Resveratrol inhibits pancreatic cancer stem cell characteristics in human and KrasG12D transgenic mice by inhibiting pluripotency maintaining factors and epithelial-mesenchymal transition

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Shankar, Sharmila ^a   Nall, Dara ^a   Tang, Su Ni ^a   Meeker, Daniel ^a   Passarini, Jenna ^b   Sharma, Jay ^b   Srivastava, Rakesh K ^a  

^a UNIVERSITY OF KANSAS CANCER CENTER   (United States)

^b Celprogen   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; ANTIGEN; BREAST CANCER RESISTANCE PROTEIN; CASPASE 3; CASPASE 7; CD133 ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; EARLY SECRETORY ANTIGEN; HERMES ANTIGEN; IMMEDIATE EARLY PROTEIN BZLF1; K RAS PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MYC PROTEIN; NOTCH1 RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN BCL 2; RESVERATROL; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS; ANTIOXIDANT; KRAS2 PROTEIN, MOUSE; PROTEIN P21; STILBENE DERIVATIVE; TRANSCRIPTION FACTOR;

APOPTOSIS; ARTICLE; CANCER CELL; CANCER INHIBITION; CANCER INVASION; CANCER STEM CELL; CELL MIGRATION; CELL RENEWAL; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENETIC MARKER; HUMAN; HUMAN CELL; PANCREAS CANCER; PLURIPOTENT STEM CELL; TRANSGENIC MOUSE; ANIMAL; CELL MOTION; DRUG EFFECT; GENETICS; MOUSE; PANCREAS TUMOR; PATHOLOGY;

GASTROPODA; MUS; MUS MUSCULUS;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MICE; MICE, TRANSGENIC; NEOPLASTIC STEM CELLS; PANCREATIC NEOPLASMS; PLURIPOTENT STEM CELLS; PROTO-ONCOGENE PROTEINS P21(RAS); STILBENES; TRANSCRIPTION FACTORS;

EID: 79551617718     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016530     Document Type: Article

References (83)

