Skip to main content

Advertisement

SpringerLink
Log in

Relationships between TIMP-1, CAIX, and clinical outcomes in Egyptian breast cancer

  • Original Article
  • Published:
Comparative Clinical Pathology Aims and scope Submit manuscript

Abstract

Serum levels of carbonic anhydrase IX (CAIX) and the tissue inhibitor of metalloproteinase 1 (TIMP-1) have been demonstrated to be associated with clinical outcomes. Elevated TIMP-1 levels have been associated with a poor prognosis of breast cancer. Therefore, this study was performed to explore the relationships between serum CAIX, TIMP-1, and clinical outcomes. One hundred and five female breast cancer patients, who do not receive adjuvant therapy at Mansoura University Hospital were recruited with informed consent for this study. Preoperative serum levels of CAIX and TIMP-1 were measured using an enzyme-linked immunosorbent assay. Among the breast cancer patients, 16.1 and 20.9 % had elevated TIMP-1 and CAIX l levels, respectively. In addition, 13.3 % had elevated both CAIX and TIMP-1 levels. Elevated serum levels CAIX was significantly associated with advanced histological grade, estrogen receptor status and progesterone receptor status. Moreover, Elevated TIMP-1 was significantly associated with number of tumor-positive lymph nodes and advanced histological grade. In Kaplan–Meier analysis, the disease-free survival (DFS) was lower in patients with high serum levels of CAIX and TIMP-1 compared to patients with normal serum concentration of CAIX and TIMP-1. Including TIMP-1, CAIX, and established prognostic factors in the multivariate analysis, the presence of elevated CAIX and TIMP-1 levels remained independent predictors of overall survival time (OS). A high serum TIMP-1 and CAIX levels were significantly associated with poorer DFS and OS among Egyptian primary breast cancer patients with elevated serum levels of CAIX and TIMP-1.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alexander CM, Howard EW, Bissell MJ, Werb Z (1996) Rescue of mammary epithelial cell apoptosis and entactin degradation by a tissue inhibitor of metalloproteinases-1 transgene. J Cell Biol 135:1669–1677

    Article  CAS  PubMed  Google Scholar 

  • Bartosova M, Parkkila S, Pohlodek K, Karttunen TJ, Galbavy S, Mucha V, Harris AL, Pastorek J, Pastorekova S (2002) Expression of carbonic anhydrase IX in breast is associated with malignant tissues and is related to overexpression of c-erbB2. J Pathol 197:314–321

    Article  CAS  PubMed  Google Scholar 

  • Beketic-Oreskovic L, Ozretic P, Rabbani ZN, Jackson IL, Sarcevic B, Levanat S, Maric P, Babic I, Vujaskovic Z (2011) Prognostic significance of carbonic anhydrase IX (CA-IX), endoglin (CD105) and 8-hydroxy-2′-deoxyguanosine (8-OHdG) in breast cancer patients. Pathol Oncol Res 17(3):593–603

    Article  CAS  PubMed  Google Scholar 

  • Bigelow RL, Williams BJ, Carroll JL, Daves LK, Cardelli JA (2009) TIMP-1 overexpression promotes tumorigenesis of MDA-MB-231 breast cancer cells and alters expression of a subset of cancer promoting genes in vivo distinct from those observed in vitro. Breast Cancer Res Treat 117:31–44

    Article  CAS  PubMed  Google Scholar 

  • Birkedal-Hansen H (1995) Proteolytic remodeling of extracellular matrix. Curr Opin Cell Biol 7:728–735

    Article  CAS  PubMed  Google Scholar 

  • Brennan DJ, Jirstrom K, Kronblad A, Millikan RC, Landberg G, Duffy MJ, Rydén L, Gallagher WM, O’Brien SL (2006) CA IX is an independent prognostic marker in premenopausal breast cancer patients with one to three positive lymph nodes and a putative marker of radiation resistance. Clin Cancer Res 12:6421–6431

