Experimental therapy for colon cancer: Anti-cancer effects of TLR9 agonism, combination with other therapeutic modalities, and dependence upon p53

International Journal of Oncology

Volumn 30, Issue 6, 2007, Pages 1511-1519

  Rayburn, Elizabeth R ^a   Wang, Wei ^a   Zhang, Ruiwen ^a,b,c   Wang, Hui ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

Chemosensitization; Experimental therapy; Oligonucleotide; Radiosensitization

Indexed keywords

ANTINEOPLASTIC AGENT; OLIGONUCLEOTIDE; PROTEIN P53; TOLL LIKE RECEPTOR 9;

ANIMAL; APOPTOSIS; ARTICLE; BIOSYNTHESIS; CELL PROLIFERATION; COLON TUMOR; CPG ISLAND; DRUG EFFECT; DRUG POTENTIATION; FEMALE; HUMAN; METABOLISM; MOUSE; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; COLONIC NEOPLASMS; CPG ISLANDS; FEMALE; HUMANS; MICE; OLIGONUCLEOTIDES; TOLL-LIKE RECEPTOR 9; TUMOR SUPPRESSOR PROTEIN P53;

EID: 34447281533     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.30.6.1511     Document Type: Article

References (68)

1. American Cancer Society: Cancer Facts & Figures 2007. Atlanta, GA: American Cancer Society, 2007. Also available online: http://www.cancer.org/ docroot/STT/content/STT-1x-Cancer-Facts-Figures-2007/.asp
2. U.S. National Institutes of Health. http://www.clinicaltrials.gov/(2006) A service of the U.S. National Institutes of Health Developed by the National Library of Medicine.
3. Janeway CA Jr and Medzhitov R: Innate immune recognition. Annu Rev Immunol 20: 197-216, 2002.
4. Hemmi H, Takeuchi O, Kawai T, et al: A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745, 2000. (Pubitemid 32015992)
5. Pasare C and Medzhitov R: Toll-like receptors: linking innate and adaptive immunity. Adv Exp Med Biol 560: 11-18, 2005. (Pubitemid 43759170)
6. Sandor F and Buc M: Toll-like receptors. I. Structure, function and their ligands. Folia Biol 51: 148-157, 2005.
7. Fillatreau S and Manz RA: Tolls for B cells. Eur J Immunol 36: 798-801, 2006.
8. Kawai T and Akira S: TLR signaling. Cell Death Differ 13: 816-825, 2006.
9. Takeshita S, Gursel I, Ishii KJ, Suzuki K, Gursel M and Klinman DM: Signal transduction pathways mediated by the interaction of CpG DNA with Toll-like receptor 9. Semin Immunol 16: 17-22, 2004.
10. Barton GM, Kagan JC and Medzhitov R: Intracellular localization of Toll-like receptor 9 prevents recognition of self DNA but facilitates access to viral DNA. Nat Immunol 7: 49-56, 2006.
11. Pisetsky DS: Immune activation by bacterial DNA: a new genetic code. Immunity 5: 303-310, 1999.
12. Klinman DM, Yi AK, Beaucage SL, Conover J and Kreig AM: CpG motifs present in bacteria DNA rapidly induce lymphocytes to secrete interleukin 6, interleukin 12, and interferon gamma. Proc Natl Acad Sci USA 93: 2879-2883, 1996.
13. Agrawal S and Kandimalla ER: Modulation of Toll-like receptor 9 responses through synthetic immunostimulatory motifs of DNA. Ann NY Acad Sci 1002: 30-42, 2003. (Pubitemid 38253327)
14. Moore M, Lawrence N and Nisbet NW: Tumour inhibition mediated by BCG in immunosuppressed rats. Int J Cancer 15: 897-911, 1975.
15. Lin J, Lin E and Nemunaitis J: Bacteria in the treatment of cancer. Curr Opin Mol Ther 6: 629-639, 2004.
16. Carpentier AF, Auf G and Delattre JY: CpG-oligonucleotides for cancer immunotherapy: review of the literature and potential applications in malignant glioma. Front Biosci 8: e115-127, 2003. (Pubitemid 38918578)
