Skip to main content
Top
Published in: Breast Cancer Research and Treatment 2/2012

01-09-2012 | Preclinical Study

MMP-9 increases HER2/neu expression and alters apoptosis levels in human mammary epithelial cells (HMEC)

Authors: Matilda Fatunmbi, Justin Shelton, Susan M. Aronica

Published in: Breast Cancer Research and Treatment | Issue 2/2012

Login to get access

Abstract

HER2/neu overexpression leads to poorer prognosis and higher risk of disease reoccurrence in breast cancer patients. The causative factors responsible for increasing HER2/neu expression levels on mammary cells are not known. We investigated whether factors associated with inflammation or metastasis could induce HER2/neu expression on human mammary epithelial cells (HMECs). Human mammary epithelial cells and several human breast cancer cell lines used in our studies were treated with several agents, including estrogen and matrix metalloproteinase-9 (MMP-9), either alone or in various combinations. Relative expression of HER2/neu on the surface of target cells was assessed using fluorochrome-tagged antibodies and a fluorescence cytometer. HER2/neu gene expression was also determined by Western blot analysis and PCR. Apoptosis levels were also determined. MMP-9, administered either alone or in combination with interleukin-7 and estrogen, caused a significant rise in HER2/neu expression on the surface of HMECs. The induction in HER2/neu protein expression was suppressed using a MMP-9 inhibitor. Similar results were obtained for breast cancer cells treated with the estrogen in combination with MMP-9. MMP-9 treatment significantly decreased apoptotic levels in HMECs. Our results indicate that MMP-9 is a regulator of HER2/neu expression on human mammary epithelial cells and suggest that upregulation of HER2/neu by MMP-9 may be relevant to altering the characteristics of normal mammary cells toward a transformed phenotype.
Literature
1.
go back to reference Merlo LM, Pepper JW, Reid BJ, Maley CC (2006) Cancer as an evolutionary and ecological process. Nat Rev Cancer 6:924–935PubMedCrossRef Merlo LM, Pepper JW, Reid BJ, Maley CC (2006) Cancer as an evolutionary and ecological process. Nat Rev Cancer 6:924–935PubMedCrossRef
3.
go back to reference Zhang B, Pan X, Cobb GP, Anderson TA (2007) microRNAs as oncogenes and tumor suppressors. Dev Biol 302:1–12PubMedCrossRef Zhang B, Pan X, Cobb GP, Anderson TA (2007) microRNAs as oncogenes and tumor suppressors. Dev Biol 302:1–12PubMedCrossRef
4.
go back to reference Devilee P, Tavassoli F (2003) World Health Organization: tumours of the breast and female genital organs. Oxford University Press, Oxford Devilee P, Tavassoli F (2003) World Health Organization: tumours of the breast and female genital organs. Oxford University Press, Oxford
5.
go back to reference Olayioye MA (2001) Update on HER-2 as a target for cancer therapy: intracellular signaling pathways of ErbB2/HER-2 and family members. Breast Cancer Res 3:385–389PubMedCrossRef Olayioye MA (2001) Update on HER-2 as a target for cancer therapy: intracellular signaling pathways of ErbB2/HER-2 and family members. Breast Cancer Res 3:385–389PubMedCrossRef
6.
go back to reference Ménard S, Casalini P, Campiglio M, Pupa SM, Tagilabue E (2004) Role of HER2/neu in tumor progression and therapy. Cell Mol Life Sci 61:2965–2978PubMedCrossRef Ménard S, Casalini P, Campiglio M, Pupa SM, Tagilabue E (2004) Role of HER2/neu in tumor progression and therapy. Cell Mol Life Sci 61:2965–2978PubMedCrossRef
7.
go back to reference Zhou BP, Hung MC (2003) Dysregulation of cellular signaling by HER2/neu in breast cancer. Semin Oncol 30:38–48PubMedCrossRef Zhou BP, Hung MC (2003) Dysregulation of cellular signaling by HER2/neu in breast cancer. Semin Oncol 30:38–48PubMedCrossRef
8.
go back to reference Nanda R (2007) Targeting the human epidermal growth factor receptor 2 (HER2) in the treatment of breast cancer: recent advances and future directions. Rev Recent Clin Trials 2:111–116PubMedCrossRef Nanda R (2007) Targeting the human epidermal growth factor receptor 2 (HER2) in the treatment of breast cancer: recent advances and future directions. Rev Recent Clin Trials 2:111–116PubMedCrossRef
