Mechanistic insight into the ability of American ginseng to suppress colon cancer associated with colitis

Carcinogenesis

Volumn 31, Issue 10, 2010, Pages 1734-1741

  Cui, Xiangli ^a   Jin, Yu ^a   Poudyal, Deepak ^a   Chumanevich, Alexander A ^a   Davis, Tia ^b   Windust, Anthony ^c   Hofseth, Anne ^a   Wu, Wensong ^b   Habiger, Joshua ^b   Pena, Edsel ^b   Wood, Patricia ^d   Nagarkatti, Mitzi ^d   Nagarkatti, Prakash S ^d   Hofseth, Lorne ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF SOUTH CAROLINA   (United States)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMERICAN GINSENG EXTRACT; AZOXYMETHANE; PLANT EXTRACT; TUMOR MARKER; UNCLASSIFIED DRUG; BAG4 PROTEIN, MOUSE; DEXTRAN SULFATE; HEAT SHOCK PROTEIN 90; MITOGEN ACTIVATED PROTEIN KINASE 7; PAX2 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TRANSCRIPTION FACTOR PAX2;

AMERICAN GINSENG; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CANCER PREVENTION; CANCER RISK; CANCER SCREENING; CANCER STAGING; CARCINOGENESIS; CELL ISOLATION; COLITIS; COLON ADENOMA; COLON CANCER; COLON MUCOSA; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GINSENG; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INTESTINE CELL; MALE; MOUSE; NONHUMAN; PRECANCER; PRIORITY JOURNAL; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; COLON; COLONIC NEOPLASMS; DRUG EFFECTS; PANAX; PATHOLOGY; PHYSIOLOGY; PHYTOTHERAPY; TOXICITY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AZOXYMETHANE; COLITIS; COLON; COLONIC NEOPLASMS; DEXTRAN SULFATE; FEMALE; HSP90 HEAT-SHOCK PROTEINS; MALE; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 7; PANAX; PAX2 TRANSCRIPTION FACTOR; PHYTOTHERAPY; PLANT EXTRACTS;

EID: 77957771818     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgq163     Document Type: Article

References (77)

