Plant as a Source of Natural Antiviral Agents
Muhammad Nouman Sohail,
Idress Hamad Attitalla
Viruses are one of the main hazards for both humans and animals. They enter in the living body and redirect bodys metabolism to produce large copies of their genome and proteins. Diseases caused by these viruses are difficult to tackle with the help of currently available antiviral drugs. So the aim of this study was to explore the plants with reported antiviral activity, to get understanding for better control of these viruses. Herpes virus, Human Immunodeficiency Virus (HIV), influenza and hepatitis virus were at top among all studied viruses. Prominent modes of action against these viruses were inhibition of viral entry and its replication in host cell. Against RNA viruses plants mainly targeted their Reverse Transcriptase (RT) enzyme (like HIV) or protease (mostly found against hepatitis C virus). A range of active compounds have been identified which could be the potential antiviral agents for future drug development. Some plants like Allium sativum, Daucus maritimus, Helichrysum aureonitens, Pterocaulon sphacelatum and Quillaja saponaria emerged to have broad spectrum antiviral activity. Detail study of their phytochemicals and mode of action against these viruses could be help full for more effective control of hazardous viruses.
Virus "a piece of bad news wrapped in a protein coat" has been defined by Peter
Medawar (Oldstone, 1993). It appears as the perfect
definition after considering the list of top ten causes of death in low, middle
and high income countries. Lower respiratory infections, diarrhoeal diseases
and HIV/AIDS are the common death causes among low and middle income countries
(WHO, 2011b). All of these three health disorders are
directly or indirectly caused by viruses. Except lower respiratory infections
none of the above mentioned factors are prevalent among high income countries.
It clearly indicates that how severely these viral diseases are affecting the
people health in low and middle income/developing countries.
Our planet contains nearly 1031 viruses and their ubiquity also
invaded the marine environment, where in every 200 liter of water nearly 5000
viral genotypes are present (Breitbart and Rohwer, 2005;
Suttle, 2005). Moreover viruses are moving between the
environments and they are present almost everywhere e.g. deep sea, polar ice,
alkaline, hot and saline waters and more than 2000 m deep in terrestrial environment.
There are almost 20 families of viruses that actually infect humans (Harvey
et al., 2006) and some of them also cause diseases in animals (Mahzounieh
et al., 2006). The diseases they cause in human include chickenpox,
influenza, skin rash, hepatitis, bronchiolitis, acquired immunodeficiency syndrome,
liver infection and many others. Virus particles enter in the living system
and if they overwhelm the bodys immune system then it is almost impossible
to stop their spread in body. They direct the host metabolic pathway for the
sake of their repeated replication; this makes their treatment difficult. But
fortunately, it is now well known that viruses are unique in their mode of replication,
which can be easily targeted (Selisko et al., 2007;
Syed et al., 2010). They use specific enzymes
to infect and replicate, whose inhibition could arrest their metabolism. For
example, the proteolytic enzyme promotes virus maturation by separating the
viral polyprotein precursor, whose inhibition will stop its maturation (Wapling
et al., 2007). So the virus metabolism or replication can be stopped
by specific inhibitors.
Today many synthetic antiviral drugs e.g. moroxydine, ganciclovir, valganciclovir,
valaciclovir etc. are used, which inhibit the virus replication via different
mechanisms (Biron, 2006; Czeizel
et al., 2006). But difficulty in drug treatment arises due to their
low efficiencies, cytotoxicity and development of viral resistance against them.
