Abstract
The single nucleotide polymorphisms (SNPs) in the promoter region of matrix metalloproteinase (MMP) genes may influence tumor occurrence and progression via modifying mRNA transcription and protein expression. The study aims to explore the association of the SNPs in MMP-1, 3 and MMP-9 promoters with susceptibility to adult brain astrocytoma in northern China. Genotyping for the MMP-1 -1607 2G/1G, MMP-3 -1171 5A/6A, and MMP-9 -1562 C/T SNPs were performed by PCR-RFLP methods among 236 adult astrocytoma patients and 366 healthy controls. The results showed that the overall distribution of the MMP-1 allelotype and genotype among astrocytoma patients and healthy controls was significantly different (P = 0.002 and P < 0.001, respectively). Compared with the 2G/2G genotype, the 1G/1G genotype significantly decreased the risk of astrocytoma development (adjusted OR = 0.58, 95% CI = 0.42–0.79). The similar results were obtained when stratified by gender and age at tumor diagnosis (≤45 or >45 years). The association between MMP-3 -1171 5A/6A or MMP-9 -1562 C/T SNPs and susceptibility to astrocytoma was not observed in this study. However, MMP-1 1G-MMP-3 6A haplotype significantly reduced the risk of astrocytoma development when using MMP-1 2G-MMP-3 6A haplotype as a reference (OR = 0.45, 95% CI = 0.29–0.67). The present study suggested that, the MMP-1 -1607 1G/1G genotype and MMP-1 1G-MMP-3 6A haplotype may play protective role in the development of adult astrocytoma in northern Chinese, whereas the MMP-3 -1171 5A/6A and MMP-9 -1562 C/T polymorphisms may not be independent factors to influence susceptibility to adult astrocytoma in this population.
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References
Basset P, Okada A, Chenard MP, Kannan R, Stoll I, Anglard P, Bellocq JP, Rio MC (1997) Matrix metalloproteinases as stromal effectors of human carcinoma progression: therapeutic implications. Matrix Biol 15(8–9):535–541
Johnsen M, Lund LR, Romer J, Almholt K, Dano K (1998) Cancer invasion and tissue remodeling: common themes in proteolytic matrix degradation. Curr Opin Cell Biol 10(5):667–671
Curran S, Murray GI (1999) Matrix metalloproteinases in tumour invasion and metastasis. J Pathol 189(3):300–308
Uria JA, Stahle-Backdahl M, Seiki M, Fueyo A, Lopez-Otin C (1997) Regulation of collagenase-3 expression in human breast carcinomas is mediated by stromal-epithelial cell interactions. Cancer Res 57(21):4882–4888
Johansson N, Vaalamo M, Grenman S, Hietanen S, Klemi P, Saarialho-Kere U, Kahari VM (1999) Collagenase-3 (MMP-13) is expressed by tumor cells in invasive vulvar squamous cell carcinomas. Am J Pathol 154(2):469–480
Skobe M, Fusenig NE (1998) Tumorigenic conversion of immortal human keratinocytes through stromal cell activation. Proc Natl Acad Sci USA 95(3):1050–1055
Nishioka Y, Sagae S, Nishikawa A, Ishioka S, Kudo R (2003) A relationship between matrix metalloproteinase-1 (MMP-1) promoter polymorphism and cervical cancer progression. Cancer Lett 200(1):49–55
Hirata H, Naito K, Yoshihiro S, Matsuyama H, Suehiro Y, Hinoda Y (2003)A single nucleotide polymorphism in the matrix metalloproteinase-1 promoter is associated with conventional renal cell carcinoma. Int J Cancer 106(3):372–374
Yu C, Pan K, Xing D, Liang G, Tan W, Zhang L, Lin D (2002) Correlation between a single nucleotide polymorphism in the matrix metalloproteinase-2 promoter and risk of lung cancer. Cancer Res 62(22):6430–6433
Ghilardi G, Biondi ML, Caputo M, Leviti S, DeMonti M, Guagnellini E, Scorza R (2002) A single nucleotide polymorphism in the matrix metalloproteinase-3 promoter enhances breast cancer susceptibility. Clin Cancer Res 8(12):3820–3823
Szyllo K, Smolarz B, Romanowicz-Makowska H, Niewiadomski M, Kozlowska E, Kulig A (2002) The promoter polymorphism of the matrix metalloproteinase 3 (MMP-3) gene in women with ovarian cancer. J Exp Clin Cancer Res 21(3):357–361