1. Lennard-Jones,J.E. et al. (1983) Cancer surveillance in ulcerative colitis. Experience over 15 years. Lancet, 2, 149-152.
2. Lashner,B.A. et al. (1990) Colon cancer surveillance in chronic ulcerative colitis: historical cohort study. Am. J. Gastroenterol., 85, 1083-1087.
3. Kiesslich,R. et al. (2003) Methylene blue-aided chromoendoscopy for the detection of intraepithelial neoplasia and colon cancer in ulcerative colitis. Gastroenterology, 124, 880-888.
4. Askling,J. et al. (2001) Family history as a risk factor for colorectal cancer in inflammatory bowel disease. Gastroenterology, 120, 1356-1362.
5. Rubin,D.T. et al. (2008) Colorectal cancer prevention in inflammatory bowel disease and the role of 5-aminosalicylic acid: a clinical review and update. Inflamm. Bowel Dis., 14, 265-274.
6. Jin,Y. et al. (2008) American ginseng suppresses inflammation and DNA damage associated with mouse colitis. Carcinogenesis, 29, 2351-2359.
7. Wirtz,S. et al. (2007) Chemically induced mouse models of intestinal inflammation. Nat. Protoc., 2, 541-546.
8. Onizawa,M. et al. (2009) Signaling pathway via TNF-{alpha}/NF-{kappa}B in intestinal epithelial cells may be directly involved in colitis-associated carcinogenesis. Am. J. Physiol. Gastrointest. Liver Physiol., 296, G850-G859.
9. Clapper,M.L. et al. (2008) 5-aminosalicylic acid inhibits colitis-associated colorectal dysplasias in the mouse model of azoxymethane/dextran sulfate sodium-induced colitis. Inflamm. Bowel Dis., 14, 1341-1347.
10. Kotakadi,V.S. et al. (2008) Ginkgo biloba extract EGb 761 has anti-inflammatory properties and ameliorates colitis in mice by driving effector T cell apoptosis. Carcinogenesis, 29, 1799-1806.
11. Hofseth,L.J. et al. (2007) Inflammation, cancer, and targets of ginseng. J. Nutr., 137, 183S-185S.
12. Wang,C.Z. et al. (2009) Antiproliferative effects of different plant parts of Panax notoginseng on SW480 human colorectal cancer cells. Phytother. Res., 23, 6-13.
13. Luo,X. et al. (2008) Characterization of gene expression regulated by American ginseng and ginsenoside Rg3 in human colorectal cancer cells. Int. J. Oncol., 32, 975-983.
14. Li,X.L. et al. (2009) Panaxadiol, a purified ginseng component, enhances the anti-cancer effects of 5-fluorouracil in human colorectal cancer cells. Cancer Chemother. Pharmacol., 11, 11.
15. Yun,T.K. et al. (1983) Anticarcinogenic effect of long-term oral administration of red ginseng on newborn mice exposed to various chemical carcinogens. Cancer Detect. Prev., 6, 515-525.
16. Xu,T.M. et al. (2008) Inhibitory effect of ginsenoside Rg3 on ovarian cancer metastasis. Chin. Med. J. (Engl.), 121, 1394-1397.
17. Park,T.Y. et al. (2008) Anti-metastatic potential of ginsenoside Rp1, a novel ginsenoside derivative. Biol. Pharm. Bull., 31, 1802-1805.
18. Wang,W. et al. (2008) Experimental therapy of prostate cancer with novel natural product anti-cancer ginsenosides. Prostate, 68, 809-819.
19. Carneiro,C.S. et al. (2007) Pfaffia paniculata (Brazilian ginseng) methanolic extract reduces angiogenesis in mice. Exp. Toxicol. Pathol., 58, 427-431.
20. Yan,Y. et al. (2006) Efficacy of polyphenon E, red ginseng, and rapamycin on benzo(a)pyrene-induced lung tumorigenesis in A/J mice. Neoplasia, 8, 52-58.
21. da Silva,T.C. et al. (2005) Inhibitory effects of Pfaffia paniculata (Brazilian ginseng) on preneoplastic and neoplastic lesions in a mouse hepatocarcinogenesis model. Cancer Lett., 226, 107-113.
22. Cui,Y. et al. (2006) Association of ginseng use with survival and quality of life among breast cancer patients. Am. J. Epidemiol., 163, 645-653.
23. Chen,F.D. et al. (2001) Sensitization of a tumor, but not normal tissue, to the cytotoxic effect of ionizing radiation using Panax notoginseng extract. Am. J. Chin. Med., 29, 517-524.
24. Lee,S.J. et al. (1999) Antitumor activity of a novel ginseng saponin metabolite in human pulmonary adenocarcinoma cells resistant to cisplatin. Cancer Lett., 144, 39-43.
25. Volate,S.R. et al. (2005) Modulation of aberrant crypt foci and apoptosis by dietary herbal supplements (quercetin, curcumin, silymarin, ginseng and rutin). Carcinogenesis, 26, 1450-1456.
26. Park,S. et al. (2007) Inhibitory activities and attenuated expressions of 5-LOX with red ginseng in Helicobacter pylori-infected gastric epithelial cells. Dig. Dis. Sci., 52, 973-982.
