Nasal acai polysaccharides potentiate innate immunity to protect against pulmonary Francisella tularensis and Burkholderia pseudomallei infections

PLoS Pathogens

Volumn 8, Issue 3, 2012, Pages

  Skyberg, Jerod A ^a   Rollins, MaryClare F ^a   Holderness, Jeff S ^a   Marlenee, Nicole L ^b   Schepetkin, Igor A ^a   Goodyear, Andrew ^b   Dow, Steven W ^b   Jutila, Mark A ^a   Pascual, David W ^a  

^a MONTANA STATE UNIVERSITY   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACAI BERRY POLYSACCHARIDE; GAMMA INTERFERON; PLANT EXTRACT; UNCLASSIFIED DRUG; POLYSACCHARIDE;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL TRANSMISSION; BERRY; BURKHOLDERIA PSEUDOMALLEI; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENCY; FEMALE; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; IN VITRO STUDY; INFECTION PREVENTION; INNATE IMMUNITY; LUNG INFECTION; LYMPHOCYTE CULTURE; MACROPHAGE; MELIOIDOSIS; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; SURVIVAL RATE; TULAREMIA; ANIMAL; ARECACEAE; BAGG ALBINO MOUSE; C57BL MOUSE; CHEMISTRY; DISEASE MODEL; FRANCISELLA TULARENSIS; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION; ISOLATION AND PURIFICATION; LONGEVITY; LUNG; METABOLISM; MICROBIOLOGY; PNEUMONIA;

BACTERIA (MICROORGANISMS); BURKHOLDERIA PSEUDOMALLEI; FRANCISELLA; FRANCISELLA TULARENSIS; MUS;

ADMINISTRATION, INTRANASAL; ANIMALS; ARECACEAE; BURKHOLDERIA PSEUDOMALLEI; DISEASE MODELS, ANIMAL; FEMALE; FRANCISELLA TULARENSIS; IMMUNITY, INNATE; INTERFERON-GAMMA; KILLER CELLS, NATURAL; LONGEVITY; LUNG; MACROPHAGES; MELIOIDOSIS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PLANT EXTRACTS; PNEUMONIA; POLYSACCHARIDES; TULAREMIA;

EID: 84861211085     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002587     Document Type: Article

References (65)

