The anticancer effect of probiotic Bacillus polyfermenticus on human colon cancer cells is mediated through ErbB2 and ErbB3 inhibition

International Journal of Cancer

Volumn 127, Issue 4, 2010, Pages 780-790

  Ma, Elise L ^a   Choi, Yoon Jeong ^a   Choi, Jinyoung ^a   Pothoulakis, Charalabos ^a   Rhee, Sang Hoon ^a   Im, Eunok ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bacillus polyfermenticus; Colon cancer; ErbB2; ErbB3; Probiotics

Indexed keywords

CYCLIN D1; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; INTERLEUKIN 8; PROBIOTIC AGENT; TRANSCRIPTION FACTOR E2F1; ANTINEOPLASTIC AGENT; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BACILLUS; BACILLUS POLYFERMENTICUS; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CARCINOGENESIS; CELL ASSAY; CELL PROLIFERATION; CELL STRAIN CACO 2; CELL STRAIN HT29; CELL TRANSFORMATION; COLON CANCER; COLON MUCOSA; COLONY FORMING CELL; CONTROLLED STUDY; CULTURAL ANTHROPOLOGY; CULTURE MEDIUM; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FEMALE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TUMOR GROWTH; TUMOR VOLUME; ANIMAL; APOPTOSIS; COLON TUMOR; DRUG ANTAGONISM; ENZYME IMMUNOASSAY; GENETICS; METABOLISM; MICROBIOLOGY; NUDE MOUSE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE; WESTERN BLOTTING;

ANIMALS; ANTICARCINOGENIC AGENTS; APOPTOSIS; BACILLUS; BLOTTING, WESTERN; CELL PROLIFERATION; COLONIC NEOPLASMS; CULTURE MEDIA, CONDITIONED; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; MICE; MICE, NUDE; PROBIOTICS; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR CELLS, CULTURED;

EID: 77954751968     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.25011     Document Type: Article

References (49)

