Inhibition of sonic hedgehog pathway and pluripotency maintaining factors regulate human pancreatic cancer stem cell characteristics
Activation of the sonic hedgehog (SHh) pathway is required for the growth of numerous tissues and organs and recent evidence indicates that this pathway is often recruited to stimulate growth of cancer stem cells (CSCs) and to orchestrate the reprogramming of cancer cells via epithelial mesenchymal...
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| Published in | International journal of cancer Vol. 131; no. 1; pp. 30 - 40 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Hoboken
Wiley Subscription Services, Inc., A Wiley Company
01.07.2012
Wiley-Blackwell Wiley Subscription Services, Inc |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Activation of the sonic hedgehog (SHh) pathway is required for the growth of numerous tissues and organs and recent evidence indicates that this pathway is often recruited to stimulate growth of cancer stem cells (CSCs) and to orchestrate the reprogramming of cancer cells via epithelial mesenchymal transition (EMT). The objectives of this study were to examine the molecular mechanisms by which (‐)‐epigallocatechin‐3‐gallate (EGCG), an active compound in green tea, inhibits self‐renewal capacity of pancreatic CSCs and synergizes with quercetin, a major polyphenol and flavonoid commonly detected in many fruits and vegetables. Our data demonstrated that EGCG inhibited the expression of pluripotency maintaining transcription factors (Nanog, c‐Myc and Oct‐4) and self‐renewal capacity of pancreatic CSCs. Inhibition of Nanog by shRNA enhanced the inhibitory effects of EGCG on self‐renewal capacity of CSCs. EGCG inhibited cell proliferation and induced apoptosis by inhibiting the expression of Bcl‐2 and XIAP and activating caspase‐3. Interestingly, EGCG also inhibited the components of SHh pathway (smoothened, patched, Gli1 and Gli2) and Gli transcriptional activity. Furthermore, EGCG inhibited EMT by inhibiting the expression of Snail, Slug and ZEB1, and TCF/LEF transcriptional activity, which correlated with significantly reduced CSC's migration and invasion, suggesting the blockade of signaling involved in early metastasis. Furthermore, combination of quercetin with EGCG had synergistic inhibitory effects on self‐renewal capacity of CSCs through attenuation of TCF/LEF and Gli activities. Since aberrant SHh signaling occurs in pancreatic tumorigenesis, therapeutics that target SHh pathway may improve the outcomes of patients with pancreatic cancer by targeting CSCs. |
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| AbstractList | Activation of the sonic hedgehog (SHh) pathway is required for the growth of numerous tissues and organs and recent evidence indicates that this pathway is often recruited to stimulate growth of cancer stem cells (CSCs) and to orchestrate the reprogramming of cancer cells via epithelial mesenchymal transition (EMT). The objectives of this study were to examine the molecular mechanisms by which (-)-epigallocatechin-3-gallate (EGCG), an active compound in green tea, inhibits self-renewal capacity of pancreatic CSCs and synergizes with quercetin, a major polyphenol and flavonoid commonly detected in many fruits and vegetables. Our data demonstrated that EGCG inhibited the expression of pluripotency maintaining transcription factors (Nanog, c-Myc and Oct-4) and self-renewal capacity of pancreatic CSCs. Inhibition of Nanog by shRNA enhanced the inhibitory effects of EGCG on self-renewal capacity of CSCs. EGCG inhibited cell proliferation and induced apoptosis by inhibiting the expression of Bcl-2 and XIAP and activating caspase-3. Interestingly, EGCG also inhibited the components of SHh pathway (smoothened, patched, Gli1 and Gli2) and Gli transcriptional activity. Furthermore, EGCG inhibited EMT by inhibiting the expression of Snail, Slug and ZEB1, and TCF/LEF transcriptional activity, which correlated with significantly reduced CSC's migration and invasion, suggesting the blockade of signaling involved in early metastasis. Furthermore, combination of quercetin with EGCG had synergistic inhibitory effects on self-renewal capacity of CSCs through attenuation of TCF/LEF and Gli