1. Hong KJ, Wickstrum JR, Yeh HW, Parmely MJ, (2007) Toll-like receptor 2 controls the gamma interferon response to Francisella tularensis by mouse liver lymphocytes. Infect Immun 75: 5338-5345.
2. Oyston PC, (2008) Francisella tularensis: unravelling the secrets of an intracellular pathogen. J Med Microbiol 57: 921-930.
3. Kirimanjeswara GS, Olmos S, Bakshi CS, Metzger DW, (2008) Humoral and cell-mediated immunity to the intracellular pathogen Francisella tularensis. Immunol Rev 225: 244-255.
4. Allen LA, McCaffrey RL, (2007) To activate or not to activate: distinct strategies used by Helicobacter pylori and Francisella tularensis to modulate the NADPH oxidase and survive in human neutrophils. Immunol Rev 219: 103-117.
5. Dennis DT, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, et al. (2001) Tularemia as a biological weapon: medical and public health management. JAMA 285: 2763-2773.
6. Troyer RM, Propst KL, Fairman J, Bosio CM, Dow SW, (2009) Mucosal immunotherapy for protection from pneumonic infection with Francisella tularensis. Vaccine 27: 4424-4433.
7. Peacock SJ, (2006) Melioidosis. Curr Opin Infect Dis 19: 421-428.
8. Estes DM, Dow SW, Schweizer HP, Torres AG, (2010) Present and future therapeutic strategies for melioidosis and glanders. Expert Rev Anti Infect Ther 8: 325-338.
9. Koponen MA, Zlock D, Palmer DL, Merlin TL, (1991) Melioidosis. Forgotten, but not gone! Arch Intern Med 151: 605-608.
10. Chaowagul W, (1996) Melioidosis; a treatment challenge. Scand J Infect Dis Suppl 101: 14-16.
11. Goodyear A, Kellihan L, Bielefeldt-Ohmann H, Troyer R, Propst K, Dow S, (2009) Protection from pneumonic infection with Burkholderia species by inhalational immunotherapy. Infect Immun 77: 1579-1588.
12. Lubick K, Radke M, Jutila M, (2007) Securinine, a GABAA receptor antagonist, enhances macrophage clearance of phase II C. burnetii: comparison with TLR agonists. J Leukoc Biol 82: 1062-1069.
13. Hammerbeck DM, Burleson GR, Schuller CJ, Vasilakos JP, Tomai M, et al. (2007) Administration of a dual toll-like receptor 7 and toll-like receptor 8 agonist protects against influenza in rats. Antiviral Res 73: 1-11.
14. Ireland R, Olivares-Zavaleta N, Warawa JM, Gherardini FC, Jarrett C, et al. (2010) Effective, broad spectrum control of virulent bacterial infections using cationic DNA liposome complexes combined with bacterial antigens. PLoS Pathog 6: e1000921.
15. Graff JC, Kimmel EM, Freedman B, Schepetkin IA, Holderness J, et al. (2009) Polysaccharides derived from Yamoa (Funtumia elastica) prime γδ T cells in vitro and enhance innate immune responses in vivo. Int Immunopharmacol 9: 1313-1322.
16. Graff JC, Jutila MA, (2007) Differential regulation of CD11b on γδ T cells and monocytes in response to unripe apple polyphenols. J Leukoc Biol 82: 603-607.
17. Holderness J, Jackiw L, Kimmel E, Kerns H, Radke M, et al. (2007) Select plant tannins induce IL-2Rα up-regulation and augment cell division in γδ T cells. J Immunol 179: 6468-6478.
18. Tohyama M, Kawakami K, Saito A, (1996) Anticryptococcal effect of amphotericin B is mediated through macrophage production of nitric oxide. Antimicrob Agents Chemother 40: 1919-1923.
19. Holderness J, Schepetkin IA, Freedman B, Kirpotina LN, Quinn MT, et al. (2011) Polysaccharides isolated from Acai fruit induce innate immune responses. PLoS ONE 6: e17301.
20. Yang X, Becker T, Walters N, Pascual DW, (2006) Deletion of znuA virulence factor attenuates Brucella abortus and confers protection against wild-type challenge. Infect Immun 74: 3874-3879.
21. Skyberg JA, Robison A, Golden S, Rollins MF, Callis G, et al. (2011) Apple polyphenols require T cells to ameliorate dextran sulfate sodium-induced colitis and dampen proinflammatory cytokine expression. J Leukoc Biol 90: 1043-1054.
22. Pascual DW, Pascual VH, Bost KL, McGhee JR, Oparil S, (1993) Nitric oxide mediates immune dysfunction in the spontaneously hypertensive rat. Hypertension 21: 185-194.
23. Jones JW, Kayagaki N, Broz P, Henry T, Newton K, et al. (2010) Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc Natl Acad Sci U S A 107: 9771-9776.
24. Bauler TJ, Chase JC, Bosio CM, (2011) IFN-β mediates suppression of IL-12p40 in human dendritic cells following infection with virulent Francisella tularensis. J Immunol 187: 1845-1855.