27. Oh,G.S. et al. (2004) 20(S)-Protopanaxatriol, one of ginsenoside metabolites, inhibits inducible nitric oxide synthase and cyclooxygenase-2 expressions through inactivation of nuclear factor-kappaB in RAW 264.7 macrophages stimulated with lipopolysaccharide. Cancer Lett., 205, 23-29.
28. Behrens,J. (2000) Control of beta-catenin signaling in tumor development. Ann. N. Y. Acad. Sci., 910, 21-33; discussion 33-35.
29. Weiss,C. et al. (2004) Deregulated repression of c-Jun provides a potential link to its role in tumorigenesis. Cell Cycle, 3, 111-113.
30. Eferl,R. et al. (2003) Liver tumor development. c-Jun antagonizes the proapoptotic activity of p53. Cell, 112, 181-192.
31. Dressler,G.R. et al. (1992) Pax-2 is a DNA-binding protein expressed in em-bryonic kidney and Wilms tumor. Proc. Natl Acad. Sci. USA, 89, 1179-1183.
32. Muratovska,A. et al. (2003) Paired-Box genes are frequently expressed in cancer and often required for cancer cell survival. Oncogene, 22, 7989-7997.
33. Busse,A. et al. (2009) An intron 9 containing splice variant of PAX2. J. Transl. Med., 7, 36.
34. Wu,W.K. et al. (2009) Expression of ErbB receptors and their cognate ligands in gastric and colon cancer cell lines. Anticancer Res., 29, 229-234.
35. Ross,J.S. (2009) Breast cancer biomarkers and HER2 testing after 10 years of anti-HER2 therapy. Drug News Perspect., 22, 93-106.
36. Kuremsky,J.G. et al. (2009) Biomarkers for response to neoadjuvant chemoradiation for rectal cancer. Int. J. Radiat. Oncol. Biol. Phys., 74, 673-688.
37. Baron,A.T. et al. (2009) Clinical implementation of soluble EGFR (sEGFR) as a theragnostic serum biomarker of breast, lung and ovarian cancer. IDrugs, 12, 302-308.
38. Shen,L. et al. (2008) EGFR and HER2 expression in primary cervical cancers and corresponding lymph node metastases: implications for targeted radiotherapy. BMC Cancer, 8, 232.
39. Yamaoka,T. et al. (2008) Transactivation of EGF receptor and ErbB2 protects intestinal epithelial cells from TNF-induced apoptosis. Proc. Natl Acad. Sci. USA, 105, 11772-11777.
40. Pi,X. et al. (2004) Big mitogen-activated protein kinase (BMK1)/ERK5 protects endothelial cells from apoptosis. Circ. Res., 94, 362-369.
41. Akao,Y. et al. (2009) Role of microRNA-143 in Fas-mediated apoptosis in human T-cell leukemia Jurkat cells. Leuk. Res., 20, 20.
42. Guo,Y.S. et al. (2002) Gastrin stimulates cyclooxygenase-2 expression in intestinal epithelial cells through multiple signaling pathways. Evidence for involvement of ERK5 kinase and transactivation of the epidermal growth factor receptor. J. Biol. Chem., 277, 48755-48763.
43. Yoo,J. et al. (2009) Protein kinase D mediates synergistic expression of COX-2 induced by TNF-{alpha} and bradykinin in human colonic myofibroblasts. Am. J. Physiol. Cell Physiol., 297, C1576-C1587.
44. Trauzold,A. et al. (2003) PKCmu prevents CD95-mediated apoptosis and enhances proliferation in pancreatic tumour cells. Oncogene, 22, 8939-8947.
45. Kusunoki,M. et al. (1992) Protein kinase C activity in human colonic adenoma and colorectal carcinoma. Cancer, 69, 24-30.
46. Wali,R.K. et al. (1995) Mechanism of action of chemoprotective ursodeoxycholate in the azoxymethane model of rat colonic carcinogenesis: potential roles of protein kinase C-alpha, -beta II, and -zeta. Cancer Res., 55, 5257-5264.
47. Ozawa,F. et al. (2000) Enhanced expression of Silencer of death domains (SODD/BAG-4) in pancreatic cancer. Biochem. Biophys. Res. Commun., 271, 409-413.
48. Takada,H. et al. (2003) Role of SODD in regulation of tumor necrosis factor responses. Mol. Cell. Biol., 23, 4026-4033.
49. Lania,A.G. et al. (2004) Proliferation of transformed somatotroph cells related to low or absent expression of protein kinase a regulatory subunit 1A protein. Cancer Res., 64, 9193-9198.
50. Mantovani,G. et al. (2008) Different expression of protein kinase A (PKA) regulatory subunits in cortisol-secreting adrenocortical tumors: relationship with cell proliferation. Exp. Cell Res., 314, 123-130.
51. Farrow,B. et al. (2003) Inhibition of pancreatic cancer cell growth and induction of apoptosis with novel therapies directed against protein kinase A. Surgery, 134, 197-205.