1. Warshaw AL, Fernandez-del Castillo C (1992) Pancreatic carcinoma. N Engl J Med 326: 455-465.
2. Magee CJ, Ghaneh P, Neoptolemos JP (2002) Surgical and medical therapy for pancreatic carcinoma. Best Pract Res Clin Gastroenterol 16: 435-455.
3. Yeo TP, Hruban RH, Leach SD, Wilentz RE, Sohn TA, et al. (2002) Pancreatic cancer. Curr Probl Cancer 26: 176-275.
4. Reya T, Morrison SJ, Clarke MF, Weissman IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414: 105-111.
5. Ischenko I, Seeliger H, Kleespies A, Angele MK, Eichhorn ME, et al. (2010) Pancreatic cancer stem cells: new understanding of tumorigenesis, clinical implications. Langenbecks Arch Surg 395: 1-10.
6. Tang SN, Singh C, Nall D, Meeker D, Shankar S, et al. (2010) 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 5: 14.
7. Srivastava RK, Tang SN, Zhu W, Meeker D, Shankar S (2010) Sulforaphane inhibits self-renewal capacity of pancreatic cancer stem cells and synergizes with quercetin. Front Biosci in press.
8. Li G, Liu C, Yuan J, Xiao X, Tang N, et al. (2010) CD133(+) single cell-derived progenies of colorectal cancer cell line SW480 with different invasive and metastatic potential. Clin Exp Metastasis.
9. Lee A, Kessler JD, Read TA, Kaiser C, Corbeil D, et al. (2005) Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci 8: 723-729.
10. Shankar S, Singh G, Srivastava RK (2007) Chemoprevention by resveratrol: molecular mechanisms and therapeutic potential. Front Biosci 12: 4839-4854.
11. Delmas D, Jannin B, Latruffe N (2005) Resveratrol: preventing properties against vascular alterations and ageing. Mol Nutr Food Res 49: 377-395.
12. Ma ZH, Ma QY (2005) Resveratrol: a medical drug for acute pancreatitis. World J Gastroenterol 11: 3171-3174.
13. Sarkar FH, Li Y, Wang Z, Kong D (2009) Cellular signaling perturbation by natural products. Cell Signal 21: 1541-1547.
14. Sarkar FH, Li Y, Wang Z, Kong D (2010) The role of nutraceuticals in the regulation of Wnt and Hedgehog signaling in cancer. Cancer Metastasis Rev 29: 383-394.
15. Chan C, Lin HJ, Lin J (2008) Stress-associated hormone, norepinephrine, increases proliferation and IL-6 levels of human pancreatic duct epithelial cells and can be inhibited by the dietary agent, sulforaphane. Int J Oncol 33: 415-419.
16. Ding XZ, Adrian TE (2002) Resveratrol inhibits proliferation and induces apoptosis in human pancreatic cancer cells. Pancreas 25: e71-76.
17. Feick P, Gerloff A, Singer MV (2007) Effect of non-alcoholic compounds of alcoholic drinks on the pancreas. Pancreatology 7: 124-130.
18. Gerloff A, Singer MV, Feick P (2010) Beer and its non-alcoholic compounds: role in pancreatic exocrine secretion, alcoholic pancreatitis and pancreatic carcinoma. Int J Environ Res Public Health 7: 1093-1104.
19. Harikumar KB, Kunnumakkara AB, Sethi G, Diagaradjane P, Anand P, et al. (2010) Resveratrol, a multitargeted agent, can enhance antitumor activity of gemcitabine in vitro and in orthotopic mouse model of human pancreatic cancer. Int J Cancer 127: 257-268.
20. Kallifatidis G, Rausch V, Baumann B, Apel A, Beckermann BM, et al. (2008) Sulforaphane targets pancreatic tumor-initiating cells by NF-{kappa}B-induced anti-apoptotic signaling. Gut.
21. Aggarwal BB, Takada Y, Oommen OV (2004) From chemoprevention to chemotherapy: common targets and common goals. Expert Opin Investig Drugs 13: 1327-1338.
22. Pervaiz S (2004) Chemotherapeutic potential of the chemopreventive phytoalexin resveratrol. Drug Resist Updat 7: 333-344.
23. Shankar S, Siddiqui I, Srivastava RK (2007) Molecular mechanisms of resveratrol (3,4,5-trihydroxy-trans-stilbene) and its interaction with TNF-related apoptosis inducing ligand (TRAIL) in androgen-insensitive prostate cancer cells. Mol Cell Biochem 304: 273-285.
24. Gupta PB, Chaffer CL, Weinberg RA (2009) Cancer stem cells: mirage or reality? Nat Med 15: 1010-1012.
25. Klarmann GJ, Hurt EM, Mathews LA, Zhang X, Duhagon MA, et al. (2009) Invasive prostate cancer cells are tumor initiating cells that have a stem cell-like genomic signature. Clin Exp Metastasis 26: 433-446.
26. Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, et al. (2009) Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 27: 2059-2068.
27. Sarkar FH, Li Y, Wang Z, Kong D (2009) Pancreatic cancer stem cells and EMT in drug resistance and metastasis. Minerva Chir 64: 489-500.
28. Singh A, Settleman J (2010) EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene.
29. Lee CJ, Dosch J, Simeone DM (2008) Pancreatic cancer stem cells. J Clin Oncol 26: 2806-2812.
30. Simeone DM (2008) Pancreatic cancer stem cells: implications for the treatment of pancreatic cancer. Clin Cancer Res 14: 5646-5648.
31. Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, et al. (2007) Identification of pancreatic cancer stem cells. Cancer Res 67: 1030-1037.
32. Kalluri R, Weinberg RA (2009) The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428.
33. Wendt MK, Allington TM, Schiemann WP (2009) Mechanisms of the epithelialmesenchymal transition by TGF-beta. Future Oncol 5: 1145-1168.
34. Battula VL, Evans KW, Hollier BG, Shi Y, Marini FC, et al. (2010) Epithelial- Mesenchymal Transition-Derived Cells Exhibit Multi-Lineage Differentiation Potential Similar to Mesenchymal Stem Cells. Stem Cells.
35. Raimondi C, Cortesi E, Gianni W, Gazzaniga P (2010) Cancer Stem Cells and Epithelial-Mesenchymal Transition: Revisiting Minimal Residual Disease. Curr Cancer Drug Targets.
36. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, et al. (2003) Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 4: 437-450.
37. Ailles LE, Weissman IL (2007) Cancer stem cells in solid tumors. Curr Opin Biotechnol 18: 460-466.
38. Alison MR, Murphy G, Leedham S (2008) Stem cells and cancer: a deadly mix. Cell Tissue Res 331: 109-124.
39. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988.
40. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, et al. (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567.
41. Jones RJ, Gocke CD, Kasamon YL, Miller CB, Perkins B, et al. (2009) Circulating clonotypic B cells in classic Hodgkin lymphoma. Blood 113: 5920-5926.
