Breast Cancer Research and Treatment

, Volume 136, Issue 3, pp 837–845

Plasma matrix metalloproteinases and postmenopausal breast cancer risk: a nested case–control study in the Multiethnic Cohort study

  • Yeonju Kim
  • Nicholas J. Ollberding
  • Yurii B. Shvetsov
  • Adrian A. Franke
  • Lynne R. Wilkens
  • Gertraud Maskarinec
  • Brenda Y. Hernandez
  • Loïc Le Marchand
  • Brian E. Henderson
  • Laurence N. Kolonel
  • Marc T. Goodman
Epidemiology

Abstract

The survival of malignant breast cells depends upon the remodeling of the extracellular matrix, including complex interactions with matrix metalloproteinases (MMPs). It has been hypothesized that circulating MMPs may serve as early indicators of breast cancer development in hospital-based case–control studies. A nested case–control study of the association of pre-diagnostic plasma levels of MMPs with the subsequent risk of postmenopausal breast cancer was conducted within the Multiethnic Cohort. During the follow-up period, 713 women with incident invasive breast cancer were identified and individually (1:1) matched to controls. Four types of MMPs (1, 2, 3, and 7) were analyzed by microsphere immunofluorescence assay. Mean plasma levels of MMPs did not differ significantly between cases and controls; nor were there differences in breast cancer risk by MMP level. No difference in the risk of breast cancer by plasma level of the MMPs was found within strata of age, or ethnicity, although MMP-1 levels were positively associated with breast cancer risk in obese women and women by hormone replacement medications (P values for interaction <0.05). Few significant differences in risk by levels of the MMPs were found by any of the clinical variables. Circulating MMPs were not associated with postmenopausal breast cancer risk.

Keywords

Breast cancer Matrix metalloproteinases Body mass index Hormone replacement therapy Neoplasm staging Nested case–control study 

