Breast cancer associated a2 isoform vacuolar ATPase immunomodulates neutrophils: Potential role in tumor progression

Oncotarget

Volumn 6, Issue 32, 2015, Pages 33033-33045

  Ibrahim, Safaa A ^a,b   Katara, Gajendra K ^a   Kulshrestha, Arpita ^a   Jaiswal, Mukesh K ^a   Amin, Magdy A ^b   Beaman, Kenneth D ^a  

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

^b CAIRO UNIVERSITY   (Egypt)

Author keywords

A2 vacuolar ATPase; Angiogenesis; Breast cancer; Invasion; Tumor associated neutrophils

Indexed keywords

A2 ISOFORM VACUOLAR ATPASE; ADENOSINE TRIPHOSPHATASE; GELATINASE B; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR ALPHA; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; SECONDARY LYMPHOID TISSUE CHEMOKINE; UNCLASSIFIED DRUG; VASCULOTROPIN; ISOENZYME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ADULT; ANGIOGENESIS; ARTICLE; BLOOD VESSEL DENSITY; BLOOD VESSEL PARAMETERS; BREAST CANCER; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; INFLAMMATION; NEUTROPHIL; NORMAL HUMAN; PROTEIN EXPRESSION; TUMOR GROWTH; BREAST TUMOR; ENZYMOLOGY; FEMALE; IMMUNOLOGY; MCF-7 CELL LINE; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; TUMOR MICROENVIRONMENT; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULARIZATION;

BREAST NEOPLASMS; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; ISOENZYMES; MCF-7 CELLS; NEOVASCULARIZATION, PATHOLOGIC; NEUTROPHILS; TUMOR MICROENVIRONMENT; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84946050055     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5439     Document Type: Article

References (53)

