The Vacuolar ATPase a2-subunit regulates Notch signaling in triple-negative breast cancer cells

Oncotarget

Volumn 6, Issue 33, 2015, Pages 34206-34220

  Pamarthy, Sahithi ^a   Jaiswal, Mukesh K ^a   Kulshreshtha, Arpita ^a   Katara, Gajendra K ^a   Gilman Sachs, Alice ^a   Beaman, Kenneth D ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

a2V ATPase; Autophagy; Bafilomycin; Notch signaling; Triple negative breast cancer

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BAFILOMYCIN A1; BETA CATENIN; NOTCH RECEPTOR; NOTCH1 INTRACELLULAR DOMAIN; NOTCH1 RECEPTOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VACUOLAR ADENOSINE TRIPHOSPHATASE A2; NOTCH1 PROTEIN, HUMAN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ACIDIFICATION; ARTICLE; AUTOPHAGY; BREAST CANCER CELL LINE; BREAST CARCINOGENESIS; CANCER TISSUE; CELL MEMBRANE; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOLYSOSOME; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; LYSOSOME; MIGRATION INHIBITION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER; APOPTOSIS; FEMALE; FLOW CYTOMETRY; GENETIC TRANSFECTION; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

APOPTOSIS; CELL LINE, TUMOR; FEMALE; FLOW CYTOMETRY; GENE KNOCKDOWN TECHNIQUES; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; RECEPTOR, NOTCH1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION; TRIPLE NEGATIVE BREAST NEOPLASMS; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84946552068     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5275     Document Type: Article

References (61)

