Tumor-associated vacuolar ATPase subunit promotes tumorigenic characteristics in macrophages

Oncogene

Volumn 33, Issue 49, 2014, Pages 5649-5654

  Katara, G K ^a   Jaiswal, M K ^a   Kulshrestha, A ^a   Kolli, B ^a   Gilman Sachs, A ^a   Beaman, K D ^a  

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

Author keywords

a2NTD; a2V ATPase; angiogenesis; invasion assay; M2 macrophages; tumor associated macrophages

Indexed keywords

PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RECOMBINANT PROTEIN;

ANIMAL; BAGG ALBINO MOUSE; CYTOLOGY; DISEASE COURSE; GENE EXPRESSION REGULATION; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MACROPHAGE; METABOLISM; MONOCYTE; MOUSE; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PHENOTYPE; PROTEIN TERTIARY STRUCTURE; T LYMPHOCYTE; TUMOR CELL LINE; TUMOR INVASION;

ANIMALS; CELL LINE, TUMOR; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; LYMPHOCYTE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED BALB C; MONOCYTES; NEOPLASM INVASIVENESS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PHENOTYPE; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; T-LYMPHOCYTES; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84890523431     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.532     Document Type: Article

References (25)

1. Sennoune SR, Luo D, Martínez-Zaguilán R. Plasmalemmal vacuolar-type H+-ATPase in cancer biology. Cell Biochem Biophys 2004; 40: 185-206.
2. Torigoe T, Izumi H, Ishiguchi H, Uramoto H, Murakami T, Ise T et al. Enhanced expression of the human vacuolar H-ATPase c subunit gene (ATP6L) in response to anticancer agents. J Biol Chem 2002; 277: 36534-36543.
3. Sennoune SR, Bakunts K, Martínez GM, Chua-Tuan JL, Kebir Y, Attaya MN et al. Vacuolar H+-ATPase in human breast cancer cells with distinct metastatic potential: distribution and functional activity. Am J Physiol Cell Physiol 2004; 286: C1443-C1452.
4. Ntrivalas E, Gilman-Sachs A, Kwak-Kim J, Beaman K. The N-terminus domain of the a2 isoform of vacuolar ATPase can regulate interleukin- 1b production from mononuclear cells in coculture with JEG-3 choriocarcinoma cells. Am J Reprod Immunol 2007; 57: 201-209.
5. Ntrivalas E, Derks R, Gilman-Sachs A, Kwak-Kim J, Levine R, Beaman K. Novel role for the N-terminus domain of the a2 isoform of vacuolar ATPase in interleukin-1b production. Hum Immunol 2007; 68: 469-477.
6. 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.
7. Jaiswal MK, Mallers TM, Larsen B, Kwak-Kim J, Chaouat G, Gilman-Sachs A et al. 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.
8. Kwong C, Gilman-Sachs A, Beaman K. An independent endocytic pathway stimulates different monocyte subsets by the a2 N-terminus domain of vacuolar- ATPase. Oncoimmunology 2013; 2: e22978.
9. Watkins SK, Egilmez NK, Suttles J, Stout RD. IL-12 rapidly alter the functional profiles of tumor-associated and tumor-infiltrating macrophages in vitro and in vivo. J Immunol 2007; 178: 1357-1362.
10. Martinez FO, Gordon S, Locati M, Manotvani A. Transcriptional profiling of the human monocyte to macrophage differentiation and polarization: new molecules and patterns of gene expression. J Immunol 2006; 199: 7303-7311.
11. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine systems in diverse forms of macrophage activation and polarization. Trends Immunol 2004; 25: 677-686.
12. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 2002; 23: 549-555.
13. Sica A, Schioppa T, Mantovani A, Allavena P. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur J Cancer 2006; 42: 717-727.
14. Hao NB, Lü MH, Fan YH, Cao YL, Zhang ZR, Yang SM. Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012; 2012: 948098.
15. Farber MJ, Rizaldy R, Hildebrand JD. Shroom2 regulates contractility to control endothelial morphogenesis. Mol Biol Cell 2011; 22: 795-805.
16. Martínez-Zaguilán R, Lynch RM, Martinez GM, Gillies RJ. Vacuolar-type H-ATPases are functionally expressed in plasma membranes of human tumor cells. Am J Physiol Cell Physiol 1993; 265: C1015-C1029.
17. Forgac M. Vacuolar ATPases: rotary proton pumps in physiology and pathophysiology. Nat Rev Mol Cell Biol 2007; 8: 917-929.
18. Hinton A, Sennoune SR, Bond S, Fang M, Reuveni M, Sahagian GG et al. 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.
19. Nishisho T, Hata K, Nakanishi M, Morita Y, Sun-Wada GH, Wada Y et al. The a3 isoform vacuolar type H-ATPase promotes distant metastasis in the mouse B16 melanoma cells. Mol Cancer Res 2011; 9: 845-855.
20. De Milito A, Marino ML, Fais S. A rationale for the use of proton pump inhibitors as antineoplastic agents. Curr Pharm Des 2012; 18: 1395-1406.
21. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP dependent transporters. Nat Rev Cancer 2002; 2: 48-58.
22. Lu X, Qin W, Li J, Tan N, Pan D, Zhang H et al. The growth and metastasis of human hepatocellular carcinoma xenografts are inhibited by small interfering RNA targeting to the subunit ATP6L of proton pump. Cancer Res 2005; 65: 6843-6849.
23. You H, Jin J, Shu H, Yu B, De Milito A, Lozupone F et al. Small interfering RNA targeting the subunit ATP6L of proton pump V-ATPase overcomes chemoresistance of breast cancer cells. Cancer Lett 2009; 280: 110-119.
24. Matlack R, Yeh K, Rosini L, Gonzalez D, Taylor J, Silberman D et al. Peritoneal macrophages suppress T-cell activation by amino acid catabolism. Immunology 2006; 117: 386-395.
25. Derks R, Beaman K. Regeneration and tolerance factor modulates the effect of adenosine triphosphate-induced interleukin 1b secretion in human macrophages. Hum Immunol 2004; 65: 676-682.