Tumor-Specific Urinary Matrix Metalloproteinase Fingerprinting: Identification of High Molecular Weight Urinary Matrix Metalloproteinase Species

Clinical Cancer Research - Tập 14 Số 20 - Trang 6610-6617 - 2008
Roopali Roy1,2, Gwendolyn W. Louis1,2, Kevin R. Loughlin3,2, Dmitri Wiederschain1, Susan Kilroy1, Carolyn C. Lamb4,2, David Zurakowski1,2, Marsha A. Moses1,2
11Program in Vascular Biology and Department of Surgery, Children's Hospital Boston,
24Harvard Medical School, Boston, Massachusetts;
32Brigham and Women's Hospital,
43Beth Israel Deaconess Medical Center, and

Tóm tắt

Abstract

Purpose: We have previously reported that matrix metalloproteinases MMP-2, MMP-9, and the complex MMP-9/NGAL can be detected in urine of patients with a variety of cancers including prostate and bladder carcinoma. In addition, we also detected several unidentified urinary gelatinase activities with molecular weights >125 kDa. The objective of the current study was to identify these high molecular weight (HMW) species, determine their potential as predictors of disease status, and ask whether a tumor-specific pattern existed based on urinary MMP analysis.

Experimental Design: Chromatography, zymography, and mass spectrometry was used to identify HMW gelatinase species of ∼140, 190, and >220 kDa in urine of cancer patients. To determine whether a tumor-specific pattern of appearance existed among the MMPs detected, we analyzed the urine of 189 patients with prostate or bladder cancer and controls.

Results: The ∼140, >220 kDa, and ∼190 HMW gelatinase species were identified as MMP-9/tissue inhibitor of metalloproteinase 1 complex, MMP-9 dimer, and ADAMTS-7, respectively. The frequency of detection of any MMP species was significantly higher in urine from prostate and bladder cancer groups than controls. MMP-9 dimer and MMP-9 were independent predictors for distinguishing between patients with prostate and bladder cancer (P < 0.001 for each) by multivariable analysis.

Conclusions: This study is the first to identify a tumor-specific urinary MMP fingerprint that may noninvasively facilitate identification of cancer presence and type. This information may be of diagnostic and prognostic value in the detection and/or clinical monitoring of disease progression and therapeutic efficacy in patients with bladder or prostate cancer.

Từ khóa


Tài liệu tham khảo

Roy R, Zhang B, Moses MA. Making the cut: protease-mediated regulation of angiogenesis. Exp Cell Res 2006;312:608–22.

Chambers AF, Matrisian LM. Changing views of the role of matrix metalloproteinases in metastasis. J Natl Cancer Inst 1997;89:1260–70.

Kleiner DE, Stetler-Stevenson WG. Matrix metalloproteinases and metastasis. Cancer Chemother Pharmacol 1999;43 Suppl:S42–51.

Curran S, Murray GI. Matrix metalloproteinases in tumour invasion and metastasis. J Pathol 1999;189:300–8.

Nagase H, Woessner JF, Jr. Matrix metalloproteinases. J Biol Chem 1999;274:21491–4.

Fang J, Shing Y, Wiederschain D, et al. Matrix metalloproteinase-2 is required for the switch to the angiogenic phenotype in a tumor model. Proc Natl Acad Sci U S A 2000;97:3884–9.

Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2000;2:737–44.

Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nature reviews 2002;2:161–74.

Bode W. Structural basis of matrix metalloproteinase function. Biochem Soc Symp 2003;70:1–14.

Garbisa S, Scagliotti G, Masiero L, et al. Correlation of serum metalloproteinase levels with lung cancer metastasis and response to therapy. Cancer Res 1992;52:4548–9.

Nakajima M, Welch DR, Wynn DM, Tsuruo T, Nicolson GL. Serum and plasma M(r) 92,000 progelatinase levels correlate with spontaneous metastasis of rat 13762NF mammary adenocarcinoma. Cancer Res 1993;53:5802–7.