1. Bandyopadhyay S, Ali-Fehmi R. Breast carcinoma: molecular profiling and updates. Clinics in laboratory medicine. 2013; 33:891-909.
2. O'Brien KM, Cole SR, Tse CK, Perou CM, Carey LA, Foulkes WD, Dressler LG, Geradts J, Millikan RC. Intrinsic breast tumor subtypes, race, and long-term survival in the Carolina Breast Cancer Study. Clinical cancer research: an official journal of the American Association for Cancer Research. 2010; 16:6100-6110.
3. O'Toole SA, Beith JM, Millar EK, West R, McLean A, Cazet A, Swarbrick A, Oakes SR. Therapeutic targets in triple negative breast cancer. Journal of clinical pathology. 2013; 66:530-542.
4. Mahamodhossen YA, Liu W, Rong-Rong Z. Triple-negative breast cancer: new perspectives for novel therapies. Med Oncol. 2013; 30:653.
5. Ntziachristos P, Lim JS, Sage J, Aifantis I. From fly wings to targeted cancer therapies: a centennial for notch signaling. Cancer cell. 2014; 25:318-334.
6. Raafat A, Goldhar AS, Klauzinska M, Xu K, Amirjazil I, McCurdy D, Lashin K, Salomon D, Vonderhaar BK, Egan S, Callahan R. Expression of Notch receptors, ligands, and target genes during development of the mouse mammary gland. Journal of cellular physiology. 2011; 226:1940-1952.
7. Sale S, Lafkas D, Artavanis-Tsakonas S. Notch2 genetic fate mapping reveals two previously unrecognized mammary epithelial lineages. Nature cell biology. 2013; 15:451-460.
8. Capaccione KM, Pine SR. The Notch signaling pathway as a mediator of tumor survival. Carcinogenesis. 2013; 34:1420-1430.
9. Stylianou S, Clarke RB, Brennan K. Aberrant activation of notch signaling in human breast cancer. Cancer research. 2006; 66:1517-1525.
10. Reedijk M, Odorcic S, Chang L, Zhang H, Miller N, McCready DR, Lockwood G, Egan SE. High-level coexpression of JAG1 and NOTCH1 is observed in human breast cancer and is associated with poor overall survival. Cancer research. 2005; 65:8530-8537.
11. Clementz AG, Rogowski A, Pandya K, Miele L, Osipo C. NOTCH-1 and NOTCH-4 are novel gene targets of PEA3 in breast cancer: novel therapeutic implications. Breast cancer research: BCR. 2011; 13:R63.
12. Lee CW, Simin K, Liu Q, Plescia J, Guha M, Khan A, Hsieh CC, Altieri DC. A functional Notch-survivin gene signature in basal breast cancer. Breast cancer research: BCR. 2008; 10:R97.
13. Cruciat CM, Ohkawara B, Acebron SP, Karaulanov E, Reinhard C, Ingelfinger D, Boutros M, Niehrs C. Requirement of prorenin receptor and vacuolar H+-ATPase-mediated acidification for Wnt signaling. Science. 2010; 327:459-463.
14. Kobia F, Duchi S, Deflorian G, Vaccari T. Pharmacologic inhibition of vacuolar H+ ATPase reduces physiologic and oncogenic Notch signaling. Molecular oncology. 2014; 8:207-220.
15. Lange C, Prenninger S, Knuckles P, Taylor V, Levin M, Calegari F. The H(+) vacuolar ATPase maintains neural stem cells in the developing mouse cortex. Stem cells and development. 2011; 20:843-850.
16. Sethi N, Yan Y, Quek D, Schupbach T, Kang Y. Rabconnectin-3 is a functional regulator of mammalian Notch signaling. The Journal of biological chemistry. 2010; 285:34757-34764.
17. Valapala M, Hose S, Gongora C, Dong L, Wawrousek EF, Samuel Zigler J Jr., Sinha D. Impaired endolysosomal function disrupts Notch signalling in optic nerve astrocytes. Nature communications. 2013; 4:1629.
18. Vaccari T, Duchi S, Cortese K, Tacchetti C, Bilder D. The vacuolar ATPase is required for physiological as well as pathological activation of the Notch receptor. Development. 2010; 137:1825-1832.
19. Sennoune SR, Martinez-Zaguilan R. Vacuolar H(+)-ATPase signaling pathway in cancer. Current protein & peptide science. 2012; 13:152-163.
20. Toei M, Saum R, Forgac M. Regulation and isoform function of the V-ATPases. Biochemistry. 2010; 49:4715-4723.
21. Hinton A, Sennoune SR, Bond S, Fang M, Reuveni M, Sahagian GG, Jay D, Martinez-Zaguilan R, 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. The Journal of biological chemistry. 2009; 284:16400-16408.
22. Capecci J, Forgac M. The function of vacuolar ATPase (V-ATPase) a subunit isoforms in invasiveness of MCF10a and MCF10CA1a human breast cancer cells. The Journal of biological chemistry. 2013; 288:32731-32741.