    Article  CAS  PubMed  Google Scholar 

  • Bui MH, Visapaa H, Seligson D, Kim H, Han KR, Huang Y, Horvath S, Stanbridge EJ, Palotie A, Figlin RA et al (2004) Prognostic value of carbonic anhydrase IX and KI67 as predictors of survival for renal clear cell carcinoma. J Urol 171:2461–2466

    Article  PubMed  Google Scholar 

  • Carney WP (2007) Circulating oncoproteins HER2/neu, EGFR and CAIX (MN) as novel cancer biomarkers. Expert Rev Mol Diagn 7:309–319

    Article  CAS  PubMed  Google Scholar 

  • Chia SK, Wykoff CC, Watson PH, Han C, LeekRD PJ, Gatter KC, Ratcliffe P, Harris AL (2001) Prognostic significance of a novel hypoxia-regulated marker, carbonic anhydrase IX, in invasive breast carcinoma. J Clin Oncol 19:3660–3668

    CAS  PubMed  Google Scholar 

  • Chia S, Ragaz J, Makretsov N, Cheang M, Hayes M, Gilks B, Harris A, Spinelli J, Gelmon K, Olivotto I, Huntsman D (2005) Carbonic anhydrase IX (CA IX) as a predictive marker for benefit from post-mastectomy adjuvant locoregional radiation (RT): results from the British Columbia (BC) randomized radiation trial. J Clin Oncol 23:16S

    Google Scholar 

  • Choschzick M, Woelber L, Hess S, Zu Eulenburg C, Schwarz J, Simon R, Mahner S, Jaenicke F, Müller V (2010) Overexpression of carbonic anhydrase IX (CAIX) in vulvar cancer is associated with tumor progression and development of locoregional lymph node metastases. Virchows Arch 456:483–490

    Article  CAS  PubMed  Google Scholar 

  • Deryugina EI, Quigley JP (2006) Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 25:9–34

    Article  CAS  PubMed  Google Scholar 

  • Duffy MJ, Maguire TM, Hill A, McDermott E, Metalloproteinases O’HN (2000) Role in breast carcinogenesis, invasion and metastasis. Breast Cancer Res 2:252–257

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ejlertsen B, Jensen MB, Nielsen KV et al (2010) HER2, TOP2A, and TIMP-1 and responsiveness to adjuvant anthracyclinecontaining chemotherapy in high-risk breast cancer patients. J Clin Oncol 28:984–990

    Article  CAS  PubMed  Google Scholar 

  • Garbett EA, Reed MW, Stephenson TJ, Brown NJ (2000) Proteolysis in human breast cancer. Mol Pathol 53:99–106

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Generali D, Fox SB, Berruti A, Brizzi MP, CampoL BS, Wigfield SM, Bruzzi P, Bersiga A, Allevi G, Milani M (2006) Role of carbonic anhydrase IX expression in prediction of the efficacy and outcome of primary epirubicin/tamoxifen therapy for breast cancer. Endocrine-Related Cancer 13:921–930

    Article  CAS  PubMed  Google Scholar 

  • Guedez L, Stetler-Stevenson WG, Wolff L (1998) In vitro suppression of programmed cell death of B cells by tissue inhibitor of metalloproteianses-1. J Clin Investig 102:2002–2010

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Harris L (2002) Hypoxia—a key regulatory factor in tumour growth. Nat Rev Cancer 2:38–47

    Article  CAS  PubMed  Google Scholar 

  • Harris L, Fritsche H, Mennel R, Norton L, Ravdin P, Taube S, Somerfield MR, Hayes DF, Bast RC Jr (2007) American society of clinical oncology update of recommendations for the use of tumor markers in breast cancer. J Clin Oncol 25:5287–5312

    Article  CAS  PubMed  Google Scholar 

  • Hayakawa T, Yamashita K, Tanzawa K, Uchijima E, Iwata K (1992) Growth promoting activity of tissue inhibitor of metalloproteinases-1 (TIMP-1) for a wide range of cells. A possible new growth factor in serum. FEBS Lett 298:29–32

    Article  CAS  PubMed  Google Scholar 

  • Hockel M, Vaupel P (2001) Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst 93:266–276

