Fighting arboviral diseases: low toxicity on mammalian cells, dengue growth inhibition (in vitro), and mosquitocidal activity of Centroceras clavulatum-synthesized silver nanoparticles

Parasitology Research

Volumn 115, Issue 2, 2016, Pages 651-662

  Murugan, Kadarkarai ^a   Aruna, Palanimuthu ^a   Panneerselvam, Chellasamy ^a   Madhiyazhagan, Pari ^a   Paulpandi, Manickam ^a   Subramaniam, Jayapal ^a   Rajaganesh, Rajapandian ^a   Wei, Hui ^b   Alsalhi, Mohamad Saleh ^c   Devanesan, Sandhanasamy ^c   Nicoletti, Marcello ^d   Syuhei, Ban ^e   Canale, Angelo ^f   Benelli, Giovanni ^f,g  

^a BHARATHIAR UNIVERSITY   (India)

^b INSTITUTE OF PLANT PROTECTION   (China)

^c KING SAUD UNIVERSITY   (Saudi Arabia)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e UNIVERSITY OF SHIGA PREFECTURE   (Japan)

^f UNIVERSITY OF PISA   (Italy)

^g SCUOLA SUPERIORE SANT ANNA   (Italy)

Author keywords

Arbovirus; Biopesticide; Biosafety; Cytotoxicity; Dengue fever; Mosquito borne disease; Nanotechnology

Indexed keywords

1,1 DIPHENYL 2 PICRYLHYDRAZYL; ALGAL EXTRACT; CENTROCERAS CLAVULATUM EXTRACT; NITRIC OXIDE; SILVER NANOPARTICLE; UNCLASSIFIED DRUG; 2,2-DIPHENYL-1-PICRYLHYDRAZYL; ANTIOXIDANT; BIPHENYL DERIVATIVE; INSECTICIDE; METAL NANOPARTICLE; PICRIC ACID; SILVER;

AEDES AEGYPTI; ALGA; ANTIOXIDANT ACTIVITY; ARBOVIRUS; ARTICLE; CENTROCERAS CLAVULATUM; DENGUE; IN VITRO STUDY; INFRARED SPECTROSCOPY; INSECTICIDAL ACTIVITY; LARVA; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PUPA; ROENTGEN SPECTROSCOPY; SCANNING ELECTRON MICROSCOPY; SPECTROPHOTOMETRY; SYNTHESIS; ULTRAVIOLET RADIATION; VERO CELL LINE; VIROGENESIS; VIRUS ENTRY; VIRUS INFECTION; VIRUS INHIBITION; VIRUS LOAD; VIRUS REPLICATION; X RAY DIFFRACTION; AEDES; ANIMAL; CELL SURVIVAL; CHEMISTRY; CHLOROCEBUS AETHIOPS; DENGUE VIRUS; DISEASE CARRIER; DRUG EFFECTS; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; LD50; METABOLISM; PLANT LEAF; RED ALGA; TRANSMISSION;

AEDES; ANIMALS; ANTIOXIDANTS; BIPHENYL COMPOUNDS; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; DENGUE; DENGUE VIRUS; FEMALE; INSECT VECTORS; INSECTICIDES; LARVA; LETHAL DOSE 50; METAL NANOPARTICLES; NITRIC OXIDE; PICRATES; PLANT LEAVES; PUPA; RHODOPHYTA; SILVER; VERO CELLS; VIRUS REPLICATION; X-RAY DIFFRACTION;

EID: 84955348302     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-015-4783-6     Document Type: Article

References (73)

