Central role of liver in anticancer and radioprotective activities of Toll-like receptor 5 agonist

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 20, 2013, Pages

  Burdelya, Lyudmila G ^a,b   Brackett, Craig M ^a   Kojouharov, Bojidar ^a   Gitlin, Ilya I ^a   Leonova, Katerina I ^a   Gleiberman, Anatoli S ^b   Aygun Sunar, Semra ^a   Veith, Jean ^a   Johnson, Christopher ^a   Haderski, Gary J ^b   Stanhope Baker, Patricia ^b   Allamaneni, Shyam ^a   Skitzki, Joseph ^a   Zeng, Ming ^c   Martsen, Elena ^c   Medvedev, Alexander ^c   Scheblyakov, Dmitry ^d   Artemicheva, Nataliya M ^d   Logunov, Denis Y ^d   Gintsburg, Alexander L ^d   Naroditsky, Boris S ^d   Makarov, Sergei S ^c   Gudkov, Andrei V ^a,b   more..

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b CLEVELAND BIOLABS INC   (United States)

^c Attagene Inc   (United States)

^d GAMALEYA RESEARCH INSTITUTE OF EPIDEMIOLOGY AND MICROBIOLOGY   (Russian Federation)

Author keywords

Breast cancer; Colon cancer; Natural killer cells; Neutrophils; Salmonella

Indexed keywords

ENTOLIMOD; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; STAT3 PROTEIN; TOLL LIKE RECEPTOR 5; TRANSCRIPTION FACTOR AP 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; FEMALE; IMMUNOCOMPETENT CELL; LIVER; LIVER CELL; LIVER METASTASIS; METASTASIS INHIBITION; MICROENVIRONMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; RADIATION PROTECTION;

BREAST CANCER; COLON CANCER; NATURAL KILLER CELLS; NEUTROPHILS; SALMONELLA;

ANIMALS; ANTICARCINOGENIC AGENTS; ANTIGENS, CD95; BREAST NEOPLASMS; CELL LINE, TUMOR; COLONIC NEOPLASMS; FEMALE; FLOW CYTOMETRY; HEPATOCYTES; HUMANS; KILLER CELLS, NATURAL; LIVER; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOPLASM TRANSPLANTATION; NEUTROPHILS; NF-KAPPA B; PEPTIDES; RADIATION-PROTECTIVE AGENTS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTOR 5;

EID: 84877867769     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1222805110     Document Type: Article

References (59)

