Hexamethylene amiloride engages a novel reactive oxygen species- and lysosome-dependent programmed necrotic mechanism to selectively target breast cancer cells

Cancer Letters

Volumn 375, Issue 1, 2016, Pages 62-72

  Rowson Hodel, Ashley R ^a   Berg, Anastasia L ^a   Wald, Jessica H ^a   Hatakeyama, Jason ^a   VanderVorst, Kacey ^a   Curiel, Daniel A ^a   Leon, Leonardo J ^a,b   Sweeney, Colleen ^a   Carraway, Kermit L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Apoptosis; Breast cancer; Cancer therapeutics; Cytotoxicity; Necrosis

Indexed keywords

5 (N,N HEXAMETHYLENE)AMILORIDE; CASPASE; CATHEPSIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; 5-(N,N-HEXAMETHYLENE)AMILORIDE; AMILORIDE; ANTINEOPLASTIC AGENT; CISPLATIN; DOCETAXEL; DOXORUBICIN; TAXOID;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER; BREAST CANCER CELL LINE; CELL CYCLE; CELL KILLING; CELL SUBPOPULATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG MECHANISM; EC50; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; LYSOSOME; MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; BREAST NEOPLASMS; CELL SURVIVAL; DRUG SCREENING; ENZYMOLOGY; FEMALE; NECROSIS; TUMOR CELL LINE;

AMILORIDE; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; DOXORUBICIN; DRUG SCREENING ASSAYS, ANTITUMOR; FEMALE; HUMANS; LYSOSOMES; NECROSIS; REACTIVE OXYGEN SPECIES; TAXOIDS;

EID: 84960172508     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2016.02.042     Document Type: Article

References (52)

