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Principal Investigator
Samson T Jacob
Awardee Organization
Ohio State University
United States
Fiscal Year
2018
Activity Code
R01
Project End Date
NIH RePORTER
For more information, see NIH RePORTER Project 5R01CA086978-15
Molecular mechanism of diet-induced carcinogenesis
The dramatic increase in recent years in the incidence of non-alcoholic fatty liver disease in the Western world has led to an increase in the prevalence of NASH (non-alcoholic steatohepatitis) and associated complications such as cirrhosis and hepatocellular cancer (HCC). In USA, NASH is emerging as a major risk factor for HCC with no effective therapy. Unlike HBV/HCV-induced HCC, very little is known about the mechanism(s) underlying the pathogenesis of NASH-associated HCC. We have used a mouse model of HCC in which 100% mice fed choline-deficient and amino acid defined (CDAA) diet develop NASH by 22 weeks and spontaneous HCC in ~75% mice by 65-75 weeks. Further, these mice exhibit well-defined pathological changes that are markedly similar to the progression of HCC in humans. A key finding from our study is the consistent upregulation of miR-155, a proinflammatory microRNA, from an early stage of feeding CDAA diet that correlates with development of NASH. Notably, miR-155 is elevated in human NASH and HCC patients and its level is an independent predictor of poor prognosis and recurrence-free survival in HCC patients. We hypothesize that upregulation of miR-155 in hepatocytes and Kupffer cells (inflammatory cells in the liver), plays a causal role in NASH and HCCs. This proposal is based on the novel findings that (i) miR-155 knockout (KO) mice exhibit reduced inflammation and triglyceridemia as early as 4 weeks of feeding CDAA diet, and (ii) zerumbone (ZER), a sesquiterpine phytochemical from an edible ginger suppressed both spontaneous and diet-induced inflammatory responses in mice and HCC cell growth in culture and caused downregulation of miR-155. To test our hypothesis that manipulation of miR-155 levels and treatment with ZER will inhibit NASH and HCC, we will pursue the following 3 aims. 1 (a) Elucidate the role of miR-155 in initiation and progression of diet-induced NASH and HCC using miR155KO mice, and (b) identify the underlying mechanism by focusing on miR-155 targets. 2 (a) Investigate the susceptibility of mice overexpressing miR-155 in hepatocytes or in hepatocytes+Kupffer cells to diet induced NASH and HCC, and (b) elucidate the underlying mechanism of differential pathogenesis by identifying its cell type specific targets. 3. Explore preventive/therapeutic potential of ZER by (a) assessing its anti-tumorigenic potential against HCC cells, (b) testing its anti-inflammatory function in mice, and (c) elucidating the molecular basis of its function.
Publications
- Gamage SA, Brooke DG, Redkar S, Datta J, Jacob ST, Denny WA. Structure-activity relationships for 4-anilinoquinoline derivatives as inhibitors of the DNA methyltransferase enzyme DNMT1. Bioorganic & medicinal chemistry. 2013 Jun 1;21(11):3147-53. Epub 2013 Apr 6. PMID: 23639684