Ghilardi G, Biondi ML, Erario M, Guagnellini E, Scorza R (2003) Colorectal carcinoma susceptibility and metastases are associated with matrix metalloproteinase-7 promoter polymorphisms. Clin Chem 49(11):1940–1942
Grieu F, Li WQ, Iacopetta B (2004) Genetic polymorphisms in the MMP-2 and MMP-9 genes and breast cancer phenotype. Breast Cancer Res Treat 88(3):197–204
Matsumura S, Oue N, Nakayama H, Kitadai Y, Yoshida K, Yamaguchi Y, Imai K, Nakachi K, Matsusaki K, Chayama K, Yasui W (2005) A single nucleotide polymorphism in the MMP-9 promoter affects tumor progression and invasive phenotype of gastric cancer. J Cancer Res Clin Oncol 131(1):19–25
Rutter JL, Mitchell TI, Buttice G, Meyers J, Gusella JF, Ozelius LJ, Brinckerhoff CE (1998) A single nucleotide polymorphism in the matrix metalloproteinase-1 promoter creates an Ets binding site and augments transcription. Cancer Res 58(23):5321–5325
Ye S, Watts GF, Mandalia S, Humphries SE, Henney AM (1995) Preliminary report: genetic variation in the human stromelysin promoter is associated with progression of coronary atherosclerosis. Br Heart J 73(3):209–215
Ye S, Eriksson P, Hamsten A, Kurkinen M, Humphries SE, Henney AM (1996) Progression of coronary atherosclerosis is associated with a common genetic variant of the human stromelysin-1 promoter which results in reduced gene expression. J Biol Chem 271(22):13055–13060
Opdenakker G, Van den Steen PE, Dubois B, Nelissen I, Van Coillie E, Masure S, Proost P, Van Damme J (2001) Gelatinase B functions as regulator and effector in leukocyte biology. J Leukoc Biol 69(6):851–859
van Kempen LC, Coussens LM (2002) MMP9 potentiates pulmonary metastasis formation. Cancer Cell 2(4):251–252
Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z, Hanahan D (2000) Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2(10):737–744
Zhang B, Henney A, Eriksson P, Hamsten A, Watkins H, Ye S (1999) Genetic variation at the matrix metalloproteinase-9 locus on chromosome 20q 12.2–13.1. Hum Genet 105(5):418–423
Zhang B, Ye S, Herrmann SM, Eriksson P, de Maat M, Evans A, Arveiler D, Luc G, Cambien F, Hamsten A, Watkins H, Henney AM (1999) Functional polymorphism in the regulatory region of gelatinase B gene in relation to severity of coronary atherosclerosis. Circulation 99(14):1788–1794
Hinoda Y, Okayama N, Takano N, Fujimura K, Suehiro Y, Hamanaka Y, Hazama S, Kitamura Y, Kamatani N, Oka M (2002) Association of functional polymorphisms of matrix metalloproteinase (MMP)-1 and MMP-3 genes with colorectal cancer. Int J Cancer 102(5):526–529
Zhu Y, Spitz MR, Lei L, Mills GB, Wu X (2001) A single nucleotide polymorphism in the matrix metalloproteinase-1 promoter enhances lung cancer susceptibility. Cancer Res 61(21):7825–7829
Jin X, Kuang G, Wei LZ, Li Y, Wang R, Guo W, Wang N, Fang SM, Wen DG, Chen ZF, Zhang JH (2005) No association of the matrix metalloproteinase 1 promoter polymorphism with susceptibility to esophageal squamous cell carcinoma and gastric cardiac adenocarcinoma in northern China. World J Gastroenterol 11(16):2385–2389
Zhang J, Jin X, Fang S, Li Y, Wang R, Guo W, Wang N, Wang Y, Wen D, Wei L, Kuang G, Dong Z (2004) The functional SNP in the matrix metalloproteinase-3 promoter modifies susceptibility and lymphatic metastasis in esophageal squamous cell carcinoma but not in gastric cardiac adenocarcinoma. Carcinogenesis 25(12):2519–2524
Fang S, Jin X, Wang R, Li Y, Guo W, Wang N, Wang Y, Wen D, Wei L, Zhang J (2005) Polymorphisms in the MMP1 and MMP3 promoter and non-small cell lung carcinoma in North China. Carcinogenesis 26(2):481–486
Wang Y, Fang S, Wei L, Wang R, Jin X, Wen D, Li Y, Guo W, Wang N, Zhang J (2005) No association between the C-1562T polymorphism in the promoter of matrix metalloproteinase-9 gene and non-small cell lung carcinoma. Lung Cancer 49(2):155–161