9.
go back to reference Li HP, Ji JF, Hou KY, Lei YT, Zhao HM (2010) Prediction of recurrence risk in early breast cancer using human epidermal growth factor 2 and cyclin A2. Chin Med J 123:431–437PubMed Li HP, Ji JF, Hou KY, Lei YT, Zhao HM (2010) Prediction of recurrence risk in early breast cancer using human epidermal growth factor 2 and cyclin A2. Chin Med J 123:431–437PubMed
10.
go back to reference Zell JA, Tsang WY, Taylor TH, Metha RS, Anton-Culver H (2009) Prognostic impact of human epidermal growth factor-like receptor 2 and hormone receptor status in inflammatory breast cancer (IBC): analysis of 2,014 IBC patient cases from the California Cancer Registry. Breast Cancer Res 11:1–10CrossRef Zell JA, Tsang WY, Taylor TH, Metha RS, Anton-Culver H (2009) Prognostic impact of human epidermal growth factor-like receptor 2 and hormone receptor status in inflammatory breast cancer (IBC): analysis of 2,014 IBC patient cases from the California Cancer Registry. Breast Cancer Res 11:1–10CrossRef
11.
go back to reference Lin WW, Karin M (2007) A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest 117:1175–1183PubMedCrossRef Lin WW, Karin M (2007) A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest 117:1175–1183PubMedCrossRef
12.
go back to reference Köhrmann A, Kammerer U, Kapp M, Dietl J, Anacker J (2009) Expression of matrix metalloproteinases (MMPs) in primary human breast cancer and breast cancer cell lines: new findings and review of the literature. BMC Cancer 9:188. doi:10.1186/1471-2407-9-188 PubMedCrossRef Köhrmann A, Kammerer U, Kapp M, Dietl J, Anacker J (2009) Expression of matrix metalloproteinases (MMPs) in primary human breast cancer and breast cancer cell lines: new findings and review of the literature. BMC Cancer 9:188. doi:10.​1186/​1471-2407-9-188 PubMedCrossRef
13.
go back to reference Kossakowska AE, Edwards DR, Prusinkiewicz C, Zhang MC, Guo D, Urbanski SJ, Grogan T, Marquez LA, Janowska-Wieczorek A (1999) Interleukin-6 regulation of matrix metalloproteinase (MMP-2 and MMP-9) and tissue inhibitor of metalloproteinase (TIMP-1) expression in malignant non-Hodgkin’s lymphomas. Blood 94:2080–2089PubMed Kossakowska AE, Edwards DR, Prusinkiewicz C, Zhang MC, Guo D, Urbanski SJ, Grogan T, Marquez LA, Janowska-Wieczorek A (1999) Interleukin-6 regulation of matrix metalloproteinase (MMP-2 and MMP-9) and tissue inhibitor of metalloproteinase (TIMP-1) expression in malignant non-Hodgkin’s lymphomas. Blood 94:2080–2089PubMed
14.
go back to reference Funahashi Y, Shawber CJ, Sharma A, Kanamaru E, Choi YK, Kitajewski J (2011) Notch modulates VEGF action in endothelial cells by inducing matrix metalloprotease activity. Vasc Cell 3:26. doi:10.1186/2045-824X-3-2 CrossRef Funahashi Y, Shawber CJ, Sharma A, Kanamaru E, Choi YK, Kitajewski J (2011) Notch modulates VEGF action in endothelial cells by inducing matrix metalloprotease activity. Vasc Cell 3:26. doi:10.​1186/​2045-824X-3-2 CrossRef
15.
go back to reference Wang ST, Chang CC, Yen MC, Tu CF, Chu CL, Peng YT, Chen DY, Lan JL, Lin CC (2011) RNA interference-mediated silencing of Foxo3 in antigen-presenting cells as a strategy for the enhancement of DNA vaccine potency. Gene Ther 18:372–383. doi:10.1038/gt.2010.146 PubMedCrossRef Wang ST, Chang CC, Yen MC, Tu CF, Chu CL, Peng YT, Chen DY, Lan JL, Lin CC (2011) RNA interference-mediated silencing of Foxo3 in antigen-presenting cells as a strategy for the enhancement of DNA vaccine potency. Gene Ther 18:372–383. doi:10.​1038/​gt.​2010.​146 PubMedCrossRef
16.
go back to reference Nunes RA, Harris LN (2002) The HER2 extracellular domain as a prognostic and predictive factor in breast cancer. Clin Breast Cancer 3:125–135PubMedCrossRef Nunes RA, Harris LN (2002) The HER2 extracellular domain as a prognostic and predictive factor in breast cancer. Clin Breast Cancer 3:125–135PubMedCrossRef
17.
