Sambucus nigra extracts inhibit infectious bronchitis virus at an early point during replication

BMC Veterinary Research

Volumn 10, Issue , 2014, Pages

  Chen, Christie ^a   Zuckerman, David M ^b   Brantley, Susanna ^a   Sharpe, Michka ^a   Childress, Kevin ^a   Hoiczyk, Egbert ^b   Pendleton, Amanda R ^a,c  

^a EMORY UNIVERSITY   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c AMARILLO COLLEGE   (United States)

Author keywords

Coronavirus; Infectious bronchitis virus; Nigella sativa; Rhodiola rosea; Sambucus nigra

Indexed keywords

AVIAN INFECTIOUS BRONCHITIS VIRUS; CORONAVIRUS; NIGELLA SATIVA; RHODIOLA; RHODIOLA ROSEA; SAMBUCUS NIGRA;

PLANT EXTRACT;

ANIMAL; ARTICLE; AVIAN INFECTIOUS BRONCHITIS VIRUS; BLACK CUMIN; CHEMISTRY; CHLOROCEBUS AETHIOPS; DOSE RESPONSE; DRUG EFFECT; FRUIT; PLANT ROOT; PLANT SEED; RHODIOLA; SAMBUCUS NIGRA; VERO CELL LINE; VIRUS REPLICATION;

ANIMALS; CERCOPITHECUS AETHIOPS; DOSE-RESPONSE RELATIONSHIP, DRUG; FRUIT; INFECTIOUS BRONCHITIS VIRUS; NIGELLA SATIVA; PLANT EXTRACTS; PLANT ROOTS; RHODIOLA; SAMBUCUS NIGRA; SEEDS; VERO CELLS; VIRUS REPLICATION;

EID: 84892393275     PISSN: None     EISSN: 17466148     Source Type: Journal    
DOI: 10.1186/1746-6148-10-24     Document Type: Article

References (83)