Malmer B, Gronberg H, Bergenheim AT, Lenner P, Henriksson R (1999) Familial aggregation of astrocytoma in northern Sweden: an epidemiological cohort study. Int J Cancer 81(3):366–370
Ichimura K, Ohgaki H, Kleihues P, Collins VP (2004) Molecular pathogenesis of astrocytic tumours. J Neurooncol 70(2):137–160
Wiemels JL, Wiencke JK, Patoka J, Moghadassi M, Chew T, McMillan A, Miike R, Barger G, Wrensch M (2004) Reduced immunoglobulin E and allergy among adults with glioma compared with controls. Cancer Res 64(22):8468–8473
Wiemels JL, Wiencke JK, Sison JD, Miike R, McMillan A, Wrensch M (2002) History of allergies among adults with glioma and controls. Int J Cancer 98(4):609–615
Schwartzbaum J, Ahlbom A, Malmer B, Lonn S, Brookes AJ, Doss H, Debinski W, Henriksson R, Feychting M (2005) Polymorphisms associated with asthma are inversely related to glioblastoma multiforme. Cancer Res 65(14):6459–6465
Wrensch M, Kelsey KT, Liu M, Miike R, Moghadassi M, Aldape K, McMillan A, Wiencke JK (2004) Glutathione-S-transferase variants and adult glioma. Cancer Epidemiol Biomarkers Prev 13(3):461–467
Rajaraman P, Schwartz BS, Rothman N, Yeager M, Fine HA, Shapiro WR, Selker RG, Black PM, Inskip PD (2005) Delta-aminolevulinic acid dehydratase polymorphism and risk of brain tumors in adults. Environ Health Perspect 113(9):1209–1211
Parhar P, Ezer R, Shao Y, Allen JC, Miller DC, Newcomb EW (2005) Possible association of p53 codon 72 polymorphism with susceptibility to adult and pediatric high-grade astrocytomas. Brain Res Mol Brain Res 137(1–2):98–103
Lu Z, Wang Y, Zhang Q, Zhang X, Wang S, Xie H, Li Y, Jiao B, Zhang J (2006) Association between the functional polymorphism in the matrix metalloproteinase-7 promoter and susceptibility to adult astrocytoma. Brain Res 1118(1):6–12
McCready J, Broaddus WC, Sykes V, Fillmore HL (2005) Association of a single nucleotide polymorphism in the matrix metalloproteinase-1 promoter with glioblastoma. Int J Cancer 117(5):781–785
Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16(3):1215
Gnasso A, Motti C, Irace C, Carallo C, Liberatoscioli L, Bernardini S, Massoud R, Mattioli PL, Federici G, Cortese C (2000) Genetic variation in human stromelysin gene promoter and common carotid geometry in healthy male subjects. Arterioscler Thromb Vasc Biol 20(6):1600–1605
Ferrand PE, Parry S, Sammel M, Macones GA, Kuivaniemi H, Romero R, Strauss JF III (2002) A polymorphism in the matrix metalloproteinase-9 promoter is associated with increased risk of preterm premature rupture of membranes in African Americans. Mol Hum Reprod 8(5):494–501
Wang M, Wang T, Liu S, Yoshida D, Teramoto A (2003) The expression of matrix metalloproteinase-2 and -9 in human gliomas of different pathological grades. Brain Tumor Pathol 20(2):65–72
Komatsu K, Nakanishi Y, Nemoto N, Hori T, Sawada T, Kobayashi M (2004) Expression and quantitative analysis of matrix metalloproteinase-2 and -9 in human gliomas. Brain Tumor Pathol 21(3):105–112
Li Y, Jin X, Kang S, Wang Y, Du H, Zhang J, Guo W, Wang N, Fang S (2006) Polymorphisms in the promoter regions of the matrix metalloproteinases-1, -3, -7, and -9 and the risk of epithelial ovarian cancer in China. Gynecol Oncol 101(1):92–96
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We greatly appreciate Drs. Yu Qi and Yinan Ma in the Central Laboratory of the First Affiliated Hospital of Beijing University to provide technique support in experiment assays.
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Lu, Z., Cao, Y., Wang, Y. et al. Polymorphisms in the matrix metalloproteinase-1, 3, and 9 promoters and susceptibility to adult astrocytoma in northern China. J Neurooncol 85, 65–73 (2007). https://doi.org/10.1007/s11060-007-9392-5
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DOI: https://doi.org/10.1007/s11060-007-9392-5