1. Ahmad A, Mukherjee P, Senapati S, Mandal D, Khan MI, Kumar R, Sastry M (2003) Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Colloids Surf B 28:313–318
2. Amer A, Mehlhorn H (2006a) Repellency effect of forty-one essential oils against Aedes, Anopheles and Culex mosquitoes. Parasitol Res 99:478–490
3. Amer A, Mehlhorn H (2006b) The sensilla of Aedes and Anopheles mosquitoes and their importance in repellency. Parasitol Res 99:491–499
4. Amer A, Mehlhorn H (2006c) Larvicidal effects of various essential oils against Aedes, Anopheles, and Culex larvae (Diptera, Culicidae). Parasitol Res 99:466–472
5. Amer A, Mehlhorn H (2006d) Persistency of larvicidal effects of plant oil extracts under different storage conditions. Parasitol Res 99:473–477
6. Asmathunisha N, Kathiresan K, Anburaj NMA (2010) Synthesis of antimicrobial silver nanoparticles by callus leaf extracts from saltmarsh plant Sesuvium portulacastrum L. Coll Surf B Biointer 79:488–493
7. Atmani D, Chaher N, Berboucha M, Ayouni K, Lounis H, Boudaoud H, Debbache N, Atmani D (2009) Antioxidant capacity and phenol content of selected Algerian medicinal plants. Food Chem 112:303–309
8. Azizullah A, Rehman ZU, Ali I, Murad W, Muhammad N, Ullah W, Hader D-P (2014) Chlorophyll derivatives can be an efficient weapon in the fight against dengue. Parasitol Res 113:4321–4326
9. Bankar A, Joshi B, Ravi Kumar A, Zinjardea S (2010) Banana peel extract mediated synthesis of gold nanoparticles. Colloids Surf B: Biointerfaces 80:45–50
10. Barros-Barreto MB, Mcivor L, Maggs CA, Ferreira PCG (2006) Molecular systematics of Ceramium and Centroceras (Ceramiaceae, Rhodophyta) from Brazil. J Phycol 42:905–921
11. Benelli G (2015a) Research in mosquito control: current challenges for a brighter future. Parasitol Res. doi:10.1007/s00436-015-4586-9
12. Benelli G (2015b) Plant-borne ovicides in the fight against mosquito vectors of medical and veterinary importance: a systematic review. Parasitol Res 114:3201–3212
13. Benelli G (2016) Plant-synthesized nanoparticles: an eco-friendly tool against mosquito vectors? In Mehlhorn H (ed) Nanoparticles in the fight against parasites. Parasitology Research Monographs 8, Chapter 8. Springer International Publishing Switzerland. doi:10.1007/978-3-319-25292-6_8
14. Benelli G, Flamini G, Fiore G, Cioni PL, Conti B (2013) Larvicidal and repellent activity of the essential oil of Coriandrum sativum L. (Apiaceae) fruits against the filariasis vector Aedes albopictus Skuse (Diptera: Culicidae). Parasitol Res 112:1155–1161
15. Benelli G, Bedini S, Cosci F, Toniolo C, Conti B, Nicoletti M (2015a) Larvicidal and ovideterrent properties of neem oil and fractions against the filariasis vector Aedes albopictus (Diptera: Culicidae): a bioactivity survey across production sites. Parasitol Res 114:227–236
16. Benelli G, Murugan K, Panneerselvam C, Madhiyazhagan P, Conti B, Nicoletti M (2015b) Old ingredients for a new recipe? Neem cake, a low-cost botanical by-product in the fight against mosquito-borne diseases. Parasitol Res 114:391–397
17. Blois MS (1958) Antioxidant determinations by the use of a stable free radical. Nature 181:1199–1200
18. Dhas TS, Kumar VG, Karthick V, Angel KJ, Govindaraju K (2014) Facile synthesis of silver chloride nanoparticles using marine alga and its antibacterial efficacy. Spectrochim Acta Part A Mol Biomol Spectrosc 120:416
19. Elechiguerra JL, Burt JL, Morones JR, Bragado AC, Gao X, Lara HH, Yacaman MJ (2005) Interaction of silver nanoparticles with HIV-1. J Nanobiotechnol 3:1–10
20. Finney DJ (1971) Probit analysis. Cambridge University, London, pp 68–78
21. Goel A, Patel DN, Lakhani KK et al (2004) Dengue fever—a dangerous foe. J Indian Acad Clin Med 5(3):247–258
22. 4@Ag nanoparticles. Nanotechnology 18:285604
23. Harris E, Holden KL, Edgil D et al (2006) Molecular biology of flaviviruses. Novartis Found Symp 277:23–39