1. Sevoian M, Levine PP. Effects of infectious bronchitis on the reproductive tracts, egg production, and egg quality of laying chickens. Avian Dis 1957, 1:136.
2. Raj GD, Jones RC. Infectious bronchitis virus: immunopathogenesis of infection in the chicken. Avian Pathol 1997, 26:677-706. 10.1080/03079459708419246, 18483939.
3. Cavanagh D. Coronaviruses in poultry and other birds. Avian Pathol 2005, 34:439-448. 10.1080/03079450500367682, 16537157.
4. Perlman S. Pathogenesis of coronavirus-induced infections. Review of pathological and immunological aspects. Adv Exp Med Biol 1998, 440:503-513.
5. Gelb J, Weisman Y, Ladman BS, Meir R. S1 gene characteristics and efficacy of vaccination against infectious bronchitis virus field isolates from the United States and Israel (1996 to 2000). Avian Pathol 2005, 34:194-203. 10.1080/03079450500096539, 16191702.
6. Liu S, Chen J, Han Z, Zhang Q, Shao Y, Kong X, Tong G. Infectious bronchitis virus: S1 gene characteristics of vaccines used in China and efficacy of vaccination against heterologous strains from China. Avian Pathol 2006, 35:394-399. 10.1080/03079450600920984, 16990149.
7. Rishton GM. Natural products as a robust source of new drugs and drug leads: past successes and present day issues. Am J Cardiol 2008, 101(10):S43-S49.
8. Sharma P, Sharma JD. Plants showing antiplasmodial activity-from crude extracts to isolated compounds. Indian J Malariol 1998, 35:57-110.
9. Tagboto S, Townson S. Antiparasitic properties of medicinal plants and other naturally occurring products. Adv Parasitol 2001, 50:199-295.
10. Mukhtar M, Arshad M, Ahmad M, Pomerantz RJ, Wigdahl B, Parveen Z. Antiviral potentials of medicinal plants. Virus Res 2008, 131:111-120. 10.1016/j.virusres.2007.09.008, 17981353.
11. Daglia M. Polyphenols as antimicrobial agents. Curr Opin Biotechnol 2012, 23:174-181. 10.1016/j.copbio.2011.08.007, 21925860.
12. Van Baarlen P, van Belkum A, Thomma BPHJ. Disease induction by human microbial pathogens in plant-model systems: potential, problems and prospects. Drug Discov Today 2007, 12:167-173. 10.1016/j.drudis.2006.12.007, 17275738.
13. Wink M. Evolutionary advantage and molecular modes of action of multi-component mixtures used in phytomedicine. Curr Drug Metab 2008, 9:996-1009. 10.2174/138920008786927794, 19075616.
14. Danielsson M, Lundén K, Elfstrand M, Hu J, Zhao T, Arnerup J, Ihrmark K, Swedjemark G, Borg-Karlson A-K, Stenlid J. Chemical and transcriptional responses of Norway spruce genotypes with different susceptibility to Heterobasidion spp. infection. BMC Plant Biol 2011, 11:154. 10.1186/1471-2229-11-154, 3240162, 22067529.
15. Punyasiri PAN, Abeysinghe ISB, Kumar V. Preformed and induced chemical resistance of tea leaf against Exobasidium vexans Infection. J Chem Ecol 2005, 31:1315-1324. 10.1007/s10886-005-5288-z, 16222773.
16. Yamada H, Takuma N, Daimon T, Hara Y. Gargling with tea catechin extracts for the prevention of influenza infection in elderly nursing home residents: a prospective clinical study. J Altern Complement Med 2006, 12:669-672. 10.1089/acm.2006.12.669, 16970537.
17. Matsumoto K, Yamada H, Takuma N, Niino H, Sagesaka YM. Effects of green tea catechins and theanine on preventing influenza infection among healthcare workers: a randomized controlled trial. BMC Complement Altern Med 2011, 11:15. 10.1186/1472-6882-11-15, 3049752, 21338496.
18. Jia Z, Zou B, Wang X, Qiu J, Ma H, Gou Z, Song S, Dong H. Quercetin-induced H2O2 mediates the pathogen resistance against Pseudomonas syringae pv. Tomato DC3000 in Arabidopsis thaliana. Biochem Biophys Res Commun 2010, 396:522-527. 10.1016/j.bbrc.2010.04.131, 20434432.
