Anti-leukemic effects of the V-ATPase inhibitor Archazolid A

Oncotarget

Volumn 6, Issue 41, 2015, Pages 43508-43528

  Zhang, Siwei ^a   Schneider, Lina S ^a   Vick, Binje ^b,d   Grunert, Michaela ^b   Jeremias, Irmela ^b,c,d   Menche, Dirk ^e   Müller, Rolf ^f   Vollmar, Angelika M ^a   Liebl, Johanna ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^e UNIVERSITY OF BONN   (Germany)

^f SAARLAND UNIVERSITY   (Germany)

Author keywords

Archazolid; Leukemia; Natural compounds

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE INHIBITOR; ARCHAZOLID A; IRON; NOTCH RECEPTOR; PROTEIN V ATPASE; SURVIVIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; MACROLIDE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; THIAZOLE DERIVATIVE;

ACIDIFICATION; ACUTE LYMPHOBLASTIC LEUKEMIA; ANTIANGIOGENIC ACTIVITY; ANTILEUKEMIC EFFECT; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; DRUG POTENCY; HUMAN; HUMAN CELL; IRON METABOLISM; LEUKEMIA CELL LINE; LYSOSOME; PROTEIN SYNTHESIS INHIBITION; S PHASE CELL CYCLE CHECKPOINT; T CELL LEUKEMIA; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; CONFOCAL MICROSCOPY; DRUG EFFECTS; DRUG SCREENING; GENETIC TRANSFECTION; IMMUNOBLOTTING; MOUSE; NONOBESE DIABETIC MOUSE; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; HUMANS; IMMUNOBLOTTING; MACROLIDES; MICE; MICE, INBRED NOD; MICE, SCID; MICROSCOPY, CONFOCAL; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THIAZOLES; TRANSFECTION; VACUOLAR PROTON-TRANSLOCATING ATPASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84952891536     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6180     Document Type: Article

References (76)