24. Hemingway J, Ranson H (2000) Insecticide resistance in insect vectors of human disease. Annu Rev Entomol 45:371–391
25. Kalimuthu K, Lin SM, Tseng LC, Murugan K, Hwang J-S (2014) Bioefficacy potential of seaweed Gracilaria firma with copepod, Megacyclops formosanus for the control larvae of dengue vector Aedes aegypti. Hydrobiologia 741:113–123
26. Kaviya S, Santhanalakshmi J, Viswanathan B, Muthumary J, Srinivasan K (2011) Biosynthesis of silver nanoparticles using Citrus sinensis peel extract and its antibacterial activity. Spectrochim Acta Part A Mol Biomol Spectrosc 79:594–598
27. Krishnaraj C, Jagan EG, Rajasekar S, Selvakumar P, Kalaichelvan PT, Mohan N (2010) Synthesis of silver nanoparticles using Acalypha indica leaf extracts and its antibacterial activity against water borne pathogens. Coll Surf B Biointerf 76:50–56
28. Kumar KP, Murugan K, Kovendan K, Kumar AN, Hwang JS, Barnard DR (2012a) Combined effect of seaweed (Sargassum wightii) and Bacillus thuringiensis var. israelensis on the coastal mosquito, Anopheles sundaicus, in Tamil Nadu, India. Sci Asia 38:141–146
29. Kumar P, Senthamil Selvi S, LakshmiPraba A, PremKumar K, Ganeshkumar RS, Govindaraju M (2012b) Synthesis of silver nanoparticles from Sargassum tenerrimum and screening phytochemcials for its anti-bacterial activity. Nano Biomed Eng 4:12–16
30. Lubbad MY, Al-Quraishy S, Dkhil MA (2015) Antimalarial and antioxidant activities of Indigofera oblongifolia on Plasmodium chabaudi-induced spleen tissue injury in mice. Parasitol Res 114:3431–3438
31. Madhiyazhagan P, Murugan K, Naresh Kumar A, Nataraj T, Dinesh D, Panneerselvam C, Subramaniam J, Mahesh Kumar P, Suresh U, Roni M, Nicoletti M, Alarfaj AA, Higuchi A, Munusamy MA, Benelli G (2015) Sargassum muticum-synthetized silver nanoparticles: an effective control tool against mosquito vectors and bacterial pathogens. Parasitol Res. doi:10.1007/s00436-015-4671-0
32. Manilal A, Sujith S, Seghal Kiran G, Selvin J, Shakir C, Gandhimathi R, Panikkar MVN (2009) Biopotentials of seaweeds collected from southwest coast of India. J Mar Sci Technol 17(1):67–73
33. Martinez-Castanon GA, Nino-Martinez N, Martinez-Gutierrez F, Martinez-Mendoza JR, Ruiz F (2008) Synthesis and antibacterial activity of silver nanoparticles with different sizes. J Nanopart Res 10:1343–1348
34. Mehlhorn H (ed) (2011) Nature helps. How plants and other organisms contribute to solve health problems. Parasitol Res Monographs, Springer, Berlin, pp. 1–372
35. Mehlhorn H, Schmahl G, Schmidt J (2005) Extract of the seeds of the plant Vitex agnus castus proven to be highly efficacious as a repellent against ticks, fleas, mosquitoes and biting flies. Parasitol Res 95:363–365
36. Mehlhorn H, Al-Rasheid KA, Al-Quraishy S, Abdel-Ghaffar F (2012) Research and increase of expertise in arachno-entomology are urgently needed. Parasitol Res 110:259–265
37. Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramirez JT, Yacaman MJ (2005) The bactericidal effect of silver nanoparticles. J Nanotechnol 16:2346–2353
38. Mukunthan KS, Elumalai EK, Patel TN, Murty VR (2011) Catharanthus roseus: a natural source for the synthesis of silver nanoparticles. Asian Pac J Trop Biomed 1(4):270–274
39. Murrell S, Wu SC, Butler M (2011) Review of dengue virus and the development of a vaccine. Biotechnol Adv 29:239–247
40. Murugan K, Dinesh D, Paulpandi M, Dakhellah Meqbel Althbyani A, Subramaniam J, Madhiyazhagan P, Wang L, Suresh U, Mahesh Kumar P, Mohan J, Rajaganesh R, Wei H, Kalimuthu K, Parajulee MN, Mehlhorn H, Benelli G (2015a) Nanoparticles in the fight against mosquito-borne diseases: bioactivity of Bruguiera cylindrica-synthesized nanoparticles against dengue virus DEN-2 (in vitro) and its mosquito vector Aedes aegypti (Diptera: Culicidae). Parasitol Res. doi:10.1007/s00436-015-4676-8
41. Murugan K, Aamina LM, Panneerselvam C, Dinesh D, Suresh U, Subramaniam J, Madhiyazhagan P, Hwang JS, Wang L, Nicoletti M, Benelli G (2015b) Aristolochia indica green-synthesized silver nanoparticles: a sustainable control tool against the malaria vector Anopheles stephensi? Res Vet Sci. doi:10.1016/j.rvsc.2015.08.001