25. Duckett NS, Olmos S, Durrant DM, Metzger DW, (2005) Intranasal interleukin-12 treatment for protection against respiratory infection with the Francisella tularensis live vaccine strain. Infect Immun 73: 2306-2311.
26. Propst KL, Troyer RM, Kellihan LM, Schweizer HP, Dow SW, (2010) Immunotherapy markedly increases the effectiveness of antimicrobial therapy for treatment of Burkholderia pseudomallei infection. Antimicrob Agents Chemother 54: 1785-1792.
27. Morici LA, Heang J, Tate T, Didier PJ, Roy CJ, (2010) Differential susceptibility of inbred mouse strains to Burkholderia thailandensis aerosol infection. Microb Pathog 48: 9-17.
28. Goodyear A, Jones A, Troyer R, Bielefeldt-Ohmann H, Dow S, (2010) Critical protective role for MCP-1 in pneumonic Burkholderia mallei infection. J Immunol 184: 1445-1454.
29. Lembo A, Pelletier M, Iyer R, Timko M, Dudda JC, et al. (2008) Administration of a synthetic TLR4 agonist protects mice from pneumonic tularemia. J Immunol 180: 7574-7581.
30. Sun X, Seeberger J, Alberico T, Wang C, Wheeler CT, et al. (2010) Acai palm fruit (Euterpe oleracea Mart.) pulp improves survival of flies on a high fat diet. Exp Gerontol 45: 243-251.
31. Sabbe S, Verbeke W, Deliza R, Matta V, Van Damme P, (2009) Effect of a health claim and personal characteristics on consumer acceptance of fruit juices with different concentrations of acai (Euterpe oleracea Mart). Appetite 53: 84-92.
32. Pacheco-Palencia LA, Talcott ST, Safe S, Mertens-Talcott S, (2008) Absorption and biological activity of phytochemical-rich extracts from acai (Euterpe oleracea Mart.) pulp and oil in vitro. J Agric Food Chem 56: 3593-3600.
33. Schauss AG, Wu X, Prior RL, Ou B, Huang D, et al. (2006) Antioxidant capacity and other bioactivities of the freeze-dried Amazonian palm berry, Euterpe oleraceae mart. (acai). J Agric Food Chem 54: 8604-8610.
34. Schauss AG, Wu X, Prior RL, Ou B, Patel D, et al. (2006) Phytochemical and nutrient composition of the freeze-dried amazonian palm berry, Euterpe oleraceae mart. (acai). J Agric Food Chem 54: 8598-8603.
35. Oliveira dS, Silva M, Silva ME, de Paula OR, Pedrosa ML, (2009) Diet supplementation with acai (Euterpe oleracea Mart.) pulp improves biomarkers of oxidative stress and the serum lipid profile in rats. Nutrition 26: 804-810.
36. Spada PD, Dani C, Bortolini GV, Funchal C, Henriques JA, et al. (2009) Frozen fruit pulp of Euterpe oleraceae Mart. (Acai) prevents hydrogen peroxide-induced damage in the cerebral cortex, cerebellum, and hippocampus of rats. J Med Food 12: 1084-1088.
37. Pacheco-Palencia LA, Mertens-Talcott S, Talcott ST, (2008) Chemical composition, antioxidant properties, and thermal stability of a phytochemical enriched oil from Acai (Euterpe oleracea Mart). J Agric Food Chem 56: 4631-4636.
38. Chin YW, Chai HB, Keller WJ, Kinghorn AD, (2008) Lignans and other constituents of the fruits of Euterpe oleracea (Acai) with antioxidant and cytoprotective activities. J Agric Food Chem 56: 7759-7764.
39. Shuto T, Kato K, Mori Y, Viriyakosol S, Oba M, et al. (2005) Membrane-anchored CD14 is required for LPS-induced TLR4 endocytosis in TLR4/MD-2/CD14 overexpressing CHO cells. Biochem Biophys Res Commun 338: 1402-1409.
40. Fitzgerald KA, Rowe DC, Barnes BJ, Caffrey DR, Visintin A, et al. (2003) LPS-TLR4 signaling to IRF-3/7 and NF-κB involves the toll adapters TRAM and TRIF. J Exp Med 198: 1043-1055.
41. Schneemann M, Schoedon G, Hofer S, Blau N, Guerrero L, et al. (1993) Nitric oxide synthase is not a constituent of the antimicrobial armature of human mononuclear phagocytes. J Infect Dis 167: 1358-1363.
42. Elkins KL, Colombini SM, Krieg AM, De Pascalis R, (2009) NK cells activated in vivo by bacterial DNA control the intracellular growth of Francisella tularensis LVS. Microbes Infect 11: 49-56.
43. Elkins KL, Cowley SC, Bosio CM, (2007) Innate and adaptive immunity to Francisella. Ann N Y Acad Sci 1105: 284-324.
44. Lopez MC, Duckett NS, Baron SD, Metzger DW, (2004) Early activation of NK cells after lung infection with the intracellular bacterium, Francisella tularensis LVS. Cell Immunol 232: 75-85.
45. Edwards JA, Rockx-Brouwer D, Nair V, Celli J, (2010) Restricted cytosolic growth of Francisella tularensis subsp. tularensis by IFN-γ activation of macrophages. Microbiology 156: 327-339.