activities. Since aberrant SHh signaling occurs in pancreatic tumorigenesis, therapeutics that target SHh pathway may improve the outcomes of patients with pancreatic cancer by targeting CSCs. Activation of the sonic hedgehog (SHh) pathway is required for the growth of numerous tissues and organs and recent evidence indicates that this pathway is often recruited to stimulate growth of cancer stem cells (CSCs) and to orchestrate the reprogramming of cancer cells via epithelial mesenchymal transition (EMT). The objectives of this study were to examine the molecular mechanisms by which (-)-epigallocatechin-3-gallate (EGCG), an active compound in green tea, inhibits self-renewal capacity of pancreatic CSCs and synergizes with quercetin, a major polyphenol and flavonoid commonly detected in many fruits and vegetables. Our data demonstrated that EGCG inhibited the expression of pluripotency maintaining transcription factors (Nanog, c-Myc and Oct-4) and self-renewal capacity of pancreatic CSCs. Inhibition of Nanog by shRNA enhanced the inhibitory effects of EGCG on self-renewal capacity of CSCs. EGCG inhibited cell proliferation and induced apoptosis by inhibiting the expression of Bcl-2 and XIAP and activating caspase-3. Interestingly, EGCG also inhibited the components of SHh pathway (smoothened, patched, Gli1 and Gli2) and Gli transcriptional activity. Furthermore, EGCG inhibited EMT by inhibiting the expression of Snail, Slug and ZEB1, and TCF/LEF transcriptional activity, which correlated with significantly reduced CSC's migration and invasion, suggesting the blockade of signaling involved in early metastasis. Furthermore, combination of quercetin with EGCG had synergistic inhibitory effects on self-renewal capacity of CSCs through attenuation of TCF/LEF and Gli activities. Since aberrant SHh signaling occurs in pancreatic tumorigenesis, therapeutics that target SHh pathway may improve the outcomes of patients with pancreatic cancer by targeting CSCs. [PUBLICATION ABSTRACT] Activation of the sonic hedgehog (SHh) pathway is required for the growth of numerous tissues and organs and recent evidence indicates that this pathway is often recruited to stimulate growth of cancer stem cells (CSCs) and to orchestrate the reprogramming of cancer cells via epithelial mesenchymal transition (EMT). The objectives of this study were to examine the molecular mechanisms by which (-)-epigallocatechin-3-gallate (EGCG), an active compound in green tea, inhibits self-renewal capacity of pancreatic CSCs and synergizes with quercetin, a major polyphenol and flavonoid commonly detected in many fruits and vegetables. Our data demonstrated that EGCG inhibited the expression of pluripotency maintaining transcription factors (Nanog, c-Myc and Oct-4) and self-renewal capacity of pancreatic CSCs. Inhibition of Nanog by shRNA enhanced the inhibitory effects of EGCG on self-renewal capacity of CSCs. EGCG inhibited cell proliferation and induced apoptosis by inhibiting the expression of Bcl-2 and XIAP and activating caspase-3. Interestingly, EGCG also inhibited the components of SHh pathway (smoothened, patched, Gli1 and Gli2) and Gli transcriptional activity. Furthermore, EGCG inhibited EMT by inhibiting the expression of Snail, Slug and ZEB1, and TCF/LEF transcriptional activity, which correlated with significantly reduced CSC's migration and invasion, suggesting the blockade of signaling involved in early metastasis. Furthermore, combination of quercetin with EGCG had synergistic inhibitory effects on self-renewal capacity of CSCs through attenuation of TCF/LEF and Gli activities. Since aberrant SHh signaling occurs in pancreatic tumorigenesis, therapeutics that target SHh pathway may improve the outcomes of patients with pancreatic cancer by targeting CSCs.Activation of the sonic hedgehog (SHh) pathway is required for the growth of numerous tissues and organs and recent evidence indicates that this pathway is often recruited to stimulate growth of cancer stem cells (CSCs) and to orchestrate the reprogramming of cancer cells via epithelial mesenchymal transition (EMT). The objectives of this study were to examine the molecular mechanisms by which (-)-epigallocatechin-3-gallate (EGCG), an active compound