17. Heckelsmiller K, Beck S, Rall K, et al: Combined dendritic cell- and CpG oligonucleotide-based immune therapy cures large murine tumors that resist chemotherapy. Eur J Immunol 32: 3235-3245, 2002.
18. Wang D, Li Y, Yu D, Song SS, Kandimalla ER and Agrawal S: Immunopharmacological and antitumor effects of second-generation immunomodulatory oligonucleotides containing synthetic CpR motifs. Int J Oncol 24: 901-908, 2004.
19. No Authors Listed (PMID 16922592): CpG 7909: PF 3512676, PF-3512676. Drugs R D. 7: 312-316, 2006.
20. Switaj T and Lasek W: Technology evaluation: HYB-2055, Hybridon. Curr Opin Mol Ther 7: 376-383, 2005.
21. www.clinicaltrials.gov
22. Agrawal S and Kandimalla ER: Role of Toll-like receptors in antisense and siRNA (corrected). Nat Biotechnol 22: 1533-1537, 2004. (Pubitemid 40039455)
23. Yu D, Kandimalla D, Bhagat L, Tang JY, Cong Y, Tang J and Agrawal S: Immunomers'-novel 3′-3′-linked CpG oligodeoxy-ribonucleotides as potent immunomodulatory agents. Nucleic Acids Res 30: 4460-4469, 2002.
24. Kandimalla ER, Bhagat L, Yu D, Cong Y, Tang J and Agrawal S: Conjugation of ligands at the 5′-end of CpG DNA affects immunostimulatory activity. Bioconjug Chem 13: 966-974, 2002.
25. Kandimalla ER, Bhagat L, Wang D, et al: Divergent synthetic nucleotide motif recognition pattern: design and development of potent immunomodulatory oligodeoxyribonucleotide agents with distinct cytokine induction profiles. Nucleic Acids Res 31: 2393-2400, 2003.
26. Kandimalla ER, Bhagat L, Zhu FG, et al: A dinucleotide motif in oligonucleotides shows potent immunomodulatory activity and overrides species-specific recognition observed with CpG motif. Proc Natl Acad Sci USA 100: 14303-14308, 2003.
27. Kandimalla ER, Bhagat L, Li Y, et al: Immunomodulatory oligonucleotides containing a cytosine-phosphate-2′-deoxy-7-deazaguanosine motif as potent toll-like receptor 9 agonists. Proc Natl Acad Sci USA 102: 6925-6930, 2005.
28. Damiano V, Caputo R, Bianco R, et al: Novel toll-like receptor 9 agonist induces epidermal growth factor receptor (EGFR) inhibition and synergistic antitumor activity with EGFR inhibitors. Clin Cancer Res 12: 577-583, 2006.
29. Lane DP: p53, guardian of the genome. Nature 358: 15-16, 1992.
30. Poyurovsky MV and Prives C: Unleashing the power of p53: lessons from mice and men. Genes Dev 20: 125-131, 2006.
31. Bartek J, Bartkova J, Vojtesek B, Staskova Z, Rejthar A, Kovarik J and Lane DP: Patterns of expression of the p53 tumour suppressor in human breast tissues and tumours in situ and in vitro. Int J Cancer 46: 839-844, 1990.
32. Wiman KG: Strategies for therapeutic targeting of the p53 pathway in cancer. Cell Death Differ 13: 921-926, 2006. (Pubitemid 43753482)
33. Munro AJ, Lain S and Lane DP: P53 abnormalities and outcomes in colorectal cancer: a systematic review. Br J Cancer 92: 434-444, 2005.
34. Wang H, Cai Q, Zeng X, Yu D, Agrawal S and Zhang R: Antitumor activity and pharmacokinetics of a mixed-backbone antisense oligonucleotide targeted to the RI alpha subunit of protein kinase A after oral administration. Proc Natl Acad Sci USA 96: 13989-13994, 1999.