- Kutay H, Bai S, Datta J, Motiwala T, Pogribny I, Frankel W, Jacob ST, Ghoshal K. Downregulation of miR-122 in the rodent and human hepatocellular carcinomas. Journal of cellular biochemistry. 2006 Oct 15;99(3):671-8. PMID: 16924677
- Koenig AB, Barajas JM, Guerrero MJ, Ghoshal K. A Comprehensive Analysis of Argonaute-CLIP Data Identifies Novel, Conserved and Species-Specific Targets of miR-21 in Human Liver and Hepatocellular Carcinoma. International journal of molecular sciences. 2018 Mar 14;19. (3). PMID: 29538313
- Jacob ST, Motiwala T. Epigenetic regulation of protein tyrosine phosphatases: potential molecular targets for cancer therapy. Cancer gene therapy. 2005 Aug;12(8):665-72. PMID: 15803146
- Datta J, Majumder S, Kutay H, Motiwala T, Frankel W, Costa R, Cha HC, MacDougald OA, Jacob ST, Ghoshal K. Metallothionein expression is suppressed in primary human hepatocellular carcinomas and is mediated through inactivation of CCAAT/enhancer binding protein alpha by phosphatidylinositol 3-kinase signaling cascade. Cancer research. 2007 Mar 15;67(6):2736-46. PMID: 17363595
- Barajas JM, Reyes R, Guerrero MJ, Jacob ST, Motiwala T, Ghoshal K. The role of miR-122 in the dysregulation of glucose-6-phosphate dehydrogenase (G6PD) expression in hepatocellular cancer. Scientific reports. 2018 Jun 14;8(1):9105. PMID: 29904144
- Motiwala T, Kutay H, Zanesi N, Frissora FW, Mo X, Muthusamy N, Jacob ST. PTPROt-mediated regulation of p53/Foxm1 suppresses leukemic phenotype in a CLL mouse model. Leukemia. 2015 Jun;29(6):1350-9. Epub 2014 Dec 8. PMID: 25482129
- Wang B, Hsu SH, Majumder S, Kutay H, Huang W, Jacob ST, Ghoshal K. TGFbeta-mediated upregulation of hepatic miR-181b promotes hepatocarcinogenesis by targeting TIMP3. Oncogene. 2010 Mar 25;29(12):1787-97. Epub 2009 Dec 21. PMID: 20023698
- Reyes RK, Motiwala T, Jacob ST. Regulation of glucose metabolism in hepatocarcinogenesis by microRNAs. Gene expression. 2014;16(2):85-92. PMID: 24801169
- Majumder S, Ghoshal K, Datta J, Smith DS, Bai S, Jacob ST. Role of DNA methyltransferases in regulation of human ribosomal RNA gene transcription. The Journal of biological chemistry. 2006 Aug 4;281(31):22062-22072a. Epub 2006 May 30. PMID: 16735507
- Bai S, Datta J, Jacob ST, Ghoshal K. Treatment of PC12 cells with nerve growth factor induces proteasomal degradation of T-cadherin that requires tyrosine phosphorylation of its cadherin domain. The Journal of biological chemistry. 2007 Sep 14;282(37):27171-27180. Epub 2007 Jul 13. PMID: 17631504
- Luna JM, Barajas JM, Teng KY, Sun HL, Moore MJ, Rice CM, Darnell RB, Ghoshal K. Argonaute CLIP Defines a Deregulated miR-122-Bound Transcriptome that Correlates with Patient Survival in Human Liver Cancer. Molecular cell. 2017 Aug 3;67(3):400-410.e7. Epub 2017 Jul 20. PMID: 28735896
- Kutay H, Klepper C, Wang B, Hsu SH, Datta J, Yu L, Zhang X, Majumder S, Motiwala T, Khan N, Belury M, McClain C, Jacob S, Ghoshal K. Reduced susceptibility of DNA methyltransferase 1 hypomorphic (Dnmt1N/+) mice to hepatic steatosis upon feeding liquid alcohol diet. PloS one. 2012;7(8):e41949. Epub 2012 Aug 8. PMID: 22905112