    Article  CAS  PubMed  Google Scholar 

  • Holten-Andersen MN, Stephens RW, Nielsen HJ et al (2000) High preoperative plasma tissue inhibitor of metalloproteinase-1 levels are associated with short survival of patients with colorectal cancer. Clin Cancer Res 6:4292–4299

    CAS  PubMed  Google Scholar 

  • Hussain SA, Ganesan R, Reynolds G, Gross L, Stevens A, Pastorek J, Murray PG, Perunovic B, Anwar MS, Billingham L, James ND, Spooner D, Poole CJ, Rea DW, Palmer DH (2007) Hypoxia-regulated carbonic anhydrase IX expression is associated with poor survival in patients with invasive breast cancer. Br J Cancer 96:104–109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Itoh Y, Nagase H (2002) Matrix metalloproteinases in cancer. Essays Biochem 38:21–36

    CAS  PubMed  Google Scholar 

  • Jiang Y, Goldberg ID, Shi YE (2002) Complex roles of tissue inhibitors of metalloproteinases in cancer. Oncogene 21:2245–2252

    Article  CAS  PubMed  Google Scholar 

  • Klatte T, Seligson DB, Rao JY, Yu H, de Martino M, Kawaoka K, Wong SG, Belldegrun AS, Pantuck AJ (2009) Carbonic anhydrase IX in bladder cancer: a diagnostic, prognostic, and therapeutic molecular marker. Cancer 115:1448–1458

    Article  PubMed  Google Scholar 

  • Koukourakis MI, Giatromanolaki A, Sivridis E et al (2001) Hypoxia-regulated carbonic anhydrase-9 (CA9) relates poor vascularization and resistance of squamous cell head and neck cancer to chemoradiotherapy. Clin Cancer Res 7:3399–3403

    Google Scholar 

  • Kuvaja P, Wurtz SU, Talvensaari-Mattila A, Brunner N, Paakko P, Turpeenniemi-Hujanen T (2007) High serum TIMP-1 correlates with poor prognosis in breast carcinoma—a validation study. Cancer Biomarkers 3:293–300

    CAS  PubMed  Google Scholar 

  • Kuvaja P, Talvensaari-Mattila A, Turpeenniemi-Hujanen T (2008) High preoperative plasma TIMP-1 is prognostic for early relapse in primary breast carcinoma. Int J Cancer 123:846–851

    Article  CAS  PubMed  Google Scholar 

  • Lambert E, Dasse E, Haye B, Petitfrere E (2004) TIMPs as multifacial proteins. Crit Rev Oncol Hematol 49(3):187–198

    Article  PubMed  Google Scholar 

  • Lee JH, Welch DR (1997) Suppression of metastasis in human breast carcinoma MDA-MB-435 cells after transfection with the metastasis suppressor gene, KiSS-1. Cancer Res 57(12):2384–2387

    CAS  PubMed  Google Scholar 

  • Li H, Nishio K, Yamashita K, Hayakawa T, Hoshino T (1995) Cell cycle-dependent localization of tissue inhibitor of metalloproteinases-1 immunoreactivity in cultured human gingival fibroblasts. Nagoya J Med Sci 58:133–142

    CAS  PubMed  Google Scholar 

  • Li G, Fridman R, Kim HR (1999) Tissue inhibitor of metalloproteinase-1 inhibits apoptosis of human breast epithelial cells. Cancer Res 59:6267–6275

    CAS  PubMed  Google Scholar 

  • Li G, Feng G, Gentil-Perret A, Genin C, Tostain J (2008) Serum carbonic anhydrase 9 level is associated with postoperative recurrence of conventional renal cell cancer. J Urol 180:510–513

    Article  CAS  PubMed  Google Scholar 

  • Liao SY, Darcy KM, Randall LM, Tian C, Monk BJ, Burger RA, Fruehauf JP, Peters WA, Stock RJ, Stanbridge EJ (2010) Prognostic relevance of carbonic anhydrase-IX in high-risk, early-stage cervical cancer: a gynecologic oncology group study. Gynecol Oncol 116:452–458

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liotta LA, Kohn EC (2001) The microenvironment of the tumour–host interface. Nature 411:375–379