19. Choi HJ, Song JH, Park KS, Kwon DH. Inhibitory effects of quercetin 3-rhamnoside on influenza A virus replication. Eur J Pharm Sci 2009, 37:329-333. 10.1016/j.ejps.2009.03.002, 19491023.
20. Neznanov N, Kondratova A, Chumakov KM, Neznanova L, Kondratov R, Banerjee AK, Gudkov AV. Quercetinase Pirin Makes Poliovirus Replication Resistant to Flavonoid Quercetin. DNA & Cell Biology 2008, 27:191-198. 10.1089/dna.2007.0682, 18067462.
21. Paolillo R, Romano Carratelli C, Rizzo A. Effect of resveratrol and quercetin in experimental infection by Salmonella enterica serovar Typhimurium. Int Immunopharmacol 2011, 11:149-156. 10.1016/j.intimp.2010.10.019, 21093605.
22. Davis JM, Murphy EA, McClellan JL, Carmichael MD, Gangemi JD. Quercetin reduces susceptibility to influenza infection following stressful exercise. Am J Physiol Regul Integr Comp Physiol 2008, 295:R505-R509. 10.1152/ajpregu.90319.2008, 18579649.
23. Choi HJ, Song JH, Kwon DH. Quercetin 3-rhamnoside exerts antiinfluenza A virus activity in mice. Phytother Res 2012, 26:462-464.
24. Kim Y, Narayanan S, Chang K-O. Inhibition of influenza virus replication by plant-derived isoquercetin. Antiviral Res 2010, 88:227-235. 10.1016/j.antiviral.2010.08.016, 20826184.
25. Li J, Yin J, Sui X, Li G, Ren X. Comparative analysis of the effect of glycyrrhizin diammonium and lithium chloride on infectious bronchitis virus infection in vitro. Avian Pathol 2009, 38:215-221. 10.1080/03079450902912184, 19468938.
26. Li H, Wu J, Zhang Z, Ma Y, Liao F, Zhang Y, Wu G. Forsythoside a inhibits the avian infectious bronchitis virus in cell culture. Phytother Res 2011, 25:338-342.
27. Celik MM, Karakus A, Zeren C, Demir M, Bayarogullari H, Duru M, Al M. Licorice induced hypokalemia, edema, and thrombocytopenia. Hum Exp Toxicol 2012, 31:1295-1298. 10.1177/0960327112446843, 22653692.
28. Van Uum SHM, Lenders JWM, Hermus ARMM. Cortisol, 11beta-hydroxysteroid dehydrogenases, and hypertension. Semin Vasc Med 2004, 4:121-128. 10.1055/s-2004-835369, 15478032.
29. Palermo M, Quinkler M, Stewart PM. Apparent mineralocorticoid excess syndrome: an overview. Arq Bras Endocrinol Metabol 2004, 48:687-696. 10.1590/S0004-27302004000500015, 15761540.
30. Markowitz J, Zhu H-J. Limitations of in vitro assessments of the drug interaction potential of botanical supplements. Planta Med 2012, 78:1421-1427.
31. Song X, Liu Z, Wang H, Xin Y, Wang X, Chen J, Shi Y, Zhang C, Hui R. QiHong prevents death in coxsackievirus B3 induced murine myocarditis through inhibition of virus attachment and penetration. Exp Biol Med (Maywood) 2007, 232:1441-1448. 10.3181/0704-RM-110, 18040068.
32. Panossian A, Wikman G, Sarris J. Rosenroot (Rhodiola rosea): traditional use, chemical composition, pharmacology and clinical efficacy. Phytomedicine 2010, 17:481-493. 10.1016/j.phymed.2010.02.002, 20378318.
33. Choi HJ, Song JH, Bhatt LR, Baek SH. Anti-human rhinovirus activity of gallic acid possessing antioxidant capacity. Phytother Res 2010, 24:1292-1296. 10.1002/ptr.3101, 20104501.
34. Wang G-F, Shi L-P, Ren Y-D, Liu Q-F, Liu H-F, Zhang R-J, Li Z, Zhu F-H, He P-L, Tang W, Tao P-Z, Li C, Zhao W-M, Zuo J-P. Anti-hepatitis B virus activity of chlorogenic acid, quinic acid and caffeic acid in vivo and in vitro. Antiviral Res 2009, 83:186-190. 10.1016/j.antiviral.2009.05.002, 19463857.