- Ghoshal K, Bai S. DNA methyltransferases as targets for cancer therapy. Drugs of today (Barcelona, Spain : 1998). 2007 Jun;43(6):395-422. PMID: 17612710
- Motiwala T, Jacob ST. Role of protein tyrosine phosphatases in cancer. Progress in nucleic acid research and molecular biology. 2006;81:297-329. PMID: 16891175
- Ghoshal K, Majumder S, Datta J, Motiwala T, Bai S, Sharma SM, Frankel W, Jacob ST. Role of human ribosomal RNA (rRNA) promoter methylation and of methyl-CpG-binding protein MBD2 in the suppression of rRNA gene expression. The Journal of biological chemistry. 2004 Feb 20;279(8):6783-93. Epub 2003 Nov 10. PMID: 14610093
- Regan-Fendt K, Li D, Reyes R, Yu L, Wani NA, Hu P, Jacob ST, Ghoshal K, Payne PRO, Motiwala T. Transcriptomics-Based Drug Repurposing Approach Identifies Novel Drugs against Sorafenib-Resistant Hepatocellular Carcinoma. Cancers. 2020 Sep 23;12. (10). PMID: 32977582
- Hsu SH, Wang B, Kutay H, Bid H, Shreve J, Zhang X, Costinean S, Bratasz A, Houghton P, Ghoshal K. Hepatic loss of miR-122 predisposes mice to hepatobiliary cyst and hepatocellular carcinoma upon diethylnitrosamine exposure. The American journal of pathology. 2013 Dec;183(6):1719-1730. Epub 2013 Oct 8. PMID: 24113455
- Datta J, Ghoshal K, Denny WA, Gamage SA, Brooke DG, Phiasivongsa P, Redkar S, Jacob ST. A new class of quinoline-based DNA hypomethylating agents reactivates tumor suppressor genes by blocking DNA methyltransferase 1 activity and inducing its degradation. Cancer research. 2009 May 15;69(10):4277-85. Epub 2009 May 5. PMID: 19417133
- Motiwala T, Majumder S, Kutay H, Smith DS, Neuberg DS, Lucas DM, Byrd JC, Grever M, Jacob ST. Methylation and silencing of protein tyrosine phosphatase receptor type O in chronic lymphocytic leukemia. Clinical cancer research : an official journal of the American Association for Cancer Research. 2007 Jun 1;13(11):3174-81. PMID: 17545520
- Motiwala T, Majumder S, Ghoshal K, Kutay H, Datta J, Roy S, Lucas DM, Jacob ST. PTPROt inactivates the oncogenic fusion protein BCR/ABL and suppresses transformation of K562 cells. The Journal of biological chemistry. 2009 Jan 2;284(1):455-464. Epub 2008 Nov 7. PMID: 18997174
- Wang B, Hsu SH, Wang X, Kutay H, Bid HK, Yu J, Ganju RK, Jacob ST, Yuneva M, Ghoshal K. Reciprocal regulation of microRNA-122 and c-Myc in hepatocellular cancer: role of E2F1 and transcription factor dimerization partner 2. Hepatology (Baltimore, Md.). 2014 Feb;59(2):555-66. Epub 2013 Dec 20. PMID: 24038073
- Ghoshal K, Motiwala T, Claus R, Yan P, Kutay H, Datta J, Majumder S, Bai S, Majumder A, Huang T, Plass C, Jacob ST. HOXB13, a target of DNMT3B, is methylated at an upstream CpG island, and functions as a tumor suppressor in primary colorectal tumors. PloS one. 2010 Apr 29;5(4):e10338. PMID: 20454457
- Motiwala T, Kutay H, Ghoshal K, Bai S, Seimiya H, Tsuruo T, Suster S, Morrison C, Jacob ST. Protein tyrosine phosphatase receptor-type O (PTPRO) exhibits characteristics of a candidate tumor suppressor in human lung cancer. Proceedings of the National Academy of Sciences of the United States of America. 2004 Sep 21;101(38):13844-9. Epub 2004 Sep 8. PMID: 15356345