Gohji K, Fujimoto N, Komiyama T, et al. Elevation of serum levels of matrix metalloproteinase-2 and -3 as new predictors of recurrence in patients with urothelial carcinoma. Cancer 1996;78:2379–87.

Guan KP, Ye HY, Yan Z, Wang Y, Hou SK. Serum levels of endostatin and matrix metalloproteinase-9 associated with high stage and grade primary transitional cell carcinoma of the bladder. Urology 2003;61:719–23.

Vasala K, Turpeenniemi-Hujanen T. Serum tissue inhibitor of metalloproteinase-2 (TIMP-2) and matrix metalloproteinase-2 in complex with the inhibitor (MMP-2:TIMP-2) as prognostic markers in bladder cancer. Clin Biochem 2007;40:640–4.

Wu ZS, Wu Q, Yang JH, et al. Prognostic significance of MMP-9 and TIMP-1 serum and tissue expression in breast cancer. Int J Cancer 2008;122:2050–6.

Davies B, Waxman J, Wasan H, et al. Levels of matrix metalloproteases in bladder cancer correlate with tumor grade and invasion. Cancer Res 1993;53:5365–9.

Jung K, Krell HW, Ortel B, et al. Plasma matrix metalloproteinase 9 as biomarker of prostate cancer progression in Dunning (Copenhagen) rats. Prostate 2003;54:206–11.

Moses MA, Wiederschain D, Loughlin KR, Zurakowski D, Lamb CC, Freeman MR. Increased incidence of matrix metalloproteinases in urine of cancer patients. Cancer Res 1998;58:1395–9.

Yan L, Borregaard N, Kjeldsen L, Moses MA. The high molecular weight urinary matrix metalloproteinase (MMP) activity is a complex of gelatinase B/MMP-9 and neutrophil gelatinase-associated lipocalin (NGAL). Modulation of MMP-9 activity by NGAL. J Biol Chem 2001;276:37258–65.

Fernandez CA, Yan L, Louis G, Yang J, Kutok JL, Moses MA. The matrix metalloproteinase-9/neutrophil gelatinase-associated lipocalin complex plays a role in breast tumor growth and is present in the urine of breast cancer patients. Clin Cancer Res 2005;11:5390–5.

Smith E, Zurakowski D, Saad A, Scott RM, Moses MA. Urinary biomarkers predict brain tumor presence and response to therapy. Clin Cancer Res 2008;14:2378–86.

Smith ER, Manfredi M, Scott RM, Black PM, Moses MA. A recurrent craniopharyngioma illustrates the potential usefulness of urinary matrix metalloproteinases as noninvasive biomarkers: case report. Neurosurgery 2007;60:E1148–9; discussion E9.

Sier CF, Casetta G, Verheijen JH, et al. Enhanced urinary gelatinase activities (matrix metalloproteinases 2 and 9) are associated with early-stage bladder carcinoma: a comparison with clinically used tumor markers. Clin Cancer Res 2000;6:2333–40.

Monier F, Surla A, Guillot M, Morel F. Gelatinase isoforms in urine from bladder cancer pzatients. Clin Chim Acta 2000;299:11–23.

Gerhards S, Jung K, Koenig F, et al. Excretion of matrix metalloproteinases 2 and 9 in urine is associated with a high stage and grade of bladder carcinoma. Urology 2001;57:675–9.

Durkan GC, Nutt JE, Rajjayabun PH, Neal DE, Lunec J, Mellon JK. Prognostic significance of matrix metalloproteinase-1 and tissue inhibitor of metalloproteinase-1 in voided urine samples from patients with transitional cell carcinoma of the bladder. Clin Cancer Res 2001;7:3450–6.