23. Jaiswal MK, Katara GK, Mallers T, Chaouat G, GilmanSachs A, Beaman KD. Vacuolar-ATPase isoform a2 regulates macrophages and cytokine profile necessary for normal spermatogenesis in testis. Journal of leukocyte biology. 2014; 96:337-347.
24. Jaiswal MK, Mallers TM, Larsen B, Kwak-Kim J, Chaouat G, Gilman-Sachs A, Beaman KD. V-ATPase upregulation during early pregnancy: a possible link to establishment of an inflammatory response during preimplantation period of pregnancy. Reproduction. 2012; 143:713-725.
25. Kwong C, Gilman-Sachs A, Beaman K. Tumor-associated a2 vacuolar ATPase acts as a key mediator of cancer-related inflammation by inducing pro-tumorigenic properties in monocytes. J Immunol. 2011; 186:1781-1789.
26. Kwong C, Gilman-Sachs A, Beaman K. An independent endocytic pathway stimulates different monocyte subsets by the a N-terminus domain of vacuolar-ATPase. Oncoimmunology. 2013; 2:e22978.
27. Gilman-Sachs A, Tikoo A, Akman-Anderson L, Jaiswal M, Ntrivalas E, Beaman K. Expression and role of a2 vacuolarATPase (a2V) in trafficking of human neutrophil granules and exocytosis. Journal of leukocyte biology. 2015.
28. Jaiswal MK, Agrawal V, Mallers T, Gilman-Sachs A, Hirsch E, Beaman KD. Regulation of apoptosis and innate immune stimuli in inflammation-induced preterm labor. J Immunol. 2013; 191:5702-5713.
29. Katara GK, Jaiswal MK, Kulshrestha A, Kolli B, GilmanSachs A, Beaman KD. Tumor-associated vacuolar ATPase subunit promotes tumorigenic characteristics in macrophages. Oncogene. 2014; 33:5649-5654.
30. Kornak U, Reynders E, Dimopoulou A, van Reeuwijk J, Fischer B, Rajab A, Budde B, Nurnberg P, Foulquier F, Lefeber D, Urban Z, Gruenewald S, Annaert W, Brunner HG, van Bokhoven H, Wevers R, et al. Impaired glycosylation and cutis laxa caused by mutations in the vesicular H+-ATPase subunit ATP6V0A2. Nature genetics. 2008; 40:32-34.
31. Kandachar V, Roegiers F. Endocytosis and control of Notch signaling. Current opinion in cell biology. 2012; 24:534-540.
32. Baron M. Endocytic routes to Notch activation. Seminars in cell & developmental biology. 2012; 23:437-442.
33. Agrawal V, Jaiswal MK, Mallers T, Katara GK, GilmanSachs A, Beaman KD, Hirsch E. Altered autophagic flux enhances inflammatory responses during inflammationinduced preterm labor. Scientific reports. 2015; 5:9410.
34. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell structure and function. 1998; 23:33-42.
35. Lopez-Knowles E, Zardawi SJ, McNeil CM, Millar EK, Crea P, Musgrove EA, Sutherland RL, O'Toole SA. Cytoplasmic localization of beta-catenin is a marker of poor outcome in breast cancer patients. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 2010; 19:301-309.
36. Xu J, Chen Y, Huo D, Khramtsov A, Khramtsova G, Zhang C, Goss KH, Olopade OI. beta-catenin regulates c-Myc and CDKN1A expression in breast cancer cells. Molecular carcinogenesis. 2015.
37. Collu GM, Brennan K. Cooperation between Wnt and Notch signalling in human breast cancer. Breast cancer research: BCR. 2007; 9:105.
38. Jia Z, Wang J, Wang W, Tian Y, XiangWei W, Chen P, Ma K, Zhou C. Autophagy eliminates cytoplasmic betacatenin and NICD to promote the cardiac differentiation of P19CL6 cells. Cellular signalling. 2014; 26:2299-2305.
39. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Yoshimori T, Pierron G, Codogno P, Kroemer G. Inhibition of macroautophagy triggers apoptosis. Molecular and cellular biology. 2005; 25:1025-1040.
40. Wu YC, Wu WK, Li Y, Yu L, Li ZJ, Wong CC, Li HT, Sung JJ, Cho CH. Inhibition of macroautophagy by bafilomycin A1 lowers proliferation and induces apoptosis in colon cancer cells. Biochemical and biophysical research communications. 2009; 382:451-456.
41. Yuan N, Song L, Zhang S, Lin W, Cao Y, Xu F, Fang Y, Wang Z, Zhang H, Li X, Cai J, Wang J, Zhang Y, Mao X, Zhao W, Hu S, et al. Bafilomycin A1 targets both autophagy and apoptosis pathways in pediatric B-cell acute lymphoblastic leukemia. Haematologica. 2014.