1. Masui K., Gini B., Wykosky J., Zanca C., Mischel P.S., Furnari F.B., et al. A tale of two approaches: complementary mechanisms of cytotoxic and targeted therapy resistance may inform next-generation cancer treatments. Carcinogenesis 2013, 34:725-738.
2. Liu S.Q., Yu J.P., Yu H.G., Lv P., Chen H.L. Activation of Akt and ERK signalling pathways induced by etoposide confer chemoresistance in gastric cancer cells. Dig. Liver Dis 2005, 38:310-318.
3. Marquez R.T., Tsao B.W., Faust N.F., Xu L. Drug Resistance and Molecular Cancer Therapy: Apoptosis Versus Autophagy 2013.
4. Salako L.A., Smith A.J. Changes in sodium pool and kinetics of sodium transport in frog skin produced by amiloride. Br. J. Pharmacol 1970, 39:99-109.
5. Kleyman T.R., Cragoe E.J. Cation transport probes: the amiloride series. Methods Enzymol 1990, 191:739-755.
6. Ponte-Sucre A. Availability and applications of ATP-binding cassette (ABC) transporter blockers. Appl. Microbiol. Biotechnol 2007, 76:279-286.
7. Vassalli J.D., Belin D. Amiloride selectively inhibits the urokinase-type plasminogen activator. FEBS Lett 1987, 214:187-191.
8. Wang Y., Jones C.J., Dang J., Liang X., Olsen J.E., Doe W.F. Human urokinase receptor expression is inhibited by amiloride and induced by tumor necrosis factor and phorbol ester in colon cancer cells. FEBS Lett 1994, 353:138-142.
9. Wang Y., Dang J., Liang X., Doe W. Amiloride modulates urokinase gene expression at both transcription and post-transcription levels in human colon cancer cells. Clin. Exp. Metastasis 1995, 13:196-202.
10. Lubin M., Cahn F., Coutermarsh B.A. Amiloride, protein synthesis, and activation of quiescent cells. J. Cell. Physiol 1982, 113:247-251.
11. Matthews H., Ranson M., Kelso M.J. Anti-tumour/metastasis effects of the potassium-sparing diuretic amiloride: an orally active anti-cancer drug waiting for its call-of-duty?. Int. J. Cancer 2011, 129:2051-2061.
12. Hegde M., Roscoe J., Cala P., Gorin F. Amiloride kills malignant glioma cells independent of its inhibition of the sodium-hydrogen exchanger. J. Pharmacol. Exp. Ther 2004, 310:67-74.
13. Pasupuleti N., Leon L., Carraway K.L., Gorin F. 5-Benzylglycinyl-amiloride kills proliferating and nonproliferating malignant glioma cells through caspase-independent necroptosis mediated by apoptosis-inducing factor. J. Pharmacol. Exp. Ther 2013, 344:600-615.
14. Leon L.J., Pasupuleti N., Gorin F., Carraway K.L. A cell-permeant amiloride derivative induces caspase-independent, AIF-mediated programmed necrotic death of breast cancer cells. PLoS ONE 2013, 8:e63038.
15. Pasupuleti N., Grodzki A.C., Gorin F. Mis-trafficking of endosomal urokinase proteins triggers drug-induced glioma nonapoptotic cell death. Mol. Pharmacol 2015, 87:683-696.
16. Cheng J.M., Ding M., Aribi A., Shah P., Rao K. Loss of RAB25 expression in breast cancer. Int. J. Cancer 2006, 118:2957-2964.
17. Miller J.K., Shattuck D.L., Ingalla E.Q., Yen L., Borowsky A.D., Young L.J.T., et al. Suppression of the negative regulator LRIG1 contributes to ErbB2 overexpression in breast cancer. Cancer Res 2008, 68:8286-8294.
18. Borowsky A.D., Namba R., Young L.J., Hunter K.W., Hodgson J.G., Tepper C.G., et al. Syngeneic mouse mammary carcinoma cell lines: two closely related cell lines with divergent metastatic behavior. Clin. Exp. Metastasis 2005, 22:47-59.
19. Schierack P., Nordhoff M., Pollmann M., Weyrauch K., Amasheh S., Lodemann U., et al. Characterization of a porcine intestinal epithelial cell line for in vitro studies of microbial pathogenesis in swine. Histochem. Cell Biol 2006, 125:293-305.
20. Kasibhatla S., Amarante-Mendes G.P., Finucane D., Brunner T., Bossy-Wetzel E., Green D.R. Acridine orange/ethidium bromide (AO/EB) staining to detect apoptosis. CSH Protoc 2006, 2006. pdb.prot4493.
21. Giansanti V., Santamaria G., Torriglia A., Aredia F., Scovassi A., Bottiroli G., et al. Fluorescence properties of the Na+/H+ exchanger inhibitor HMA (5-(N,N-hexamethylene) amiloride) are modulated by intracellular pH. Eur. J. Histochem 2012, 56:e3.
22. Searle J., Kerr J.F., Bishop C.J. Necrosis and apoptosis: distinct modes of cell death with fundamentally different significance. Pathol. Annu 1982, 17(Pt 2):229-259.
23. Ribble D., Goldstein N.B., Norris D.A., Shellman Y.G. A simple technique for quantifying apoptosis in 96-well plates. BMC Biotechnol 2005, 5:12.
24. Vanden Berghe T., Grootjans S., Goossens V., Dondelinger Y., Krysko D.V., Takahashi N., et al. Determination of apoptotic and necrotic cell death in vitro and in vivo. Methods 2013, 61:117-129.
25. Hariri M., Millane G., Guimond M.-P., Guay G., Dennis J.W., Nabi I.R. Biogenesis of multilamellar bodies via autophagy. Mol. Biol. Cell 2000, 11:255-268.