in green tea, inhibits self-renewal capacity of pancreatic CSCs and synergizes with quercetin, a major polyphenol and flavonoid commonly detected in many fruits and vegetables. Our data demonstrated that EGCG inhibited the expression of pluripotency maintaining transcription factors (Nanog, c-Myc and Oct-4) and self-renewal capacity of pancreatic CSCs. Inhibition of Nanog by shRNA enhanced the inhibitory effects of EGCG on self-renewal capacity of CSCs. EGCG inhibited cell proliferation and induced apoptosis by inhibiting the expression of Bcl-2 and XIAP and activating caspase-3. Interestingly, EGCG also inhibited the components of SHh pathway (smoothened, patched, Gli1 and Gli2) and Gli transcriptional activity. Furthermore, EGCG inhibited EMT by inhibiting the expression of Snail, Slug and ZEB1, and TCF/LEF transcriptional activity, which correlated with significantly reduced CSC's migration and invasion, suggesting the blockade of signaling involved in early metastasis. Furthermore, combination of quercetin with EGCG had synergistic inhibitory effects on self-renewal capacity of CSCs through attenuation of TCF/LEF and Gli activities. Since aberrant SHh signaling occurs in pancreatic tumorigenesis, therapeutics that target SHh pathway may improve the outcomes of patients with pancreatic cancer by targeting CSCs. |
| Author | Tang, Su-Ni Srivastava, Rakesh K. Fu, Junsheng Shankar, Sharmila Nall, Dara Rodova, Mariana |
| AuthorAffiliation | 2 Department of Pathology and Laboratory Medicine, The University of Kansas Cancer Center, The University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS, 66160, USA 1 Department of Pharmacology, Toxicology and Therapeutics, and Medicine, The University of Kansas Cancer Center, The University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS, 66160, USA |
| AuthorAffiliation_xml | – name: 1 Department of Pharmacology, Toxicology and Therapeutics, and Medicine, The University of Kansas Cancer Center, The University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS, 66160, USA – name: 2 Department of Pathology and Laboratory Medicine, The University of Kansas Cancer Center, The University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS, 66160, USA |
| Author_xml | – sequence: 1 givenname: Su-Ni surname: Tang fullname: Tang, Su-Ni organization: Department of Pharmacology, Toxicology and Therapeutics, and Medicine, University of Kansas Cancer Center, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS – sequence: 2 givenname: Junsheng surname: Fu fullname: Fu, Junsheng organization: Department of Pathology and Laboratory Medicine, University of Kansas Cancer Center, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS – sequence: 3 givenname: Dara surname: Nall fullname: Nall, Dara organization: Department of Pathology and Laboratory Medicine, University of Kansas Cancer Center, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS – sequence: 4 givenname: Mariana surname: Rodova fullname: Rodova, Mariana organization: Department of Pharmacology, Toxicology and Therapeutics, and Medicine, University of Kansas Cancer Center, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS – sequence: 5 givenname: Sharmila surname: Shankar fullname: Shankar, Sharmila organization: Department of Pathology and Laboratory Medicine, University of Kansas Cancer Center, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS – sequence: 6 givenname: Rakesh K. surname: Srivastava fullname: Srivastava, Rakesh K. email: rsrivastava@kumc.edu organization: Department of Pharmacology, Toxicology and Therapeutics, and Medicine, University of Kansas Cancer Center, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25905719$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/21796625$$D View this record in MEDLINE/PubMed |
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| Keywords | Human RNAi RNA interference Stem cell EGCG sonic hedgehog pathway Malignant tumor pluripotency maintaining factors Cell transformation Gene silencing pancreatic cancer Cancerology Hedgehog protein Pancreas cancer Digestive diseases Inhibitor Epithelial mesenchymal transition cancer stem cells Tumor cell Pluripotency Cancer Pancreatic disease |
| Language | English |