42. Katara GK, Kulshrestha A, Jaiswal MK, Pamarthy S, Gilman-Sachs A, Beaman KD. Inhibition of vacuolar ATPase subunit in tumor cells delays tumor growth by decreasing the essential macrophage population in the tumor microenvironment. Oncogene. 2015.
43. Sennoune SR, Martinez-Zaguilan R. Plasmalemmal vacuolar H+-ATPases in angiogenesis, diabetes and cancer. Journal of bioenergetics and biomembranes. 2007; 39:427-433.
44. Kulshrestha A, Katara GK, Ibrahim S, Pamarthy S, Jaiswal MK, Sachs AG, Beaman KD. Vacuolar ATPase 'a2' isoform exhibits distinct cell surface accumulation and modulates matrix metalloproteinase activity in ovarian cancer. Oncotarget. 2015; 6:3797-3810.
45. Chinchar E, Makey KL, Gibson J, Chen F, Cole SA, Megason GC, Vijayakumar S, Miele L, Gu JW. Sunitinib significantly suppresses the proliferation, migration, apoptosis resistance, tumor angiogenesis and growth of triplenegative breast cancers but increases breast cancer stem cells. Vascular cell. 2014; 6:12.
46. Qiu M, Peng Q, Jiang I, Carroll C, Han G, Rymer I, Lippincott J, Zachwieja J, Gajiwala K, Kraynov E, Thibault S, Stone D, Gao Y, Sofia S, Gallo J, Li G, et al. Specific inhibition of Notch1 signaling enhances the antitumor efficacy of chemotherapy in triple negative breast cancer through reduction of cancer stem cells. Cancer letters. 2013; 328:261-270.
47. Windler SL, Bilder D. Endocytic internalization routes required for delta/notch signaling. Current biology: CB. 2010; 20:538-543.
48. Vaccari T, Bilder D. The Drosophila tumor suppressor vps25 prevents nonautonomous overproliferation by regulating notch trafficking. Developmental cell. 2005; 9:687-698.
49. Gagliardi M, Piddini E, Vincent JP. Endocytosis: a positive or a negative influence on Wnt signalling? Traffic. 2008; 9:1-9.
50. Wada Y, Sun-Wada GH. Positive and negative regulation of developmental signaling by the endocytic pathway. Current opinion in genetics & development. 2013; 23:391-398.
51. Marshansky V. The V-ATPase a2-subunit as a putative endosomal pH-sensor. Biochemical Society transactions. 2007; 35:1092-1099.
52. Barth JM, Hafen E, Kohler K. The lack of autophagy triggers precocious activation of Notch signaling during Drosophila oogenesis. BMC developmental biology. 2012; 12:35.
53. Barth JM, Kohler K. How to take autophagy and endocytosis up a notch. BioMed research international. 2014; 2014:960803.
54. Cicchini M, Chakrabarti R, Kongara S, Price S, Nahar R, Lozy F, Zhong H, Vazquez A, Kang Y, Karantza V. Autophagy regulator BECN1 suppresses mammary tumorigenesis driven by WNT1 activation and following parity. Autophagy. 2014; 10:2036-2052.
55. Gao C, Cao W, Bao L, Zuo W, Xie G, Cai T, Fu W, Zhang J, Wu W, Zhang X, Chen YG. Autophagy negatively regulates Wnt signalling by promoting Dishevelled degradation. Nature cell biology. 2010; 12:781-790.
56. 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, Vollmar AM. The V-ATPase-inhibitor archazolid abrogates tumor metastasis via inhibition of endocytic activation of the Rho-GTPase Rac1. Cancer research. 2012; 72:5976-5987.
57. Cotter K, Capecci J, Sennoune S, Huss M, Maier M, Martinez-Zaguilan R, Forgac M. Activity of Plasma Membrane V-ATPases is Critical for the Invasion of MDA-MB231 Breast Cancer Cells. The Journal of biological chemistry. 2014;.
58. Wang YC, He F, Feng F, Liu XW, Dong GY, Qin HY, Hu XB, Zheng MH, Liang L, Feng L, Liang YM, Han H. Notch signaling determines the M1 versus M2 polarization of macrophages in antitumor immune responses. Cancer research. 2010; 70:4840-4849.
59. Osipo C, Golde TE, Osborne BA, Miele LA. Off the beaten pathway: the complex cross talk between Notch and NF-kappaB. Laboratory investigation; a journal of technical methods and pathology. 2008; 88:11-17.
60. Boomer JS, Derks RA, Lee GW, DuChateau BK, Gilman-Sachs A, Beaman KD. Regeneration and tolerance factor is expressed during T-lymphocyte activation and plays a role in apoptosis. Human immunology. 2001; 62:577-588.
61. Teixeira Gomes RC, Verna C, Nader HB, dos Santos Simoes R, Dreyfuss JL, Martins JR, Baracat EC, de Jesus Simoes M, Soares JM Jr. Concentration and distribution of hyaluronic acid in mouse uterus throughout the estrous cycle. Fertility and sterility. 2009; 92:785-792.