References

  1. 1.
    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90PubMedCrossRefGoogle Scholar
  2. 2.
    Harris L, Fritsche H, Mennel R, Norton L, Ravdin P, Taube S, Somerfield MR, Hayes DF, Bast RC (2007) American Society of Clinical Oncology 2007 update of recommendations for the use of tumor markers in breast cancer. J Clin Oncol 25(33):5287–5312PubMedCrossRefGoogle Scholar
  3. 3.
    Klein T, Bischoff R (2011) Physiology and pathophysiology of matrix metalloproteases. Amino Acids 41(2):271–290PubMedCrossRefGoogle Scholar
  4. 4.
    Visse R, Nagase H (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases. Circ Res 92(8):827–839PubMedCrossRefGoogle Scholar
  5. 5.
    Murphy G, Nagase H (2008) Progress in matrix metalloproteinase research. Mol Aspects Med 29(5):290–308PubMedCrossRefGoogle Scholar
  6. 6.
    Bostrom P, Soderstrom M, Vahlberg T, Soderstrom KO, Roberts PJ, Carpen O, Hirsimaki P (2011) MMP-1 expression has an independent prognostic value in breast cancer. BMC Cancer 11:348PubMedCrossRefGoogle Scholar
  7. 7.
    Perentes JY, Kirkpatrick ND, Nagano S, Smith EY, Shaver CM, Sgroi D, Garkavtsev I, Munn LL, Jain RK, Boucher Y (2011) Cancer cell-associated MT1-MMP promotes blood vessel invasion and distant metastasis in triple-negative mammary tumors. Cancer Res 71(13):4527–4538PubMedCrossRefGoogle Scholar
  8. 8.
    Ranogajec I, Jakic-Razumovic J, Puzovic V, Gabrilovac J (2012) Prognostic value of matrix metalloproteinase-2 (MMP-2), matrix metalloproteinase-9 (MMP-9) and aminopeptidase N/CD13 in breast cancer patients. Med Oncol 29(2):561–569PubMedCrossRefGoogle Scholar
  9. 9.
    Steude JS, Maskarinec G, Erber E, Verheus M, Hernandez BY, Killeen J, Cline JM (2010) Mammographic density and matrix metalloproteinases in breast tissue. Cancer Microenviron 3:57–65CrossRefGoogle Scholar
  10. 10.
    Patel S, Sumitra G, Koner BC, Saxena A (2011) Role of serum matrix metalloproteinase-2 and -9 to predict breast cancer progression. Clin Biochem 44(10–11):869–872PubMedCrossRefGoogle Scholar
  11. 11.
    Somiari SB, Somiari RI, Heckman CM, Olsen CH, Jordan RM, Russell SJ, Shriver CD (2006) Circulating MMP2 and MMP9 in breast cancer—potential role in classification of patients into low risk, high risk, benign disease and breast cancer categories. Int J Cancer 119(6):1403–1411PubMedCrossRefGoogle Scholar
  12. 12.
    Lee JH, Choi JW, Kim YS (2011) Serum TIMP-1 predicts survival outcomes of invasive breast carcinoma patients: a meta-analysis. Arch Med Res 42(6):463–468PubMedCrossRefGoogle Scholar
  13. 13.
    Lipton A, Leitzel K, Chaudri-Ross HA, Evans DB, Ali SM, Demers L, Hamer P, Brown-Shimer S, Pierce K, Gaur V et al (2008) Serum TIMP-1 and Response to the Aromatase Inhibitor Letrozole Versus Tamoxifen in Metastatic Breast Cancer. J Clin Oncol 26(16):2653–2658PubMedCrossRefGoogle Scholar
  14. 14.
    Talvensaari-Mattila A, Turpeenniemi-Hujanen T (2005) High preoperative serum TIMP-1 is a prognostic indicator for survival in breast carcinoma. Breast Cancer Res Treat 89:29–34PubMedCrossRefGoogle Scholar
  15. 15.
    Wu Z-S, Wu Q, Yang J-H, Wang H-Q, Ding X-D, Yang F, Xu X-C (2008) Prognostic significance of MMP-9 and TIMP-1 serum and tissue expression in breast cancer. Int J Cancer 122(9):2050–2056PubMedCrossRefGoogle Scholar
  16. 16.
    Würtz SØ, Møller S, Mouridsen H, Hertel PB, Friis E, Brünner N (2008) Plasma and serum levels of tissue inhibitor of metalloproteinases-1 are associated with prognosis in node-negative breast cancer. Mol Cell Proteomics 7(2):424–430PubMedGoogle Scholar
  17. 17.
    Song N, Sung H, Choi JY, Han S, Jeon S, Song M, Lee Y, Park CB, Park SK, Lee KM et al (2012) Preoperative serum levels of matrix metalloproteinase-2 (MMP-2) and survival of breast cancer among Korean women. Cancer Epidemiol Biomarkers Prev 21(8):1371–1380PubMedCrossRefGoogle Scholar
  18. 18.
    Sung H, Choi JY, Lee SA, Lee KM, Han S, Jeon S, Song M, Lee Y, Park SK, Yoo KY et al (2012) The association between the preoperative serum levels of lipocalin-2 and matrix metalloproteinase-9 (MMP-9) and prognosis of breast cancer. BMC Cancer 12(1):193PubMedCrossRefGoogle Scholar
  19. 19.
    Duffy MJ, Maguire TM, Hill A, McDermott E, O’Higgins N (2000) Metalloproteinases: role in breast carcinogenesis, invasion and metastasis. Breast Cancer Res 2(4):252–257PubMedCrossRefGoogle Scholar
  20. 20.
    Levi E, Fridman R, Miao HQ, Ma YS, Yayon A, Vlodavsky I (1996) Matrix metalloproteinase 2 releases active soluble ectodomain of fibroblast growth factor receptor 1. Proc Natl Acad Sci 93(14):7069–7074PubMedCrossRefGoogle Scholar
  21. 21.
    Kolonel LN, Henderson BE, Hankin JH, Nomura AM, Wilkens LR, Pike MC, Stram DO, Monroe KR, Earle ME, Nagamine FS (2000) A multiethnic cohort in Hawaii and Los Angeles: baseline characteristics. Am J Epidemiol 151(4):346–357PubMedCrossRefGoogle Scholar
  22. 22.
    Howlader N, Noone A, Krapcho M, Neyman N, Aminou R, Waldron W, Altekruse S, Kosary C, Ruhl J, Tatalovich Z et al. (eds) (2011) SEER cancer statistics review, 1975–2008. National Cancer Institute. Bethesda, MD. http://seer.cancer.gov/csr/1975_2008/, based on November 2010 SEER data submission, posted to the SEER web site. Accessed Oct 2010
  23. 23.
    International classification of diseases for oncology, 3rd edition (ICD-O-3) http://seer.cancer.gov/icd-o-3/. Accessed Oct 2010