    Article  CAS  PubMed  Google Scholar 

  • Lipton A, Ali SM, Leitzel K, Demers L, Evans DB, Hamer P, Brown-Shimer S, Pierce K, Carney W (2007) Elevated plasma tissue inhibitor of metalloproteinase-1 level predicts decreased response and survival in metastatic breast cancer. Cancer 109:1933–1939

    Article  CAS  PubMed  Google Scholar 

  • Lipton A, Leitzel K, Chaudri-Ross HA, Evans DB, Ali SM, Demers L, Hamer P, Brown-Shimer S, Pierce K, Gaur V, Carney W (2008) Serum TIMP-1 and response to the aromatase inhibitor letrozole versus tamoxifen in metastatic breast cancer. J Clin Oncol 26:2653–2658

    Article  CAS  PubMed  Google Scholar 

  • Liu XW, Bernardo MM, Fridman R, Kim HR (2003) Tissue inhibitor of metalloproteinase-1 protects human breast epithelial cells against intrinsic apoptotic cell death via the focal adhesion kinase/ phosphatidylinositol 3-kinase and MAPK signaling pathway. J Biol Chem 278:40364–40372

    Article  CAS  PubMed  Google Scholar 

  • Loncaster JA, Harris AL, Davidson SE, Logue JP, Hunter RD, Wycoff CC, Pastorek J, Ratcliffe PJ, Stratford IJ, West CM (2001) Carbonic anhydrase (CA IX) expression, a potential new intrinsic marker of hypoxia: correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix. Cancer Res 61:6394–6399

    CAS  PubMed  Google Scholar 

  • Lou Y, McDonald PC, Oloumi A, Chia SK, Ostlund C, Ahmadi A, Kyle A (2011) Targeting tumor hypoxia: suppression of breast tumor growth and metastasis by novel carbonic anhydrase IX inhibitors. Cancer Res 71:3364–3376

    Article  CAS  PubMed  Google Scholar 

  • Luparello C, Avanzato G, Carella C, Pucci-Minafra I (1999) Tissue inhibitor of metalloprotease (TIMP)-1 and proliferative behaviour of clonal breast cancer cells. Breast Cancer Res Treat 54:235–244

    Article  CAS  PubMed  Google Scholar 

  • Mahner S, Woelber L, Eulenburg C, Schwarz J, Carney W, Jaenicke F, Milde-Langosch K, Müller V (2010) TIMP-1 and VEGF-165 serum concentration during first-line therapy of ovarian cancer patients. BMC Cancer 10:139

    Article  PubMed Central  PubMed  Google Scholar 

  • Manenti L, Paganoni P, Floriani I et al (2003) Expression levels of vascular endothelial growth factor, matrix metalloproteinases 2 and 9 and tissue inhibitor of metalloproteinases 1 and 2 in the plasma of patients with ovarian carcinoma. Eur J Cancer 39:1948–1956

    Article  CAS  PubMed  Google Scholar 

  • McCarthy K, Maguire T, McGreal G, McDermott E, O’Higgins N, Duffy MJ (1999) High levels of tissue inhibitor of metalloproteinase-1 predict poor outcome in patients with primary breast cancer. Int J Cancer 84:44–48

    Article  CAS  PubMed  Google Scholar 

  • Morsy SM, Badawi AM, Cecchi A, Scozzafava A, Supuran CT (2009) Carbonic anhydrase inhibitors. Biphenyl sulfonamides with inhibitory action towards the transmembrane, tumor-associated isozymes IX possess cytotoxic activity against human colon, lung and breast cancer cell lines. J Enzyme Inhib Med Chem 24:499–505

    Article  CAS  PubMed  Google Scholar 

  • Murphy G (2008) The ADAMs: signalling scissors in the tumour microenvironment. Nat Rev Cancer 8:929–941

    Article  CAS  PubMed  Google Scholar 

  • Murphy FR, Issa R, Zhou X, Ratnarajah S, Nagase H, Arthur MJP, Benyon C, Iredale JP (2002) Inhibition of apoptosis of activated hepatic stellate cells by tissue inhibitor of metalloproteinase-1 is mediated via effects on matrix metalloproteinase inhibition. J Biol Chem 277:11069–11076