46. Dornand J, Lafont V, Oliaro J, Terraza A, Castaneda-Roldan E, et al. (2004) Impairment of intramacrophagic Brucella suis multiplication by human natural killer cells through a contact-dependent mechanism. Infect Immun 72: 2303-2311.
47. Kingry LC, Troyer RM, Marlenee NL, Bielefeldt-Ohmann H, Bowen RA, et al. (2011) Genetic identification of unique immunological responses in mice infected with virulent and attenuated Francisella tularensis. Microbes Infect 13: 261-275.
48. Elkins KL, Cowley SC, Bosio CM, (2003) Innate and adaptive immune responses to an intracellular bacterium, Francisella tularensis live vaccine strain. Microbes Infect 5: 135-142.
49. Crane DD, Warner SL, Bosio CM, (2009) A novel role for plasmin-mediated degradation of opsonizing antibody in the evasion of host immunity by virulent, but not attenuated, Francisella tularensis. J Immunol 183: 4593-4600.
50. Rozak DA, Gelhaus HC, Smith M, Zadeh M, Huzella L, et al. (2010) CpG oligodeoxyribonucleotides protect mice from Burkholderia pseudomallei but not Francisella tularensis Schu S4 aerosols. J Immune Based Ther Vaccines 8: 2.
51. Cole LE, Mann BJ, Shirey KA, Richard K, Yang Y, et al. (2011) Role of TLR signaling in Francisella tularensis-LPS-induced, antibody-mediated protection against Francisella tularensis challenge. J Leukoc Biol 90: 787-797.
52. Nochi T, Takagi H, Yuki Y, Yang L, Masumura T, et al. (2007) Rice-based mucosal vaccine as a global strategy for cold-chain- and needle-free vaccination. Proc Natl Acad Sci U S A 104: 10986-10991.
53. Bosio CM, Bielefeldt-Ohmann H, Belisle JT, (2007) Active suppression of the pulmonary immune response by Francisella tularensis Schu4. J Immunol 178: 4538-4547.
54. Schepetkin IA, Quinn MT, (2011) Immunomodulatory effects of botanical polysaccharides. In: Popa V, editors. Polysaccharides in medicinal and pharmaceutical applications Shawbury, U.K. Smithers pp. 211-264.
55. Skyberg JA, Thornburg T, Rollins M, Huarte E, Jutila MA, Pascual DW, (2011) Murine and Bovine γδ T Cells Enhance Innate Immunity against Brucella abortus Infections. PLoS ONE 6: e21978.
56. Hamada S, Umemura M, Shiono T, Tanaka K, Yahagi A, et al. (2008) IL-17A produced by γδ T cells plays a critical role in innate immunity against Listeria monocytogenes infection in the liver. J Immunol 181: 3456-3463.
57. Bosio CM, Dow SW, (2005) Francisella tularensis induces aberrant activation of pulmonary dendritic cells. J Immunol 175: 6792-6801.
58. Ochoa-Reparaz J, Sentissi J, Trunkle T, Riccardi C, Pascual DW, (2007) Attenuated Coxiella burnetii phase II causes a febrile response in gamma interferon knockout and Toll-like receptor 2 knockout mice and protects against reinfection. Infect Immun 75: 5845-5858.
59. Pascual DW, Trunkle T, Sura J, (2002) Fimbriated Salmonella enterica serovar typhimurium abates initial inflammatory responses by macrophages. Infect Immun 70: 4273-4281.
60. Popov A, Abdullah Z, Wickenhauser C, Saric T, Driesen J, et al. (2006) Indoleamine 2,3-dioxygenase-expressing dendritic cells form suppurative granulomas following Listeria monocytogenes infection. J Clin Invest 116: 3160-3170.
61. England K, am EC, Lu H, Sullivan TJ, Marlenee NL, et al. (2009) Substituted diphenyl ethers as a broad-spectrum platform for the development of chemotherapeutics for the treatment of tularaemia. J Antimicrob Chemother 64: 1052-1061.
62. Feng CG, Kaviratne M, Rothfuchs AG, Cheever A, Hieny S, et al. (2006) NK cell-derived IFN-γ differentially regulates innate resistance and neutrophil response in T cell-deficient hosts infected with Mycobacterium tuberculosis. J Immunol 177: 7086-7093.
63. Okamoto M, Kato S, Oizumi K, Kinoshita M, Inoue Y, et al. (2002) Interleukin 18 (IL-18) in synergy with IL-2 induces lethal lung injury in mice: a potential role for cytokines, chemokines, and natural killer cells in the pathogenesis of interstitial pneumonia. Blood 99: 1289-1298.
64. Ochoa-Reparaz J, Riccardi C, Rynda A, Jun S, Callis G, et al. (2007) Regulatory T cell vaccination without autoantigen protects against experimental autoimmune encephalomyelitis. J Immunol 178: 1791-1799.
65. Pascual DW, White MD, Larson T, Walters N, (2001) Impaired mucosal immunity in L-selectin-deficient mice orally immunized with a Salmonella vaccine vector. J Immunol 167: 407-415.