1 (2 METHOXYBENZYL) 8 OXO 1,4,5,6,7,8 HEXAHYDROCYCLOHEPTA[B]PYRROLE 2 CARBOXYLATE; ETHYL 7 [(DIMETHYLAMINO)METHYLIDENE] 1 (3 METHOXYBENZYL) 8 OXO 1,4,5,6,7,8 HEXAHYDROCYCLOHEPTA[B]PYRROLE 2 CARBOXYLATE; ETHYL 7 [2 CYANO 2 (PHENYLSULFONYL)ETHENYL] 8 (DIMETHYLAMINO) 1 (2 METHOXYBENZYL) 1,4,5,6 TETRAHYDRCYCLOHEPTA[B] PYRROLE 2 CARBOXYLATE; PYRIDINE DERIVATIVE; PYRROLO[3' ,2' :6,7]CYCLOHEPTA[1,2 B]PYRIDINE DERIVATIVE; UNCLASSIFIED DRUG; UNINDEXED DRUG; ANTIOXIDANT; PHOTOSENSITIZING AGENT; PYRROLE DERIVATIVE; REACTIVE OXYGEN METABOLITE;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CELL MEDIATED CYTOTOXICITY; CELL VIABILITY; CLEMMENSEN REDUCTION; CONTROLLED STUDY; CYTOTOXICITY; DRUG SYNTHESIS; EC50; FRIEDEL CRAFTS REACTION; HUMAN; HUMAN CELL; JURKAT CELL LINE; LIPID PEROXIDATION; MCF-7 CELL LINE; PHOTOACTIVATION; PHOTOCYTOTOXICITY; PHOTOSENSITIZATION; PHOTOTOXICITY; PROTON NUCLEAR MAGNETIC RESONANCE; ULTRAVIOLET IRRADIATION; WESTERN BLOTTING; CELL PROLIFERATION; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; LIGHT; METABOLISM; NEOPLASMS; PATHOLOGY; STRUCTURE ACTIVITY RELATION; TUMOR CELL CULTURE;

ANTINEOPLASTIC AGENTS; ANTIOXIDANTS; BLOTTING, WESTERN; CELL PROLIFERATION; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; LIGHT; NEOPLASMS; PHOTOSENSITIZING AGENTS; PYRIDINES; PYRROLES; REACTIVE OXYGEN SPECIES; STRUCTURE-ACTIVITY RELATIONSHIP; TUMOR CELLS, CULTURED;

EID: 85012894226     PISSN: 02235234     EISSN: 17683254     Source Type: Journal    
DOI: 10.1016/j.ejmech.2017.02.008     Document Type: Article

References (57)

1. [1] Feng, Y., Yang, D., Chen, H., Cheng, W., Wang, L., Sun, H., Tang, Y., Stabilization of G-quadruplex DNA and inhibition of Bcl-2 expression by a pyridostatin analog. Bioorg. Med. Chem. Lett. 26 (2016), 1660–1663.
2. [2] Carbone, A., Pennati, M., Parrino, B., Lopergolo, A., Barraja, P., Montalbano, A., Spanò, V., Sbarra, S., Doldi, V., De Cesare, M., Cirrincione, G., Diana, P., Zaffaroni, N., Novel 1H-pyrrolo[2,3-b]pyridine derivative nortopsentin analogues: synthesis and antitumor activity in peritoneal mesothelioma experimental models. J. Med. Chem. 56 (2013), 7060–7072.
3. [3] Parrino, B., Carbone, A., Muscarella, M., Spanò, V., Montalbano, A., Barraja, P., Salvador, A., Vedaldi, D., Cirrincione, G., Diana, P., 11H-Pyrido[3′,2′:4,5]pyrrolo[3,2-c]cinnoline and pyrido[3′,2′:4,5]pyrrolo[1,2-c][1,2,3]benzotriazine: two new ring systems with antitumor activity. J. Med. Chem. 57 (2014), 9495–9511.
4. [4] Carbone, A., Pennati, M., Barraja, P., Montalbano, A., Parrino, B., Spanò, V., Lopergolo, A., Sbarra, S., Doldi, V., Zaffaroni, N., Cirrincione, G., Diana, P., Synthesis and antiproliferative activity of substituted 3[2-(1H-indol-3-yl)-1,3-thiazol-4-yl]-1H-pyrrolo[3,2-b]pyridines, marine alkaloid nortopsentin analogues. Curr. Med. Chem. 21 (2014), 1654–1666.