    Article  CAS  PubMed  Google Scholar 

  • Nakopoulou L, Giannopoulou I, Stefanaki K et al (2002) Enhanced mRNA expression of tissue inhibitor of metalloproteinase-1 (TIMP-1) in breast carcinomas is correlated with adverse prognosis, J Pathol 197:307–313

    Article  CAS  PubMed  Google Scholar 

  • Nakopoulou L, Giannopoulou I, Lazaris AC et al (2003) The favorable prognostic impact of tissue inhibitor of matrix metalloproteinases-1 protein overexpression in breast cancer cells. Acta Pathol Microbiol Immunol Scand 111:1027–1036

    Article  CAS  Google Scholar 

  • Nikkola J, Vihinen P, Vuoristo MS, Kellokumpu-Lehtinen P, Kähäri VM, Pyrhönen S (2005) High serum levels of matrix metalloproteinase-9 and matrix metalloproteinase-1 are associated with rapid progression in patients with metastatic melanoma. Clin Cancer Res 11:5158–5166

    Article  CAS  PubMed  Google Scholar 

  • Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8:221–233

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pellikainen JM, Ropponen KM, Kataja VV, Kellokoski JK, Eskelinen MJ, Kosma VM (2004) Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in breast cancer with a special reference to activator protein-2, HER2, and prognosis. Clin Cancer Res 10:7621–7628

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro C, Sousa B, Albergaria A, Paredes J, Dufloth R, Vieira D, Schmitt F, Baltazar LF (2011) GLUT1 and CAIX expression profiles in breast cancer correlate with adverse prognostic factors and MCT1 overexpression. Histol Histopathol 26:1279–1286

    CAS  PubMed  Google Scholar 

  • Porter P (2008) Westernizing women’s risks? Breast cancer in lower-income countries. N Engl J Med 358(3):213–216

    Article  CAS  PubMed  Google Scholar 

  • Rakha EA, Reis-Filho JS, Baehner F et al (2010) Breast cancer prognostic classification in the molecular era: the role of histological grade. Breast Cancer Research 12(4):207

    PubMed Central  PubMed  Google Scholar 

  • Rauvala M, Puistola U, Turpeenniemi-Hujanen T (2005) Gelatinases and their tissue inhibitors in ovarian tumors; TIMP-1 is a predictive as well as a prognostic factor. Gynecol Oncol 99:656–663

    Article  CAS  PubMed  Google Scholar 

  • Ree AH, Florenes VA, Berg JP et al (1997) High levels of messenger RNAs for tissue inhibitors of metalloproteinases (TIMP-1 and TIMP-2) in primary breast carcinomas are associated with development of distant metastases. Clin Cancer Res 3:1623–1628

    CAS  PubMed  Google Scholar 

  • Robertson N, Potter C, Harris AL (2004) Role of carbonic anhydrase IX in human tumor cell growth, survival, and invasion. Cancer Res 64:6160–6165

    Article  CAS  PubMed  Google Scholar 

  • Schrohl AS, Christensen IJ, Pedersen AN, Jensen V, Mouridsen H, Murphy G, Foekens JA, Brunner N, Holten-Andersen MN (2003) Tumor tissue concentrations of the proteinase inhibitors tissue inhibitor of metalloproteinases-1 (TIMP-1) and plasminogen activator inhibitor type-1 (PAI-1) are complementary in determining prognosis in primary breast cancer. Mol Cell Proteomics 2:164–172

    Article  CAS  PubMed  Google Scholar 

  • Schrohl AS, Holten-Andersen MN, Peters HA, Look MP, Meijer-van Gelder ME, Klijn JGM, Brunner N, Foekens JA (2004) Tumor tissue levels of tissue inhibitor of metalloproteinase-1 as a prognostic marker in primary breast cancer. Clin Cancer Res 10:2289–2298