Another antiviral treatment; vaccination, can be applied but they are still
under development, as they often provide incomplete protection against virus
and their reliability needs more research (Pervez, 2000b;
Subbarao and Joseph, 2007). Thus the treatment through
antiviral synthetic drugs and vaccines need more scientific investigation. Nature
provides another, more reliable source of antiviral agents; viz. plants phytochemicals;
almost 40% of currently available drugs are direct or indirect derivatives of
plants. A number of ethnobotanical studies aiming to identify potential therapeutic
plants for more effective control of health issues demonstrate the importance
of plant species in health care system (Shinwari and Khan,
2000; Heneidy and Bidak, 2004; Appidi
et al., 2008; Ky et al., 2009; Ansari
and Inamdar, 2010; Makambila-Koubemba et al.,
2011). Plants are rich source of phytochemicals like alkaloids, anthocyanins,
carotenoids, flavonoids, isoflavones, lignans, monoterpenes, organosulfides,
phenolic acids, saponins and many more (Al-Yahya, 2005;
Hassan et al., 2006; Anitha
and Ranjitha Kumari, 2006; Akomo et al., 2009;
Rahman et al., 2009; Amabeoku
and Kinyua, 2010; Ndjonka et al., 2010).
These phytochemicals have been proved to be responsible for their antimicrobial
(Sampathkumar et al., 2008; Krishnan
et al., 2010), antihypertensive (Amalia et
al., 2008), anti-diabetic (Qureshi et al.,
2009), antioxidant (Momtaz and Abdollahi, 2010),
hepatoprotective (Mahalakshmi et al., 2010; Ansari
et al., 2011), cardioprotective (Ojha et al.,
2008; Fard et al., 2008) and other therapeutic
activities. Thus this study is aimed to analyze the previously reported antiviral
plants and identify potential mode of action and compounds that are responsible
for their antiviral activity. Better understanding of natural antiviral agents
mode of action and identification of responsible compounds will be helpful to
provide a new insight for the development of new antiviral drugs for more effective
Basic viral structure and its mode of action: Viruses are organic objects,
which are metabolically inactive outside the host body but become active on
their entry into the host cell (Dupre and O'Malley, 2009).
These are mainly composed of proteins and nucleic acid; the proteins majorly
contribute to their specific shape and form a coat called capsid (Andersson,
2010). Thus viruses are of various shapes e.g. simple, helical, icosahedral
or complex and some viruses are surrounded by a lipid bilayer, derived from
host membrane, which is called as envelope (Geng et al.,
2007; Raja et al., 2003). Some capsid proteins
are also associated with virus nucleic acid and called as nucleocapsid, while
nucleic acid proteins, are the direct part of the nucleic acid, known as nucleoproteins.
The nucleic acid of virus is either made up of DNA or RNA, is the basic source
of information required for the regulation of its metabolic activities. Theses
DNA and RNA can be further divided into two types depending upon the number
of strands i.e. single stranded or double stranded DNA/RNA (Firth
et al., 2010; Pichlmair et al., 2006).
The single stranded RNA viruses can be further distinguished depending upon
the sense of strand as some RNA viruses have positive-sense RNA (+VE ssRNA)
and some viruses have negative-sense RNA (-VE ssRNA) (Gorbalenya
et al., 2006). The shape of nucleic acid (DNA/RNA) is also an important
source of differentiation, because all the viruses did not contain same-shape
nucleic acid (Gao and Hu, 2007). It can be either in
circular, linear or coiled form.
Virus (either DNA or RNA) life cycle can be divided into some predefined stages;
adhesion, adsorption (entry), replication, maturation and release, which involve
some enzymes and proteins. For example, the process of virus entry is carried
out by cell surface proteins; HCV entry involves claudin-1, occludin, tetraspanin
as main receptors proteins (Burlone and Budkowska, 2009).
Its entry is also mediated by some other lipoproteins and an enzyme; lipoprotein
lipase. On the other hand the influenza virus infection is mediated by protease
enzyme, which activates the viral surface protein haemagglutinin (Zambon,
2001). The protease enzyme is also important in the expression of viral
proteins; it splits the proteins into groups depending upon their structural
and nonstructural functions (Appel et al., 2006).
But the RNA viruses need two additional enzymes for their survival; reverse
transcriptase and integrase, former transcribes the viral RNA into DNA at the
time of replication (Briones et al., 2010; Sluis-Cremer
and Tachedjian, 2008). While the second enzyme is used to incorporate the
viral DNA into host genome, furthermore it is also needed for proper uncoating
of virus core proteins. Thus virus is needy of enzymatic and non-enzymatic proteins,
which can be targeted to stop their replication and infection.