42. Murugan K, Benelli G, Panneerselvam C, Subramaniam J, Jeyalalitha T, Dinesh D, Nicoletti M, Hwang JS, Suresh U, Madhiyazhagan P (2015c) Cymbopogon citratus-synthesized gold nanoparticles boost the predation efficiency of copepod Mesocyclops aspericornis against malaria and dengue mosquitoes. Exp Parasitol 153:129–138
43. Murugan K, Priyanka V, Dinesh D, Madhiyazhagan P, Panneerselvam C, Subramaniam J, Suresh U, Chandramohan B, Roni M, Nicoletti M, Alarfaj AA, Higuchi A, Munusamy MA, Khater HF, Messing RH, Benelli G (2015d) Enhanced predation by Asian bullfrog tadpoles, Hoplobatrachus tigerinus, against the dengue vector Aedes aegypti in an aquatic environment treated with mosquitocidal nanoparticles. Parasitol Res. doi:10.1007/s00436-015-4582-0
44. Murugan K, Samidoss CM, Panneerselvam C, Higuchi A, Roni M, Suresh U, Chandramohan B, Subramaniam J, Madhiyazhagan P, Dinesh D, Rajaganesh R, Alarfaj AA, Nicoletti M, Kumar S, Wei H, Canale A, Mehlhorn H, Benelli G (2015e) Seaweed-synthesized silver nanoparticles: an eco-friendly tool in the fight against Plasmodium falciparum and its vector Anopheles stephensi? Parasitol Res. doi:10.1007/s00436-015-4638-1
45. Murugan K, Venus JSE, Panneerselvam C, Bedini S, Conti B, Nicoletti M, Kumar Sarkar S, Hwang JS, Subramaniam J, Madhiyazhagan P, Mahesh Kumar P, Dinesh D, Suresh U, Benelli G (2015f) Biosynthesis, mosquitocidal and antibacterial properties of Toddalia asiatica-synthesized silver nanoparticles: do they impact predation of guppy Poecilia reticulata against the filariasis mosquito Culex quinquefasciatus? Environ Sci Poll Res. doi:10.1007/s11356-015-4920-x
46. Murugan K, Sanoopa CP, Madhiyazhagan P, Dinesh D, Subramaniam J, Panneerselvam C, Roni M, Suresh U, Nicoletti M, Alarfaj AA, Munusamy MA, Higuchi A, Kumar S, Perumalsamy H, Ahn JY, Benelli G (2015g) Rapid biosynthesis of silver nanoparticles using Crotalaria verrucosa leaves against the dengue vector Aedes aegypti: what happens around? An analysis of dragonfly predatory behaviour after exposure at ultra-low doses. Nat Prod Res. doi:10.1080/14786419.2015.1074230
47. Murugan K, Benelli G, Ayyappan S, Dinesh D, Panneerselvam C, Nicoletti M, Hwang JS, Mahesh Kumar P, Subramaniam J, Suresh U (2015h) Toxicity of seaweed-synthesized silver nanoparticles against the filariasis vector Culex quinquefasciatus and its impact on predation efficiency of the cyclopoid crustacean Mesocyclops longisetus. Parasitol Res 114(6):2243–2253
48. Murugan K, Dinesh D, Jenil Kumar P, Panneerselvam C, Subramaniam J, Madhiyazhagan P, Suresh U, Nicoletti M, Alarfaj AA, Munusamy MA, Higuchi A, Mehlhorn H, Benelli G (2015i) Datura metel-synthesized silver nanoparticles magnify predation of dragonfly nymphs against the malaria vector Anopheles stephensi. Parasitol Res. doi:10.1007/s00436-015-4710-x
49. Nivedhini V, Chandran R, Parimelazhagan T (2014) Chemical composition and antioxidant activity of Cucumis dipsaceus Ehrenb. Ex Spach fruit. Int Food Res J 21(4):1465–1472
50. Padma Sree TN, Krishna Kumar S, Senthilkumar A (2007) In vitro effect of Terminalia arjuna bark extracts on antioxidant enzyme catalase. J Pharm Toxicol 2(8):698–708
51. Papp SC, Ludwig K, Roskamp M, Bottcher C, Schlecht S, Herrmann A, Haag R (2010) Inhibition of influenza virus infection by multivalent sialic-acid-functionalized gold nanoparticles. Small 6(24):2900
52. Prasad TNVKV, Elumalai EK (2011) Biofabrication of Ag nanoparticles using Moringa oleifera leaf extract and their antimicrobial activity. Asian Pac J Trop Biomed 1(6):439–443
53. Rajan R, Chandran K, Harper SL, Yun SI, Kalaichelvan PT (2015) Plant extract synthesized nanoparticles: an ongoing source of novel biocompatible materials. Ind Crop Prod 70:356–373
54. 4 nanoparticles. RSC Adv 4:13409