42. Matsui W, Wang Q, Barber JP, Brennan S, Smith BD, et al. (2008) Clonogenic multiple myeloma progenitors, stem cell properties, and drug resistance. Cancer Res 68: 190-197.
43. Rasheed ZA, Yang J, Wang Q, Kowalski J, Freed I, et al. (2010) Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J Natl Cancer Inst 102: 340-351.
44. Hermann PC, Bhaskar S, Cioffi M, Heeschen C (2010) Cancer stem cells in solid tumors. Semin Cancer Biol 20: 77-84.
45. Baumann M, Krause M, Hill R (2008) Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 8: 545-554.
46. Dalerba P, Cho RW, Clarke MF (2007) Cancer stem cells: models and concepts. Annu Rev Med 58: 267-284.
47. Dean M, Fojo T, Bates S (2005) Tumour stem cells and drug resistance. Nat Rev Cancer 5: 275-284.
48. Pfeiffer MJ, Schalken JA (2010) Stem cell characteristics in prostate cancer cell lines. Eur Urol 57: 246-254.
49. Clarke MF (2008) What can we learn about breast cancer from stem cells? Adv Exp Med Biol 617: 17-22.
50. Fillmore CM, Kuperwasser C (2008) Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 10: R25.
51. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, et al. (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367: 645-648.
52. Al-Hajj M, Clarke MF (2004) Self-renewal and solid tumor stem cells. Oncogene 23: 7274-7282.
53. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, et al. (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828.
54. Deng S, Yang X, Lassus H, Liang S, Kaur S, et al. (2010) Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers. PLoS One 5: e10277.
55. Papailiou J, Bramis KJ, Gazouli M, Theodoropoulos G (2010) Stem cells in colon cancer. A new era in cancer theory begins. Int J Colorectal Dis.
56. Saif MW, Chu E (2010) Biology of colorectal cancer. Cancer J 16: 196-201.
57. Collins AT, Berry PA, Hyde C, Stower MJ, Maitland NJ (2005) Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 65: 10946-10951.
58. Collins AT, Maitland NJ (2006) Prostate cancer stem cells. Eur J Cancer 42: 1213-1218.
59. Marchitti SA, Brocker C, Stagos D, Vasiliou V (2008) Non-P450 aldehyde oxidizing enzymes: the aldehyde dehydrogenase superfamily. Expert Opin Drug Metab Toxicol 4: 697-720.
60. Charafe-Jauffret E, Ginestier C, Iovino F, Tarpin C, Diebel M, et al. (2010) Aldehyde dehydrogenase 1-positive cancer stem cells mediate metastasis and poor clinical outcome in inflammatory breast cancer. Clin Cancer Res 16: 45-55.
61. Clay MR, Tabor M, Owen JH, Carey TE, Bradford CR, et al. (2010) Singlemarker identification of head and neck squamous cell carcinoma cancer stem cells with aldehyde dehydrogenase. Head Neck.
62. Sun S, Wang Z (2010) ALDH high adenoid cystic carcinoma cells display cancer stem cell properties and are responsible for mediating metastasis. Biochem Biophys Res Commun 396: 843-848.
63. Ucar D, Cogle CR, Zucali JR, Ostmark B, Scott EW, et al. (2009) Aldehyde dehydrogenase activity as a functional marker for lung cancer. Chem Biol Interact 178: 48-55.
64. Wang L, Park P, Zhang H, La Marca F, Lin CY (2010) Prospective identification of tumorigenic osteosarcoma cancer stem cells in OS99-1 cells based on high aldehyde dehydrogenase activity. Int J Cancer.
65. Li T, Su Y, Mei Y, Leng Q, Leng B, et al. (2010) ALDH1A1 is a marker for malignant prostate stem cells and predictor of prostate cancer patients' outcome. Lab Invest 90: 234-244.
66. Huang EH, Hynes MJ, Zhang T, Ginestier C, Dontu G, et al. (2009) Aldehyde dehydrogenase 1 is a marker for normal and malignant human colonic stem cells (SC) and tracks SC overpopulation during colon tumorigenesis. Cancer Res 69: 3382-3389.
67. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, et al. (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1: 313-323.
68. Rasheed Z, Wang Q, Matsui W (2010) Isolation of stem cells from human pancreatic cancer xenografts. J Vis Exp.
69. Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, et al. (2005) Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 280: 24731-24737.
70. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
71. Kuroda T, Tada M, Kubota H, Kimura H, Hatano SY, et al. (2005) Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol Cell Biol 25: 2475-2485.
72. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, et al. (2003) The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113: 631-642.
73. Chambers I, Colby D, Robertson M, Nichols J, Lee S, et al. (2003) Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113: 643-655.
74. Hoei-Hansen CE, Nielsen JE, Almstrup K, Hansen MA, Skakkebaek NE, et al. (2004) Identification of genes differentially expressed in testes containing carcinoma in situ. Mol Hum Reprod 10: 423-431.
75. Chiou SH, Yu CC, Huang CY, Lin SC, Liu CJ, et al. (2008) Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clin Cancer Res 14: 4085-4095.
76. Lu KH, Chen YW, Tsai PH, Tsai ML, Lee YY, et al. (2009) Evaluation of radiotherapy effect in resveratrol-treated medulloblastoma cancer stem-like cells. Childs Nerv Syst 25: 543-550.
77. Lee JM, Dedhar S, Kalluri R, Thompson EW (2006) The epithelialmesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 172: 973-981.
78. Takeichi M (1988) The cadherins: cell-cell adhesion molecules controlling animal morphogenesis. Development 102: 639-655.
79. Hazan RB, Phillips GR, Qiao RF, Norton L, Aaronson SA (2000) Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J Cell Biol 148: 779-790.
80. Li C, Lee CJ, Simeone DM (2009) Identification of human pancreatic cancer stem cells. Methods Mol Biol 568: 161-173.
81. Reya T, Duncan AW, Ailles L, Domen J, Scherer DC, et al. (2003) A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 423: 409-414.
82. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, et al. (1998) A thirdgeneration lentivirus vector with a conditional packaging system. J Virol 72: 8463-8471.
83. Shankar S, Ganapathy S, Srivastava RK (2008) Sulforaphane enhances the therapeutic potential of TRAIL in prostate cancer orthotopic model through regulation of apoptosis, metastasis, and angiogenesis. Clin Cancer Res 14: 6855-6866.