1. Takeda K, Kaisho T, Akira S (2003) Toll-like receptors. Annu Rev Immunol 21:335-376. (Pubitemid 37174535)
2. Curigliano G, et al. (2007) Vaccine immunotherapy in breast cancer treatment: Promising, but still early. Expert Rev Anticancer Ther 7(9):1225-1241. (Pubitemid 47521019)
3. Waterston AM, Cassidy J (2005) Adjuvant treatment strategies for early colon cancer. Drugs 65(14):1935-1947. (Pubitemid 41324056)
4. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R (2004) Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118(2):229-241. (Pubitemid 38962578)
5. Jiménez-Baranda S, Silva IP, Bhardwaj N (2012) Plasmacytoid dendritic cells lead the charge against tumors. J Clin Invest 122(2):481-484.
6. Gilmore TD, Wolenski FS (2012) NF-κB: Where did it come from and why? Immunol Rev 246(1):14-35.
7. Hayden MS, Ghosh S (2011) NF-κB in immunobiology. Cell Res 21(2):223-244.
8. Burdelya LG, et al. (2008) An agonist of toll-like receptor 5 has radioprotective activity in mouse and primate models. Science 320(5873):226-230. (Pubitemid 351521417)
9. Burdelya LG, et al. (2012) Toll-like receptor 5 agonist protects mice from dermatitis and oral mucositis caused by local radiation: Implications for head-and-neck cancer radiotherapy. Int J Radiat Oncol Biol Phys 83(1):228-234.
10. Fukuzawa N, Petro M, Baldwin WM, 3rd, Gudkov AV, Fairchild RL (2011) A TLR5 agonist inhibits acute renal ischemic failure. J Immunol 187(7):3831-3839.
11. Soto LJ, 3rd, et al. (2003) Attenuated Salmonella typhimurium prevents the establishment of unresectable hepatic metastases and improves survival in a murine model. J Pediatr Surg 38(7):1075-1079. (Pubitemid 36828879)
12. Yam C, et al. (2010) Monotherapy with a tumor-targeting mutant of S. typhimurium inhibits liver metastasis in a mouse model of pancreatic cancer. J Surg Res 164(2): 248-255.
13. Cai Z, et al. (2011) Activation of Toll-like receptor 5 on breast cancer cells by flagellin suppresses cell proliferation and tumor growth. Cancer Res 71(7):2466-2475.
14. Rhee SH, Im E, Pothoulakis C (2008) Toll-like receptor 5 engagement modulates tumor development and growth in a mouse xenograft model of human colon cancer. Gastroenterology 135(2):518-528.
15. Akira S, Takeda K (2004) Functions of toll-like receptors: Lessons from KO mice. C R Biol 327(6):581-589. (Pubitemid 38979508)
16. Carvalho FA, Aitken JD, Gewirtz AT, Vijay-Kumar M (2011) TLR5 activation induces secretory interleukin-1 receptor antagonist (sIL-1Ra) and reduces inflammasomeassociated tissue damage. Mucosal Immunol 4(1):102-111.
17. Vijay-Kumar M, et al. (2008) Toll-like receptor 5-deficient mice have dysregulated intestinal gene expression and nonspecific resistance to Salmonella-induced typhoidlike disease. Infect Immun 76(3):1276-1281. (Pubitemid 351428091)
18. Romanov S, et al. (2008) Homogeneous reporter system enables quantitative functional assessment of multiple transcription factors. Nat Methods 5(3):253-260. (Pubitemid 351325650)
19. Tallant T, et al. (2004) Flagellin acting via TLR5 is the major activator of key signaling pathways leading to NF-kappa B and proinflammatory gene program activation in intestinal epithelial cells. BMC Microbiol 4:33.
20. Zhang G, Budker V, Wolff JA (1999) High levels of foreign gene expression in hepatocytes after tail vein injections of naked plasmid DNA. Hum Gene Ther 10(10): 1735-1737. (Pubitemid 29328217)
21. Yu H, Pardoll D, Jove R (2009) STATs in cancer inflammation and immunity: A leading role for STAT3. Nat Rev Cancer 9(11):798-809.
22. Lise M, Mocellin S, Pilati P, Nitti D (2005) Colorectal liver metastasis: Towards the integration of conventional and molecularly targeted therapeutic approaches. Front Biosci 10:3042-3057. (Pubitemid 40910543)
23. Pulaski BA, Ostrand-Rosenberg S (1998) Reduction of established spontaneous mammary carcinoma metastases following immunotherapy with major histocompatibility complex class II and B7.1 cell-based tumor vaccines. Cancer Res 58(7):1486-1493. (Pubitemid 28193612)
24. Kasai M, et al. (1981) In vivo effect of anti-asialo GM1 antibody on natural killer activity. Nature 291(5813):334-335. (Pubitemid 11083436)
25. Berke G (1995) The CTL's kiss of death. Cell 81(1):9-12.
26. Smyth MJ, et al. (2005) Activation of NK cell cytotoxicity. Mol Immunol 42(4):501-510. (Pubitemid 39655961)
27. Malhi H, Gores GJ, Lemasters JJ (2006) Apoptosis and necrosis in the liver: A tale of two deaths? Hepatology 43(2 Suppl 1):S31-S44.
28. Galle PR, et al. (1995) Involvement of the CD95 (APO-1/Fas) receptor and ligand in liver damage. J Exp Med 182(5):1223-1230.
29. Yin XM, Ding WX (2003) Death receptor activation-induced hepatocyte apoptosis and liver injury. Curr Mol Med 3(6):491-508.
30. Ogasawara J, et al. (1993) Lethal effect of the anti-Fas antibody in mice. Nature 364(6440):806-809. (Pubitemid 23261761)
31. Nishimura M, Naito S (2005) Tissue-specific mRNA expression profiles of human tolllike receptors and related genes. Biol Pharm Bull 28(5):886-892. (Pubitemid 40740661)
32. Ozer J, Ratner M, Shaw M, Bailey W, Schomaker S (2008) The current state of serum biomarkers of hepatotoxicity. Toxicology 245(3):194-205.