Monier F, Mollier S, Guillot M, Rambeaud JJ, Morel F, Zaoui P. Urinary release of 72 and 92 kDa gelatinases, TIMPs, N-GAL and conventional prognostic factors in urothelial carcinomas. Eur Urol 2002;42:356–63.

Eissa S, Swellam M, el-Mosallamy H, et al. Diagnostic value of urinary molecular markers in bladder cancer. Anticancer Res 2003;23:4347–55.

Nutt JE, Durkan GC, Mellon JK, Lunec J. Matrix metalloproteinases (MMPs) in bladder cancer: the induction of MMP9 by epidermal growth factor and its detection in urine. BJU Int 2003;91:99–104.

Saito M, Kimoto M, Araki T, et al. Proteome analysis of gelatin-bound urinary proteins from patients with bladder cancers. Eur Urol 2005;48:865–71.

Roy R, Wewer UM, Zurakowski D, Pories SE, Moses MA. ADAM 12 cleaves extracellular matrix proteins and correlates with cancer status and stage. J Biol Chem 2004;279:51323–30.

MacCoss MJ, Wu CC, Yates JR III. Probability-based validation of protein identifications using a modified SEQUEST algorithm. Anal Chem 2002;74:5593–9.

Jaeschke R, Guyatt GH, Sackett DL. Users' guides to the medical literature. III. How to use an article about a diagnostic test. B. What are the results and will they help me in caring for my patients? The Evidence-Based Medicine Working Group. JAMA 1994;271:703–7.

Chatterjee S, Price B. Regression analysis by example. 4th ed. New York: John Wiley; 2006. p. 317–40.

Goldberg GI, Strongin A, Collier IE, Genrich LT, Marmer BL. Interaction of 92-kDa type IV collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitial collagenase, and activation of the proenzyme with stromelysin. J Biol Chem 1992;267:4583–91.

Kjeldsen L, Johnsen AH, Sengelov H, Borregaard N. Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J Biol Chem 1993;268:10425–32.

Toth M, Gervasi DC, Fridman R. Phorbol ester-induced cell surface association of matrix metalloproteinase-9 in human MCF10A breast epithelial cells. Cancer Res 1997;57:3159–67.

Vartio T, Baumann M. Human gelatinase/type IV procollagenase is a regular plasma component. FEBS Lett 1989;255:285–9.

Olson MW, Bernardo MM, Pietila M, et al. Characterization of the monomeric and dimeric forms of latent and active matrix metalloproteinase-9. Differential rates for activation by stromelysin 1. J Biol Chem 2000;275:2661–8.

Jinga DC, Blidaru A, Condrea I, et al. MMP-9 and MMP-2 gelatinases and TIMP-1 and TIMP-2 inhibitors in breast cancer: correlations with prognostic factors. J Cell Mol Med 2006;10:499–510.

Seo YS, Park JJ, Kim JH, et al. Usefulness of MMP-9/TIMP-1 in predicting tumor recurrence in patients undergoing curative surgical resection for gastric carcinoma. Dig Dis Sci 2007;52:753–9.

Morgia G, Falsaperla M, Malaponte G, et al. Matrix metalloproteinases as diagnostic (MMP-13) and prognostic (MMP-2, MMP-9) markers of prostate cancer. Neurol Res 2005;33:44–50.

Lebensztejn DM, Sobaniec-Lotowska ME, Bauer M, Kaczmarski M, Voelker M, Schuppan D. Serum fibrosis markers as predictors of an antifibrotic effect of interferon alfa in children with chronic hepatitis B. Eur J Gastroenterol Hepatol 2005;17:843–8.

Apte SS. A disintegrin-like and metalloprotease (reprolysin type) with thrombospondin type 1 motifs: the ADAMTS family. Int J Biochem Cell Biol 2004;36:981–5.

Liu CJ, Kong W, Ilalov K, et al. ADAMTS-7: a metalloproteinase that directly binds to and degrades cartilage oligomeric matrix protein. FASEB J 2006;20:988–90.