1. Guarner F, Malagelada JR. Gut flora in health and disease. Lancet 2003;361:512-19.
2. Reid G, Jass J, Sebulsky MT, McCormick JK. Potential uses of probiotics in clinical practice. Clin Microbiol Rev 2003;16:658-72. (Pubitemid 37296554)
3. Sartor RB. Probiotic therapy of intestinal inflammation and infections. Curr Opin Gastroenterol 2005;21:44-50.
4. Fedorak RN, Madsen KL. Probiotics and the management of inflammatory bowel disease. Inflamm Bowel Dis 2004;10:286-99.
5. Huebner ES, Surawicz CM. Probiotics in the prevention and treatment of gastrointestinal infections. Gastroenterol Clin North Am 2006;35:355-65.
6. Pool-Zobel BL, Neudecker C, Domizlaff I, Ji S, Schillinger U, Rumney C, Moretti M, Vilarini I, Scassellati-Sforzolini R, Rowland I. Lactobacillus- and bifidobacterium-mediated antigenotoxicity in the colon of rats. Nutr Cancer 1996;26:365-80. (Pubitemid 26362074)
7. Goldin BR, Gualtieri LJ, Moore RP. The effect of Lactobacillus GG on the initiation and promotion of DMH-induced intestinal tumors in the rat. Nutr Cancer 1996;25:197-204. (Pubitemid 26114220)
8. Arimochi H, Kinouchi T, Kataoka K, Kuwahara T, Ohnishi Y. Effect of intestinal bacteria on formation of azoxymethane-induced aberrant crypt foci in the rat colon. Biochem Biophys Res Commun 1997;238:753-7. (Pubitemid 27472647)
9. Yasutake N, Matsuzaki T, Kimura K, Hashimoto S, Yokokura T, Yoshikai Y. The role of tumor necrosis factor (TNF)-alpha in the antitumor effect of intrapleural injection of Lactobacillus casei strain Shirota in mice. Med Microbiol Immunol 1999;188:9-14. (Pubitemid 29419585)
10. Kato I, Kobayashi S, Yokokura T, Mutai M. Antitumor activity of Lactobacillus casei in mice. Gann 1981;72:517-23. (Pubitemid 11056171)
11. Lee KH, Jun KD, Kim WS, Paik HD. Partial characterization of polyfermenticin SCD, a newly identified bacteriocin of Bacillus polyfermenticus. Lett Appl Microbiol 2001;32:146-51.
12. Kim HS, Park H, Cho IY, Paik HD, Park E. Dietary supplementation of probiotic Bacillus polyfermenticus. Bispan strain, modulates natural killer cell and T cell subset populations and immunoglobulin G levels in human subjects. J Med Food 2006;9:321-7. (Pubitemid 44850714)
13. Lee NK, Park JS, Park E, Paik HD. Adherence and anticarcinogenic effects of Bacillus polyfermenticus SCD in the large intestine. Lett Appl Microbiol 2007;44:274-8. (Pubitemid 46277016)
14. Park E, Jeon GI, Park JS, Paik HD. A probiotic strain of Bacillus polyfermenticus reduces DMH induced precancerous lesions in F344 male rat. Biol Pharm Bull 207;30:569-74.
15. Guix M, Faber AC, Wang SE, Olivares MG, Song Y, Qu S, Rinehart C, Seidel B, Yee D, Arteaga CL, Engelman JA. Acquired resistance to EGFR tyrosine kinase inhibitors in cancer cells is mediated by loss of IGF-binding proteins. J Clin Invest 2008;118:2609-19. (Pubitemid 351949788)
16. Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas CF, III, Hynes NE. The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc Natl Acad Sci USA 2003;100:8933-8. (Pubitemid 36899201)
17. Kamath S, Buolamwini JK. Targeting EGFR and HER-2 receptor tyrosine kinases for cancer drug discovery and development. Med Res Rev 2006;26:569-94. (Pubitemid 44230413)
18. Naidu R, Yadav M, Nair S, Kutty MK. Expression of c-erbB3 protein in primary breast carcinomas. Br J Cancer 1998;78:1385-90. (Pubitemid 28495255)
19. Chow NH, Chan SH, Tzai TS, Ho CL, Liu HS. Expression profiles of ErbB family receptors and prognosis in primary transitional cell carcinoma of the urinary bladder. Clin Cancer Res 2001;7:1957-62.
20. Guy PM, Platko JV, Cantley LC, Cerione RA, Carraway KL, III. Insect cell-expressed p180erbB3 possesses an impaired tyrosine kinase activity. Proc Natl Acad Sci USA 1994;91:8132-6.
21. Kim HH, Vijapurkar U, Hellyer NJ, Bravo D, Koland JG. Signal transduction by epidermal growth factor and heregulin via the kinase-deficient ErbB3 protein. Biochem J 1998;334(Part 1):189-95. (Pubitemid 28420988)
22. Baselga J, Albanell J, Molina MA, Arribas J. Mechanism of action of trastuzumab and scientific update. Semin Oncol 2001;28:4-11. (Pubitemid 33065104)
23. Albanell J, Codony J, Rovira A, Mellado B, Gascon P. Mechanism of action of anti-HER2 monoclonal antibodies: scientific update on trastuzumab and 2C4. Adv Exp Med Biol 2003;532:253-68. (Pubitemid 37176793)
24. Valius M, Kazlauskas A. Phospholipase C-gamma 1 and phosphatidylinositol 3 kinase are the downstream mediators of the PDGF receptor's mitogenic signal. Cell 1993;73:321-34. (Pubitemid 23123310)
25. Rhee SH, Keates AC, Moyer MP, Pothoulakis C. MEK is a key modulator for TLR5-induced interleukin-8 and MIP3alpha gene expression in non-transformed human colonic epithelial cells. J Biol Chem 2004;279:25179-88. (Pubitemid 38756768)