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| Notes | ark:/67375/WNG-GDPCNK6D-T National Institutes of Health - No. R01CA125262; No. RO1CA114469; No. RO1CA125262-02S1; and Kansas Bioscience Authority ArticleID:IJC26323 istex:DF4D7E7D00CF1BA77191F33523F8F3CE9F970F3A ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 |
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| PublicationDate | 1 July 2012 |
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| PublicationPlace | Hoboken |
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| PublicationTitle | International journal of cancer |
| PublicationTitleAlternate | Int. J. Cancer |
| PublicationYear | 2012 |
| Publisher | Wiley Subscription Services, Inc., A Wiley Company Wiley-Blackwell Wiley Subscription Services, Inc |
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| References | Kashyap V, Rezende NC, Scotland KB, Shaffer SM, Persson JL, Gudas LJ, Mongan NP. Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG. OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell micro. RNAs. Stem Cells Dev 2009; 18: 1093-108. Dai J, Ai K, Du Y, Chen G. Sonic hedgehog expression correlates with distant metastasis in pancreatic adenocarcinoma. Pancreas 2011; 40: 233-6. Maitra A, Hruban RH. Pancreatic cancer. Annu Rev Pathol 2008; 3: 157-88. Jeter CR, Badeaux M, Choy G, Chandra D, Patrawala L, Liu C, Calhoun-Davis T, Zaehres H, Daley GQ, Tang DG. Functional evidence that the self-renewal gene NANOG regulates human tumor development. Stem Cells 2009; 27: 993-1005. Iwatsuki M, Mimori K, Yokobori T, Ishi H, Beppu T, Nakamori S, Baba H, Mori M. Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer Sci 2010; 101: 293-9. Pliarchopoulou K, Pectasides D. Pancreatic cancer: current and future treatment strategies. Cancer Treat Rev 2009; 35: 431-6. Magee CJ, Ghaneh P, Neoptolemos JP. Surgical and medical therapy for pancreatic carcinoma. Best Pract Res Clin Gastroenterol 2002; 16: 435-55. Feldmann G, Habbe N, Dhara S, Bisht S, Alvarez H, Fendrich V, Beaty R, Mullendore M, Karikari C, Bardeesy N, Ouellette MM, Yu W, et al. Hedgehog inhibition prolongs survival in a genetically engineered mouse model of pancreatic cancer. Gut 2008; 57: 1420-30. Tang SN, Singh C, Nall D, Meeker D, Shankar S, Srivastava RK. The dietary bioflavonoid quercetin synergizes with epigallocathechin gallate (EGCG) to inhibit prostate cancer stem cell characteristics, invasion, migration and epithelial-mesenchymal transition. J Mol Signal 2010; 5: 14. Yeo TP, Hruban RH, Leach SD, Wilentz RE, Sohn TA, Kern SE, Iacobuzio-Donahue CA, Maitra A, Goggins M, Canto MI, Abrams RA, Laheru D, et al. Pancreatic cancer. Curr Probl Cancer 2002; 26: 176-275. Shankar S, Nall D, Tang SN, Meeker D, Passarini J, Sharma J, Srivastava RK. Resveratrol inhibits pancreatic cancer stem cell characteristics in human and KrasG12D transgenic mice by inhibiting pluripotency maintaining factors and epithelial-mesenchymal transition. PLoS One 2011; 6: e16530. Osterlund T, Kogerman P. Hedgehog signalling: how to get from Smo to Ci and Gli. Trends Cell Biol 2006; 16: 176-80. Bae KM, Su Z, Frye C, McClellan S, Allan RW, Andrejewski JT, Kelley V, Jorgensen M, Steindler DA, Vieweg J, Siemann DW. Expression of pluripotent stem cell reprogramming factors by prostate tumor initiating cells. J Urol 2010; 183: 2045-53. Cavaleri F, Scholer HR. Nanog: a new recruit to the embryonic stem cell orchestra. Cell 2003; 113: 551-2. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003; 113: 643-55. Jones RJ, Matsui WH, Smith BD. Cancer stem cells: are we missing the target?. J Natl Cancer Inst 2004; 96: 583-5. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-90. Varjosalo M, Taipale J. Hedgehog: functions and mechanisms. Genes Dev 2008; 22: 2454-72. Srivastava RK, Tang SN, Zhu W, Meeker D, Shankar S. Sulforaphane synergizes with quercetin to inhibit self-renewal capacity of pancreatic cancer stem cells. Front Biosci (Elite Ed) 2011; 3: 515-28. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-11. Ischenko I, Seeliger H, Kleespies A, Angele MK, Eichhorn ME, Jauch KW, Bruns CJ. Pancreatic cancer stem cells: new understanding of tumorigenesis, clinical implications. Langenbecks Arch Surg 2010; 395: 1-10. Srivastava RK. TRAIL/Apo-2L: mechanisms and clinical applications in cancer. Neoplasia 2001; 3: 535-46. Warshaw AL, Fernandez-del Castillo C. Pancreatic carcinoma. N Engl J Med 1992; 326: 455-65. Mueller MT, Hermann PC, Witthauer J, Rubio-Viqueira B, Leicht SF, Huber S, Ellwart JW, Mustafa M, Bartenstein P, D'Haese JG, Schoenberg MH, Berger F, et al. Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology 2009; 137: 1102-13. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003; 113: 631-42. Lee CJ, Dosch J, Simeone DM. Pancreatic cancer stem cells. J Clin Oncol 2008; 26: 2806-12. Hoei-Hansen CE, Nielsen JE, Almstrup K, Sonne SB, Graem N, Skakkebaek NE, Leffers H, Rajpert-De Meyts E. Transcription factor AP-2gamma is a developmentally regulated marker of testicular carcinoma in situ and germ cell tumors. Clin Cancer Res 2004; 10: 8521-30. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010; 60: 277-300. Ishizawa K, Izawa-Ishizawa Y, Ohnishi S, Motobayashi Y, Kawazoe K, Hamano S, Tsuchiya K, Tomita S, Minakuchi K, Tamaki T. Quercetin glucuronide inhibits cell migration and proliferation by platelet-derived growth factor in vascular smooth muscle cells. J Pharmacol Sci 2009; 109: 257-64. Jones RJ. Cancer stem cells: clinical relevance. J Mol Med 2009; 87: 1105-10. Knekt P, Jarvinen R, Seppanen R, Hellovaara M, Teppo L, Pukkala E, Aromaa A. Dietary flavonoids and the risk of lung cancer and other malignant neoplasms. Am J Epidemiol 1997; 146: 223-30. Rohatgi R, Scott MP. Patching the gaps in Hedgehog signalling. Nat Cell Biol 2007; 9: 1005-9. Wang Z, Li Y, Ahmad A, Banerjee S, Azmi AS, Kong D, Sarkar FH. Pancreatic cancer: understanding and overcoming chemoresistance. Nat Rev Gastroenterol Hepatol 2011; 8: 27-33. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, Madhu B, Goldgraben MA, Caldwell ME, Allard D, Frese KK, Denicola G, et al. Inhibition of hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009; 324: 1457-61. Mueller MT, Hermann PC, Heeschen C. Cancer stem cells as new therapeutic target to prevent tumour progression and metastasis. Front Biosci (Elite Ed) 2010; 2: 602-13. Beachy PA, Karhadkar SS, Berman DM. Tissue repair and stem cell renewal in carcinogenesis. Nature 2004; 432: 324-31. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, Hong SM, Fu B, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008; 321: 1801-6. Psahoulia FH, Drosopoulos KG, Doubravska L, Andera L, Pintzas A. Quercetin enhances TRAIL-mediated apoptosis in colon cancer cells by inducing the accumulation of death receptors in lipid rafts. Mol Cancer Ther 2007; 6: 2591-9. Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, Ng HH, Robson P. Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 2005; 280: 24731-7. Wong MY, Chiu GN. Simultaneous liposomal delivery of quercetin and vincristine for enhanced estrogen-receptor-negative breast cancer treatment. Anticancer Drugs 2010; 21: 401-10. Zhang L, Angst E, Park JL, Moro A, Dawson DW, Reber HA, Eibl G, Hines OJ, Go VL, Lu QY. Quercetin aglycone is bioavailable in murine pancreas and pancreatic xenografts. J Agric Food Chem 2010; 58: 7252-7. Duraj J, Zazrivcova K, Bodo J, Sulikova M, Sedlak J. Flavonoid quercetin, but not apigenin or luteolin, induced apoptosis in human myeloid leukemia cells and their resistant variants. Neoplasma 2005; 52: 273-9. Mi Y, Zhang C, Li C, Taneda S, Watanabe G, Suzuki AK, Taya K. Quercetin attenuates oxidative damage induced by treatment of embryonic chicken spermatogonial cells with 4-nitro-3-phenylphenol in diesel exhaust particles. Biosci Biotechnol Biochem 2010; 74: 934-8. Dashwood WM, Carter O, Al-Fageeh M, Li Q, Dashwood RH. Lysosomal trafficking of beta-catenin induced by the tea polyphenol epigallocatechin-3-gallate. Mutat Res 2005; 591: 161-72. Nair HB, Sung B, Yadav VR, Kannappan R, Chaturvedi MM, Aggarwal BB. Delivery of anti-inflammatory nutraceuticals by nanoparticles for the prevention and treatment of cancer. Biochem Pharmacol 2010;80:1833-43. 