35. Zhang Z, Li M, Wang H, Agrawal S and Zhang R: Antisense therapy targeting MDM2 oncogene in prostate cancer: effects on proliferation, apoptosis, multiple gene expression, and chemotherapy. Proc Natl Acad Sci USA 100: 11636-11641, 2003.
36. Wang H, Yu D, Agrawal S and Zhang R: Experimental therapy of human prostate cancer by inhibiting MDM2 expression with novel mixed-backbone antisense oligonucleotides: in vitro and in vivo activities and mechanisms. Prostate 54: 194-205, 2003. (Pubitemid 36120317)
37. Rayburn ER, Wang W, Zhang Z, Li M, Zhang R and Wang H: Experimental therapy of prostate cancer with an immunomodulatory oligonucleotide: effects on tumor growth, apoptosis, proliferation, and potentiation of chemotherapy. Prostate 66: 1653-1663, 2006.
38. Bauer S, Kirschning CJ, Hacker H, et al: Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc Natl Acad Sci USA 98: 9237-9242, 2001.
39. Oren M: Relationship of p53 to the control of apoptotic cell death. Semin Cancer Biol 5: 221-227, 1994. (Pubitemid 124006732)
40. Bristow RG, Benchimol S and Hill RP: The p53 gene as a modifier of intrinsic radiosensitivity: implications for radiotherapy. Radiother Oncol 40: 197-223, 1996.
41. Goyle S and Maraveyas A: Chemotherapy for colorectal cancer. Dig Surg 22: 401-414, 2005.
42. McWilliams RR and Erlichman C: Novel therapeutics in colorectal cancer. Dis Colon Rectum 48: 1632-1650, 2005.
43. Tokunaga T, Yamamoto H, Shimada S, et al: Antitumor activity of deoxyribonucleic acid fraction from Mycobacterium bovis BCG. I. Isolation, physicochemical characterization, and antitumor activity. J Natl Cancer Inst 72: 955-962, 1984.
44. Kataoka T, Yamamoto S, Yamamoto T, Kuramoto E, Kimura Y, Yano O and Tokunaga T: Antitumor activity of synthetic oligonucleotides with sequences from cDNA encoding proteins of Mycobacterium bovis BCG. Jpn J Cancer Res 83: 244-247, 1992.
45. Krieg AM, Yi AK and Hartmann G: Mechanisms and therapeutic applications of immune stimulatory CpG DNA. Pharmacol Ther 84: 113-120, 1999.
46. Zimmermann S, Egeter O, Hausmann S, Lipford GB, Rocken M, Wagner H and Heeg K: CpG oligodeoxynucleotides trigger protective and curative Th1 responses in lethal murine leishmaniasis. J Immunol 160: 3627-3630, 1998.
47. Wang H, Rayburn E and Zhang R: Synthetic oligodeoxynucleotides containing deoxycytidyl-deoxyguanosine dinucleotides (CpG ODNs) and modified analogs as novel anticancer therapeutics. Curr Pharm Des 11: 2889-2907, 2005. (Pubitemid 41051873)
48. Dittmer U and Olbrich AR: Treatment of infectious diseases with immunostimulatory oligodeoxynucleotides containing CpG motifs. Curr Opin Microbiol 6: 472-477, 2003.
49. Racila DM and Kline JN: Perspectives in asthma: molecular use of microbial products in asthma prevention and treatment. J Allergy Clin Immunol 116: 1202-1205, 2005.
50. Wooldridge JE and Weiner GJ: CpG DNA and cancer immunotherapy: orchestrating the antitumor immune response. Curr Opin Oncol 15: 440-445, 2003.
51. Ulevitch RJ: Therapeutics targeting the innate immune system. Nat Rev Immunol 4: 512-520, 2004. (Pubitemid 38931766)
52. Lain S and Lane D: Improving cancer therapy by non-genotoxic activation of p53. Eur J Cancer 39: 1053-1060, 2003.
53. Gartel AL, Serfas MS and Tyner AL: p21-negative regulator of the cell cycle. Proc Soc Exp Biol Med 213: 138-149, 1996.