- Datta J, Majumder S, Bai S, Ghoshal K, Kutay H, Smith DS, Crabb JW, Jacob ST. Physical and functional interaction of DNA methyltransferase 3A with Mbd3 and Brg1 in mouse lymphosarcoma cells. Cancer research. 2005 Dec 1;65(23):10891-900. PMID: 16322236
- Bai S, Ghoshal K, Jacob ST. Identification of T-cadherin as a novel target of DNA methyltransferase 3B and its role in the suppression of nerve growth factor-mediated neurite outgrowth in PC12 cells. The Journal of biological chemistry. 2006 May 12;281(19):13604-13611. Epub 2006 Mar 14. PMID: 16537533
- Hsu SH, Wang B, Kota J, Yu J, Costinean S, Kutay H, Yu L, Bai S, La Perle K, Chivukula RR, Mao H, Wei M, Clark KR, Mendell JR, Caligiuri MA, Jacob ST, Mendell JT, Ghoshal K. Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver. The Journal of clinical investigation. 2012 Aug;122(8):2871-83. Epub 2012 Jul 23. PMID: 22820288
- Badawi M, Kim J, Dauki A, Sutaria D, Motiwala T, Reyes R, Wani N, Kolli S, Jiang J, Coss CC, Jacob ST, Phelps MA, Schmittgen TD. CD44 positive and sorafenib insensitive hepatocellular carcinomas respond to the ATP-competitive mTOR inhibitor INK128. Oncotarget. 2018 May 25;9(40):26032-26045. doi: 10.18632/oncotarget.25430. eCollection 2018 May 25. PMID: 29899840
- Wang B, Majumder S, Nuovo G, Kutay H, Volinia S, Patel T, Schmittgen TD, Croce C, Ghoshal K, Jacob ST. Role of microRNA-155 at early stages of hepatocarcinogenesis induced by choline-deficient and amino acid-defined diet in C57BL/6 mice. Hepatology (Baltimore, Md.). 2009 Oct;50(4):1152-61. PMID: 19711427
- Teng KY, Han J, Zhang X, Hsu SH, He S, Wani NA, Barajas JM, Snyder LA, Frankel WL, Caligiuri MA, Jacob ST, Yu J, Ghoshal K. Blocking the CCL2-CCR2 Axis Using CCL2-Neutralizing Antibody Is an Effective Therapy for Hepatocellular Cancer in a Mouse Model. Molecular cancer therapeutics. 2017 Feb;16(2):312-322. Epub 2016 Dec 15. PMID: 27980102
- Lin CH, Elkholy KH, Wani NA, Li D, Hu P, Barajas JM, Yu L, Zhang X, Jacob ST, Khan WN, Bai XF, Noonan AM, Ghoshal K. Ibrutinib Potentiates Antihepatocarcinogenic Efficacy of Sorafenib by Targeting EGFR in Tumor Cells and BTK in Immune Cells in the Stroma. Molecular cancer therapeutics. 2020 Feb;19(2):384-396. Epub 2019 Oct 3. PMID: 31582534
- Bai S, Ghoshal K, Datta J, Majumder S, Yoon SO, Jacob ST. DNA methyltransferase 3b regulates nerve growth factor-induced differentiation of PC12 cells by recruiting histone deacetylase 2. Molecular and cellular biology. 2005 Jan;25(2):751-66. PMID: 15632075
- Majumder S, Alinari L, Roy S, Miller T, Datta J, Sif S, Baiocchi R, Jacob ST. Methylation of histone H3 and H4 by PRMT5 regulates ribosomal RNA gene transcription. Journal of cellular biochemistry. 2010 Feb 15;109(3):553-63. PMID: 19998411
- Reyes R, Wani NA, Ghoshal K, Jacob ST, Motiwala T. Sorafenib and 2-Deoxyglucose Synergistically Inhibit Proliferation of Both Sorafenib-Sensitive and -Resistant HCC Cells by Inhibiting ATP Production. Gene expression. 2017 Feb 10;17(2):129-140. Epub 2016 Nov 16. PMID: 27938509