    Article  CAS  PubMed  Google Scholar 

  • Schrohl AS, Meijer-van Gelder ME, Holten-Andersen MN, Christensen I, Look MP, Mouridsen HT, Brunner FJA (2006) Primary tumor levels of tissue inhibitor of metalloproteinases-1 are predictive of resistance to chemotherapy in patients with metastatic breast cancer. Clin Cancer Res 12:7054–7058

    Article  CAS  PubMed  Google Scholar 

  • Schrohl AS, Look MP, Meijer-van Gelder ME, Foekens JA, Nils B, Tumor tissue levels of Tissue Inhibitor of Metalloproteinases-1 (2009) (TIMP-1) and outcome following adjuvant chemotherapy in premenopausal lymph node-positive breast cancer patients. A retrospective study. BMC Cancer 9:322

    Article  PubMed Central  PubMed  Google Scholar 

  • Scrideli CA, Cortez MA, Yunes JA et al (2010) mRNA expression of matrix metalloproteinases (MMPs) 2 and 9 and tissue inhibitor of matrix metalloproteinases (TIMPs) 1 and 2 in childhood acute lymphoblastic leukemia: potential role of TIMP1 as an adverse prognostic factor, Leuk Res 34:32–37

    Article  CAS  PubMed  Google Scholar 

  • Sorensen NM, Sørensen IV, Wurtz SO et al (2008) Biology and potential clinical implications of tissue inhibitor of metalloproteinases-1 in colorectal cancer treatment. Scand J Gastroenterol 43:774–786

    Article  CAS  Google Scholar 

  • Span PN, Bussink J, Manders P, Beex LV, Sweep CG (2003) Carbonic anhydrase-9 expression levels and prognosis in human breast cancer: association with treatment outcome. Br J Cancer 89:271–276

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Swietach P, Hulikova A, Vaughan-Jones RD, Harris AL (2010) New insights into the physiological role of carbonic anhydrase IX in tumour pH regulation. Oncogene 29:6509–6521

    Article  CAS  PubMed  Google Scholar 

  • Swinson DE, Jones JL, Richardson D, Wykoff C, Turley H, Pastorek J, Taub N, Harris AL, O’Byrne KJ (2003) Carbonic anhydrase IX expression, a novel surrogate marker of tumor hypoxia, is associated with a poor prognosis in non-small-cell lung cancer. J Clin Oncol 21:473–482

    Article  CAS  PubMed  Google Scholar 

  • Talvensaari-Mattila A, Turpeenniemi-Hujanen T (2005) Preoperative serum MMP-9 immunoreactive protein is a prognostic indicator for relapsefree survival in breast carcinoma. Cancer Lett 217:237–242

    Article  CAS  PubMed  Google Scholar 

  • Talvensaari-Mattila A, Paakko P, Turpeenniemi-Hujanen T (2003) Matrix metalloproteinase-2 (MMP-2) is associated with survival in breast carcinoma. Br J Cancer 89:1270–1275

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tan EY, Yan M, Campo L, Han C, Takano E, Turley H, Candiloro I, Pezzella F, Gatter KC, Millar EK, O’Toole SA, McNeil CM, Crea P, Segara D, Sutherland RL, Harris AL, Fox SB (2009) The key hypoxia regulated gene CAIX is upregulated in basal-like breast tumours and is associated with resistance to chemotherapy. Br J Cancer 100:405–411

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Trastour C, Benizri E, Ettore F, Ramaioli A, Chamorey E, Pouyssegur J, Berra E (2007) HIF-1alpha and CA IX staining in invasive breast carcinomas: prognosis and treatment outcome. Int J Cancer 120:1451–1458

    Article  CAS  PubMed  Google Scholar 

  • Tripp BC, Smith K, Ferry JG (2001) Carbonic anhydrase: new insights for an ancient enzyme. J Biol Chem 276:48615–48618

    Article  CAS  PubMed  Google Scholar 

  • Vernon AE, LaBonne C (2004) Tumor metastasis: a new twist on epithelial mesenchymal transitions. Curr Biol 14(17):719–721

    Article  Google Scholar 

  • Visse R, Nagase H (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92(8):827–839