1. Van Vlierberghe P and Ferrando A. The molecular basis of T cell acute lymphoblastic leukemia. J Clin Invest. 2012; 122:3398-3406.
2. Koch U and Radtke F. Notch in T-ALL: new players in a complex disease. Trends Immunol. 2011; 32:434-442.
3. Pancewicz J and Nicot C. Current views on the role of Notch signaling and the pathogenesis of human leukemia. BMC Cancer. 2011; 11:502.
4. De Falco F, Sabatini R, Del Papa B, Falzetti F, Di Ianni M, Sportoletti P, Baldoni S, Screpanti I, Marconi P and Rosati E. Notch signaling sustains the expression of Mcl-1 and the activity of eIF4E to promote cell survival in CLL. Oncotarget. 2015; 6:16559-16572.
5. Rosati E, Sabatini R, Rampino G, Tabilio A, Di Ianni M, Fettucciari K, Bartoli A, Coaccioli S, Screpanti I and Marconi P. Constitutively activated Notch signaling is involved in survival and apoptosis resistance of B-CLL cells. Blood. 2009; 113:856-865.
6. Rosati E, Sabatini R, De Falco F, Del Papa B, Falzetti F, Di Ianni M, Cavalli L, Fettucciari K, Bartoli A, Screpanti I and Marconi P. gamma-Secretase inhibitor I induces apoptosis in chronic lymphocytic leukemia cells by proteasome inhibition, endoplasmic reticulum stress increase and notch down-regulation. Int J Cancer. 2013; 132:1940-1953.
7. Tian C, Yu Y, Jia Y, Zhu L and Zhang Y. HES1 activation suppresses proliferation of leukemia cells in acute myeloid leukemia. Annals of hematology. 2015; 94:1477-83.
8. Kannan S, Sutphin RM, Hall MG, Golfman LS, Fang W, Nolo RM, Akers LJ, Hammitt RA, McMurray JS, Kornblau SM, Melnick AM, Figueroa ME and Zweidler-McKay PA. Notch activation inhibits AML growth and survival: a potential therapeutic approach. J Exp Med. 2013; 210:321-337.
9. Kato T, Sakata-Yanagimoto M, Nishikii H, Ueno M, Miyake Y, Yokoyama Y, Asabe Y, Kamada Y, Muto H, Obara N, Suzukawa K, Hasegawa Y, Kitabayashi I, Uchida K, Hirao A, Yagita H, et al. Hes1 suppresses acute myeloid leukemia development through FLT3 repression. Leukemia. 2015; 29:576-585.
10. Vaccari T, Lu H, Kanwar R, Fortini ME and Bilder D. Endosomal entry regulates Notch receptor activation in Drosophila melanogaster. J Cell Biol. 2008; 180:755-762.
11. Vaccari T, Duchi S, Cortese K, Tacchetti C and Bilder D. The vacuolar ATPase is required for physiological as well as pathological activation of the Notch receptor. Development. 2010; 137:1825-1832.
12. Nishi T and Forgac M. The vacuolar (H+)-ATPases-nature's most versatile proton pumps. Nat Rev Mol Cell Biol. 2002; 3:94-103.
13. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol. 2007; 8:917-929.
14. Cotter K, Capecci J, Sennoune S, Huss M, Maier M, Martinez-Zaguilan R and Forgac M. Activity of plasma membrane V-ATPases is critical for the invasion of MDAMB231 breast cancer cells. J Biol Chem. 2015; 290:3680-3692.
15. von Schwarzenberg K, Wiedmann RM, Oak P, Schulz S, Zischka H, Wanner G, Efferth T, Trauner D and Vollmar AM. Mode of cell death induction by pharmacological vacuolar H+-ATPase (V-ATPase) inhibition. J Biol Chem. 2013; 288:1385-1396.
16. Wiedmann RM, von Schwarzenberg K, Palamidessi A, Schreiner L, Kubisch R, Liebl J, Schempp C, Trauner D, Vereb G, Zahler S, Wagner E, Muller R, Scita G and Vollmar AM. The V-ATPase-inhibitor archazolid abrogates tumor metastasis via inhibition of endocytic activation of the Rho-GTPase Rac1. Cancer Res. 2012; 72:5976-5987.
17. Schempp CM, von Schwarzenberg K, Schreiner L, Kubisch R, Muller R, Wagner E and Vollmar AM. V-ATPase inhibition regulates anoikis resistance and metastasis of cancer cells. Mol Cancer Ther. 2014; 13:926-937.
18. Kubisch R, Frohlich T, Arnold GJ, Schreiner L, von Schwarzenberg K, Roidl A, Vollmar AM and Wagner E. V-ATPase inhibition by archazolid leads to lysosomal dysfunction resulting in impaired cathepsin B activation in vivo. Int J Cancer. 2014; 134:2478-2488.
19. Chung C, Mader CC, Schmitz JC, Atladottir J, Fitchev P, Cornwell ML, Koleske AJ, Crawford SE and Gorelick F. The vacuolar-ATPase modulates matrix metalloproteinase isoforms in human pancreatic cancer. Laboratory investigation; a journal of technical methods and pathology. 2011; 91:732-743.