go back to reference Page-McCaw A, Ewald A, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodeling. Nat Rev 8:221–233CrossRef Page-McCaw A, Ewald A, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodeling. Nat Rev 8:221–233CrossRef
18.
go back to reference Codony-Servat J, Albanell J, Lopez-Talavera JC, Arribas J, Baselga J (1999) Cleavage of the HER2 ectodomain is a pervanadate activable process that is inhibited by the tissue inhibitor of metalloprotease TIMP-1 in breast cancer cells. Cancer Res 59:1196–1201PubMed Codony-Servat J, Albanell J, Lopez-Talavera JC, Arribas J, Baselga J (1999) Cleavage of the HER2 ectodomain is a pervanadate activable process that is inhibited by the tissue inhibitor of metalloprotease TIMP-1 in breast cancer cells. Cancer Res 59:1196–1201PubMed
19.
go back to reference Provatopoulou X, Gounaris A, Kalogera E, Zagouri F, Flessas E, Goussetis E, Nonni A, Papassotiriou I, Zografos G (2009) Circulating levels of matrix metalloproteinase-9 (mmp-9), neutrophil gelatinase-associated lipocalin (ngal) and their complex mmp-9/ngal in breast cancer disease. BMC Cancer 9:1–7CrossRef Provatopoulou X, Gounaris A, Kalogera E, Zagouri F, Flessas E, Goussetis E, Nonni A, Papassotiriou I, Zografos G (2009) Circulating levels of matrix metalloproteinase-9 (mmp-9), neutrophil gelatinase-associated lipocalin (ngal) and their complex mmp-9/ngal in breast cancer disease. BMC Cancer 9:1–7CrossRef
20.
go back to reference Olmeda D, Moreno-Bueno G, Flores J, Fabra A, Portillo F, Cano A (2007) Snai1 is required for tumor growth and lymph node metastasis of human breast carcinoma MDA-MB-231 cells. Cancer Res 67:11721–11731PubMedCrossRef Olmeda D, Moreno-Bueno G, Flores J, Fabra A, Portillo F, Cano A (2007) Snai1 is required for tumor growth and lymph node metastasis of human breast carcinoma MDA-MB-231 cells. Cancer Res 67:11721–11731PubMedCrossRef
21.
go back to reference Kauraniemi P, Kallioniemi A (2006) Activation of multiple cancer-associated genes at the ERBB2 amplicon in breast cancer. Endocr Relat Cancer 13:39–49PubMedCrossRef Kauraniemi P, Kallioniemi A (2006) Activation of multiple cancer-associated genes at the ERBB2 amplicon in breast cancer. Endocr Relat Cancer 13:39–49PubMedCrossRef
22.
go back to reference Konecny G, Pauletti G, Pegram M, Untch M, Dandekar S (2003) Quantitative association between HER-2/neu and steroid hormone receptors in hormone receptor-positive primary breast cancer. J Natl Cancer Inst 95:142–153PubMedCrossRef Konecny G, Pauletti G, Pegram M, Untch M, Dandekar S (2003) Quantitative association between HER-2/neu and steroid hormone receptors in hormone receptor-positive primary breast cancer. J Natl Cancer Inst 95:142–153PubMedCrossRef
23.
go back to reference Freudenberg J, Wang Q, Katsumata M, Drebin J, Nagamoto I, Greene M (2009) The role of Her2 in early breast cancer metastasis and the origins of resistance to Her2-targeted therapies. Exp Mol Pathol 87:1–11PubMedCrossRef Freudenberg J, Wang Q, Katsumata M, Drebin J, Nagamoto I, Greene M (2009) The role of Her2 in early breast cancer metastasis and the origins of resistance to Her2-targeted therapies. Exp Mol Pathol 87:1–11PubMedCrossRef
24.
go back to reference Hsu MC, Chang HC, Hung WC (2006) HER2/neu represses the metastasis suppressor RECK via ERK and Sp transcription factors to promote cell invasion. J Biol Chem 281:4718–4725PubMedCrossRef Hsu MC, Chang HC, Hung WC (2006) HER2/neu represses the metastasis suppressor RECK via ERK and Sp transcription factors to promote cell invasion. J Biol Chem 281:4718–4725PubMedCrossRef
25.
go back to reference Faltus T, Yuan J, Zimmer B, Krämer A, Loibl S, Kaufmann M, Strebhardt K (2004) Silencing of the HER2/neu gene by siRNA inhibits proliferation and induces apoptosis in HER2/neu-overexpressing breast cancer cells. Neoplasia 6:786–795PubMedCrossRef Faltus T, Yuan J, Zimmer B, Krämer A, Loibl S, Kaufmann M, Strebhardt K (2004) Silencing of the HER2/neu gene by siRNA inhibits proliferation and induces apoptosis in HER2/neu-overexpressing breast cancer cells. Neoplasia 6:786–795PubMedCrossRef
26.