5. [5] Carbone, A., Parrino, B., Di Vita, G., Attanzio, A., Spanò, V., Montalbano, A., Barraja, P., Tesoriere, L., Livrea, M.A., Diana, P., Cirrincione, G., Synthesis and antiproliferative activity of thiazolyl-bis-pyrrolo[2,3-b]pyridines and indolyl-thiazolyl-pyrrolo[2,3-c]pyridines, nortopsentin analogues. Mar. Drugs 13 (2015), 460–492.
6. [6] Barraja, P., Diana, P., Spanò, V., Montalbano, A., Carbone, A., Parrino, B., Cirrincione, G., An efficient synthesis of pyrrolo[3’,2’:4,5]thiopyrano[3,2-b]pyridin-2-one: a new ring system of pharmaceutical interest. Tetrahedron 68 (2012), 5087–5094.
7. [7] Barraja, P., Caracausi, L., Diana, P., Spanò, V., Montalbano, A., Carbone, A., Parrino, B., Cirrincione, G., Synthesis and antiproliferative activity of the ring system [1,2]oxazolo[4,5-g]indole. ChemMedChem 7 (2012), 1901–1904.
8. [8] Parrino, B., Carbone, A., Di Vita, G., Ciancimino, C., Attanzio, A., Spanò, V., Montalbano, A., Barraja, P., Tesoriere, L., Livrea, M.A., Diana, P., Cirrincione, G., 3-[4-(1H-Indol-3-yl)-1,3-thiazol-2-yl]-1H-pyrrolo[2,3-b]pyridines, nortopsentin analogues with antiproliferative activity. Mar. Drugs 13 (2015), 1901–1924.
9. [9] Parrino, B., Spanò, V., Carbone, A., Barraja, P., Diana, P., Cirrincione, G., Montalbano, A., Synthesis of the new ring system bispyrido[4’,3’:4,5]pyrrolo[1,2-a:1’,2’-d]pyrazine and its deaza analogue. Molecules 19 (2014), 13342–13357.
10. [10] Ferretti, M.D., Neto, A.T., Morel, A.F., Kaufman, T.S., Larghi, E.L., Synthesis of symmetrically substituted 3,3-dibenzyl-4-hydroxy-3,4-dihydro-1H-quinolin-2-ones, as novel quinoline derivatives with antibacterial activity. Eur. J. Med. Chem. 81 (2014), 253–266.
11. [11] Hewawasam, P., Fan, W., Ding, M., Flint, K., Cook, D., Goggins, G.D., Myers, R.A., Gribkoff, V.K., Boissard, C.G., Dworetzky, S.I., Starrett, J.E., Lodge, N.J., 4-Aryl-3-(hydroxyalkyl)quinolin-2-ones: novel maxi-K channel opening relaxants of corporal smooth muscle targeted for erectile dysfunction. J. Med. Chem. 46 (2003), 2819–2822.
12. [12] Cretton, S., Dorsaz, S., Azzollini, A., Favre–Godal, Q., Marcourt, L., Ebrahimi, S.N., Voinesco, F., Michellod, E., Sanglard, D., Gindro, K., Wolfender, J.–L., Cuendet, M., Christen, P., Antifungal quinoline alkaloids from Waltheria indica. J. Nat. Prod. 79 (2016), 300–307.
13. [13] Cretton, S., Breant, L., Pourrez, L., Ambuehl, C., Marcourt, L., Ebrahimi, S.N., Hamburger, M., Perozzo, R., Karimou, S., Kaiser, M., Cuendet, M., Christen, P., Antitrypanosomal quinoline alkaloids from the roots of Waltheria indica. J. Nat. Prod. 77 (2014), 2304–2311.
14. [14] Barraja, P., Diana, P., Montalbano, A., Dattolo, G., Cirrincione, G., Viola, G., Vedaldi, D., Dall'Acqua, F., Pyrrolo[2,3-h]quinolinones: a new ring system with potent photoantiproliferative activity. Bioorg. Med. Chem. 14 (2006), 8712–8728.
15. [15] Shiro, T., Fukaya, T., Tobe, M., The chemistry and biological activity of heterocycle-fused quinolinone derivatives: a review. Eur. J. Med. Chem. 97 (2015), 397–408.