35. Hanafy MS, Hatem ME. Studies on the antimicrobial activity of Nigella sativa seed (black cumin). J Ethnopharmacol 1991, 34:275-278. 10.1016/0378-8741(91)90047-H, 1795532.
36. Salem ML, Hossain MS. Protective effect of black seed oil from Nigella sativa against murine cytomegalovirus infection. Int J Immunopharmacol 2000, 22:729-740. 10.1016/S0192-0561(00)00036-9, 10884593.
37. Barakat EMF, El Wakeel LM, Hagag RS. Effects of Nigella sativa on outcome of hepatitis C in Egypt. World J Gastroenterol 2013, 19:2529-2536. 10.3748/wjg.v19.i16.2529, 3646144, 23674855.
38. Mehta B, Sharma U, Agrawal S, Pandit V, Joshi N, Gupta M. Isolation and characterization of new compounds from seeds of Nigella sativa. Med Chem Res 2008, 17:462-473.
39. Liu X, Abd El-Aty AM, Cho S-K, Yang A, Park J-H, Shim J-H. Characterization of secondary volatile profiles in Nigella sativa seeds from two different origins using accelerated solvent extraction and gas chromatography-mass spectrometry. Biomed Chromatogr 2012, 26:1157-1162. 10.1002/bmc.2671, 22290690.
40. Ali BH, Blunden G. Pharmacological and toxicological properties of Nigella sativa. Phytother Res 2003, 17:299-305. 10.1002/ptr.1309, 12722128.
41. Zakay-Rones Z, Varsano N, Zlotnik M, Manor O, Regev L, Schlesinger M, Mumcuoglu M. Inhibition of several strains of influenza virus in vitro and reduction of symptoms by an Elderberry extract (Sambucus nigra L.) during an outbreak of influenza B Panama. J Altern Complement Med 1995, 1:361-369. 10.1089/acm.1995.1.361, 9395631.
42. Veberic R, Jakopic J, Stampar F, Schmitzer V. European elderberry (Sambucus nigra L.) rich in sugars, organic acids, anthocyanins and selected polyphenols. Food Chem 2009, 114:511-515.
43. Mazza G. Anthocyanins and Other Phenolic Compounds of Saskatoon Berries Amelanchier alnifolia Nutt. J Food Sci 1986, 51:1260-1264.
44. McCutcheon AR, Roberts TE, Gibbons E, Ellis SM, Babiuk LA, Hancock REW, Towers GHN. Antiviral screening of British Columbian medicinal plants. J Ethnopharmacol 1995, 49:101-110. 10.1016/0378-8741(95)90037-3, 8847882.
45. Machamer CE, Rose JK. A specific transmembrane domain of a coronavirus E1 glycoprotein is required for its retention in the Golgi region. J Cell Biol 1987, 105:1205-1214. 10.1083/jcb.105.3.1205, 2114809, 2821010.
46. Benhaddou-Andaloussi A, Martineau L, Vuong T, Meddah B, Madiraju P, Settaf A, Haddad PS. The In Vivo Antidiabetic Activity of Nigella sativa Is Mediated through Activation of the AMPK Pathway and Increased Muscle Glut4 Content. Evid Based Complement Alternat Med 2011, 2011:538671. 3092603, 21584245.
47. Swamy SM, Tan BK. Cytotoxic and immunopotentiating effects of ethanolic extract of Nigella sativa L. seeds. J Ethnopharmacol 2000, 70:1-7. 10.1016/S0378-8741(98)00241-4, 10720783.
48. Roschek B, Fink RC, McMichael MD, Li D, Alberte RS. Elderberry flavonoids bind to and prevent H1N1 infection in vitro. Phytochemistry 2009, 70:1255-1261. 10.1016/j.phytochem.2009.06.003, 19682714.
49. Hidari KIPJ, Abe T, Suzuki T. Crabohydrate-related inhibitors of dengue virus entry. Viruses 2013, 5:605-618. 10.3390/v5020605, 3640517, 23389466.
50. François KO, Balzarini J. Potential of carbohydrate-binding agents as therapeutics against enveloped viruses. Med Res Rev 2012, 32:349-387. 10.1002/med.20216, 20577974.
51. Wu L, Bao J-K. Anti-tumor and anti-viral activities of Galanthus nivalis agglutinin (GNA)-related lectins. Glycoconj J 2013, 30:269-279. 10.1007/s10719-012-9440-z, 22893111.
52. Stuart AD, Brown TDK. Alpha2,6-linked sialic acid acts as a receptor for Feline calicivirus. J Gen Virol 2007, 88(Pt 1):177-186.