Antiviral plants: In this review a total of 105 plant species have been
identified that were reported for their potential antiviral activities (Fig.
1). Maximum number of plants were reported for their activity against
herpes viruses, indicating that herpes viruses were the highly studied viruses
with respect to antiviral plants. After herpes virus, HIV, influenza and hepatitis
were among other viruses that were addressed in most of the studies in order
to discover the plant with antiviral properties. In next sections a brief description
with respect to the available antiviral plants against some important viruses
has been provided.
Plants with antiviral activity against herpes virus: An enveloped double
stranded DNA virus with linear genome; it belongs to the family Herpesviridae,
which is recently reclassified to separate the mammals virus from other
non-mammalian viruses (Davison et al., 2009).
It is also known as human herpesvirus and Varicella-zoster virus.
||Mostly studied viruses found during current review
It is highly infectious and prevalent disease especially in developing countries
with almost 50 % prevalence in adults, disease symptoms are often unnoticeable
(WHO, 2001). It is a sexually transmitted disease and
highly prevalent in females as they often get infected with it before the age
of fertility (Ziyaeyan et al., 2007). It also
causes febrile rash and graft-versus-host disease in humans, who got hematopoietic
stem cell transplantation (Pichereau et al., 2011).
It is also the casual agent of genital herpes disease; vaccines against it are
currently under developmental stages (Soleimanjahi et
Total 57 plants were identified with antiviral activity against herpes virus
(Table 1). Binns et al.
(2002) reported that h-hexane extracts of Echinacea purpurea showed
in vitro antiviral activity against herpes virus in another study polysaccharide
and cichoric acid were found among the active phytochemicals of various plant
parts extracts (Vimalanathan et al., 2005). Another
compound of Phyllanthus urinaria from its acetone extract (hippomanin
A) showed its activity against herpes simplex virus type 2 (Yang
et al., 2007); in another study Cheng et al.
(2011) identifies a compound (excoecarianin) from this herb with same activity.
Anthraquinones has been identified as potential compound responsible for antiviral
properties of Rhamnus frangula, Rhamnus purshianus and Rheum
officinale (Sydiskia et al., 1991). This organic
compound has also been reported in many studies to be responsible for positive
health attributes of many medicinal plants (Kumar et
al., 2007; Hussein et al., 2010; Karou
et al., 2011; Mbaya and Ibrahim, 2011; Sonibare
et al., 2011). Kurokawa et al. (1999)
reported the antiviral activity of Rhus javanica against herpes virus
and found moronic acid as potential active agent from its herbal extract. Plants
mainly showed activities like restriction of entry host into cell (Weber
et al., 1992; Zandi et al., 2007),
reduced viral replication (Duarte et al., 2001;
Chiang et al., 2003; Alche
et al., 2003) and partial destruction of viral envelope (Sydiskia
et al., 1991). Active compound present in most of the plants were
anthraquinones, terpenes, quercetin, lectins and phenolics (Amoros
et al., 1987; Sydiskia et al., 1991;
Chiang et al., 2003; Ooi et
al., 2004; Kan et al., 2009). Allium
sativum is a medicinal plant with a lot of health benefits (Ishtiaq
et al., 2007; Sukandar et al., 2010;
Abdelaziz and Kandeel, 2011; Weber
et al., 1992) found its extract effective against this virus. The
extract of Aloe vera another important medicinal plant (Alqasoumi
et al., 2008; Semalty et al., 2010)
has been reported to be effective against this virus by inhibiting the viral
entry and replication into the host cell(Zandi et al.,
Plants with antiviral activity against HIV: HIV is highly infectious
enveloped virus of family Retroviridae; it has liner ssRNA positive sense genome
and cause high morbidity. During year 2004, HIV infection was one of the leading
factors responsible for almost 2.65 million deaths in low income countries (Patton
et al., 2009). It is also prevalent in high income countries, as
in United States almost 55400 new HIV cases were observed each year from 2003-06
(Hall et al., 2008). It increases the chances
of bacteria and other viruses infections, which poorly effects the health; transmission
of HIV from mother to child could lead to the death (Corbett
et al., 2003; Ahasan et al., 2004;
Ilboudo et al., 2007; Abongo
et al., 2008). Its chemo-treatments are scarce, because of their
potential side effects on human body, non-significant efficiencies and increased
divergence in HIV genome (Fokunang et al., 2006;
Jaffary et al., 2007; Kagone
et al., 2011). But a nutrient rich food can reduce the HIV caused
decreased weight and help in improving the patients health (Oguntibeju
et al., 2007).