    Article  CAS  PubMed  Google Scholar 

  • Waas ET, Hendriks T, Lomme RM, Wobbes T (2005) Plasma levels of matrix metalloproteinase-2 and tissue inhibitor of metalloproteinase-1 correlate with disease stage and survival in colorectal cancer. Dis Colon Rectum 48:700–710

    Article  PubMed  Google Scholar 

  • Winum JY, Scozzafava A, Montero JL, Supuran CT (2009) Inhibition of carbonic anhydrase IX: a new strategy against cancer. Anticancer Agents Med Chem 9:693–702

    Article  CAS  PubMed  Google Scholar 

  • Wu ZS, Wu Q, Yang JH et al (2008) Prognostic significance of MMP-9 and TIMP-1 serum and tissue expression in breast cancer. Int J Cancer 122:2050–2056

    Article  CAS  PubMed  Google Scholar 

  • Wurtz SU, Schrohl AS, Sørensen MN et al (2005) Tissue inhibitor of metalloproteinases-1 in breast cancer. Endocrine- Related Cancer 12:215–227

    Article  CAS  PubMed  Google Scholar 

  • Wurtz SO, Schrohl AS, Mouridsen H, Brunner N (2008a) TIMP-1 as a tumor marker in breast cancer–an update. Acta Oncol 47:580–590

    Article  PubMed  Google Scholar 

  • Wurtz SU, Moller S, Mouridsen H, Hertel PB, Friis E, Brunner N (2008b) Plasma and serum levels of tissue inhibitor of metalloproteinases-1 are associated with prognosis in node-negative breast cancer: a prospective study. Mol Cell Proteomics 7:424–430

    Article  CAS  PubMed  Google Scholar 

  • Wykoff CC, Beasley NJ, Watson PH, Turner KJ, Pastorek J, Sibtain A, Wilson GD, Turley H, Talks KL, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL (2000) Hypoxia-inducible expression of tumor associated carbonic anhydrases. Cancer Res 60:7075–7083

    CAS  PubMed  Google Scholar 

  • Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117(7):927–939

    Article  CAS  PubMed  Google Scholar 

  • Ylisirniö S, Höyhtyä M, Turpeenniemi-Hujanen T (2000) Serum matrix metalloproteinases-2, -9 and tissue inhibitors of metalloproteinases-1, -2 in lung cancer—TIMP-1 as a prognostic marker. Anticancer Res 20:1311–1316

    PubMed  Google Scholar 

  • Yoshikawa T, Cho H, Tsuburaya A, Kobayashi O (2009) Impact of plasma tissue inhibitor of metalloproteinase-1 on long-term survival in patients with gastric cancer. Gastric Cancer 12:31–36

    Article  CAS  PubMed  Google Scholar 

  • Yukawa N, Yoshikawa T, Akaike M et al (2007) Impact of plasma tissue inhibitor of matrix metalloproteinase-1 on long-term survival in patients with colorectal cancer. Oncology 72:205–208

    Article  CAS  PubMed  Google Scholar 

  • Zavada J, Zavadova Z, Zat’ovicova M, Hyrsl L, Kawaciuk I (2003) Soluble form of carbonic anhydrase IX (CA IX) in the serum and urine of renal carcinoma patients. Br J Cancer 89:1067–1071

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu D, Zha X, Hu M, Tao A, Zhou H, Zhou X, Sun Y (2012) High expression of TIMP-1 in human breast cancer tissues is a predictive of resistance to paclitaxel-based chemotherapy. Med Oncol 29(5):3207–3215

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Clinical Pathology, Mansoura University, Mansoura, Egypt

    Rabab Aly & Doaa M. Elghannam

  2. Department of Internal Medicine, Mansoura University, Mansoura, Egypt

    Ansaf B. Yousef

Authors
  1. Rabab Aly
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Doaa M. Elghannam
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ansaf B. Yousef
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rabab Aly.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aly, R., Elghannam, D.M. & Yousef, A.B. Relationships between TIMP-1, CAIX, and clinical outcomes in Egyptian breast cancer. Comp Clin Pathol 23, 907–916 (2014). https://doi.org/10.1007/s00580-013-1712-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00580-013-1712-x

Keywords

Search

Navigation