2002; 16 2005; 591 2009; 87 2010; 58 2006; 16 2010; 101 2011; 40 1992; 326 2008; 57 2010; 183 2008; 3 2008; 321 2010; 80 2011; 3 2011; 6 2003; 113 2009; 27 2011; 8 2009; 137 2010; 60 2009; 139 1997; 146 2004; 10 2004; 96 2005; 280 2010; 21 2009; 35 2002; 26 2004; 432 2007; 9 2008; 26 2005; 52 2007; 6 2010; 395 2001; 3 2008; 22 2010; 2 2009; 109 2010; 5 2010; 74 2009; 324 2001; 414 2009; 18 e_1_2_7_5_2 e_1_2_7_4_2 e_1_2_7_3_2 e_1_2_7_2_2 e_1_2_7_9_2 e_1_2_7_8_2 e_1_2_7_7_2 e_1_2_7_6_2 e_1_2_7_19_2 e_1_2_7_18_2 e_1_2_7_17_2 e_1_2_7_16_2 e_1_2_7_15_2 e_1_2_7_14_2 e_1_2_7_40_2 e_1_2_7_13_2 e_1_2_7_41_2 e_1_2_7_12_2 e_1_2_7_42_2 e_1_2_7_11_2 e_1_2_7_43_2 e_1_2_7_10_2 e_1_2_7_44_2 e_1_2_7_45_2 e_1_2_7_46_2 e_1_2_7_26_2 e_1_2_7_27_2 e_1_2_7_28_2 e_1_2_7_29_2 Duraj J (e_1_2_7_23_2) 2005; 52 e_1_2_7_25_2 e_1_2_7_24_2 e_1_2_7_30_2 e_1_2_7_31_2 e_1_2_7_22_2 e_1_2_7_32_2 e_1_2_7_21_2 e_1_2_7_33_2 e_1_2_7_20_2 e_1_2_7_34_2 e_1_2_7_35_2 e_1_2_7_36_2 e_1_2_7_37_2 e_1_2_7_38_2 e_1_2_7_39_2 19415763 - Stem Cells. 2009 May;27(5):993-1005 15549094 - Nature. 2004 Nov 18;432(7015):324-31 19421768 - Langenbecks Arch Surg. 2010 Jan;395(1):1-10 9247006 - Am J Epidemiol. 1997 Aug 1;146(3):223-30 15860457 - J Biol Chem. 2005 Jul 1;280(26):24731-7 16516476 - Trends Cell Biol. 2006 Apr;16(4):176-80 18039136 - Annu Rev Pathol. 2008;3:157-88 18539958 - J Clin Oncol. 2008 Jun 10;26(17):2806-12 20654584 - Biochem Pharmacol. 2010 Dec 15;80(12):1833-43 20110806 - Anticancer Drugs. 2010 Apr;21(4):401-10 19945376 - Cell. 2009 Nov 25;139(5):871-90 20303530 - J Urol. 2010 May;183(5):2045-53 18515410 - Gut. 2008 Oct;57(10):1420-30 12399802 - Curr Probl Cancer. 2002 Jul-Aug;26(4):176-275 12787504 - Cell. 2003 May 30;113(5):631-42 20610543 - CA Cancer J Clin. 2010 Sep-Oct;60(5):277-300 18794343 - Genes Dev. 2008 Sep 15;22(18):2454-72 12787505 - Cell. 2003 May 30;113(5):643-55 19202317 - J Pharmacol Sci. 2009 Feb;109(2):257-64 20718984 - J Mol Signal. 2010 Aug 18;5:14 20499918 - J Agric Food Chem. 2010 Jun 23;58(12):7252-7 16054165 - Mutat Res. 2005 Dec 11;591(1-2):161-72 20036905 - Front Biosci (Elite Ed). 2010;2:602-13 21304978 - PLoS One. 2011;6(1):e16530 16059641 - Neoplasma. 2005;52(4):273-9 19480567 - Stem Cells Dev. 2009 Sep;18(7):1093-108 20938369 - Pancreas. 2011 Mar;40(2):233-6 21102532 - Nat Rev Gastroenterol Hepatol. 2011 Jan;8(1):27-33 19328630 - Cancer Treat Rev. 2009 Aug;35(5):431-6 12787492 - Cell. 2003 May 30;113(5):551-2 1732772 - N Engl J Med. 1992 Feb 13;326(7):455-65 19816664 - J Mol Med (Berl). 2009 Nov;87(11):1105-10 11689955 - Nature. 2001 Nov 1;414(6859):105-11 19501590 - Gastroenterology. 2009 Sep;137(3):1102-13 18772397 - Science. 2008 Sep 26;321(5897):1801-6 17762891 - Nat Cell Biol. 2007 Sep;9(9):1005-9 19460966 - Science. 2009 Jun 12;324(5933):1457-61 17876056 - Mol Cancer Ther. 2007 Sep;6(9):2591-9 15623634 - Clin Cancer Res. 2004 Dec 15;10(24):8521-30 11774036 - Neoplasia. 2001 Nov-Dec;3(6):535-46 19961486 - Cancer Sci. 2010 Feb;101(2):293-9 20460716 - Biosci Biotechnol Biochem. 2010;74(5):934-8 21196331 - Front Biosci (Elite Ed). 2011;3:515-28 15100335 - J Natl Cancer Inst. 2004 Apr 21;96(8):583-5 12079268 - Best Pract Res Clin Gastroenterol. 2002 Jun;16(3):435-55 |
| References_xml | – reference: Mueller MT, Hermann PC, Witthauer J, Rubio-Viqueira B, Leicht SF, Huber S, Ellwart JW, Mustafa M, Bartenstein P, D'Haese JG, Schoenberg MH, Berger F, et al. Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology 2009; 137: 1102-13. – reference: Jones RJ. Cancer stem cells: clinical relevance. J Mol Med 2009; 87: 1105-10. – reference: Feldmann G, Habbe N, Dhara S, Bisht S, Alvarez H, Fendrich V, Beaty R, Mullendore M, Karikari C, Bardeesy N, Ouellette MM, Yu W, et al. Hedgehog inhibition prolongs survival in a genetically engineered mouse model of pancreatic cancer. Gut 2008; 57: 1420-30. – reference: Wang Z, Li Y, Ahmad A, Banerjee S, Azmi AS, Kong D, Sarkar FH. Pancreatic cancer: understanding and overcoming chemoresistance. Nat Rev Gastroenterol Hepatol 2011; 8: 27-33. – reference: Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003; 113: 643-55. – reference: Srivastava RK. TRAIL/Apo-2L: mechanisms and clinical applications in cancer. Neoplasia 2001; 3: 535-46. – reference: Varjosalo M, Taipale J. Hedgehog: functions and mechanisms. Genes Dev 2008; 22: 2454-72. – reference: Rohatgi R, Scott MP. Patching the gaps in Hedgehog signalling. Nat Cell Biol 2007; 9: 1005-9. – reference: Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003; 