  24. 24.
    Ognjanovic S, Yamamoto J, Saltzman B, Franke A, Ognjanovic M, Yokochi L, Vogt T, Decker R, Le Marchand L (2010) Serum CRP and IL-6, genetic variants and risk of colorectal adenoma in a multiethnic population. Cancer Causes Control 21(7):1131–1138PubMedCrossRefGoogle Scholar
  25. 25.
    Maskarinec G, Woolcott C, Steude JS, Franke AA, Cooney RV (2010) The relation of leptin and adiponectin with breast density among premenopausal women. Eur J Cancer Prev 19(1):55–60PubMedCrossRefGoogle Scholar
  26. 26.
    Mercapide J, Lopez De Cicco R, Castresana JS, Klein-Szanto AJP (2003) Stromelysin-1/matrix metalloproteinase-3 (MMP-3) expression accounts for invasive properties of human astrocytoma cell lines. Int J Cancer 106(5):676–682PubMedCrossRefGoogle Scholar
  27. 27.
    Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8(3):221–233PubMedCrossRefGoogle Scholar
  28. 28.
    Overall CM, Kleifeld O (2006) Tumour microenvironment—opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat Rev Cancer 6(3):227–239PubMedCrossRefGoogle Scholar
  29. 29.
    Nakamura M, Miyamoto S, Maeda H, Ishii G, Hasebe T, Chiba T, Asaka M, Ochiai A (2005) Matrix metalloproteinase-7 degrades all insulin-like growth factor binding proteins and facilitates insulin-like growth factor bioavailability. Biochem Biophys Res Commun 333(3):1011–1016PubMedCrossRefGoogle Scholar
  30. 30.
    Ii M, Yamamoto H, Adachi Y, Maruyama Y, Shinomura Y (2006) Role of matrix metalloproteinase-7 (matrilysin) in human cancer invasion, apoptosis, growth, and angiogenesis. Exp Biol Med 231(1):20–27Google Scholar
  31. 31.
    Lynch CC (2011) Matrix metalloproteinases as master regulators of the vicious cycle of bone metastasis. Bone 48(1):44–53PubMedCrossRefGoogle Scholar
  32. 32.
    Maquoi E, Assent D, Detilleux J, Pequeux C, Foidart JM, Noel A (2012) MT1-MMP protects breast carcinoma cells against type I collagen-induced apoptosis. Oncogene 31(4):480–493PubMedCrossRefGoogle Scholar
  33. 33.
    Muller V, Riethdorf S, Rack B, Janni W, Fasching PA, Solomayer E, Aktas B, Kasimir-Bauer S, Zeitz J, Pantel K et al (2011) Prospective evaluation of serum tissue inhibitor of metalloproteinase 1 and carbonic anhydrase IX in correlation to circulating tumor cells in patients with metastatic breast cancer. Breast Cancer Res 13(4):R71PubMedCrossRefGoogle Scholar
  34. 34.
    Mannello F (2011) What does matrix metalloproteinase-1 expression in patients with breast cancer really tell us? BMC Med 9:95PubMedCrossRefGoogle Scholar
  35. 35.
    Gialeli C, Theocharis AD, Karamanos NK (2011) Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J 278(1):16–27PubMedCrossRefGoogle Scholar
  36. 36.
    Gupta GP, Nguyen DX, Chiang AC, Bos PD, Kim JY, Nadal C, Gomis RR, Manova-Todorova K, Massague J (2007) Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 446(7137):765–770PubMedCrossRefGoogle Scholar
  37. 37.
    Gaubatz JW, Ballantyne CM, Wasserman BA, He M, Chambless LE, Boerwinkle E, Hoogeveen RC (2010) Association of circulating matrix metalloproteinases with carotid artery characteristics. Arterioscler Thromb Vasc Biol 30(5):1034–1042PubMedCrossRefGoogle Scholar
  38. 38.
    Zhou P, Du LF, Lv GQ, Yu XM, Gu YL, Li JP, Zhang C (2011) Current evidence on the relationship between four polymorphisms in the matrix metalloproteinases (MMP) gene and breast cancer risk: a meta-analysis. Breast Cancer Res Treat 127(3):813–818PubMedCrossRefGoogle Scholar
  39. 39.
    Abdallah MA, Abdullah HI, Kang S, Taylor DD, Nakajima ST, Gercel-Taylor C (2007) Effects of the components of hormone therapy on matrix metalloproteinases in breast-cancer cells: an in vitro study. Fertil Steril 87(4):978–981PubMedCrossRefGoogle Scholar
  40. 40.
    Wiseman BS, Sternlicht MD, Lund LR, Alexander CM, Mott J, Bissell MJ, Soloway P, Itohara S, Werb Z (2003) Site-specific inductive and inhibitory activities of MMP-2 and MMP-3 orchestrate mammary gland branching morphogenesis. J Cell Biol 162(6):1123–1133PubMedCrossRefGoogle Scholar
  41. 41.
    Lekontseva O, Jiang Y, Davidge ST (2009) Estrogen replacement increases matrix metalloproteinase contribution to vasoconstriction in a rat model of menopause. J Hypertens 27(8):1602–1608PubMedCrossRefGoogle Scholar
  42. 42.
    Lewandowski KC, Komorowski J, Mikhalidis DP, Bienkiewicz M, Tan BK, O’Callaghan CJ, Lewinski A, Prelevic G, Randeva HS (2006) Effects of hormone replacement therapy type and route of administration on plasma matrix metalloproteinases and their tissue inhibitors in postmenopausal women. J Clin Endocrinol Metab 91(8):3123–3130PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Yeonju Kim
    • 1
  • Nicholas J. Ollberding
    • 1
  • Yurii B. Shvetsov
    • 1
  • Adrian A. Franke
    • 2
  • Lynne R. Wilkens
    • 1
  • Gertraud Maskarinec
    • 1
  • Brenda Y. Hernandez
    • 1
  • Loïc Le Marchand
    • 1
  • Brian E. Henderson
    • 3
  • Laurence N. Kolonel
    • 1
  • Marc T. Goodman
    • 1
  1. 1.Epidemiology ProgramUniversity of Hawai’i Cancer CenterHonoluluUSA
  2. 2.Cancer Biology ProgramUniversity of Hawai’i Cancer CenterHonoluluUSA
  3. 3.Department of Preventive Medicine, Keck School of MedicineUniversity of Southern CaliforniaLos AngelesUSA

Personalised recommendations