In vitro effects of anthocyanidins on sinonasal epithelial nitric oxide production and bacterial physiology

American Journal of Rhinology and Allergy

Volumn 30, Issue 4, 2016, Pages 261-268

  Hariri, Benjamin M ^a   Payne, Sakeena J ^b   Chen, Bei ^a   Mansfield, Corrine ^c   Doghramji, Laurel J ^a   Adappa, Nithin D ^a   Palmer, James N ^a   Kennedy, David W ^a   Niv, Masha Y ^d   Lee, Robert J ^a,e  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^b PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^c MONELL CHEMICAL SENSES CENTER   (United States)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 2,5 PYRROLIDINEDIONE; ANTHOCYANIDIN DERIVATIVE; ANTHOCYANIN; COLISTIN; CYANIDIN; DELPHINIDIN; FLAVONOID; KERACYANIN; MYRICETIN; N(G) NITRO DEXTRO ARGININE METHYL ESTER; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; REACTIVE NITROGEN SPECIES; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; TASTE RECEPTORS, TYPE 2;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL SWARMING MOTILITY; BACTERIAL SWIMMING; BIOFILM; CILIARY MOTILITY; CONTROLLED STUDY; DIGITAL IMAGING; HUMAN; HUMAN CELL; IN VITRO STUDY; INNATE IMMUNITY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; NOSE MUCOSA; PSEUDOMONAS AERUGINOSA; SINONASAL EPITHELIAL CELL; BACTERIUM; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; EUKARYOTIC FLAGELLUM; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; PHYSIOLOGY;

ANTHOCYANINS; BACTERIA; BIOFILMS; CELLS, CULTURED; CILIA; HUMANS; IMMUNITY, INNATE; NASAL MUCOSA; NITRIC OXIDE; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84979710925     PISSN: 19458924     EISSN: 19458932     Source Type: Journal    
DOI: 10.2500/ajra.2016.30.4331     Document Type: Article

References (80)

1. Settipane RA, Peters AT, and Chandra R. Chapter 4: Chronic rhinosinusitis. Am J Rhinol Allergy 27(suppl. 1):S11-S15, 2013.
2. Gudis D, Zhao KQ, and Cohen NA. Acquired cilia dysfunction in chronic rhinosinusitis. Am J Rhinol Allergy 26:1-6, 2012.
3. Fokkens WJ, Lund VJ, Mullol J, et al. European Position Paper on Rhinosinusitis and Nasal Polyps 2012. Rhinol Suppl (23):3 p preceding table of contents, 1-298, 2012.
4. Bhattacharyya N. Incremental health care utilization and expenditures for chronic rhinosinusitis in the United States. Ann Otol Rhinol Laryngol 120:423-427, 2011.
5. Bhattacharyya N, Grebner J, and Martinson NG. Recurrent acute rhinosinusitis: Epidemiology and health care cost burden. Otolaryngol Head Neck Surg 146:307-312, 2012.
6. Smith KA, Orlandi RR, and Rudmik L. Cost of adult chronic rhinosinusitis: A systematic review. Laryngoscope 125:1547-1556, 2015.
7. Antunes MB, Gudis DA, and Cohen NA. Epithelium, cilia, and mucus: Their importance in chronic rhinosinusitis. Immunol Allergy Clin North Am 29:631-643, 2009.
8. Al-Mutairi D, and Kilty SJ. Bacterial biofilms and the pathophysiology of chronic rhinosinusitis. Curr Opin Allergy Clin Immunol 11: 18-23, 2011.
9. Toledano A, Rodriguez G, Martin AM, et al. Quality of life in patients with smell loss due to upper respiratory tract infections. Am J Otolaryngol 32:504-510, 2011.
10. Manes RP, and Batra PS. Bacteriology and antibiotic resistance in chronic rhinosinusitis. Facial Plast Surg Clin North Am 20:87-91, 2012.
11. Kennedy JL, and Borish L. Chronic rhinosinusitis and antibiotics: The good, the bad, and the ugly. Am J Rhinol Allergy 27:467-472, 2013.
12. Lee RJ, and Cohen NA. Bitter and sweet taste receptors in the respiratory epithelium in health and disease. J Mol Med 92:1235-1244, 2014.
13. Lee RJ, and Cohen NA. Taste receptors in innate immunity. Cell Mol Life Sci 72:217-236, 2015.
14. Lee RJ, and Cohen NA. Role of the bitter taste receptor T2R38 in upper respiratory infection and chronic rhinosinusitis. Curr Opin Allergy Clin Immunol 15:14-20, 2015.