- Sengupta D, Cassel T, Teng KY, Aljuhani M, Chowdhary VK, Hu P, Zhang X, Fan TW, Ghoshal K. Regulation of hepatic glutamine metabolism by miR-122. Molecular metabolism. 2020 Apr;34:174-186. Epub 2020 Jan 9. PMID: 32180557
- Teng KY, Ghoshal K. Role of Noncoding RNAs as Biomarker and Therapeutic Targets for Liver Fibrosis. Gene expression. 2015;16(4):155-62. PMID: 26637395
- Motiwala T, Datta J, Kutay H, Roy S, Jacob ST. Lyn kinase and ZAP70 are substrates of PTPROt in B-cells: Lyn inactivation by PTPROt sensitizes leukemia cells to VEGF-R inhibitor pazopanib. Journal of cellular biochemistry. 2010 Jul 1;110(4):846-56. PMID: 20564182
- Bai S, Nasser MW, Wang B, Hsu SH, Datta J, Kutay H, Yadav A, Nuovo G, Kumar P, Ghoshal K. MicroRNA-122 inhibits tumorigenic properties of hepatocellular carcinoma cells and sensitizes these cells to sorafenib. The Journal of biological chemistry. 2009 Nov 13;284(46):32015-27. Epub 2009 Sep 2. PMID: 19726678
- Ramaswamy B, Majumder S, Roy S, Ghoshal K, Kutay H, Datta J, Younes M, Shapiro CL, Motiwala T, Jacob ST. Estrogen-mediated suppression of the gene encoding protein tyrosine phosphatase PTPRO in human breast cancer: mechanism and role in tamoxifen sensitivity. Molecular endocrinology (Baltimore, Md.). 2009 Feb;23(2):176-87. Epub 2008 Dec 18. PMID: 19095770
- Wang B, Hsu SH, Frankel W, Ghoshal K, Jacob ST. Stat3-mediated activation of microRNA-23a suppresses gluconeogenesis in hepatocellular carcinoma by down-regulating glucose-6-phosphatase and peroxisome proliferator-activated receptor gamma, coactivator 1 alpha. Hepatology (Baltimore, Md.). 2012 Jul;56(1):186-97. Epub 2012 Jun 5. PMID: 22318941
- Wang B, Jacob ST. Role of cancer stem cells in hepatocarcinogenesis. Genome medicine. 2011 Feb 22;3(2):11. PMID: 21345246
- Majumder S, Roy S, Kaffenberger T, Wang B, Costinean S, Frankel W, Bratasz A, Kuppusamy P, Hai T, Ghoshal K, Jacob ST. Loss of metallothionein predisposes mice to diethylnitrosamine-induced hepatocarcinogenesis by activating NF-kappaB target genes. Cancer research. 2010 Dec 15;70(24):10265-76. PMID: 21159647
- Motiwala T, Ghoshal K, Das A, Majumder S, Weichenhan D, Wu YZ, Holman K, James SJ, Jacob ST, Plass C. Suppression of the protein tyrosine phosphatase receptor type O gene (PTPRO) by methylation in hepatocellular carcinomas. Oncogene. 2003 Sep 25;22(41):6319-31. PMID: 14508512
- Datta J, Ghoshal K, Motiwala T, Jacob ST. Novel Insights into the Molecular Mechanism of Action of DNA Hypomethylating Agents: Role of Protein Kinase C δ in Decitabine-Induced Degradation of DNA Methyltransferase 1. Genes & cancer. 2012 Jan;3(1):71-81. PMID: 22893792
- Ghoshal K, Datta J, Majumder S, Bai S, Kutay H, Motiwala T, Jacob ST. 5-Aza-deoxycytidine induces selective degradation of DNA methyltransferase 1 by a proteasomal pathway that requires the KEN box, bromo-adjacent homology domain, and nuclear localization signal. Molecular and cellular biology. 2005 Jun;25(11):4727-41. PMID: 15899874