16. [16] Cai, S.X., Zhang, H.–Z., Drewe, J., Kasibhatla, S., Preparation of 4-aryl-3-(3-aryl-1-oxo-2-propenyl)-2(1H)-quinolinones and analogs as activators of caspases and inducers of apoptosis for treatment of cancer and other proliferative disorders, PCT Int. Appl. WO 2002098425. Chem. Abstr., 138, 2002, 24647.
17. [17] Xie, L., Qian, X., Cui, J., Xiao, Y., Wang, K., Wu, P., Cong, L., Novel angular furoquinolinones bearing flexible chain as antitumor agent: design, synthesis, cytotoxic evaluation, and DNA-binding studies. Bioorg. Med. Chem. 16 (2008), 8713–8718.
18. [18] Nagarapu, L., Gaikwad, H.K., Bantu, R., Manikonda, S.R., Chemoenzymatic synthesis with lipase catalyzed resolution and evaluation of antitumor activity of (R/S)-2-[2-hydroxy-3-(4-phenylpiperazin-1-yl)propyl]-1H-pyrrolo[3,4-b]quinolin-3(2H)-one. Eur. J. Med. Chem. 46 (2011), 2152–2156.
19. [19] Barraja, P., Caracausi, L., Diana, P., Carbone, A., Montalbano, A., Cirrincione, G., Brun, P., Palù, G., Castagliuolo, I., Dall'Acqua, F., Vedaldi, D., Salvador, A., Synthesis of pyrrolo[3,2-h]quinolinones with good photochemotherapeutic activity and no DNA damage. Bioorg. Med. Chem. 18 (2010), 4830–4843.
20. [20] Diana, P., Carbone, A., Barraja, P., Montalbano, A., Parrino, B., Lopergolo, A., Pennati, M., Zaffaroni, N., Cirrincione, G., Synthesis and antitumor activity of 3-(2-Phenyl-1,3-thiazol-4-yl)-1H-indoles and 3-(2-phenyl-1,3-thiazol-4-yl)-1H-7-azaindoles. ChemMedChem 6 (2011), 1300–1309.
21. [21] Carbone, A., Parrino, B., Barraja, P., Spanò, V., Cirrincione, G., Diana, P., Maier, A., Kelter, G., Fiebig, H.-H., Synthesis and antiproliferative activity of 2,5-bis(3′-indolyl)pyrroles, analogues of the marine alkaloid nortopsentin. Mar. Drugs 11 (2013), 643–654.
22. [22] Diana, P., Stagno, A., Barraja, P., Carbone, A., Parrino, B., Dall'Acqua, F., Vedaldi, D., Salvador, A., Brun, P., Castagliuolo, I., Issinger, O.G., Cirrincione, G., Synthesis of triazenoazaindoles: a new class of triazenes with antitumor activity. ChemMedChem 6 (2011), 1291–1299.
23. [23] Spanò, V., Pennati, M., Parrino, B., Carbone, A., Montalbano, A., Cilibrasi, V., Zuco, V., Lopergolo, A., Cominetti, D., Diana, P., Cirrincione, G., Zaffaroni, N., Barraja, P., Preclinical activity of new [1,2]oxazolo[5,4-e]isoindole derivatives in diffuse malignant peritoneal mesothelioma. J. Med. Chem. 59 (2016), 7223–7238.
24. [24] Montalbano, A., Parrino, B., Diana, P., Barraja, P., Carbone, A., Spanò, V., Cirrincione, G., Synthesis of the new oligopeptide pyrrole derivative isonetropsin and its one pyrrole unit analogue. Tetrahedron 69 (2013), 2550–2554.
25. [25] Spanò, V., Montalbano, A., Carbone, A., Parrino, B., Diana, P., Cirrincione, G., Castagliuolo, I., Brun, P., Issinger, O.–G., Tisi, S., Primac, I., Vedaldi, D., Salvador, A., Barraja, P., Synthesis of a new class of pyrrolo[3,4-h]quinazolines with antimitotic activity. Eur. J. Med. Chem. 74 (2014), 340–357.
26. [26] Parrino, B., Carbone, A., Spanò, V., Montalbano, A., Giallombardo, D., Barraja, P., Attanzio, A., Tesoriere, L., Sissi, C., Palumbo, M., Cirrincione, G., Diana, P., Aza-isoindolo and isoindolo-azaquinoxaline derivatives with antiproliferative activity. Eur. J. Med. Chem. 94 (2015), 367–377.