52. Whitesell,L. et al. (1994) Inhibition of heat shock protein HSP90-pp60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc. Natl Acad. Sci. USA, 91, 8324-8328.
53. Banerji,U. (2009) Heat shock protein 90 as a drug target: some like it hot. Clin. Cancer Res., 15, 9-14.
54. Lundgren,K. et al. (2009) BIIB021, an orally available, fully synthetic small-molecule inhibitor of the heat shock protein Hsp90. Mol. Cancer Ther., 8, 921-929.
55. Smith,N.F. et al. (2006) Preclinical pharmacokinetics and metabolism of a novel diaryl pyrazole resorcinol series of heat shock protein 90 inhibitors. Mol. Cancer Ther., 5, 1628-1637.
56. McDonald,E. et al. (2006) Inhibitors of the HSP90 molecular chaperone: attacking the master regulator in cancer. Curr. Top Med. Chem., 6, 1091-1107.
57. Nosho,K. et al. (2006) Overexpression of poly(ADP-ribose) polymerase-1 (PARP-1) in the early stage of colorectal carcinogenesis. Eur. J. Cancer, 42, 2374-2381.
58. Li,M. et al. (2009) Poly(ADP-ribose) polymerase inhibition down-regulates expression of metastasis-related genes in CT26 colon carcinoma cells. Pathobiology, 76, 108-116.
59. Ratnam,K. et al. (2007) Current development of clinical inhibitors of poly(ADP-ribose) polymerase in oncology. Clin. Cancer Res., 13, 1383-1388.
60. Gottipati,S. et al. (2008) IRAK1: a critical signaling mediator of innate immunity. Cell Signal., 20, 269-276.
61. Fujiki,H. et al. (2009) Carcinogenic aspects of protein phosphatase 1 and 2A inhibitors. Prog. Mol. Subcell. Biol., 46, 221-254.
62. Douglas,P. et al. (2010) Protein phosphatase 6 interacts with the DNA-dependent protein kinase catalytic subunit and dephosphorylates gamma-H2AX. Mol. Cell. Biol., 30, 1368-1381.
63. Lemieux,E. et al. (2009) Constitutively active MEK1 is sufficient to induce epithelial-to-mesenchymal transition in intestinal epithelial cells and to promote tumor invasion and metastasis. Int. J. Cancer, 125, 1575-1586.
64. Hersey,P. et al. (2009) Small molecules and targeted therapies in distant metastatic disease. Ann. Oncol., 20, vi35-vi40.
65. Sachdev,D. et al. (2007) Disrupting insulin-like growth factor signaling as a potential cancer therapy. Mol. Cancer Ther., 6, 1-12.
66. Frasca,F. et al. (2008) The role of insulin receptors and IGF-I receptors in cancer and other diseases. Arch. Physiol. Biochem., 114, 23-37.
67. Kamradt,M.C. et al. (2001) The small heat shock protein alpha B-crystallin negatively regulates cytochrome c- and caspase-8-dependent activation of caspase-3 by inhibiting its autoproteolytic maturation. J. Biol. Chem., 276, 16059-16063.
68. Kamradt,M.C. et al. (2005) The small heat shock protein alpha B-crystallin is a novel inhibitor of TRAIL-induced apoptosis that suppresses the activation of caspase-3. J. Biol. Chem., 280, 11059-11066.
69. Mao,Y.W. et al. (2004) Human alphaA-and alphaB-crystallins bind to Bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ., 11, 512-526.
70. Liu,S. et al. (2007) Small heat shock protein alphaB-crystallin binds to p53 to sequester its translocation to mitochondria during hydrogen peroxide-induced apoptosis. Biochem. Biophys. Res. Commun., 354, 109-114.
71. Klemenz,R. et al. (1993) Expression of the murine small heat shock proteins hsp 25 and alpha B crystallin in the absence of stress. J. Cell Biol., 120, 639-645.
72. Weekes,J. et al. (2009) Irinotecan and colorectal cancer: the role of p53, VEGF-C and alpha-B-crystallin expression. Int. J. Colorectal Dis., 10, 10.
73. Even,Y. et al. (2006) CDC2L5, a Cdk-like kinase with RS domain, interacts with the ASF/SF2-associated protein p32 and affects splicing in vivo. J. Cell. Biochem., 99, 890-904.
74. Hook,S.S. et al. (2001) Ca(2+)/CaM-dependent kinases: from activation to function. Annu. Rev. Pharmacol. Toxicol., 41, 471-505.
75. Takai,N. et al. (2009) Targeting calcium/calmodulin-dependence kinase I and II as a potential anti-proliferation remedy for endometrial carcinomas. Cancer Lett., 277, 235-243.
76. Smith,J.A. et al. (2005) Identification of the first specific inhibitor of p90 ribosomal S6 kinase (RSK) reveals an unexpected role for RSK in cancer cell proliferation. Cancer Res., 65, 1027-1034.
77. Lee,K.W. et al. (2008) Enzastaurin, a protein kinase C beta inhibitor, suppresses signaling through the ribosomal S6 kinase and bad pathways and induces apoptosis in human gastric cancer cells. Cancer Res., 68, 1916-1926.