go back to reference Roh H, Pippin J, Drebin JA (2000) Down-regulation of HER2/neu expression induces apoptosis in human cancer cells that over express HER2/neu. Cancer Res 60:560–565PubMed Roh H, Pippin J, Drebin JA (2000) Down-regulation of HER2/neu expression induces apoptosis in human cancer cells that over express HER2/neu. Cancer Res 60:560–565PubMed
27.
go back to reference Arnould C, Lelièvre-Pégorier M, Ronco P, Lelongt B (2009) MMP9 limits apoptosis and stimulates branching morphogenesis during kidney development. J Am Soc Nephrol 20:2171–2180PubMedCrossRef Arnould C, Lelièvre-Pégorier M, Ronco P, Lelongt B (2009) MMP9 limits apoptosis and stimulates branching morphogenesis during kidney development. J Am Soc Nephrol 20:2171–2180PubMedCrossRef
28.
go back to reference Siziopikou K, Khan S (2005) Correlation HER2 gene amplification with expression of the apoptosis-suppressing genes bcl-2 and bcl-x-l in ductal carcinoma in situ of the breast. Appl Immunohistochem Mol Morphol 13:4–18 Siziopikou K, Khan S (2005) Correlation HER2 gene amplification with expression of the apoptosis-suppressing genes bcl-2 and bcl-x-l in ductal carcinoma in situ of the breast. Appl Immunohistochem Mol Morphol 13:4–18
29.
go back to reference Redondo-Munoz J, Ugarte-Berzal E, Terol MJ, Van den Steen PE, del Cerro MH, Roderfeld M, Roeb E, Opdenakker G, Garcia-Marco JA, Garcia-Pardo A (2010) Matrix metalloproteinase-9 promotes chronic lymphocytic leukemia b cell survival through its hemopexin domain. Cancer Cell 17:160–172PubMedCrossRef Redondo-Munoz J, Ugarte-Berzal E, Terol MJ, Van den Steen PE, del Cerro MH, Roderfeld M, Roeb E, Opdenakker G, Garcia-Marco JA, Garcia-Pardo A (2010) Matrix metalloproteinase-9 promotes chronic lymphocytic leukemia b cell survival through its hemopexin domain. Cancer Cell 17:160–172PubMedCrossRef
30.
go back to reference Myers E, Hill ADK, Kelly G, McDermott EW, O’Higgins NJ, Young LS (2006) A positive role for PEA3 in HER2-mediated breast tumour progression. Br J Cancer 95:1404–1409PubMedCrossRef Myers E, Hill ADK, Kelly G, McDermott EW, O’Higgins NJ, Young LS (2006) A positive role for PEA3 in HER2-mediated breast tumour progression. Br J Cancer 95:1404–1409PubMedCrossRef
31.
go back to reference Crowe D, Brown T (1999) Transcriptional inhibition of matrix metalloproteinase 9 (MMP-9) activity by a c-fos/estrogen receptor fusion protein is mediated by the proximal AP-1 site of the MMP-9 promoter and correlates with reduced tumor cell invasion. Neoplasia 1:368–372PubMedCrossRef Crowe D, Brown T (1999) Transcriptional inhibition of matrix metalloproteinase 9 (MMP-9) activity by a c-fos/estrogen receptor fusion protein is mediated by the proximal AP-1 site of the MMP-9 promoter and correlates with reduced tumor cell invasion. Neoplasia 1:368–372PubMedCrossRef
32.
go back to reference Seal M, Chia S (2010) What is the difference between triple-negative and basal breast cancers? Cancer J 16:12–16PubMedCrossRef Seal M, Chia S (2010) What is the difference between triple-negative and basal breast cancers? Cancer J 16:12–16PubMedCrossRef
33.
go back to reference DiGiovanna M, Chu P, Davison T, Howe C, Carter D, Claus E, Stern D (2002) Active signaling by HER-2/neu in a subpopulation of HER-2/neu-overexpressing ductal carcinoma in situ. Cancer Res 62:6667–6673PubMed DiGiovanna M, Chu P, Davison T, Howe C, Carter D, Claus E, Stern D (2002) Active signaling by HER-2/neu in a subpopulation of HER-2/neu-overexpressing ductal carcinoma in situ. Cancer Res 62:6667–6673PubMed
Metadata
Title
MMP-9 increases HER2/neu expression and alters apoptosis levels in human mammary epithelial cells (HMEC)
Authors
Matilda Fatunmbi
Justin Shelton
Susan M. Aronica
Publication date
01-09-2012
Publisher
Springer US
Published in
Breast Cancer Research and Treatment / Issue 2/2012
Print ISSN: 0167-6806
Electronic ISSN: 1573-7217
DOI
https://doi.org/10.1007/s10549-012-2191-5

Other articles of this Issue 2/2012

Breast Cancer Research and Treatment 2/2012 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine