Sains Malaysiana 47(7)(2018): 1431–1438

http://dx.doi.org/10.17576/jsm-2018-4707-10

Eleusine indica Inhibits Early and Late Phases of Herpes Simplex Virus Type 1 Replication Cycle and Reduces Progeny Infectivity

(Eleusine indica Merencat Fasa Awal dan Lewat Kitar Replikasi Virus Herpes Simpleks

Jenis 1 dan Menurunkan Kebolehjangkitan Progeni)

RASHIDAH IBERAHIM¹, NOREFRINA SHAFINAZ MD. NOR¹, WAN AHMAD YAACOB²

& NAZLINA IBRAHIM¹*

¹School of Bioscience and Biotechnology, Faculty of Science and Technology

Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor Darul Ehsan, Malaysia

²School of Chemical Sciences and Food Technology, Faculty of Science and Technology

Universiti Kebangsaan Malaysia, 43600 UKM Bangi, Selangor Darul Ehsan, Malaysia

Received: 11 September 2017/Accepted: 28 February 2018

ABSTRACT

The present study was aimed at determining the compounds available in Eleusine indica methanol extract and the effects on herpes simplex virus type 1 (HHV1) replication cycle and progeny infectivity. Twelve compounds mostly from the flavonoid and phenolic groups were identified by Liquid Chromatography-Tandem Mass Spectrometry (LC-MS/MS) analysis. The effect on replication phases of HHV1 was determined by time-of-addition, time-removal and virus yield reduction assays with expression of selected genes analysed by quantitative Real Time-Polymerase Chain Reaction (qRT-PCR). The extract inhibited plaque formation the most during the first 2 h and at 24 h of infection. Plaque formation inhibition was also noted at all other time points but at lesser percentage. Treatment with E. indica reduced progeny infectivity when treated for 10 h and was dose-dependent. E. indica methanol extract inhibited immediate early, early and late phases of HHV1 replication cycle by modifying the expression of UL54, UL27 and UL30 genes during the infection. Immunostaining of infected cells confirmed that E. indica inhibited mainly Glycoproteins B but not Glycoprotein C and D. Thus, the methanol extract of E. indica has the ability to alter HHV1 replication cycle at almost all stages and reduce progeny infectivity.

Keywords: Eleusine indica methanol extract; HHV1 replication cycle; progeny infectivity

ABSTRAK

Kajian ini bertujuan menentukan sebatian yang hadir dalam ekstrak metanol Eleusine indica serta kesan terhadap kitar replikasi virus herpes simpleks jenis 1 (HHV1) dan kebolehjangkitan progeni. Dua belas sebatian yang kebanyakannya terdiri daripada kumpulan flavonoid dan fenolik telah dikenal pasti melalui analisis kromatografi cecair-beriring spektrometri jisim (LC-MS/MS). Kesan terhadap fasa replikasi HHV1 dikenal pasti melalui asai masa-penambahan, masa-penyingkiran dan penurunan bilangan virus serta penentuan pengekspresan beberapa gen terpilih melalui tindak balas rantaian polimerase-kuantitatif masa nyata (qRT-PCR). Kesan perencatan ekstrak terhadap pembentukan plak paling tinggi semasa 2 dan 24 jam selepas jangkitan. Perencatan pembentukan plak juga dikesan pada semua masa ujian tetapi pada peratusan yang lebih rendah. Rawatan dengan E. indica menurunkan kebolehjangkitan progeni selepas dirawat selama 10 jam dan tindakannya bergantung kepada dos. Ekstrak metanol E. indica merencat fasa paling awal, awal dan lewat kitar replikasi HHV1 melalui pengubahan jangkitan kepada pengekspresan gen UL54, UL27 dan UL30 semasa jangkitan. Imuno-penandaan terhadap sel terjangkit mengesahkan E. indica menindas terutamanya glikoprotein B pada sel terjangkit tetapi bukan glikoprotein C dan D. Maka, ekstrak metanol E. indica berupaya mengubah kitar replikasi HHV1 pada setiap tahap replikasi dan menurunkan kebolehjangkitan progeni.

Kata kunci: Ekstrak metanol Eleusine indica; kebolehjangkitan progeni; kitar replikasi HHV1

REFERENCES

Blaho, J.A., Morton, E.R. & Yedowitz, J.C. 2006. Herpes simplex virus: Propagation, quantification and storage. Current Protocol in Microbiology 0(1): 1-23.

Butcher, M., Raviprakash, K. & Ghosh, H.P. 1990. Acid pH-induced fusion of cells by herpes simplex virus glycoproteins. Journal of Biological Chemistry 265: 5862-5868.

Cheng, H., Yang, C.M., Lin, T.C., Shieh, D.E. & Lin, C.C. 2006. ent-epiafzelechin-(4α®8)-epiafzelechin extracted from Cassia javanica inhibits herpes simplex virus type 2 replication. Journal of Medical Microbiology 55(1): 201-206.

Ferguson, L.R., Shuo-tun, Z. & Harris, P.J. 2005. Antioxidant and antigenotoxic effects of plant cell wall hydroxycinnamic acids in cultured HT-29. Molecular Nutrition & Food Research 49(6): 585-693.

Gilbert, C., Bestman-Smith, J. & Boivin, G. 2002. Resistance of herpesviruses to antiviral drugs: Clinical impacts and molecular mechanisms. Drug Resistance Update 5: 88-114.

Honess, R.W. & Roizman, B. 1974. Regulation of herpesvirus macromolecular synthesis. I. Cascade regulation of the synthesis of three groups of viral proteins. Journal of Virology 14: 8-19.

Hou, J., Zhang, Z., Huang, Q., Yan, J., Zhang, X., Yu, X., Tan, G., Zheng, C., Xu, F. & He, S. 2017. Antiviral activity of PHA767491 against human herpes simplex virus in vitro and in vivo. BMC Infectious Diseases 17: 217.

Iberahim, R., Bahtiar, A.A. & Ibrahim, N. 2016. Anti-herpes simplex virus type-1 activity of Eleusine indica methanol extract. Malaysian Journal of Microbiology 12(6): 471-474.

Iberahim, R., Yaacob, W.A. & Ibrahim, N. 2015. Phytochemistry, cytotoxicity and antiviral activity of Eleusine indica (sambau). AIP Conference Proceedings 1678: 030013.

Kamel, M.R., Nafady, A.M., Allam, A.E., Hassanein, A.M.M. & Haggag, E.G. 2016. Phytochemical and biological study of the aerial parts of Chrozophora oblongifolia (Delile) Spreng. (Euphorbiaceae). Journal of Pharmacognosy and Phytochemical 5(4): 17-24.

Kassim, M., Achoui, M., Mustafa, M.R., Mohd, M.A. & Yusoff, K.M. 2010. Ellagic acid, phenolic acids, and flavonoids in Malaysian honey extracts demonstrate in vitro anti-inflammatory activity. Journal of Nutrition Research 30: 650-659.

Korneev, S.M. 2013. Hydrocinnamic acids: Application and strategy of synthesis. Journal of Synthesis 45(8): 1000-1015.

Kratz, J.M., Andrighetti-Frohner, C.R., Kolling, D.J., Leal, P.C., Cirne-Santos, C.C., Nunes, R.J., Trybala, E., Bergstrom, T., Frugulhetti, I.C., Barardi, C.R.M. & Simoes, C.M.O. 2008. Anti-HSV-1 and anti-HIV-1 activity of gallic acid and pentyl gallate. Memorias do Instituto Oswaldo Cruz 103(5): 437-442.

Looker, K.J., Magaret, A.S., May, M.T., Turner, K.M.E., Vickerman, P. & Gottlieb, S.L. 2015. Global and regional estimates of prevalent and incident herpes simplex virus type 1 infections in 2012. PLoS One 10(10): e0140765.

Lyu, S.Y., Rhim, J.Y. & Park, W.B. 2005. Antiherpetic activities of flavonoids against herpes simplex virus type 1 (HSV-1) and type 2 (HSV-2) in vitro. Archives of Pharmacology Research 28(11): 1293-1301.

Nakama, S., Tamaki, K., Ishikawa, C., Tadano, M. & Mori, N. 2012. Efficacy of Bidens pilosa extract against herpes simplex virus infection in vitro and in vivo, Evidence-Based Complementary and Alternative Medicine 2012. Article ID: 413453.

Piret, J. & Boivin, G. 2011. Resistance of herpes simplex viruses to nucleoside analogues: Mechanisms, prevalence, and management. Antimicrobial Agents Chemotherapy 55(2): 459-472.

Philchenkov, A.A. & Zavelevych, M.P. 2015. Rhamnazin inhibits proliferation and induces apoptosis of human jurkat leukemia cells in vitro. Ukrainian Journal of Biochemical 87(6): 122- 128.

Reardon, J.E. & Spector, T. 1989. Herpes simplex virus type 1 DNA polymerase: Mechanism of inhibition by acyclovir triphosphate. Journal of Biology and Chemistry 264: 7405- 7411.

Rice, S.A. & Knipe, D.M. 1990. Genetic evidence for two distinct transactivation functions of the herpes simplex virus a protein ICP27. Journal of Virology 64: 1704-1715.

Roizman, B., Knipe, D.M. & Whitley, R.J. 2006. Herpes Simplex Viruses, 5th ed. Philadelphia: Lippincott Williams & Wilkins. pp. 2501-2601.

Rungsimakan, S. 2011. Phytochemical and biological activity studies on Salvia viridis L. PhD Thesis, University of Bath (Unpublished).

Saddi, M., Sanna, A., Cottiglia, F., Chisu, L., Casu, L., Bonsignore, L. & De Logu, A. 2007. Antiherpevirus activity of Artemisia arborescens essential oil and inhibition of lateral diffusion in Vero cells. Annals of Clinical Microbiology and Antimicrobials 6: 10-17.

Sagnia, B., Fedell, D., Casetti, R., Montesano, C. & Faldoni, G. 2014. Antioxidant and anti-inflammatory activities of extracts from Cassia alata, Eleusine indica, Eremomastax speciosa, Carica papaya and Polyscias fulva medicinal plants collected in Cameroon. PLoS One 9: 1-10.

Sydiskis, R.J., Owen, D.G., Lohr, J.L., Rosler, K.H.A. & Blomster, R.N. 1991. Inactivation of enveloped viruses by anthraquinones extracted from plants. Antimicrobial Agents and Chemotherapy 35(12): 2463-2466.

Shukla, D. & Spear, P.G. 2001. Herpesviruses and hepa- ran sulfate: An intimate relationship in aid of viral entry. Journal of Clinical Investigation 108(4): 503-510.

Spear, P.G. & Longnecker, R. 2003. Herpes virus entry: An update. Journal of Virology 77: 10179-10185.

Tahir, M.M., Ibrahim, N. & Yaacob, W.A., 2014. Cytotoxicity and antiviral activities of Asplenium nidus, Phaleria macrocarpa and Eleusine indica. AIP Conference Proceedings 1614: 549-552.

Turner, A., Bruun, B., Minson, T. & Browne, H. 1998. Glycoprotein gB, gD gH and gL of herpes simplex virus type 1 are necessary and sufficient to mediate membrane fusion in a Cos cell transfection system. Journal of Virology 72(1): 873-875.

Taheri Rouhi, S.Z., Sarker, M.M.R., Rahmat, A., Alkahtani, S.A. & Othman, F. 2017. The effect of pomegranate fresh juice versus pomegranate seed powder on metabolic indices, lipid profile, inflammatory biomarkers and the histopathology of pancreatic islets of Langerhans in Streptozotocin-nicotinamide induced type 2 Diabetic Sprague-Dawley rats. BMC Complementary and Alternative Medicine 17(1): 156-163.

Uprichard, S.L. & Knipe, D.M. 1996. Herpes simplex ICP27 mutant viruses exhibit reduced expression of specific DNA replication genes. Journal of Virology 70(3): 1969-1980.

Wagner, E.K., Hewlett, M.J., Bloom, D.C. & Camerini, D. 2010. Replication of some nuclear-replicating eukaryotic DNA viruses with large genomes. In Basic Virology edited by Wagner, E.K., Hewlett, M.J., Bloom, D.C. & Camerini, D. Massachusetts: Blackwell Publishing. pp. 331-343.

Zhen, H., Fang, F., Ye, D.Y., Shu, S.N., Zhou, Y.F., Dong, Y.S., Nie, X.C. & Li, G. 2006. Experimental study on the action of allitridin against human cytomegalovirus in vitro: Inhibitory effects on immediate-early genes. Antiviral Research 72: 68-74.

*Corresponding author; email: nazlina@ukm.edu.my