15. Lee RJ, and Cohen NA. Sinonasal solitary chemosensory cells taste the upper respiratory environment to regulate innate immunity. Am J Rhinol Allergy 28:366-373, 2014.
16. Lee RJ, and Cohen NA. The emerging role of the bitter taste receptor T2R38 in upper respiratory infection and chronic rhinosinusitis. Am J Rhinol Allergy 27:283-286, 2013.
17. Adappa ND, Howland TJ, Palmer JN, et al. Genetics of the taste receptor T2R38 correlates with chronic rhinosinusitis necessitating surgical intervention. Int Forum Allergy Rhinol 3:184-187, 2013.
18. Adappa ND, Zhang Z, Palmer JN, et al. The bitter taste receptor T2R38 is an independent risk factor for chronic rhinosinusitis requiring sinus surgery. Int Forum Allergy Rhinol 4:3-7, 2014.
19. Lee RJ, Xiong G, Kofonow JM, et al. T2R38 taste receptor polymorphisms underlie susceptibility to upper respiratory infection. J Clin Invest 122:4145-4159, 2012.
20. Lee RJ, Kofonow JM, Rosen PL, et al. Bitter and sweet taste receptors regulate human upper respiratory innate immunity. J Clin Invest 124:1393-1405, 2014.
21. Mfuna Endam L, Filali-Mouhim A, Boisvert P, et al. Genetic variations in taste receptors are associated with chronic rhinosinusitis: A replication study. Int Forum Allergy Rhinol 4:200-206, 2014.
22. Adappa ND, Farquhar D, Palmer JN, et al. TAS2R38 genotype predicts surgical outcome in nonpolypoid chronic rhinosinusitis. Int Forum Allergy Rhinol 6:25-33, 2016.
23. Ksonzekova P, Mariychuk R, Eliasova A, et al. In vitro study of biological activities of anthocyanin-rich berry extracts on porcine intestinal epithelial cells. J Sci Food Agric 96:1093-1100, 2016.
24. Roland WS, van Buren L, Gruppen H, et al. Bitter taste receptor activation by flavonoids and isoflavonoids: Modeled structural requirements for activation of hTAS2R14 and hTAS2R39. J Agric Food Chem 61:10454-10466, 2013.
25. Narukawa M, Noga C, Ueno Y, et al. Evaluation of the bitterness of green tea catechins by a cell-based assay with the human bitter taste receptor hTAS2R39. Biochem Biophys Res Commun 405:620-625, 2011.
26. Edwards M, Czank C, Woodward GM, et al. Phenolic metabolites of anthocyanins modulate mechanisms of endothelial function. J Agric Food Chem 63:2423-2431, 2015.
27. Jeong JH, Yoo HS, Lee SH, et al. Nasal and exhaled nitric oxide in chronic rhinosinusitis with polyps. Am J Rhinol Allergy 28:e11-e16, 2014.
28. Phillips PS, Sacks R, Marcells GN, et al. Nasal nitric oxide and sinonasal disease: A systematic review of published evidence. Otolaryngol Head Neck Surg 144:159-169, 2011.
29. Pala CU, Zorba NN, and Ozcan G. Microbial inactivation and physicochemical properties of ultrasound processed pomegranate juice. J Food Prot 78:531-539, 2015.
30. Leitao DP, Polizello AC, Ito IY, and Spadaro AC. Antibacterial screening of anthocyanic and proanthocyanic fractions from cranberry juice. J Med Food 8:36-40, 2005.
31. Junqueira-Goncalves MP, Yanez L, Morales C, et al. Isolation and characterization of phenolic compounds and anthocyanins from Murta (Ugni molinae Turcz.) fruits. Assessment of antioxidant and antibacterial activity. Molecules 20:5698-5713, 2015.
32. Krauze-Baranowska M, Majdan M, Halasa R, et al. The antimicrobial activity of fruits from some cultivar varieties of Rubus idaeus and Rubus occidentalis. Food Funct 5:2536-2541, 2014.
33. Viskelis P, Rubinskiene M, Jasutiene I, et al. Anthocyanins, antioxidative, and antimicrobial properties of American cranberry (Vaccinium macrocarpon Ait.) and their press cakes. J Food Sci 74:C157-C161, 2009.
34. Ombra MN, Fratianni F, Granese T, et al. In vitro antioxidant, antimicrobial and anti-proliferative activities of purple potato extracts (Solanum tuberosum cv Vitelotte noire) following simulated gastrointestinal digestion. Nat Prod Res 29:1087-1091, 2015.