20. Nishisho T, Hata K, Nakanishi M, Morita Y, Sun-Wada GH, Wada Y, Yasui N and Yoneda T. The a3 isoform vacuolar type H(+)-ATPase promotes distant metastasis in the mouse B16 melanoma cells. Mol Cancer Res. 2011; 9:845-855.
21. Michel V, Licon-Munoz Y, Trujillo K, Bisoffi M and Parra KJ. Inhibitors of vacuolar ATPase proton pumps inhibit human prostate cancer cell invasion and prostate-specific antigen expression and secretion. Int J Cancer. 2013; 132:E1-10.
22. Avnet S, Di Pompo G, Lemma S, Salerno M, Perut F, Bonuccelli G, Granchi D, Zini N and Baldini N. V-ATPase is a candidate therapeutic target for Ewing sarcoma. Biochimica et biophysica acta. 2013; 1832:1105-1116.
23. Perut F, Avnet S, Fotia C, Baglio SR, Salerno M, Hosogi S, Kusuzaki K and Baldini N. V-ATPase as an effective therapeutic target for sarcomas. Exp Cell Res. 2014; 320:21-32.
24. Di Cristofori A, Ferrero S, Bertolini I, Gaudioso G, Russo MV, Berno V, Vanini M, Locatelli M, Zavanone M, Rampini P, Vaccari T, Caroli M and Vaira V. The vacuolar H+ ATPase is a novel therapeutic target for glioblastoma. Oncotarget. 2015; 6:17514-31.
25. Hamm R, Zeino M, Frewert S and Efferth T. Up-regulation of cholesterol associated genes as novel resistance mechanism in glioblastoma cells in response to archazolid B. Toxicology and applied pharmacology. 2014; 281:78-86.
26. Huss M and Wieczorek H. Inhibitors of V-ATPases: old and new players. J Exp Biol. 2009; 212(Pt 3):341-346.
27. Bockelmann S, Menche D, Rudolph S, Bender T, Grond S, von Zezschwitz P, Muench SP, Wieczorek H and Huss M. Archazolid A binds to the equatorial region of the c-ring of the vacuolar H+-ATPase. J Biol Chem. 2010; 285:38304-38314.
28. Huss M, Sasse F, Kunze B, Jansen R, Steinmetz H, Ingenhorst G, Zeeck A and Wieczorek H. Archazolid and apicularen: novel specific V-ATPase inhibitors. BMC biochemistry. 2005; 6:13.
29. Huss M, Vitavska O, Albertmelcher A, Bockelmann S, Nardmann C, Tabke K, Tiburcy F and Wieczorek H. Vacuolar H(+)-ATPases: intra-and intermolecular interactions. Eur J Cell Biol. 2011; 90:688-695.
30. Sasse F, Steinmetz H, Hofle G and Reichenbach H. Archazolids, new cytotoxic macrolactones from Archangium gephyra (Myxobacteria). Production, isolation, physico-chemical and biological properties. The Journal of antibiotics. 2003; 56:520-525.
31. Menche D, Hassfeld J, Li J and Rudolph S. Total synthesis of archazolid A. Journal of the American Chemical Society. 2007; 129:6100-6101.
32. Roethle PA, Chen IT and Trauner D. Total synthesis of (-)-archazolid B. Journal of the American Chemical Society. 2007; 129:8960-8961.
33. Rath S, Liebl J, Furst R, Vollmar AM and Zahler S. Regulation of endothelial signaling and migration by v-ATPase. Angiogenesis. 2014; 17:587-601.
34. von Schwarzenberg K, Lajtos T, Simon L, Muller R, Vereb G and Vollmar AM. V-ATPase inhibition overcomes trastuzumab resistance in breast cancer. Mol Oncol. 2014; 8:9-19.
35. Kobia F, Duchi S, Deflorian G and Vaccari T. Pharmacologic inhibition of vacuolar H+ ATPase reduces physiologic and oncogenic Notch signaling. Mol Oncol. 2014; 8:207-220.
36. Perez-Sayans M, Somoza-Martin JM, Barros-Angueira F, Rey JM and Garcia-Garcia A. V-ATPase inhibitors and implication in cancer treatment. Cancer Treat Rev. 2009; 35:707-713.
37. Yan Y, Denef N and Schupbach T. The vacuolar proton pump, V-ATPase, is required for notch signaling and endosomal trafficking in Drosophila. Dev Cell. 2009; 17:387-402.
38. Valapala M, Hose S, Gongora C, Dong L, Wawrousek EF, Samuel Zigler J, Jr. and Sinha D. Impaired endolysosomal function disrupts Notch signalling in optic nerve astrocytes. Nat Commun. 2013; 4:1629.
39. Terziyska N, Castro Alves C, Groiss V, Schneider K, Farkasova K, Ogris M, Wagner E, Ehrhardt H, Brentjens RJ, zur Stadt U, Horstmann M, Quintanilla-Martinez L and Jeremias I. In vivo imaging enables high resolution preclinical trials on patients' leukemia cells growing in mice. PLoS One. 2012; 7:e52798.
40. Vick B, Rothenberg M, Sandhofer N, Carlet M, Finkenzeller C, Krupka C, Grunert M, Trumpp A, Corbacioglu S, Ebinger M, Andre MC, Hiddemann W, Schneider S, Subklewe M, Metzeler KH, Spiekermann K, et al. An advanced preclinical mouse model for acute myeloid leukemia using patients' cells of various genetic subgroups and in vivo bioluminescence imaging. PLoS One. 2015; 10:e0120925.