33. Barnhart BC, Alappat EC, Peter ME (2003) The CD95 type I/type II model. Semin Immunol 15(3):185-193. (Pubitemid 38155825)
34. Lacronique V, et al. (1996) Bcl-2 protects from lethal hepatic apoptosis induced by an anti-Fas antibody in mice. Nat Med 2(1):80-86. (Pubitemid 26028076)
35. Taub R (2003) Hepatoprotection via the IL-6/Stat3 pathway. J Clin Invest 112(7): 978-980. (Pubitemid 38056310)
36. Xu HR, Hsu HS (1992) Dissemination and proliferation of Salmonella typhimurium in genetically resistant and susceptible mice. J Med Microbiol 36(6):377-381.
37. Shimizu H, et al. (2002) Toll-like receptor 2 contributes to liver injury by Salmonella infection through Fas ligand expression on NKT cells in mice. Gastroenterology 123(4):1265-1277.
38. Zbell AL, Maier SE, Maier RJ (2008) Salmonella enterica serovar Typhimurium NiFe uptake-type hydrogenases are differentially expressed in vivo. Infect Immun 76(10): 4445-4454.
39. Uematsu S, et al. (2006) Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat Immunol 7(8):868-874. (Pubitemid 44084094)
40. Beutler B, Milsark IW, Cerami AC (1985) Passive immunization against cachectin/ tumor necrosis factor protects mice from lethal effect of endotoxin. Science, 1985, 229(4716):869-871. Classical article. J Immunol 181(1):7-9.
41. Dinarello CA, Orencole SF, Savage N (1989) Interleukin-1 induced T-lymphocyte proliferation and its relation to IL-1 receptors. Adv Exp Med Biol 254:45-53.
42. Le J, Vilcek J (1987) Tumor necrosis factor and interleukin 1: Cytokines with multiple overlapping biological activities. Lab Invest 56(3):234-248. (Pubitemid 17065343)
43. Takeda K, et al. (2005) TRAIL identifies immature natural killer cells in newborn mice and adult mouse liver. Blood 105(5):2082-2089. (Pubitemid 40731795)
44. Terunuma H, Deng X, Dewan Z, Fujimoto S, Yamamoto N (2008) Potential role of NK cells in the induction of immune responses: Implications for NK cell-based immunotherapy for cancers and viral infections. Int Rev Immunol 27(3):93-110. (Pubitemid 351589824)
45. Jaeger BN, et al. (2012) Neutrophil depletion impairs natural killer cell maturation, function, and homeostasis. J Exp Med 209(3):565-580.
46. Karin M, Greten FR (2005) NF-kappaB: Linking inflammation and immunity to cancer development and progression. Nat Rev Immunol 5(10):749-759. (Pubitemid 41400849)
47. Takeda K, et al. (1998) Stat3 activation is responsible for IL-6-dependent T cell proliferation through preventing apoptosis: Generation and characterization of T cell-specific Stat3-deficient mice. J Immunol 161(9):4652-4660. (Pubitemid 28492039)
48. Turkson J, Jove R (2000) STAT proteins: Novel molecular targets for cancer drug discovery. Oncogene 19(56):6613-6626. (Pubitemid 32197700)
49. Trierweiler C, Blum HE, Hasselblatt P (2012) The transcription factor c-Jun protects against liver damage following activated β-Catenin signaling. PLoS ONE 7(7):e40638.
50. Gnerre C, et al. (2005) LXR deficiency and cholesterol feeding affect the expression and phenobarbital-mediated induction of cytochromes P450 in mouse liver. J Lipid Res 46(8):1633-1642. (Pubitemid 41099330)
51. Patchen ML, Fischer R, MacVittie TJ (1993) Effects of combined administration of interleukin-6 and granulocyte colony-stimulating factor on recovery from radiationinduced hemopoietic aplasia. Exp Hematol 21(2):338-344. (Pubitemid 24216777)
52. MacVittie TJ, et al. (1991) Cytokine therapy in canine and primate models of radiation-induced marrow aplasia. Behring Inst Mitt (90):1-13.
53. Patchen ML, MacVittie TJ, Solberg BD, Souza LM (1990) Survival enhancement and hemopoietic regeneration following radiation exposure: Therapeutic approach using glucan and granulocyte colony-stimulating factor. Exp Hematol 18(9):1042-1048.
54. Zhu H, Itoh K, YamamotoM, Zweier JL, Li Y (2005) Role of Nrf2 signaling in regulation of antioxidants and phase 2 enzymes in cardiac fibroblasts: Protection against reactive oxygen and nitrogen species-induced cell injury. FEBS Lett 579(14): 3029-3036. (Pubitemid 40797830)
55. Krivokrysenko VI, et al. (2012) Identification of granulocyte colony-stimulating factor and interleukin-6 as candidate biomarkers of CBLB502 efficacy as a medical radiation countermeasure. J Pharmacol Exp Ther 343(2):497-508.
56. Gleiberman AS, Sharovskaya YuYu, Chailakhjan LM (1989) "Contact inhibition" of alpha-fetoprotein synthesis and junctional communication in adult mouse hepatocyte culture. Exp Cell Res 184(1):228-234. (Pubitemid 19233402)
57. Fougère-Deschatrette C, et al. (2006) Plasticity of hepatic cell differentiation: Bipotential adult mouse liver clonal cell lines competent to differentiate in vitro and in vivo. Stem Cells 24(9):2098-2109. (Pubitemid 44477135)
58. Klein I, et al. (2007) Kupffer cell heterogeneity: Functional properties of bone marrow derived and sessile hepatic macrophages. Blood 110(12):4077-4085. (Pubitemid 350248465)
59. Abe Y, et al. (2009) Mouse model of liver ischemia and reperfusion injury: Method for studying reactive oxygen and nitrogen metabolites in vivo. Free Radic Biol Med 46(1):1-7.