35. Lacombe A, Wu VC, Tyler S, et al. Antimicrobial action of the American cranberry constituents; Phenolics, anthocyanins, and organic acids, against E. coli O157:H7. Int J Food Microbiol 139:102-107, 2010.
36. Kim JM, Kim KM, Park EH, et al. Anthocyanins from black soybean inhibit Helicobacter pylori-induced inflammation in human gastric epithelial AGS cells. Microbiol Immunol 57:366-373, 2013.
37. Faria A, Fernandes I, Norberto S, et al. Interplay between anthocyanins and gut microbiota. J Agric Food Chem 62:6898-6902, 2014.
38. Cisowska A, Wojnicz D, and Hendrich AB. Anthocyanins as antimicrobial agents of natural plant origin. Nat Prod Commun 6:149-156, 2011.
39. Aura AM, Martin-Lopez P, O'Leary KA, et al. In vitro metabolism of anthocyanins by human gut microflora. Eur J Nutr 44:133-142, 2005.
40. Xia EQ, Deng GF, Guo YJ, and LI HB. Biological activities of polyphenols from grapes. Int J Mol Sci 11:622-646, 2010.
41. Chang JH, Song KJ, Kim HJ, et al. Dietary polyphenols affect MUC5AC expression and ciliary movement in respiratory cells and nasal mucosa. Am J Rhinol Allergy 24:e59-e62, 2010.
42. Lee RJ, Chen B, Redding KM, et al. Mouse nasal epithelial innate immune responses to Pseudomonas aeruginosa quorum-sensing molecules require taste signaling components. Innate Immun 20:606-617, 2014.
43. Zhao KQ, Cowan AT, Lee RJ, et al. Molecular modulation of airway epithelial ciliary response to sneezing. FASEB J 26:3178-3187, 2012.
44. Lee RJ, Chen B, Doghramji L, et al. Vasoactive intestinal peptide regulates sinonasal mucociliary clearance and synergizes with histamine in stimulating sinonasal fluid secretion. FASEB J 27:5094-5103, 2013.
45. Abad A, Fernandez-Molina JV, Bikandi J, et al. What makes Aspergillus fumigatus a successful pathogen? Genes and molecules involved in invasive aspergillosis. Rev Iberoam Micol 27:155-182, 2010.
46. Lai Y, Chen B, Shi J, et al. Inflammation-mediated upregulation of centrosomal protein 110, a negative modulator of ciliogenesis, in patients with chronic rhinosinusitis. J Allergy Clin Immunol 128: 1207-1215.e1, 2011.
47. Carey RM, Workman AD, Chen B, et al. Staphylococcus aureus triggers nitric oxide production in human upper airway epithelium. Int Forum Allergy Rhinol 5:808-813, 2015.
48. Zhao KQ, Goldstein N, Yang H, et al. Inherent differences in nasal and tracheal ciliary function in response to Pseudomonas aeruginosa challenge. Am J Rhinol Allergy 25:209-213, 2011.
49. O'Toole GA. Microtiter dish biofilm formation assay. J Vis Exp (47): pii: 2437, 2011.
50. Antunes MB, Chi JJ, Liu Z, et al. Molecular basis of tobacco-induced bacterial biofilms: An in vitro study. Otolaryngol Head Neck Surg 147:876-884, 2012.
51. Goldstein-Daruech N, Cope EK, Zhao KQ, et al. Tobacco smoke mediated induction of sinonasal microbial biofilms. PloS One 6:e15700, 2011.
52. Harro JM, Daugherty S, Bruno VM, et al. Draft genome sequence of the methicillin-resistant Staphylococcus aureus isolate MRSA-M2. Genome Announc (1): pii: e00037-12. 2013.
53. Ha DG, Kuchma SL, and O'Toole GA. Plate-based assay for swimming motility in Pseudomonas aeruginosa. Methods Mol Biol 1149:59-65, 2014.
54. Ha DG, Kuchma SL, and O'Toole GA. Plate-based assay for swarming motility in Pseudomonas aeruginosa. Methods Mol Biol 1149:67-72, 2014.
55. Schindelin J, Arganda-Carreras I, Frise E, et al. Fiji: An open-source platform for biological-image analysis. Nat Methods 9:676-682, 2012.
56. Forstermann U, and Sessa WC. Nitric oxide synthases: Regulation and function. Eur Heart J 33:829-837, 837a-837d, 2012.