55. Ravikumar S, Syed Ali M, Beula M (2011) Mosquito larvicidal efficacy of seaweed extracts against dengue vector of Aedes aegypti. Asian Pac J Trop Biomed 1:S143–S146
56. Rocha OP, De Felício R, Rodrigues AHB, Ambrósio DL, Cicarelli RMB, De Albuquerque S, Young MCM, Yokoya NS, Debonsi HM (2011) Chemical profile and biological potential of non-polar fractions from Centroceras clavulatum (C. Agardh) Montagne (Ceramiales, Rhodophyta). Molecules 16(8):7105–7114
57. Roni M, Murugan K, Panneerselvam C, Subramaniam J, Nicoletti M, Madhiyazhagan P, Dinesh D, Suresh U, Khater HF, Wei H, Canale A, Alarfaj AA, Munusamy MA, Higuchi A, Benelli G (2015) Characterization and biotoxicity of Hypnea musciformis-synthesized silver nanoparticles as potential eco-friendly control tool against Aedes aegypti and Plutella xylostella. Ecotoxicol Environ Saf. doi:10.1016/j.ecoenv.2015.07.005
58. Rupiasih N, Aher A, Gosavi S, Vidyasaga PB (2013) Green synthesis of silver nanoparticles using latex extract of Thevetia peruviana: a novel approach towards poisonous plant utilization. J Phys Confer Ser 423:012032. doi:10.1088/1742-6596/423/1/012032
59. Saravanan S, Parimelazhagan T (2014) In vitro antioxidant, antimicrobial and anti-diabetic properties of polyphenols of Passiflora ligularis Juss. fruit pulp. Food Sci Human Wellness 3:56–64
60. Sathya A, Ambikapathy V (2012) Studies on the phytochemistry, antimicrobial activity and green synthesis of nanoparticles using Cassia tora L. Drug Invent Today 4:408–410
61. Sathyavathi R, Balamurali Krishna M, Venugopal Rao S, Saritha R, Narayana Rao D (2010) Biosynthesis of silver nanoparticles using Coriandrum sativum leaf extract and their application in nonlinear optics. Adv Sci Lett 3:1–6
62. Semmler M, Abdel-Ghaffar F, Al-Rasheid KAS, Mehlhorn H (2009) Nature helps: from research to products against blood sucking arthropods. Parasitol Res 105:1483–1487
63. Shankar SS, Rai A, Ahmad A, Sastry M (2004) Biosynthesis of silver and gold nanoparticles from extracts of different parts of the geranium plant. Appl Nano Sci 1:69–77
64. Singh D, Mishra M, Gupta M, Singh P, Gupta A, Nema R (2012) Nitric Oxide radical scavenging assay of bioactive compounds present in methanol Extract of Centella asiatica. Int J Pharm Pharma Sci Res 2(3):42–44
65. Sivaraman SK, Elango I, Kumar S, Santhanam V (2009) A green protocol for room temperature synthesis of silver nanoparticles in seconds. Curr Sci 3:1055–1059
66. Speshock JL, Murdock RC, Braydich-Stolle LK, Schrand AM, Hussain SM (2010) Interaction of silver nanoparticles with Tacaribe virus. J Nanobiotechnol 8:19–27
67. Sreejayan N, Rao MNA (1997) Nitric oxide scavenging by curcuminoids. J Pharm Pharmacol 49:105
68. Stuart BH (2002) Polymer analysis. John Wiley & Sons, United Kingdom
69. Sujitha V, Murugan K, Paulpandi M, Panneerselvam C, Suresh U, Roni M, Nicoletti M, Higuchi A, Madhiyazhagan P, Subramaniam J, Dinesh D, Vadivalagan C, Chandramohan B, Alarfaj AA, Munusamy MA, Barnard DR, Benelli G (2015) Green synthesized silver nanoparticles as a novel control tool against dengue virus (DEN-2) and its primary vector Aedes aegypti. Parasitol Res 114:3315–3325
70. Suresh U, Murugan K, Benelli G, Nicoletti M, Barnard DR, Panneerselvam C, Mahesh Kumar P, Subramaniam J, Dinesh D, Chandramohan B (2015) Tackling the growing threat of dengue: Phyllanthus niruri-mediated synthesis of silver nanoparticles and their mosquitocidal properties against the dengue vector Aedes aegypti (Diptera: Culicidae). Parasitol Res 114:1551–1562
71. Tarafdar JC, Sharma S, Raliya R (2013) Nanotechnology: interdisciplinary science of applications. Afr J Biotechnol 12:219–226
72. Vinayaga Moorthi P, Balasubramanian C, Mohan S (2015) An improved insecticidal activity of silver nanoparticle synthesized by using Sargassum muticum. Appl Biochem Biotechnol 175:135–140
73. WHO (2015) Dengue and severe dengue. Fact sheet N° 117, Geneva, World Health Organization