In present study 26 plant species were found effective against HIV. Terpenoids,
lectins, alkaloids and flavonoids were common among the active compound of these
plants (Table 2). Roja and Heble
(1995) reported the positive activity of an alkaloid (castanospermine) isolated
from seeds of Castanospermum austral against this virus.
||Detail description of studies focusing on antiviral plant
activities against herpes virus
|n/a: Not available
||Detail description of studies focusing on antiviral plant
activities against HIV
|n/a = Not available
Wang and Ng (2001) reported that gossypol and alkaloids
of Corydalis yanhusuo might be responsible for it inhibitory activity
on HIV virus. Ethanolic extract of Monotes africanus, which is a rich
source of various flavonoids has been reported for its antiviral activity against
HIV (Meragelman et al., 2001; Reutrakul
et al., 2007). Most of the plants mainly affect the Reverse Trancriptase
(RT) activity or penetration of virus particles into host cell. Calanolides
which exhibits potential RT inhibitory activity have been found in the hexane
extract of Calophyllum brasiliense leaves (Cesar
et al., 2011). The hexane extract of this plant was found to have
inhibitory effect on RT enzyme of HIV. Lectins derived from Phaseolus vulgaris
are reported for their potential inhibitory effect on HIV RT activity (Ye
et al., 2001; Fang et al., 2010).
Another seed protein isolated from Vigna unguiculata possesses the same
effect on RT activity in addition to inhibitory effect on glycohydrolases α-
and β-glucosidases (Ye et al., 2000; Ye
and Ng, 2001). Oh et al. (2011) reported
that aqueous extract of Prunella vulgaris interferes with the viron post
binding events. Extract of Rhizophora mucronata and Rhizophora apiculata
(a rich source of polysaccharides) blocks the viral binding to the cell surface
(Premanathan et al., 1999a; Premanathan
et al., 1999b). In another study Lee-Huang et
al. (1995) studied the effect of a protein isolated from Gelonium
multiflorum and found that it reduces the virus replication by inhibiting
the integration of viral DNA into host genome. Panax ginseng, which is
also effective against cardiovascular diseases (Jun et
al., 2007) has been reported to be effective against HIV by inhibiting
the RT activity (Ng and Wang, 2001). Ricinus communis
an important medicinal plant (Onwuliri and Anekwe, 2001)
showed inhibitory effect on RT and N-glycohydrolases of HIV (Wang
and Ng, 2001). Another plant Terminalia chebula, which has been proven
to have many beneficial medicinal properties (Gupta et
al., 2008a, b; Shinde et
al., 2009; Anam et al., 2009) posses
significant anti-HIV activity (Lee et al., 2011).
Its methanolic extract showed antiviral activity against HIV when tested on
virus infected baby hamster kidney cells.
Plants with antiviral activity against influenza virus: It is a single
stranded RNA virus with negative sense linear fragmented genome enclosed in
a capsid, it belongs to family Orthomyxoviridae and infects both mammals and
birds. It has seasonal epidemiology and mainly spread through air when the environment
is dry and cold (Lowen et al., 2007). The hospitalization
and death rate associated with influenza vary with the age and type of virus,
as influenza virus A-caused infection rate is higher than type-B (Thompson
et al., 2004). Influenza virus, especially of avian origin is highly
virulent disease causing agent in humans and birds; it has long history, put
huge burden on human health since 1580 (Farooq et al.,
2006; Lazzari and Stohr, 2004). It is responsible
for deaths of millions of people; its pandemic nature is due to its variable
strains which develop via the reassortment of genetic information. Thus the
development of vaccine against it is difficult both in humans and birds.