27. [27] Barraja, P., Spanò, V., Giallombardo, D., Diana, P., Montalbano, A., Carbone, A., Parrino, B., Cirrincione, G., Synthesis of [1,2]oxazolo[5,4-e]indazoles as antitumor agents. Tetrahedron 69 (2013), 6474–6477.
28. [28] Parrino, B., Ciancimino, C., Carbone, A., Spanò, V., Montalbano, A., Barraja, P., Cirrincione, G., Diana, P., Synthesis of isoindolo[1,4]benzoxazinone and isoindolo[1,5]benzoxazepine: two new ring systems of pharmaceutical interest. Tetrahedron 71 (2015), 7332–7338.
29. [29] Parrino, B., Carbone, A., Ciancimino, C., Spanò, V., Montalbano, A., Barraja, P., Cirrincione, G., Diana, P., Sissi, C., Palumbo, M., Pinato, O., Pennati, M., Beretta, G., Folini, M., Matyus, P., Balogh, B., Zaffaroni, N., Water-soluble isoindolo[2,1-a]quinoxalin-6-imines: in vitro antiproliferative activity and molecular mechanism(s) of action. Eur. J. Med. Chem. 94 (2015), 149–162.
30. [30] Spanò, V., Pennati, M., Parrino, B., Carbone, A., Montalbano, A., Lopergolo, A., Zuco, V., Cominetti, D., Diana, P., Cirrincione, G., Zaffaroni, N., Barraja, P., [1,2]Oxazolo[5,4-e]isoindoles as promising tubulin polymerization inhibitors. Eur. J. Med. Chem. 124 (2016), 840–851.
31. [31] Barraja, P., Spanò, V., Diana, P., Carbone, A., Cirrincione, G., Vedaldi, D., Salvador, A., Viola, G., Dall'Acqua, F., Pyrano[2,3-e]isoindol-2-ones, new angelicin heteroanalogues. Bioorg. Med. Chem. Lett. 19 (2009), 1711–1714.
32. [32] Barraja, P., Caracausi, L., Diana, P., Montalbano, A., Carbone, A., Salvador, A., Brun, P., Castagliuolo, I., Tisi, S., Dall'Acqua, F., Vedaldi, D., Cirrincione, G., Pyrrolo[3,2-h]quinazolines as photochemotherapeutic agents. ChemMedChem 6 (2011), 1238–1248.
33. [33] Spanò, V., Parrino, B., Carbone, A., Montalbano, A., Salvador, A., Brun, P., Vedaldi, D., Diana, P., Cirrincione, G., Barraja, P., Pyrazolo[3,4-h]quinolines promising PS agents in the treatment of cancer. Eur. J. Med. Chem. 102 (2015), 334–351.
34. [34] Dolmans, D.E.J.G.J., Fukumura, D., Jain, R.K., Photodynamic therapy for cancer. Nat. Rev. Cancer 3 (2003), 380–387.
35. [35] Barraja, P., Diana, P., Montalbano, A., Carbone, A., Viola, G., Basso, G., Salvador, A., Vedaldi, D., Dall'Acqua, F., Cirrincione, G., Pyrrolo[3,4-h]quinolinones a new class of photochemotherapeutic agents. Bioorg. Med. Chem. 19 (2011), 2326–2341.
36. [36] Bergers, J.G., Teller, S.R., Pachter, I.J., Cycloalkapyrrolones via decarboxylative ring closure of pyrrole-3-alkanoic acids and derivatives. J. Org. Chem. 35 (1970), 3122–3126.
37. [37] Soma, N., Studies on seven-membered ring compounds. VII. The reaction of 2-amino-3-bromotropone with active methylene compounds. Yakugaku Zasshi 82 (1962), 898–902.
38. [38] Spanò, V., Frasson, I., Giallombardo, D., Doria, F., Parrino, B., Carbone, A., Montalbano, A., Nadai, M., Diana, P., Cirrincione, G., Freccero, M., Richter, S.N., Barraja, P., Synthesis and antiproliferative mechanism of action of pyrrolo[3′,2′:6,7]cyclohepta[1,2-d]pyrimidin-2-amines as singlet oxygen photosensitizers. Eur. J. Med. Chem. 123 (2016), 447–461.
39. [39] Doria, F., Manet, I., Grande, V., Monti, S., Freccero, M., Water-soluble naphthalene diimides as singlet oxygen sensitizers. J. Org. Chem. 78 (2013), 8065–8073.