53. Van Breedam W, Pöhlmann S, Favoreel HW, de Groot RJ, Nauwynck HJ. Bitter-sweet symphony: glycan-lectin interactions in virus biology. FEMS Microbiol Rev 2013, Epub ahead of print.
54. Balzarini J. Targeting the glycans of glycoproteins: a novel paradigm for antiviral therapy. Nat Rev Microbiol 2007, 5:583-597. 10.1038/nrmicro1707, 17632570.
55. Van Damme EJ, Barre A, Rougé P, Van Leuven F, Peumans WJ. Characterization and molecular cloning of Sambucus nigra agglutinin V (nigrin b), a GalNAc-specific type-2 ribosome-inactivating protein from the bark of elderberry (Sambucus nigra). Eur J Biochem 1996, 237:505-513. 10.1111/j.1432-1033.1996.0505k.x, 8647092.
56. Peumans WJ, Roy S, Barre A, Rouge P, van Leuven F, van Damme EJ. Elderberry (Sambucus nigra) contains truncated Neu5Ac(alpha-2,6)Gal/GalNAc-binding type 2 ribosome-inactivating proteins. FEBS Lett 1998, 425:35-39. 10.1016/S0014-5793(98)00193-8, 9541002.
57. Chen Y, Vandenbussche F, Rougé P, Proost P, Peumans WJ, Van Damme EJM. A complex fruit-specific type-2 ribosome-inactivating protein from elderberry (Sambucus nigra) is correctly processed and assembled in transgenic tobacco plants. Eur J Biochem 2002, 269:2897-2906. 10.1046/j.1432-1033.2002.02962.x, 12071953.
58. Mach L, Kerschbaumer R, Schwihla H, Glössl J. Elder (Sambucus nigra L.)-fruit lectin (SNA-IV) occurs in monomeric, dimeric and oligomeric isoforms. Biochem J 1996, 315(3):1061. 1217262, 8645145.
59. Mach L, Scherf W, Ammann M, Poetsch J, Bertsch W, März L, Glössl J. Purification and partial characterization of a novel lectin from elder (Sambucus nigra L.) fruit. Biochem J 1991, 278(3):667-671. 1151398, 1910334.
60. Winter C, Herrler G, Neumann U. Infection of the tracheal epithelium by infectious bronchitis virus is sialic acid dependent. Microbes Infect 2008, 10:367-373. 10.1016/j.micinf.2007.12.009, 18396435.
61. Binns MM, Boursnell ME, Tomley FM, Brown DK. Comparison of the spike precursor sequences of coronavirus IBV strains M41 and 6/82 with that of IBV Beaudette. J Gen Virol 1986, 67(Pt 12):2825-2831.
62. Van der Meer FJUM, de Haan CAM, Schuurman NMP, Haijema BJ, Verheije MH, Bosch BJ, Balzarini J, Egberink HF. The carbohydrate-binding plant lectins and the non-peptidic antibiotic pradimicin A target the glycans of the coronavirus envelope glycoproteins. J Antimicrob Chemother 2007, 60:741-749. 10.1093/jac/dkm301, 17704516.
63. Ansari AA, Hassan S, Kenne L. Atta-Ur-Rahman, Wehler T: structural studies on a saponin isolated from Nigella sativa. Phytochemistry 1988, 27:3977-3979.
64. Mehta BK, Mehta P, Gupta M. Note: a new naturally acetylated triterpene saponin from Nigella sativa. Carbohydr Res 2009, 344:149-151. 10.1016/j.carres.2008.10.004, 19036356.
65. Mehta BK, Verma M, Gupta M. Novel lipid constituents identified in seeds of Nigella sativa (Linn). J Braz Chem Soc 2008, 19:458-462.
66. Merfort I, Wray V, Barakat HH, Hussein SAM, Nawwar MAM, Willuhn G. Flavonol triglycosides from seeds of Nigella sativa. Phytochemistry 1997, 46:359-363.
67. Morikawa T, Xu F, Kashima Y, Matsuda H, Ninomiya K, Yoshikawa M. Novel dolabellane-type diterpene alkaloids with lipid metabolism promoting activities from the seeds of Nigella sativa. Org Lett 2004, 6:869-872. 10.1021/ol036239c, 15012052.
68. Naithani R, Huma LC, Holland LE, Shukla D, McCormick DL, Mehta RG, Moriarty RM. Antiviral activity of phytochemicals: a comprehensive review. Mini Rev Med Chem 2008, 8:1106-1133. 10.2174/138955708785909943, 18855727.