- Huang W, Mehta D, Sif S, Kent LN, Jacob ST, Ghoshal K, Mehta KD. Dietary fat/cholesterol-sensitive PKCβ-RB signaling: Potential role in NASH/HCC axis. Oncotarget. 2017 May 15;8(43):73757-73765. doi: 10.18632/oncotarget.17890. eCollection 2017 Sep 26. PMID: 29088742
- Wani NA, Zhang B, Teng KY, Barajas JM, Motiwala T, Hu P, Yu L, Brüschweiler R, Ghoshal K, Jacob ST. Reprograming of Glucose Metabolism by Zerumbone Suppresses Hepatocarcinogenesis. Molecular cancer research : MCR. 2018 Feb;16(2):256-268. Epub 2017 Nov 29. PMID: 29187559
- Wang X, Yu B, Ren W, Mo X, Zhou C, He H, Jia H, Wang L, Jacob ST, Lee RJ, Ghoshal K, Lee LJ. Enhanced hepatic delivery of siRNA and microRNA using oleic acid based lipid nanoparticle formulations. Journal of controlled release : official journal of the Controlled Release Society. 2013 Dec 28;172(3):690-8. Epub 2013 Oct 8. PMID: 24121065
- Ghoshal K, Li X, Datta J, Bai S, Pogribny I, Pogribny M, Huang Y, Young D, Jacob ST. A folate- and methyl-deficient diet alters the expression of DNA methyltransferases and methyl CpG binding proteins involved in epigenetic gene silencing in livers of F344 rats. The Journal of nutrition. 2006 Jun;136(6):1522-7. PMID: 16702315
- Thakral S, Ghoshal K. miR-122 is a unique molecule with great potential in diagnosis, prognosis of liver disease, and therapy both as miRNA mimic and antimir. Current gene therapy. 2015;15(2):142-50. PMID: 25537773
- Hsu SH, Motiwala T, Roy S, Claus R, Mustafa M, Plass C, Freitas MA, Ghoshal K, Jacob ST. Methylation of the PTPRO gene in human hepatocellular carcinoma and identification of VCP as its substrate. Journal of cellular biochemistry. 2013 Aug;114(8):1810-8. PMID: 23533167
- Motiwala T, Zanesi N, Datta J, Roy S, Kutay H, Checovich AM, Kaou M, Zhong Y, Johnson AJ, Lucas DM, Heerema NA, Hagan J, Mo X, Jarjoura D, Byrd JC, Croce CM, Jacob ST. AP-1 elements and TCL1 protein regulate expression of the gene encoding protein tyrosine phosphatase PTPROt in leukemia. Blood. 2011 Dec 1;118(23):6132-40. Epub 2011 Oct 14. PMID: 22001392
- Datta J, Kutay H, Nasser MW, Nuovo GJ, Wang B, Majumder S, Liu CG, Volinia S, Croce CM, Schmittgen TD, Ghoshal K, Jacob ST. Methylation mediated silencing of MicroRNA-1 gene and its role in hepatocellular carcinogenesis. Cancer research. 2008 Jul 1;68(13):5049-58. PMID: 18593903
- Teng KY, Barajas JM, Hu P, Jacob ST, Ghoshal K. Role of B Cell Lymphoma 2 in the Regulation of Liver Fibrosis in miR-122 Knockout Mice. Biology. 2020 Jul 8;9. (7). PMID: 32650615
- Wang X, He H, Lu Y, Ren W, Teng KY, Chiang CL, Yang Z, Yu B, Hsu S, Jacob ST, Ghoshal K, Lee LJ. Indole-3-carbinol inhibits tumorigenicity of hepatocellular carcinoma cells via suppression of microRNA-21 and upregulation of phosphatase and tensin homolog. Biochimica et biophysica acta. 2015 Jan;1853(1):244-53. Epub 2014 Oct 25. PMID: 25447674
- Miller TE, Ghoshal K, Ramaswamy B, Roy S, Datta J, Shapiro CL, Jacob S, Majumder S. MicroRNA-221/222 confers tamoxifen resistance in breast cancer by targeting p27Kip1. The Journal of biological chemistry. 2008 Oct 31;283(44):29897-903. Epub 2008 Aug 15. PMID: 18708351