40. [40] Traore, K., Trush, M.A., George, M., Spannhake, E.W., Anderson, W., Asseffa, A., Signal transduction of phorbol 12-myristate 13-acetate (PMA)-induced growth inhibition of human monocytic leukemia THP-1 cells is reactive oxygen dependent. Leuk. Res. 29 (2005), 863–879.
41. [41] Keshari, R.S., Verma, A., Barthwal, M.K., Dikshit, M., Reactive oxygen species-induced activation of ERK and p38 MAPK mediates PMA-induced NETs release from human neutrophils. J. Cell. Biochem. 114 (2013), 532–540.
42. [42] Halasi, M., Wang, M., Chavan, T.S., Gaponenko, V., Hay, N., Gartel, A.L., ROS inhibitor N-acetyl-L-cysteine antagonizes the activity of proteasome inhibitors. Biochem. J. 454 (2013), 201–208.
43. [43] Sun, S.Y., N-acetylcysteine, reactive oxygen species and beyond. Cancer Biol. Ther. 9 (2010), 109–110.
44. [44] Tajeddine, N., How do reactive oxygen species and calcium trigger mitochondrial membrane permeabilization?. Biochim. Biophys. Acta 1860 (2016), 1079–1088.
45. [45] Zhao, Y., Qu, T., Wang, P., Li, X., Unravelling the relationship between macroautophagy and mitochondrial ROS in cancer therapy. Apoptosis 21 (2016), 517–531.
46. [46] Vargas, H.H., Palacios, J., Bueno, G.M., Molecular profiling of docetaxel cytotoxicity in breast cancer cells: uncoupling of aberrant mitosis and apoptosis. Oncogene 26 (2007), 2902–2913.
47. [47] Hausmann, G., O'Reilly, L.A., Van Driel, R., Beaumont, J.G., Strasser, A., Adams, J.M., Huang, D.C.S., Pro-apoptotic apoptosis protease-activating factor 1 (Apaf-1) has a cytoplasmic localization distinct from Bcl-2 or Bcl-XL. J. Cell Biol. 149 (2000), 623–633.
48. [48] Zhao, J., Zhang, J., Yu, M., Xie, Y., Huang, Y., Wolff, D.W., Abel, P.W., Tu, Y., Mitochondrial dynamics regulates migration and invasion of breast cancer cells. Oncogene 32 (2013), 4814–4824.
49. [49] Boya, P., Kroemer, G., Lysosomal membrane permeabilization in cell death. Oncogene 27 (2008), 6434–6451.
50. [50] De Milito, A., Iessi, E., Logozzi, M., Lozupone, F., Spada, M., Marino, M.L., Federici, C., Perdicchio, M., Matarrese, P., Lugini, L., Nilsson, A., Fais, S., Proton pump inhibitors induce apoptosis of human B-cell tumors through a caspase-independent mechanisn involving reactive oxygen species. Cancer Res. 67 (2007), 5408–5417.
51. [51] Ciulla, T.A., Van Camp, J.R., Rosenfeld, E., Kochevar, I.E., Photosensitization of single-strand breaks in pBR322 DNA by Rose Bengal. Photochem. Photobiol. 49 (1989), 293–298.
52. [52] Ryder, K.S., Morris, D.G., Cooper, J.M., Tailored polymers to probe the nature of the bioelectrochemical interface. Langmuir 12 (1996), 5681–5688.
53. [53] Krohn, K., Rieger, H., Khanbabaee, K., A new synthesis of ortho-quinones by transition-metal-mediated oxygenation of phenols with tert-butylhydroperoxide and the mimoun oxodiperoxo molybdenum complex [Mo(O2)2]·Py·HMPT. Chem. Ber. 122 (1989), 2323–2330.
54. [54] Doria, F., Lena, A., Bargiggia, R., Freccero, M., Conjugation, substituent, and solvent effects on the photogeneration of quinone methides. J. Org. Chem. 81 (2016), 3665–3673.
55. [55] Miolo, G., Salvador, A., Mazzoli, A., Spalletti, A., Marzaro, G., Chilin, A., Photochemical and photobiological studies on furoquinazolines as new psoralen analogs. J. Photochem. Photobiol. B Biol. 138 (2014), 43–54.
56. [56] Peterson, L., A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83 (1977), 346–356.
57. [57] Morliere, P., Moysan, A., Santus, R., Huppe, G., Maziere, J.C., Dubertrer, L., UVA-induced lipid peroxidation in cultured human fibroblasts. Biochim. Biophys. Acta 1084 (1991), 261–268.