41. Altieri DC. Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer. 2008; 8:61-70.
42. Park E, Gang EJ, Hsieh YT, Schaefer P, Chae S, Klemm L, Huantes S, Loh M, Conway EM, Kang ES, Hoe Koo H, Hofmann WK, Heisterkamp N, Pelus L, Keerthivasan G, Crispino J, et al. Targeting survivin overcomes drug resistance in acute lymphoblastic leukemia. Blood. 2011; 118:2191-2199.
43. Purroy N, Abrisqueta P, Carabia J, Carpio C, Calpe E, Palacio C, Castellvi J, Crespo M and Bosch F. Targeting the proliferative and chemoresistant compartment in chronic lymphocytic leukemia by inhibiting survivin protein. Leukemia. 2014; 28(10):1993-2004.
44. Schneider LS, von Schwarzenberg K, Lehr T, Ulrich M, Kubisch-Dohmen R, Liebl J, Trauner D, Menche D and Vollmar AM. Vacuolar-ATPase Inhibition Blocks Iron Metabolism to Mediate Therapeutic Effects in Breast Cancer. Cancer Res. 2015; 75:2863-2874.
45. Greijer AE and van der Wall E. The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. Journal of clinical pathology. 2004; 57:1009-1014.
46. Koshiji M and Huang LE. Dynamic balancing of the dual nature of HIF-1alpha for cell survival. Cell Cycle. 2004; 3:853-854.
47. Sermeus A and Michiels C. Reciprocal influence of the p53 and the hypoxic pathways. Cell death & disease. 2011; 2:e164.
48. Fridman JS and Lowe SW. Control of apoptosis by p53. Oncogene. 2003; 22:9030-9040.
49. Sennoune SR, Bermudez LE, Lees JC, Hirsch J, Filleur S and Martinez-Zaguilan R. Vacuolar H+-ATPase is down-regulated by the angiogenesis-inhibitory pigment epithelium-derived factor in metastatic prostate cancer cells. Cell Mol Biol (Noisy-le-grand). 2014; 60:45-52.
50. Hinton A, Sennoune SR, Bond S, Fang M, Reuveni M, Sahagian GG, Jay D, Martinez-Zaguilan R and Forgac M. Function of a subunit isoforms of the V-ATPase in pH homeostasis and in vitro invasion of MDA-MB231 human breast cancer cells. J Biol Chem. 2009; 284:16400-16408.
51. Fan SH, Wang YY, Lu J, Zheng YL, Wu DM, Zhang ZF, Shan Q, Hu B, Li MQ and Cheng W. CERS2 Suppresses Tumor Cell Invasion and Is Associated with Decreased V-ATPase and MMP-2/MMP-9 activities in Breast Cancer. J Cell Biochem. 2015; 116:502-13.
52. Graham RM, Thompson JW and Webster KA. Inhibition of the vacuolar ATPase induces Bnip3-dependent death of cancer cells and a reduction in tumor burden and metastasis. Oncotarget. 2014; 5:1162-1173.
53. Scherer O, Steinmetz H, Kaether C, Weinigel C, Barz D, Kleinert H, Menche D, Muller R, Pergola C and Werz O. Targeting V-ATPase in primary human monocytes by archazolid potently represses the classical secretion of cytokines due to accumulation at the endoplasmic reticulum. Biochem Pharmacol. 2014; 91:490-500.
54. De Milito A, Iessi E, Logozzi M, Lozupone F, Spada M, Marino ML, Federici C, Perdicchio M, Matarrese P, Lugini L, Nilsson A and Fais S. Proton pump inhibitors induce apoptosis of human B-cell tumors through a caspaseindependent mechanism involving reactive oxygen species. Cancer Res. 2007; 67:5408-5417.
55. Sukhai MA, Prabha S, Hurren R, Rutledge AC, Lee AY, Sriskanthadevan S, Sun H, Wang X, Skrtic M, Seneviratne A, Cusimano M, Jhas B, Gronda M, MacLean N, Cho EE, Spagnuolo PA, et al. Lysosomal disruption preferentially targets acute myeloid leukemia cells and progenitors. J Clin Invest. 2013; 123:315-328.
56. Funayama K, Murai F, Shimane M, Nomura H and Asano S. Adhesion-induced drug resistance in leukemia stem cells. Pharmacology. 2010; 86:79-84.
57. O'Neil J, Grim J, Strack P, Rao S, Tibbitts D, Winter C, Hardwick J, Welcker M, Meijerink JP, Pieters R, Draetta G, Sears R, Clurman BE and Look AT. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors. J Exp Med. 2007; 204:1813-1824.
58. Breit S, Stanulla M, Flohr T, Schrappe M, Ludwig WD, Tolle G, Happich M, Muckenthaler MU and Kulozik AE. Activating NOTCH1 mutations predict favorable early treatment response and long-term outcome in childhood precursor T-cell lymphoblastic leukemia. Blood. 2006; 108:1151-1157.