26. Grabig A, Paclik D, Guzy C, Dankof A, Baumgart DC, Erckenbrecht J, Raupach B, Sonnenborn U, Eckert J, Schumann RR, Wiedenmann B, Dignass AU, et al. Escherichia coli strain Nissle 1917 ameliorates experimental colitis via toll-like receptor 2- and toll-like receptor 4-dependent pathways. Infect Immunol 2006;74:4075-82.
27. Masuda A, Kondo M, Saito T, Yatabe Y, Kobayashi T, Okamoto M, Suyama M, Takahashi T. Establishment of human peripheral lung epithelial cell lines (HPL1) retaining differentiated characteristics and responsiveness to epidermal growth factor, hepatocyte growth factor, and transforming growth factor beta1. Cancer Res 1997;57:4898-904. (Pubitemid 27469000)
28. Rhee SH, Im E, Pothoulakis C. Toll-like receptor 5 engagement modulates tumor development and growth in a mouse xenograft model of human colon cancer. Gastroenterology 2008;135:518-28.
29. Yashiro M, Nakazawa K, Tendo M, Kosaka K, Shinto O, Hirakawa K. Selective cyclooxygenase-2 inhibitor downregulates the paracrine epithelial-mesenchymal interactions of growth in scirrhous gastric carcinoma. Int J Cancer 2007;120:686-93. (Pubitemid 44969042)
30. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-8.
31. Rhee SH, Im E, Riegler M, Kokkotou E, O'brien M, Pothoulakis C. Pathophysiological role of Toll-like receptor 5 engagement by bacterial flagellin in colonic inflammation. Proc Natl Acad Sci USA 2005;102:13610-15.
32. Biffi A, Coradini D, Larsen R, Riva L, Di Fronzo G. Antiproliferative effect of fermented milk on the growth of a human breast cancer cell line. Nutr Cancer 1997;28:93-9. (Pubitemid 27287634)
33. Folkman J. Angiogenesis. Annu Rev Med 2006;57:1-18.
34. Sherr CJ. Cancer cell cycles. Science 1996;274:1672-7.
35. Weinberg RA. The retinoblastoma protein and cell cycle control. Cell 1995;81:323-30.
36. Lee RJ, Albanese C, Fu M, D'Amico M, Lin B, Watanabe G, Haines GK, III, Siegel PM, Hung MC, Yarden Y, Horowitz JM, Muller WJ, et al. Cyclin D1 is required for transformation by activated Neu and is induced through an E2F-dependent signaling pathway. Mol Cell Biol 2000;20:672-83. (Pubitemid 30023109)
37. Rafter J. The effects of probiotics on colon cancer development. Nutr Res Rev 2004;17:277-84.
38. Sekine K, Toida T, Saito M, Kuboyama M, Kawashima T, Hashimoto Y. A new morphologically characterized cell wall preparation (whole peptidoglycan) from Bifidobacterium infantis with a higher efficacy on the regression of an established tumor in mice. Cancer Res 1985;45:1300-7. (Pubitemid 15111296)
39. Challa A, Rao DR, Chawan CB, Shackelford L. Bifidobacterium longum and lactulose suppress azoxymethane-induced colonic aberrant crypt foci in rats. Carcinogenesis 1997;18:517-21. (Pubitemid 28132489)
40. Hayatsu H, Hayatsu T. Suppressing effect of Lactobacillus casei administration on the urinary mutagenicity arising from ingestion of fried ground beef in the human. Cancer Lett 1993;73:173-9. (Pubitemid 23322297)
41. Ohkawara S, Furuya H, Nagashima K, Asanuma N, Hino T. Oral administration of Butyrivibrio fibrisolvens, a butyrate-producing bacterium, decreases the formation of aberrant crypt foci in the colon and rectum of mice. J Nutr 2005;135:2878-83. (Pubitemid 43156557)
42. Jan G, Belzacq AS, Haouzi D, Rouault A, Metivier D, Kroemer G, Brenner C. Propionibacteria induce apoptosis of colorectal carcinoma cells via short-chain fatty acids acting on mitochondria. Cell Death Differ 2002;9:179-88. (Pubitemid 34144777)
43. Tichomirowa M, Theodoropoulou M, Lohrer P, Schaaf L, Losa M, Uhl E, Lange M, Arzt E, Stalla GK, Renner U. Bacterial endotoxin (lipopolysaccharide) stimulates interleukin-6 production and inhibits growth of pituitary tumour cells expressing the toll-like receptor 4. J Neuroendocrinol 2005;17:152-60. (Pubitemid 40553014)
44. Muller-Decker K, Manegold G, Butz H, Hinz DE, Huttner D, Richter KH, Tremmel M, Weissflog R, Marks F. Inhibition of cell proliferation by bacterial lipopolysaccharides in TLR4-positive epithelial cells: independence of nitric oxide and cytokine release. J Invest Dermatol 2005;124:553-61. (Pubitemid 40381578)
45. Burdelya LG, Krivokrysenko VI, Tallant TC, Strom E, Gleiberman AS, Gupta D, Kurnasov OV, Fort FL, Osterman AL, Didonato JA, Feinstein E, Gudkov AV. An agonist of toll-like receptor 5 has radioprotective activity in mouse and primate models. Science 2008;320:226-30. (Pubitemid 351521417)
46. Slansky JE, Farnham PJ. Introduction to the E2F family: protein structure and gene regulation. Curr Top Microbiol Immunol 1996;208:1-30.
47. Helin K. Regulation of cell proliferation by the E2F transcription factors. Curr Opin Genet Dev 1998;8:28-35.
48. Cobrinik D. Regulatory interactions among E2Fs and cell cycle control proteins. Curr Top Microbiol Immunol 1996;208:31-61.
49. Hateboer G, Kerkhoven RM, Shvarts A, Bernards R, Beijersbergen RL. Degradation of E2F by the ubiquitin-proteasome pathway: regulation by retinoblastoma family proteins and adenovirus transforming proteins. Genes Dev 1996;10:2960-70.