57. Nyman NA, and Kumpulainen JT. Determination of anthocyanidins in berries and red wine by high-performance liquid chromatography. J Agric Food Chem 49:4183-4187, 2001.
58. Ryan JM, and Revilla E. Anthocyanin composition of Cabernet Sauvignon and Tempranillo grapes at different stages of ripening. J Agric Food Chem 51:3372-3378, 2003.
59. Tulio AZ Jr, Reese RN, Wyzgoski FJ, et al. Cyanidin 3-rutinoside and cyanidin 3-xylosylrutinoside as primary phenolic antioxidants in black raspberry. J Agric Food Chem 56:1880-1888, 2008.
60. Lipchock SV, Mennella JA, Spielman AI, and Reed DR. Human bitter perception correlates with bitter receptor messenger RNA expression in taste cells. Am J Clin Nutr 98:1136-1143, 2013.
61. Bufe B, Breslin PA, Kuhn C, et al. The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. Curr Biol 15:322-327, 2005.
62. Caiazza NC, Shanks RM, and O'Toole GA. Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187:7351-7361, 2005.
63. Read RC, Roberts P, Munro N, et al. Effect of Pseudomonas aeruginosa rhamnolipids on mucociliary transport and ciliary beating. J Appl Physiol 72:2271-2277, 1992.
64. Zulianello L, Canard C, Kohler T, et al. Rhamnolipids are virulence factors that promote early infiltration of primary human airway epithelia by Pseudomonas aeruginosa. Infect Immun 74:3134-3147, 2006.
65. Conrad JC, Gibiansky ML, Jin F, et al. Flagella and pili-mediated near-surface single-cell motility mechanisms in P. aeruginosa. Biophys J 100:1608-1616, 2011.
66. Keller JB. Effect of viscosity on swimming velocity of bacteria. Proc Natl Acad Sci U S A 71:3253-3254, 1974.
67. Sampedro I, Parales RE, Krell T, and Hill JE. Pseudomonas chemotaxis. FEMS Microbiol Rev 39:17-46, 2015.
68. Mattick JS. Type IV pili and twitching motility. Annu Rev Microbiol 56:289-314, 2002.
69. Shi W, and Sun H. Type IV pilus-dependent motility and its possible role in bacterial pathogenesis. Infect Immun 70:1-4, 2002.
70. Kazmierczak BI, Schniederberend M, and Jain R. Cross-regulation of Pseudomonas motility systems: The intimate relationship between flagella, pili and virulence. Curr Opin Microbiol 28:78-82, 2015.
71. Li Y, Xia H, Bai F, et al. Identification of a new gene PA5017 involved in flagella-mediated motility, chemotaxis and biofilm formation in Pseudomonas aeruginosa. FEMS Microbiol Lett 272:188-195, 2007.
72. Adams H, Horrevoets WM, Adema SM, et al. Inhibition of biofilm formation by Camelid single-domain antibodies against the flagellum of Pseudomonas aeruginosa. J Biotechnol 186:66-73, 2014.
73. Marcinkiewicz J. Nitric oxide and antimicrobial activity of reactive oxygen intermediates. Immunopharmacology 37:35-41, 1997.
74. Fang FC. Perspectives series: Host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest 99: 2818-2825, 1997.
75. Salathe M. Regulation of mammalian ciliary beating. Annu Rev Physiol 69:401-422, 2007.
76. Ulrey RK, Barksdale SM, Zhou W, and van Hoek ML. Cranberry proanthocyanidins have anti-biofilm properties against Pseudomonas aeruginosa. BMC Complement Altern Med 14:499, 2014.
77. O'May C, and Tufenkji N. The swarming motility of Pseudomonas aeruginosa is blocked by cranberry proanthocyanidins and other tannin-containing materials. Appl Environ Microbiol 77:3061-3067, 2011.
78. Virgin F, Zhang S, Schuster D, et al. The bioflavonoid compound, sinupret, stimulates transepithelial chloride transport in vitro and in vivo. Laryngoscope 120:1051-1056, 2010.
79. Zhang S, Skinner D, Hicks SB, et al. Sinupret activates CFTR and TMEM16A-dependent transepithelial chloride transport and improves indicators of mucociliary clearance. PloS One 9:e104090, 2014.
80. Lai Y, Dilidaer D, Chen B, et al. In vitro studies of a distillate of rectified essential oils on sinonasal components of mucociliary clearance. Am J Rhinol Allergy 28:244-248, 2014.