26. Berghe T.V., Linkermann A., Jouan-Lanhouet S., Walczak H., Vandenabeele P. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat. Rev. Mol. Cell Biol 2014, 15:135-147.
27. Degterev A., Huang Z., Boyce M., Li Y., Jagtap P., Mizushima N., et al. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol 2005, 1:112-119.
28. Li J.X., Feng J.M., Wang Y., Li X.H., Chen X.X., Su Y., et al. The B-Raf(V600E) inhibitor dabrafenib selectively inhibits RIP3 and alleviates acetaminophen-induced liver injury. Cell Death Dis 2014, 5:e1278.
29. Sun L., Wang H., Wang Z., He S., Chen S., Liao D., et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 2012, 148:213-227.
30. Zhao J., Jitkaew S., Cai Z., Choksi S., Li Q., Luo J., et al. Mixed lineage kinase domain-like is a key receptor interacting protein 3 downstream component of TNF-induced necrosis. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:5322-5327.
31. McCall K. Genetic control of necrosis - another type of programmed cell death. Curr. Opin. Cell Biol 2010, 22:882-888.
32. Kim S.J., Li J. Caspase blockade induces RIP3-mediated programmed necrosis in Toll-like receptor-activated microglia. Cell Death Dis 2013, 4:e716.
33. Fortes G.B., Alves L.S., de Oliveira R., Dutra F.F., Rodrigues D., Fernandez P.L., et al. Heme induces programmed necrosis on macrophages through autocrine TNF and ROS production. Blood 2012, 119:2368-2375.
34. Bursch W., Ellinger A., Gerner C., Frohwein U., Schulte-Hermann R. Programmed cell death (PCD). Apoptosis, autophagic PCD, or others?. Ann. N. Y. Acad. Sci 2000, 926:1-12.
35. Aredia F., Giansanti V., Mazzini G., Savio M., Ortiz L., Jaadane I., et al. Multiple effects of the Na+/H+ antiporter inhibitor HMA on cancer cells. Apoptosis 2013, 18:1586-1598.
36. Seglen P.O., Gordon P.B. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. U.S.A. 1982, 79:1889-1892.
37. Puertollano R. mTOR and lysosome regulation. F1000Prime Rep 2014, 6:52.
38. Liu Q., Qiu J., Liang M., Golinski J., van Leyen K., Jung J.E., et al. Akt and mTOR mediate programmed necrosis in neurons. Cell Death Dis 2014, 5:e1084.
39. Martelotto L., Ng C., Piscuoglio S., Weigelt B., Reis-Filho J. Breast cancer intra-tumor heterogeneity. Breast Cancer Res 2014, 16:210.
40. Polyak K. Heterogeneity in breast cancer. J. Clin. Invest 2011, 121:3786-3788.
41. Reshkin S.J., Bellizzi A., Caldeira S., Albarani V., Malanchi I., Poignee M., et al. Na+/H+ exchanger-dependent intracellular alkalinization is an early event in malignant transformation and plays an essential role in the development of subsequent transformation-associated phenotypes. FASEB J. 2000, 14:2185-2197.
42. Costa C.J., Kirschner L.B., Cragoe E.J. Intracellular binding of spin-labeled amiloride: an alternative explanation for amiloride's effects at high concentration. J. Cell. Physiol 1987, 130:392-396.
43. Yuan T.L., Cantley L.C. PI3K pathway alterations in cancer: variations on a theme. Oncogene 2008, 27:5497-5510.
44. Davis R.J., Czech M.P. Amiloride directly inhibits growth factor receptor tyrosine kinase activity. J. Biol. Chem 1985, 260:2543-2551.
45. Cho Y.-L., Lee K.-S., Lee S.-J., Namkoong S., Kim Y.-M., Lee H., et al. Amiloride potentiates TRAIL-induced tumor cell apoptosis by intracellular acidification-dependent Akt inactivation. Biochem. Biophys. Res. Commun 2005, 326:752-758.
46. Lin Y., Choksi S., Shen H.M., Yang Q.F., Hur G.M., Kim Y.S., et al. Tumor necrosis factor-induced nonapoptotic cell death requires receptor-interacting protein-mediated cellular reactive oxygen species accumulation. J. Biol. Chem 2004, 279:10822-10828.
47. Sakon S., Xue X., Takekawa M., Sasazuki T., Okazaki T., Kojima Y., et al. NF-κB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J. 2003, 22:3898-3909.
48. Shen H.M., Lin Y., Choksi S., Tran J., Jin T., Chang L., et al. Essential roles of receptor-interacting protein and TRAF2 in oxidative stress-induced cell death. Mol. Cell. Biol 2004, 24:5914-5922.
49. Benhar M., Dalyot I., Engelberg D., Levitzki A. Enhanced ROS production in oncogenically transformed cells potentiates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase activation and sensitization to genotoxic stress. Mol. Cell. Biol 2001, 21:6913-6926.
50. Zoncu R., Bar-Peled L., Efeyan A., Wang S., Sancak Y., Sabatini D.M. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the Vacuolar H(+)-ATPase. Science 2011, 334:678-683.
51. Soltoff S.P., Mandel L.J. Amiloride directly inhibits the Na,K-ATPase activity of rabbit kidney proximal tubules. Science 1983, 220:957-958.
52. Scaringi L., Cornacchione P., Ayroldi E., Corazzi L., Capodicasa E., Rossi R., et al. Omeprazole induces apoptosis in jurkat cells. Int. J. Immunopathol. Pharmacol 2004, 17:331-342.