Sixteen plants were identified which showed antiviral activity against influenza
virus. Anthocyanin and polyphenols were among the commonly found active phytochemicals
in these plants (Table 3). Camellia sinensis
is an important herbal plant having significant antioxidant, photochemoprotective,
hyperglycemic, antibacterial and many other beneficial heath benefits (Adiloglu
and Adiloglu, 2006; Bakar et al., 2006; Shokrzadeh
et al., 2006; Hassani et al., 2008;
Mohamed and Metwally, 2009; Amutha
et al., 2010; Chakraborty and Chakraborti, 2010;
Kaur and Saraf, 2011; Obaid et
al., 2011). Catechin derivatives obtained from the tea of this plant
showed significant inhibitory effect on influenza strains (Song
et al., 2005).
||Detail description of studies focusing on antiviral plant
activities against influenza virus
|n/a = Not available
Ehrhardt et al. (2007) found that Cistus
incanus possess the antiviral activity by modulating the viral surface in
order to inhibit its entry into Madin-Darby Canine Kidney (MDCK) cells. Inhibitory
effect against influenza virus has also been reported in human patients (Kalus
et al., 2009). Another herb Echinacea purpurea also restrict
the viral entry by inhibiting the binding of viral receptors to the host cells
surface (Pleschka et al., 2009). Geranium
sanguineum, a rich source of polyphenols showed antiviral activity by effecting
the expression of viral proteins on cell surface (Serkedjieva,
1996; Sokmen et al., 2005). A lectin isolated
from bulbs of Narcissus tazetta showed significant antiviral activity
against various strains of influenza virus (Ooi et al.,
2010). In another study Ooi et al., 2004)
reported the anti-influenza activity of a lectin isolated from saline extract
of Pandanus amaryllifolius leaves. Scutellaria baicalensis an
important medicinal plant (Yeh et al., 2010)
possess a compound (isoscutellarein-8-methylether) which is thought to be responsible
for it antiviral activity against influenza virus (Nagai
et al., 1995).
Plants with antiviral activity against Hepatitis C Virus (HCV): Hepatitis
C is an enveloped virus with +VE single stranded linear RNA, which belongs to
the family Flaviviridae. It cause mild-chronic liver disease infecting more
than three million people each year, which results in almost 350 000 deaths
(WHO, 2011a). It has worldwide spread with 4.8% infection
rate in Pakistan. It is a global problem nearly affecting 130 million people;
moreover, alone it is responsible for about 27% of cirrhosis and almost 25%
of worlds hepatocellular carcinoma (Alter, 2007).
Its high spread is attributed to poor moral and health conditions, use of drugs,
alcohol and contaminated syringes (Roshandel et al.,
2007; Zakizad et al., 2009). It is detectable
through serum proteins and blood analysis; its chemotherapeutic treatment is
difficult but can be treated through herbal products (Ansari
et al., 2011; Joseph and Raj, 2011; Pervez,
2000a; Moundipa et al., 2007; Tabassum
et al., 2000).