113: 631-42. – reference: Ischenko I, Seeliger H, Kleespies A, Angele MK, Eichhorn ME, Jauch KW, Bruns CJ. Pancreatic cancer stem cells: new understanding of tumorigenesis, clinical implications. Langenbecks Arch Surg 2010; 395: 1-10. – reference: Dashwood WM, Carter O, Al-Fageeh M, Li Q, Dashwood RH. Lysosomal trafficking of beta-catenin induced by the tea polyphenol epigallocatechin-3-gallate. Mutat Res 2005; 591: 161-72. – reference: Beachy PA, Karhadkar SS, Berman DM. Tissue repair and stem cell renewal in carcinogenesis. Nature 2004; 432: 324-31. – reference: Jones RJ, Matsui WH, Smith BD. Cancer stem cells: are we missing the target?. J Natl Cancer Inst 2004; 96: 583-5. – reference: Lee CJ, Dosch J, Simeone DM. Pancreatic cancer stem cells. J Clin Oncol 2008; 26: 2806-12. – reference: Iwatsuki M, Mimori K, Yokobori T, Ishi H, Beppu T, Nakamori S, Baba H, Mori M. Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer Sci 2010; 101: 293-9. – reference: Jeter CR, Badeaux M, Choy G, Chandra D, Patrawala L, Liu C, Calhoun-Davis T, Zaehres H, Daley GQ, Tang DG. Functional evidence that the self-renewal gene NANOG regulates human tumor development. Stem Cells 2009; 27: 993-1005. – reference: Kashyap V, Rezende NC, Scotland KB, Shaffer SM, Persson JL, Gudas LJ, Mongan NP. Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG. OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell micro. RNAs. Stem Cells Dev 2009; 18: 1093-108. – reference: Magee CJ, Ghaneh P, Neoptolemos JP. Surgical and medical therapy for pancreatic carcinoma. Best Pract Res Clin Gastroenterol 2002; 16: 435-55. – reference: Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, Madhu B, Goldgraben MA, Caldwell ME, Allard D, Frese KK, Denicola G, et al. Inhibition of hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009; 324: 1457-61. – reference: Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010; 60: 277-300. – reference: Mi Y, Zhang C, Li C, Taneda S, Watanabe G, Suzuki AK, Taya K. Quercetin attenuates oxidative damage induced by treatment of embryonic chicken spermatogonial cells with 4-nitro-3-phenylphenol in diesel exhaust particles. Biosci Biotechnol Biochem 2010; 74: 934-8. – reference: Osterlund T, Kogerman P. Hedgehog signalling: how to get from Smo to Ci and Gli. Trends Cell Biol 2006; 16: 176-80. – reference: Zhang L, Angst E, Park JL, Moro A, Dawson DW, Reber HA, Eibl G, Hines OJ, Go VL, Lu QY. Quercetin aglycone is bioavailable in murine pancreas and pancreatic xenografts. J Agric Food Chem 2010; 58: 7252-7. – reference: Duraj J, Zazrivcova K, Bodo J, Sulikova M, Sedlak J. Flavonoid quercetin, but not apigenin or luteolin, induced apoptosis in human myeloid leukemia cells and their resistant variants. Neoplasma 2005; 52: 273-9. – reference: Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-90. – reference: Mueller MT, Hermann PC, Heeschen C. Cancer stem cells as new therapeutic target to prevent tumour progression and metastasis. Front Biosci (Elite Ed) 2010; 2: 602-13. – reference: Dai J, Ai K, Du Y, Chen G. Sonic hedgehog expression correlates with distant metastasis in pancreatic adenocarcinoma. Pancreas 2011; 40: 233-6. – reference: Yeo TP, Hruban RH, Leach SD, Wilentz RE, Sohn TA, Kern SE, Iacobuzio-Donahue CA, Maitra A, Goggins M, Canto MI, Abrams RA, Laheru D, et al. Pancreatic cancer. Curr Probl Cancer 2002; 26: 176-275. – reference: Srivastava RK, Tang SN, Zhu W, Meeker D, Shankar S. Sulforaphane synergizes with quercetin to inhibit self-renewal capacity of pancreatic cancer stem cells. Front Biosci (Elite Ed) 2011; 3: 515-28. – reference: Tang SN, Singh C, Nall D, Meeker D, Shankar S, Srivastava RK. The dietary bioflavonoid quercetin synergizes with epigallocathechin gallate (EGCG) to inhibit prostate cancer stem cell characteristics, invasion, migration and epithelial-mesenchymal transition. J Mol Signal 2010; 5: 14. – reference: Bae KM, Su Z, Frye C, McClellan S, Allan RW, Andrejewski JT, Kelley V, Jorgensen M, Steindler DA, Vieweg J, Siemann DW. Expression of pluripotent stem cell reprogramming factors by prostate tumor initiating cells. J Urol 2010; 183: 2045-53. – reference: Cavaleri F, Scholer HR. Nanog: a new recruit to the embryonic