54. Pratesi G, Petrangolini G, Tortoreto M, et al: Therapeutic synergism of gemcitabine and CpG-oligodeoxynucleotides in an orthotopic human pancreatic carcinoma xenograft. Cancer Res 65: 6388-6393, 2005.
55. Li Y, Kandimalla ER, Yu D and Agrawal S: Oligodeoxynucleotides containing synthetic immunostimulatory motifs augment potent Th1 immune responses to HBsAg in mice. Int Immunopharmacol 5: 981-991, 2005. (Pubitemid 40501743)
56. Sparwasser T, Vabulas RM, Villmow B, Lipford GB and Wagner H: Bacterial CpG-DNA activates dendritic cells in vivo: T helper cell-independent cytotoxic T cell responses to soluble proteins. Eur J Immunol 30: 3591-3597, 2000.
57. Buhtoiarov IN, Lum HD, Berke G, Sondel PM and Rakhmilevich AL: Synergistic activation of macrophages via CD40 and TLR9 results in T cell independent antitumor effects. J Immunol 176: 309-318, 2006.
58. Pedersen G, Andresen L, Matthiessen MW, Rask-Madsen J and Brynskov J: Expression of Toll-like receptor 9 and response to bacterial CpG oligodeoxynucleotides in human intestinal epithelium. Clin Exp Immunol 141: 298-306, 2005.
59. Droemann D, Albrecht D, Gerdes J, et al: Human lung cancer cells express functionally active Toll-like receptor 9. Respir Res 6: 1, 2005.
60. Brunner C, Seiderer J, Schlamp A, et al: Enhanced dendritic cell maturation by TNF-alpha or cytidine-phosphate-guanosine DNA drives T cell activation in vitro and therapeutic anti-tumor immune responses in vivo. J Immunol 165: 6278-6286, 2000.
61. Okano F, Merad M, Furumoto K and Engleman EG: In vivo manipulation of dendritic cells overcomes tolerance to unmodified tumor-associated self antigens and induces potent antitumor immunity. J Immunol 174: 2645-2652, 2005.
62. Bourquin C, Schreiber S, Beck S, Hartmann G and Endres S: Immunotherapy with dendritic cells and CpG oligonucleotides can be combined with chemotherapy without loss of efficacy in a mouse model of colon cancer. Int J Cancer 118: 2790-2795, 2006. (Pubitemid 43673358)
63. Saha A, Baral RN, Chatterjee SK, et al: CpG oligonucleotides enhance the tumor antigen-specific immune response of an anti-idiotype antibody-based vaccine strategy in CEA transgenic mice. Cancer Immunol Immunother 55: 515-527, 2006.
64. Daftarian P, Song GY, Ali S, Faynsod M, Longmate J, Diamond DJ and Ellenhorn JD: Two distinct pathways of immuno-modulation improve potency of p53 immunization in rejecting established tumors. Cancer Res 64: 5407-5414, 2004.
65. Heckelsmiller K, Rall K, Beck S, et al: Peritumoral CpG DNA elicits a coordinated response of CD8 T cells and innate effectors to cure established tumors in a murine colon carcinoma model. J Immunol 169: 3892-3899, 2002.
66. Sharma S, Karakousis CP, Takita H, Shin K and Brooks SP: Intra-tumoral injection of CpG results in the inhibition of tumor growth in murine Colon-26 and B-16 tumors. Biotechnol Lett 25: 149-153, 2003.
67. Sharma S, Karakousis CP, Takita H, Shin K and Brooks SP: Cytokines and chemokines are expressed at different levels in small and large murine colon-26 tumors following intratumoral injections of CpG ODN. Neoplasia 6: 523-528, 2004.
68. Balsari A, Tortoreto M, Besusso D, et al: Combination of a CpG-oligodeoxynucleotide and a topoisomerase I inhibitor in the therapy of human tumour xenografts. Eur J Cancer 40: 1275-1281, 2004.