59. van Grotel M, Meijerink JP, Beverloo HB, Langerak AW, Buys-Gladdines JG, Schneider P, Poulsen TS, den Boer ML, Horstmann M, Kamps WA, Veerman AJ, van Wering ER, van Noesel MM and Pieters R. The outcome of molecular-cytogenetic subgroups in pediatric T-cell acute lymphoblastic leukemia: a retrospective study of patients treated according to DCOG or COALL protocols. Haematologica. 2006; 91:1212-1221.
60. Mansour MR, Sulis ML, Duke V, Foroni L, Jenkinson S, Koo K, Allen CG, Gale RE, Buck G, Richards S, Paietta E, Rowe JM, Tallman MS, Goldstone AH, Ferrando AA and Linch DC. Prognostic implications of NOTCH1 and FBXW7 mutations in adults with T-cell acute lymphoblastic leukemia treated on the MRC UKALLXII/ECOG E2993 protocol. J Clin Oncol. 2009; 27:4352-4356.
61. Carter BZ, Milella M, Altieri DC and Andreeff M. Cytokine-regulated expression of survivin in myeloid leukemia. Blood. 2001; 97:2784-2790.
62. Carter BZ, Qiu Y, Huang X, Diao L, Zhang N, Coombes KR, Mak DH, Konopleva M, Cortes J, Kantarjian HM, Mills GB, Andreeff M and Kornblau SM. Survivin is highly expressed in CD34(+)38(-) leukemic stem/progenitor cells and predicts poor clinical outcomes in AML. Blood. 2012; 120:173-180.
63. Fukuda S, Hoggatt J, Singh P, Abe M, Speth JM, Hu P, Conway EM, Nucifora G, Yamaguchi S and Pelus LM. Survivin modulates genes with divergent molecular functions and regulates proliferation of hematopoietic stem cells through Evi-1. Leukemia. 2015; 29:433-40.
64. Smolewski P and Robak T. Inhibitors of apoptosis proteins (IAPs) as potential molecular targets for therapy of hematological malignancies. Curr Mol Med. 2011; 11:633-649.
65. Glodkowska-Mrowka E, Solarska I, Mrowka P, Bajorek K, Niesiobedzka-Krezel J, Seferynska I, Borg K and Stoklosa T. Differential expression of BIRC family genes in chronic myeloid leukaemia-BIRC3 and BIRC8 as potential new candidates to identify disease progression. Br J Haematol. 2014; 164:740-742.
66. Moore AS, Alonzo TA, Gerbing RB, Lange BJ, Heerema NA, Franklin J, Raimondi SC, Hirsch BA, Gamis AS and Meshinchi S. BIRC5 (survivin) splice variant expression correlates with refractory disease and poor outcome in pediatric acute myeloid leukemia: a report from the Children's Oncology Group. Pediatr Blood Cancer. 2014; 61:647-652.
67. Altieri DC. Targeting survivin in cancer. Cancer Lett. 2013; 332:225-228.
68. Raetz EA, Morrison D, Romanos-Sirakis E, Gaynon P, Sposto R, Bhojwani D, Bostrom BC, Brown P, Eckroth E, Cassar J, Malvar J, Buchbinder A and Carroll WL. A phase I study of EZN-3042, a novel survivin messenger ribonucleic acid (mRNA) antagonist, administered in combination with chemotherapy in children with relapsed acute lymphoblastic leukemia (ALL): a report from the therapeutic advances in childhood leukemia and lymphoma (TACL) consortium. J Pediatr Hematol Oncol. 2014; 36:458-463.
69. Chen J, Pise-Masison CA, Shih JH, Morris JC, Janik JE, Conlon KC, Keating A and Waldmann TA. Markedly additive antitumor activity with the combination of a selective survivin suppressant YM155 and alemtuzumab in adult T-cell leukemia. Blood. 2013; 121:2029-2037.
70. Andersen MH, Svane IM, Becker JC and Straten PT. The universal character of the tumor-associated antigen survivin. Clin Cancer Res. 2007; 13:5991-5994.
71. Altieri DC. Validating survivin as a cancer therapeutic target. Nat Rev Cancer. 2003; 3:46-54.
72. Bulycheva E, Rauner M, Medyouf H, Theurl I, Bornhauser M, Hofbauer LC and Platzbecker U. Myelodysplasia is in the niche-novel concepts and emerging therapies. Leukemia. 2015; 29:259-68.
73. Breccia M and Alimena G. Efficacy and safety of deferasirox in myelodysplastic syndromes. Ann Hematol. 2013; 92:863-870.
74. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F and Riccardi C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods. 1991; 139:271-279.
75. Muscolini M, Cianfrocca R, Sajeva A, Mozzetti S, Ferrandina G, Costanzo A and Tuosto L. Trichostatin A up-regulates p73 and induces Bax-dependent apoptosis in cisplatin-resistant ovarian cancer cells. Mol Cancer Ther. 2008; 7:1410-1419.
76. Liebl J, Zhang S, Moser M, Agalarov Y, Demir CS, Hager B, Bibb JA, Adams RH, Kiefer F, Miura N, Petrova TV, Vollmar AM and Zahler S. Cdk5 controls lymphatic vessel development and function by phosphorylation of Foxc2. Nat Commun. 2015; 6:7274.