1. Cortez-Retamozo V, Etzrodt M, Newton A, Rauch PJ, Chudnovskiy A, Berger C, et al. Origins of tumorassociated macrophages and neutrophils. Proc. Natl. Acad. Sci. 2012; 109:2491-6.
2. Mantovani A. Macrophages, Neutrophils, and Cancer: A Double Edged Sword. New J. Sci. 2014; Article ID 271940.
3. Queen MM, Ryan RE, Holzer RG, Keller-Peck CR, Jorcyk CL. Breast cancer cells stimulate neutrophils to produce oncostatin M: potential implications for tumor progression. Cancer Res. 2005; 65:8896-904.
4. Swierczak A. The role of myeloid cells in breast cancer metastasis. 2012.
5. Acharyya S, Oskarsson T, Vanharanta S, Malladi S, Kim J, Morris PG, et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell. 2012; 150:165-78.
6. Katara GK, Jaiswal MK, Kulshrestha A, Kolli B, Gilman-Sachs A, Beaman KD. Tumor-associated vacuolar ATPase subunit promotes tumorigenic characteristics in macrophages. Oncogene. 2014; 33:5649-54.
7. Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, et al. Polarization of tumor-associated neutrophil phenotype by TGF-β:"N1" versus "N2" TAN. Cancer Cell. 2009; 16:183-94.
8. Eruslanov EB, Bhojnagarwala PS, Quatromoni JG, Stephen TL, Ranganathan A, Deshpande C, et al. Tumorassociated neutrophils stimulate T cell responses in earlystage human lung cancer. J. Clin. Invest. 2014; 124:5466-80.
9. Fridlender ZG, Sun J, Mishalian I, Singhal S, Cheng G, Kapoor V, et al. Transcriptomic analysis comparing tumorassociated neutrophils with granulocytic myeloid-derived suppressor cells and normal neutrophils. PloS One. 2012; 7:e31524.
10. Kuang D-M, Zhao Q, Wu Y, Peng C, Wang J, Xu Z, et al. Peritumoral neutrophils link inflammatory response to disease progression by fostering angiogenesis in hepatocellular carcinoma. J. Hepatol. 2011; 54:948-55.
11. 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:C1443-52.
12. Feng S, Zhu G, McConnell M, Deng L, Zhao Q, Wu M, et al. Silencing of atp6v1c1 prevents breast cancer growth and bone metastasis. Int. J. Biol. Sci. 2013; 9:853.
13. 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; 280:110-9.
14. Von Schwarzenberg K, Lajtos T, Simon L, Müller R, Vereb G, Vollmar AM. V-ATPase inhibition overcomes trastuzumab resistance in breast cancer. Mol. Oncol. 2014; 8:9-19.
15. Wiedmann RM, von Schwarzenberg K, Palamidessi A, Schreiner L, Kubisch R, Liebl J, et al. The V-ATPaseinhibitor archazolid abrogates tumor metastasis via inhibition of endocytic activation of the Rho-GTPase Rac1. Cancer Res. 2012; 72:5976-87.
16. 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-1β production. Hum. Immunol. 2007; 68:469-77.
17. 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; 186:1781-9.
18. 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.
19. 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; 143:713-25.
20. Ntrivalas E, Gilman-Sachs A, Kwak-Kim J, Beaman K. The N-terminus Domain of the a2 Isoform of Vacuolar ATPase Can Regulate Interleukin-1β Production from Mononuclear Cells in Co-culture with JEG-3 Choriocarcinoma Cells. Am. J. Reprod. Immunol. 2007; 57:201-9.
21. 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. doi: 10.1038/onc.2015.159. [Epub ahead of print]
22. Mandal M, Beaman KD. Purification and Characterization of a Pregnancy-Associated Protein: TJ6s. Am. J. Reprod. Immunol. 1995; 33:60-7.
23. Beaman K, Angkachatchai V, Gilman-Sachs A. TJ6: The Pregnancy-Associated Cytokine. Am. J. Reprod. Immunol. 1996; 35:338-41.
24. Lee GW, Boomer JS, Gilman-Sachs A, Chedid A, Gudelj L, Rukavina D, et al. Regeneration and tolerance factor of the human placenta induces IL-10 production. Eur. J. Immunol. 2001; 31:687-91.
25. Roth P, Aulwurm S, Gekel I, Beier D, Sperry RG, Mittelbronn M, et al. Regeneration and tolerance factor: a novel mediator of glioblastoma-associated immunosuppression. Cancer Res. 2006; 66:3852-8.
26. Jubb AM, Soilleux EJ, Turley H, Steers G, Parker A, Low I, et al. Expression of vascular notch ligand delta-like 4 and inflammatory markers in breast cancer. Am. J. Pathol. 2010; 176:2019-28.
27. Tazzyman S, Lewis CE, Murdoch C. Neutrophils: key mediators of tumour angiogenesis. Int. J. Exp. Pathol. 2009; 90:222-31.
28. Gregory AD, Houghton AM. Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res. 2011; 71:2411-6.
29. Nozawa H, Chiu C, Hanahan D. Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc. Natl. Acad. Sci. 2006; 103:12493-8.