69. Jeong HJ, Ryu YB, Park S-J, Kim JH, Kwon H-J, Kim JH, Park KH, Rho M-C, Lee WS. Neuraminidase inhibitory activities of flavonols isolated from Rhodiola rosea roots and their in vitro anti-influenza viral activities. Bioorg Med Chem 2009, 17:6816-6823. 10.1016/j.bmc.2009.08.036, 19729316.
70. Wang H, Ding Y, Zhou J, Sun X, Wang S. The in vitro and in vivo antiviral effects of salidroside from Rhodiola rosea L. against coxsackievirus B3. Phytomedicine 2009, 16:146-155. 10.1016/j.phymed.2008.07.013, 18818064.
71. Lee J, Finn CE. Anthocyanins and other polyphenolics in American elderberry (Sambucus canadensis) and European elderberry (S. nigra) cultivars. J Sci Food Agric 2007, 87:2665-2675. 10.1002/jsfa.3029, 20836175.
72. Schmitzer V, Veberic R, Slatnar A, Stampar F. Elderberry (Sambucus nigra L.) wine: a product rich in health promoting compounds. J Agric Food Chem 2010, 58:10143-10146. 10.1021/jf102083s, 20735034.
73. Lavola A, Karjalainen R, Julkunen-Tiitto R. Bioactive Polyphenols in Leaves, Stems, and Berries of Saskatoon (Amelanchier alnifolia Nutt.) Cultivars. J Agric Food Chem 2012, 60:1020-1027. 10.1021/jf204056s, 22220589.
74. Graham DRM, Chertova E, Hilburn JM, Arthur LO, Hildreth JEK. Cholesterol depletion of human immunodeficiency virus type 1 and Simian Immunodeficiency virus with β-Cyclodextrin inactivates and permeabilizes the virions: evidence for virion-associated lipid rafts. J Virol 2003, 77:8237-8248. 10.1128/JVI.77.15.8237-8248.2003, 165256, 12857892.
75. Kaack K, Austed T. Interaction of vitamin C and flavonoids in elderberry (Sambucus nigra L.) during juice processing. Plant Foods Hum Nutr 1998, 52:187-198. 10.1023/A:1008069422202, 9950080.
76. Jackwood MW, Rosenbloom R, Petteruti M, Hilt DA, McCall AW, Williams SM. Avian coronavirus infectious bronchitis virus susceptibility to botanical oleoresins and essential oils in vitro and in vivo. Virus Res 2010, 149:86-94. 10.1016/j.virusres.2010.01.006, 20096315.
77. Guozhong Z, Feng J, Yanxin H, Zhijun M, Qi Y, Jixun Z, Xiaodong L. Virulent Avian Infectious Bronchitis Virus, People's Republic of China. Emerg Infect Dis 2012, 18:1994-2001. 10.3201/eid1812.120552, 3557894, 23171741.
78. Wit JJ D, Bijlenga G, Cook JKA, Gelb J. Development and use of the H strain of avian infectious bronchitis virus from the Netherlands as a vaccine: a review. Avian Pathol 2004, 33:550-557. 10.1080/03079450400013154, 15763721.
79. Li L, Xue C, Chen F, Qin J, Xie Q, Bi Y, Cao Y. Isolation and genetic analysis revealed no predominant new strains of avian infectious bronchitis virus circulating in South China during 2004-2008. Vet Microbiol 2010, 143:145-154. 10.1016/j.vetmic.2009.11.022, 20022714.
80. Hadipour MM, Habibi PG GH. The role of avian influenza, newcastle disease and infectious bronchitis viruses during the respiratory disease outbreak in commercial broiler farms of Iran. Int J Anim Vet Adv 2011, 3:69-72.
81. Lim PL, Lee TH, Rowe EK. Middle East Respiratory Syndrome coronavirus (MERS CoV): Update 2013. Curr Infect Dis Rep 2013, 15:295-298. 10.1007/s11908-013-0344-2, 23793899.
82. Wevers BA, van der Hoek L. Recently discovered human coronaviruses. Clin Lab Med 2009, 29:715-724. 10.1016/j.cll.2009.07.007, 19892230.
83. Cinatl J, Morgenstern B, Bauer G, Chandra P, Rabenau H, Doerr HW. Glycyrrhizin, an active component of liquorice roots, and replication of SARS-associated coronavirus. Lancet 2003, 361:2045-2046. 10.1016/S0140-6736(03)13615-X, 12814717.