Mechanisms of Tumor Suppressor Gene Demethylation in Colon Cancer by Berries
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1 Mechanisms of Tumor Suppressor Gene Demethylation in Colon Cancer by Berries Li-Shu Wang, PhD Assistant Professor Department of Medicine Medical College of Wisconsin Cancer Center
2 Ten Leading Cancer Types for the Estimated New Cancer Cases and Deaths by Sex, 2010 Colorectal cancers are third most common cancer and third major cause of cancer mortality in U.S. 5-year survival ( ) = 66% Jemal, A. et al. CA Cancer J Clin 2010;0:caac.20073v1
3 Black Raspberries (BRBs) Freeze-dried powder
4 Some Chemopreventive Agents in Black Raspberries Vitamins: A, C, E, folic acid Minerals: calcium, selenium Simple phenols: ellagic acid, ferulic acid, coumaric acid, quercetin Complex phenols: anthocyanins Phytosterols: β-sitosterol, campesterol, stigmasterol Stoner GD, Cancer Prev Res. 2009;2:665.
5 Anthocyanins in Black Raspberries Cyanidin 3-O-glucoside Cyanidin 3-O-sambubioside Cyanidin 3-O-rutinoside Cyanidin 3-O-(2 G -xylosylrutinoside) Hecht SS et al., Carcinogenesis 2006;27:1617.
6 Effects of Whole BRBs and BRB Anthocyanins on Cellular Events and Associated Genes in NMBA- Treated Rat Esophagus Proliferation Ki-67/MIB-1 COX-2 PGE 2 Erk1/2 Inflammation COX-2 PGE 2 NF- 2 B CD45 Whole BRBs or BRB anthocyanins Apoptosis TUNEL Bcl-2 Bax Angiogenesis VEGF-1 HIF-1 CD34 CD45 leukocyte common antigen, CD34 Microvessel marker Wang LS et al., Cancer Prev Res. 2009;2:84.
7 DNA Methylation and Tumor Suppressor Gene Silencing Promoter CpG island CGCG CG CG Normal M CG M CG M CG M CG C: cytosine Cancer m C: methylcytosine X Cytosine C DNMT CH 3 5-MethylCytosine C DNMT: DNA methyltransferase DNMT family: DNMT1, DNMT3A, DNMT3B, etc DNA DNA
8 Wnt pathway WIF WNT L R P 5/ 6 Frizzled SFRP Ub Ub Proteasome Ub P GSK3 AXIN APC P AXIN GSK3 APC Degradation c-myc CYCD1 AXIN2 TCF/ LEF Target Genes
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10 Colorectal Cancer Study Pre-surgical model 1. Pre-Treatment Colorectal Biopsies - Adjacent normal and tumor 2. Blood and Urine Samples 1. Post-Treatment Colorectal Biopsies - Adjacent normal and tumor 2. Blood and Urine Samples 20 Patients - Black Raspberry Slurry (20g/3x/day) Treatment Time (Range 1-9 wks, Average 3 wks)
11 Black Raspberry Slurry
12 Colorectal Cancer Patient Demographics No. of Patients (%) Gender Female 3 (15) Male 17 (85) Age <45 2 (10) (40) >60 10 (50) Average 59 Tumor location Transverse, descending, and sigmoid colon 3 (15) Cecum and ascending colon 3 (15) Rectum 14 (70) Metastatic disease Lymph node involved 2 (10) No evidence 18 (90)
13 Colon Cancer Patient Demographics (cont d) Berry treatment (wks) No. of Patients (%) 3 11 (55) (30) >4 3 (15) Range 1-9, Average 3 Berry doses (20g/dose, 3 doses/day) 50 8 (40) (50) >100 2 (10) Average 67 No. of Patients (%) Compliance (%) (5) (40) (55) Toxicities reported Diarrhea 3 (15) Constipation 4 (20) None 13 (65) Improved bowel movements 15 (75)
14 BRB Anthocyanins Were Detected in Urine and Tissue from Colorectal Cancer Patients After Average 3 Wks of BRB Treatment Pre-treatment Mean S.D. (Range) Post-treatment Mean S.D. (Range) Urine (pmol/ml) ( ) ( ) Adjacent normal (fmol/mg) Adenocarcinoma (fmol/mg) ( ) ( ) ( ) ( ) p=0.21 Wang LS et al., Clin Cancer Res. 2011;17:598.
15 Effects of BRBs on promoter methylation and on LINE-1 repetitive element in adjacent normal tissues and colorectal adenocarcinomas from 20 patients before and after 1-to-9 wks of berry treatment A. SFRP2 C. p16 E. WIF1 Methylation (%) * B. PAX6a D. SFRP5 F. LINE-1 Methylation (%) * Pre Post Pre Post Pre Post Pre Post Pre Post Pre Post N T N T N T Wang LS et al., Clin Cancer Res. 2011;17:598.
16 Percent Change from Baseline in DNMT1 Protein Expression in Adjacent Normal and Tumor Tissues in Colorectal Cancer Patients Who Were Treated with Berries High vs Low Doses Adjacent normal Berry doses p= N/H 52 N/L % change from baseline DNMT1 p= N/H DNMT1-11 N/L Adenocarcinoma Berry doses p= T/H 53 T/L % change from baseline DNMT1 p= T/H -8 DNMT1 T/L Wang LS et al., Clin Cancer Res. 2011;17:598.