30. Wu Q-W, Yang Q-M, Huang Y-F, She H-Q, Liang J, Yang Q-L, et al. Expression and clinical significance of matrix metalloproteinase-9 in lymphatic invasiveness and metastasis of breast cancer. PloS One. 2014; 9:e97804.
31. Lu X, Qin W. Deep Insight Section. HttpAtlasGenetics Oncology Org. 2012; 252.
32. Fais S, De Milito A, You H, Qin W. Targeting vacuolar H+-ATPases as a new strategy against cancer. Cancer Res. 2007; 67:10627-30.
33. Von Schwarzenberg K, Wiedmann RM, Oak P, Schulz S, Zischka H, Wanner G, et al. Mode of cell death induction by pharmacological vacuolar H+-ATPase (V-ATPase) inhibition. J. Biol. Chem. 2013; 288:1385-96.
34. Derks R, Beaman K. Regeneration and tolerance factor modulates the effect of adenosine triphosphate-induced interleukin 1β secretion in human macrophages. Hum. Immunol. 2004; 65:676-82.
35. Kulshrestha A, Katara GK, Ibrahim S, Pamarthy S, Jaiswal MK, Sachs AG, et al. Vacuolar ATPase "a2" isoform exhibits distinct cell surface accumulation and modulates matrix metalloproteinase activity in ovarian cancer. Oncotarget. 2015; 6:3797.
36. Subik K, Lee J-F, Baxter L, Strzepek T, Costello D, Crowley P, et al. The expression patterns of ER, PR, HER2, CK5/6, EGFR, Ki-67 and AR by immunohistochemical analysis in breast cancer cell lines. Breast Cancer Basic Clin. Res. 2010; 4:35.
37. Kennecke H, Yerushalmi R, Woods R, Cheang MCU, Voduc D, Speers CH, et al. Metastatic behavior of breast cancer subtypes. J. Clin. Oncol. 2010; 28:3271-7.
38. Mantovani A, Allavena P, Sica A, Balkwill F. Cancerrelated inflammation. Nature. 2008; 454:436-44.
39. Johansson M, DeNardo DG, Coussens LM. Polarized immune responses differentially regulate cancer development. Immunol. Rev. 2008; 222:145-54.
40. Mantovani A. The yin-yang of tumor-associated neutrophils. Cancer Cell. 2009; 16:173-4.
41. Wislez M, Rabbe N, Marchal J, Milleron B, Crestani B, Mayaud C, et al. Hepatocyte growth factor production by neutrophils infiltrating bronchioloalveolar subtype pulmonary adenocarcinoma role in tumor progression and death. Cancer Res. 2003; 63:1405-12.
42. Jensen HK, Donskov F, Marcussen N, Nordsmark M, Lundbeck F, von der Maase H. Presence of intratumoral neutrophils is an independent prognostic factor in localized renal cell carcinoma. J. Clin. Oncol. 2009; 27:4709-17.
43. Reid MD, Basturk O, Thirabanjasak D, Hruban RH, Klimstra DS, Bagci P, et al. Tumor-infiltrating neutrophils in pancreatic neoplasia. Mod. Pathol. 2011; 24:1612-9.
44. Ben-Baruch A. Host microenvironment in breast cancer development: Inflammatory cells, cytokines and chemokines in breast cancer progression-reciprocal tumor-microenvironment interactions. Breast Cancer Res. 2002; 5:31.
45. Leek RD, Landers R, Fox SB, Ng F, Harris AL, Lewis CE. Association of tumour necrosis factor alpha and its receptors with thymidine phosphorylase expression in invasive breast carcinoma. Br. J. Cancer. 1998; 77:2246.
46. Madhusudan S, Foster M, Muthuramalingam SR, Braybrooke JP, Wilner S, Kaur K, et al. A phase II study of etanercept (Enbrel), a tumor necrosis factor a inhibitor in patients with metastatic breast cancer. Clin. Cancer Res. 2004; 10:6528-34.
47. Kurebayashi J. Regulation of interleukin-6 secretion from breast cancer cells and its clinical implications. Breast Cancer. 2000; 7:124-9.
48. Jin L, Yuan RQ, Fuchs A, Yao Y, Joseph A, Schwall R, et al. Expression of interleukin-1β in human breast carcinoma. Cancer. 1997; 80:421-34.
49. Ardi VC, Kupriyanova TA, Deryugina EI, Quigley JP. Human neutrophils uniquely release TIMP-free MMP-9 to provide a potent catalytic stimulator of angiogenesis. Proc. Natl. Acad. Sci. 2007; 104:20262-7.
50. Shang K, Bai Y-P, Wang C, Wang Z, Gu H-Y, Du X, et al. Crucial involvement of tumor-associated neutrophils in the regulation of chronic colitis-associated carcinogenesis in mice. PLoS One. 2012; 7:e51848.
51. Coussens LM, Tinkle CL, Hanahan D, Werb Z. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell. 2000; 103:481-90.
52. Hirota Y, Osuga Y, Hirata T, Harada M, Morimoto C, Yoshino O, et al. Activation of protease-activated receptor 2 stimulates proliferation and interleukin (IL)-6 and IL-8 secretion of endometriotic stromal cells. Hum. Reprod. 2005; 20:3547-53.
53. Righi L, Deaglio S, Pecchioni C, Gregorini A, Horenstein AL, Bussolati G, et al. Role of CD31/platelet endothelial cell adhesion molecule-1 expression in in vitro and in vivo growth and differentiation of human breast cancer cells. Am. J. Pathol. 2003; 162:1163-74.