In current study six plants have been identified with proved antiviral activity
against HCV. Mainly plant showed inhibitory effect on HCV protease. Hussein
et al. (2000) reported the inhibitory effect of Trachyspermum
ammi and Embelia schimper methanol extract on HCV protease. Solanum
nigrum which also exhibits hepatoprotective activity (Subash
et al., 2011) has also been reported to have inhibitory effect on
HCV (Javed et al., 2011). Cannabis a commonly used
drug (Richardson, 2010) is a phytochemical of Cannabis
sativa a medicinal plant with many beneficial health effects (Arshad
and Khan, 2000; Qureshi et al., 2001; Tehranipour
and Ebrahimpour, 2009). Acacia nilotica has remained the focus of
many studies for its multipurpose applications (Shirazi et
al., 2001; Banerjee et al., 2004; Ghosh
et al., 2004; Elkhalifa et al., 2005;
Emtehani and Tabari, 2007) its acetonic and methanolic
extracts have sown anti-HCV effect on liver cells (Rehman
et al., 2011). Sylvestre et al. (2006)
reported the anti-HCV activity of cannabis in human patients. Mainly these plants
showed their activity against HCV by targeting its protease (Table
Plants with antiviral activity against respiratory syncytial virus:
It belongs to the family Paramyxoviridae and is single stranded RNA virus, which
is enclosed in an envelope. It is a highly prevalent virus throughout the world
with large variation in its genome (Trento et al.,
2010). It cause bronchiolitis and other respiratory problems and is a major
cause of lower respiratory tract infections; it mostly infects the children
under age of six months and also responsible for asthma problems (Mohapatra
and Boyapalle, 2008). It causes an infection in 3-7% of healthy adults and
4-7% in the non-healthy adults, who already suffers from lung and heart diseases
(Falsey et al., 2005).
||Detail description of studies focusing on antiviral plant
activities against hepatitis, respiratory syncytial virus and vesicular
|n/a: Not available
Moreover it cause burden on population equal to that of influenza A virus,
as the patients needs more health facilities and care. Ma
et al. (2001) found that ethanol extract of Selaginella sinensis
possess significant activity against respiratory syncytial virus. They further
elaborated that this activity of plant could be due to the presence of a biflavonoid
(amentoflavone) in its plant extract. A lectin isolated from Narcissus tazetta
also showed antiviral activity against this virus (Ooi et
al., 2010). Li et al. (2005) reported
the Schefflera heptaphylla antiviral activity against respiratory syncytial
virus and concluded that this activity was due to the inhibition of fusion of
viral particles to the host cell.
Plant with broad spectrum antiviral activity: Based on the data presented
in Table 1-5 plant with broad spectrum
antiviral activity (plants reported for their antiviral activity against two
or more than two viruses) were identified. Total 24 plants were found that were
resistant to two or more than two viruses (Fig. 2).
Two plant species showed antiviral activity against four viruses.
||Plant with broad spectrum antiviral activity
||Detail description of studies addressing rarely studied viruses
|n/a = Not available
Allium sativum showed resistance against Herpes virus, Parainfluenza
virus-3, Rhinovirus and Vesicular stomatitis virus. Daucus maritimus
has been reported for its activity against Dengue virus, Hepatitis C virus,
HIV and West Nile virus. Helichrysum aureonitens, Pterocaulon sphacelatum
and Quillaja saponaria have been reported for their antiviral activity
against three viruses each. As shown in figure 2 Helichrysum
aureonitens is effective against Coxsackievirus, Herpes virus and Reovirus.
Pterocaulon sphacelatum showed antiviral activity against Herpes virus,
Picornavirus and Polio virus. Quillaja saponaria has been reported for
its activity against Herpes virus, HIV and Reovirus. Almost all plants with
broad spectrum activity were effective against herpes viruses. Moreover five
plants which were effective against Herpes virus, also showed antiviral activity
against Influenza virus. In the same way three plant species showed resistance
against both Herpes virus and Vesicular stomatitis virus.
Majority of the studied viruses belongs to the Flaviviridae, Herpesviridae and Picornaviridae family. A large number of plants are available in nature which could act as a source of lead antiviral compounds. Mainly these plants target the enzymes that are involved in replication and integration of virus into host cell. In case of DNA viruses restricted entry of viral particles into host cell or inhibition of viral replication into the host cells were most frequent mode of actions. Destruction of viral envelop was also one of the identified mode of action against DNA viruses. RT plays a significant role in replication of RNA viruses and most of the plants restrict the activity of RT enzyme of virus. In order to design effective drugs against viruses their enzymes that are involved in the key metabolic activities (integration, replication) should be focused. A lot of plant population with possible potential is still uncovered as few plants have been studied in detail in order to identify the active phytochemicals against these viruses. More detailed studies in future will help not only to identify the potential antiviral compounds but also in better understanding of their mode of action for more effective control of these lethal viruses.
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