stem cell orchestra. Cell 2003; 113: 551-2. – reference: Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-11. – reference: Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, Hong SM, Fu B, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008; 321: 1801-6. – reference: Psahoulia FH, Drosopoulos KG, Doubravska L, Andera L, Pintzas A. Quercetin enhances TRAIL-mediated apoptosis in colon cancer cells by inducing the accumulation of death receptors in lipid rafts. Mol Cancer Ther 2007; 6: 2591-9. – reference: Knekt P, Jarvinen R, Seppanen R, Hellovaara M, Teppo L, Pukkala E, Aromaa A. Dietary flavonoids and the risk of lung cancer and other malignant neoplasms. Am J Epidemiol 1997; 146: 223-30. – reference: Wong MY, Chiu GN. Simultaneous liposomal delivery of quercetin and vincristine for enhanced estrogen-receptor-negative breast cancer treatment. Anticancer Drugs 2010; 21: 401-10. – reference: Maitra A, Hruban RH. Pancreatic cancer. Annu Rev Pathol 2008; 3: 157-88. – reference: Ishizawa K, Izawa-Ishizawa Y, Ohnishi S, Motobayashi Y, Kawazoe K, Hamano S, Tsuchiya K, Tomita S, Minakuchi K, Tamaki T. Quercetin glucuronide inhibits cell migration and proliferation by platelet-derived growth factor in vascular smooth muscle cells. J Pharmacol Sci 2009; 109: 257-64. – reference: Shankar S, Nall D, Tang SN, Meeker D, Passarini J, Sharma J, Srivastava RK. Resveratrol inhibits pancreatic cancer stem cell characteristics in human and KrasG12D transgenic mice by inhibiting pluripotency maintaining factors and epithelial-mesenchymal transition. PLoS One 2011; 6: e16530. – reference: Nair HB, Sung B, Yadav VR, Kannappan R, Chaturvedi MM, Aggarwal BB. Delivery of anti-inflammatory nutraceuticals by nanoparticles for the prevention and treatment of cancer. Biochem Pharmacol 2010;80:1833-43. – reference: Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, Ng HH, Robson P. Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 2005; 280: 24731-7. – reference: Hoei-Hansen CE, Nielsen JE, Almstrup K, Sonne SB, Graem N, Skakkebaek NE, Leffers H, Rajpert-De Meyts E. Transcription factor AP-2gamma is a developmentally regulated marker of testicular carcinoma in situ and germ cell tumors. Clin Cancer Res 2004; 10: 8521-30. – reference: Pliarchopoulou K, Pectasides D. Pancreatic cancer: current and future treatment strategies. Cancer Treat Rev 2009; 35: 431-6. – reference: Warshaw AL, Fernandez-del Castillo C. Pancreatic carcinoma. 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| SubjectTerms | Apoptosis Apoptosis - drug effects Biological and medical sciences Cancer cancer stem cells Caspase Caspase 3 - biosynthesis Catechin - analogs & derivatives Catechin - pharmacology Cell activation Cell Line, Tumor Cell proliferation Cell Proliferation - drug effects Drug Synergism EGCG Epigallocatechin gallate epithelial mesenchymal transition Epithelial-Mesenchymal Transition - drug effects Flavonoids Gastroenterology. Liver. Pancreas. Abdomen Green tea Hedgehog protein Hedgehog Proteins - metabolism Homeodomain Proteins - biosynthesis Humans LEF/TCF protein Liver. Biliary tract. Portal circulation. Exocrine pancreas Medical research Medical sciences Metastases Molecular modelling Myc protein Nanog Homeobox Protein Neoplastic Stem Cells - drug effects Neoplastic Stem Cells - metabolism Neoplastic Stem Cells - pathology Octamer Transcription Factor-3 - biosynthesis Pancreas Pancreatic cancer Pancreatic Neoplasms - metabolism Pancreatic Neoplasms - pathology Plant Extracts - pharmacology Pluripotency pluripotency maintaining factors Pluripotent Stem Cells Proto-Oncogene Proteins c-bcl-2 - biosynthesis Proto-Oncogene Proteins c-myc - biosynthesis Quercetin Quercetin - pharmacology RNAi Rodents Signal transduction Signal Transduction - drug effects Snail protein sonic hedgehog pathway Stem cells TCF Transcription Factors - antagonists & inhibitors Tea Transcription factors Transcription, Genetic - drug effects Tumorigenesis Tumors X-Linked Inhibitor of Apoptosis Protein - biosynthesis XIAP protein |
| Title | Inhibition of sonic hedgehog pathway and pluripotency maintaining factors regulate human pancreatic cancer stem cell characteristics |
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