17 Wang LS et al., Clin Cancer Res. 2011;17:598. Percent Change from Baseline in Promoter Methylation in Adjacent Normal Tissues in Colorectal Cancer Patients Who Were Treated with Berries High vs Low Doses SFRP2 PAX6a p16 p=0.008 p=0.004 p=0.620 % change from baseline % change from baseline N/H N/L N/H N/L N/H N/L SFRP5 WIF1 All p=0.283 p=0.488 p= Berry dose N/H = 83 N/L = 52 N/H N/L N/H N/L N/H N/L
18 Percent Change from Baseline in Promoter Methylation in Adenocarcinoma in Colorectal Cancer Patients Who Were Treated with Berries High vs Low Doses SFRP2 PAX6a p16 p=0.001 p=0.028 p=0.064 % change from baseline % change from baseline T/H T/L T/H T/L T/H T/L SFRP5 WIF1 All p=0.189 p=0.032 p< T/H T/L T/H T/L T/H T/L Berry dose T/H = 85 T/L = 53 Wang LS et al., Clin Cancer Res. 2011;17:598.
19 Wang LS et al., Clin Cancer Res. 2011;17:598. Heat-maps of Promoter Methylation Changes from Baseline of SFRP2, PAX6a, p16, SFRP5 and WIF1, and Protein Expression Change of DNMT1 Promoter methylation Protein Adjacent normal Adenocarcinoma N/H N/L T/H T/L SFRP2 PAX6a p16 SFRP5 WIF1 DNMT1 pts pts % change from baseline
20 Correlation of Methylation Change with Total Berry Dose Berry dose p=0.035 R 2 =0.118 N/H N/L T/H T/L Promoter methylation % change from baseline Wang LS et al., Clin Cancer Res. 2011;17:598.
21 BRB Treatment Did Not Affect Global Methylation LINE-1 % change from baseline p=0.303 p= N/H N/L N/H+N/L T/H T/L T/H+T/L Wang LS et al., Clin Cancer Res. 2011;17:598.
22 Correlation of Methylation Change with DNMT1 Changes DNMT1 protein % change from baseline Promoter methylation % change from baseline DNMT1, P = 0.006, R 2 = 0.181
23 Representative Immunohistochemical Staining in Adjacent Normal and Colorectal Tumors -catenin E-cadherin c-myc Ki-67 TUNEL p16 CD105 N T Wang LS et al., Clin Cancer Res. 2011;17:598.
24 Percent Change from Baseline in Protein Expression in Adjacent Normal Tissues in Colorectal Cancer Patients Who Were Treated with Berries High vs Low Doses -catenin E-cadherin c-myc p=0.03 p=0.042 p=0.110 % change from baseline Berry dose N/H = 83 N/L = 52 N/H N/L N/H N/L N/H N/L Ki-67 TUNEL p16 p=0.045 p=0.024 p=0.229 CD105 p=0.531 % change from baseline N/H N/L N/H N/L N/H N/L N/H N/L Wang LS et al., Clin Cancer Res. 2011;17:598.
25 Percent Change from Baseline in Protein Expression in Adenocarcinoma in Colorectal Cancer Patients Who Were Treated with Berries High vs Low Doses -catenin E-cadherin c-myc p=0.011 p=0.34 p=0.413 % change from baseline Berry dose T/H = 85 T/L = 53 T/H T/L T/H T/L T/H T/L Ki-67 TUNEL p16 p=0.034 p=0.006 p=0.004 CD105 p=0.043 % change from baseline T/H T/L T/H T/L T/H T/L T/H T/L Wang LS et al., Clin Cancer Res. 2011;17:598.
26 Differential Responses of Adenocarcinoma from the Colon and Rectum to Berry Treatment p=0.105 p=0.011 p=0.656 Methylation % change from baseline Methylation % change from baseline N/H C T/H C p=0.790 N/H R T/H R N/L C p< p=0.025 N/L R N/H normal / high dose N/L normal / low dose T/H Tumor / high dose T/L Tumor / low dose C, Colon R, Rectum T/L C T/L R Wang LS et al., Clin Cancer Res. 2011;17:598.
27 Summary The methylation of three Wnt inhibitors, SFRP2, SFRP5 and WIF1, upstream genes in the Wnt pathway, and PAX6a, a developmental regulator, was modulated in a protective direction by BRBs in adjacent normal colon and in colorectal tumors. This was associated with decreased expression of DNMT1. BRBs also modulated the expression of genes downstream of the Wnt pathway as well as cell proliferation, apoptosis and angiogenesis in a protective direction. Rectal adjacent normal and adenocarcinomas were less responsive to short-term (~2 wks) berry treatment. Wang LS et al., Clin Cancer Res. 2011;17:598.
28 Conclusions Pilot study in humans indicate that black raspberries (BRBs): Are well tolerated. Protectively modulated DNA methylation markers. This was associated with decreased expression of DNMT1 and protective modulation of cellular functions e.g. cell proliferation and apoptosis. Could be chemopreventive in human colorectal cancer.
29 Acknowledgments Ohio State University Stoner Lab Gary Stoner Cassandra Henry Chieh-Ti Kuo Bethany Larue Claudio Rocha Christine Sardo Claire Seguin Kristen Stoner Dept. of Surgery Mark Arnold Edward Martin Dept. of Pathology Wendy Frankel Human Cancer Genetics Yi-Wen Huang Tim Huang Dept. of Food Science & Technology Ken Riedl Steven Schwartz Ohio State University Dept. of Biomedical Informatics Victor Jin Xun Lan Univ. of Minnesota Stephen Hecht Steve Carmella All patients who participated in berry trials Supported by USDA NCI R01 CA (Wang) NCI R01 CA (Stoner)
30
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