Chemical constituents and biological activities of species of Justicia: a review

Chemical constituents and biological activities of species of Justicia - a review

Geone M. Corrêa^{I, II}; Antônio F. de C. Alcântara^I

^IDepartamento de Química, ICEx, Universidade Federal de Minas Gerais, Brazil

^IIInstituto de Ciências Exatas e Tecnologia, Universidade Federal do Amazonas, Brazil

^{Correspondence}

ABSTRACT

The Acanthaceae family is an important source of therapeutic drugs, and the ethnopharmacological knowledge of this family requires urgent documentation as several of its species are near extinction. Justicia is the largest genus of Acanthaceae, with approximately 600 species. The present work provides a review addressing the chemistry and pharmacology of the genus Justicia. In addition, the biological activities of compounds isolated from the genus are also covered. The chemical and pharmacological information in the present work may inspire new biomedical applications for the species of Justicia, considering atom economy, the synthesis of environmentally benign products without producing toxic by-products, the use of renewable sources of raw materials, and the search for processes with maximal efficiency of energy.

Keywords: Acanthaceae, biological activity, Justicia, lignans, medicinal plants

Introduction

The Acanthaceae family, order Scrophulariales, superorder Lamiiflorae (sensu Dahlgren), comprises almost 250 genera with 2500 species. Its species are widespread in tropical regions of the world (Wasshausen & Wood, 2004) and are poorly represented in temperate regions (Mabberley, 1997). Justicia is the largest genus of Acanthaceae, with approximately 600 species that are found in pantropical and tropical regions (Durkee, 1986).

The species of Justicia are described as erect or scandent perennial herbs or subshrubs. Leaves present cystoliths and are petiolate with a leaf margin that is usually entire. Inflorescences are in spikes or panicles cimas, and the species rarely has solitary, terminal, or axillary flowers. The bracts and bracteoles are usually conspicuous and imbricate. The species of Justicia can be easily recognized by their bilabial corolla, with a posterior lip that is generally two-lobed, an anterior lip that is three-lobed, two stamens, a capsule with four seeds, and a basal sterile portion (Graham, 1990; Braz et al, 2002).

Table 1 shows the vegetal species of the genus Justicia with previous chemical and/or biological studies, indicating their botanical synonymy, popular name, and geographical distribution. Few species of Justicia have been studied (36 species of approximately 600 cataloged species), with fifteen species found in the Americas, thirteen species in Asia, and eight species in Africa. Among the studied species, 31 species have ethnopharmacological/pharmacological information, 23 species were chemically investigated, and only eighteen species were chemically and biologically studied, mainly in the last decade. The most studied species are Justicia pectoralis Jacq., Justicia procumbens L., Justicia gendarussa Burm. f., and Justicia anselliana (Nees) T. Anderson. Consequently, the phytochemical and biological potential of other species of Justicia have yet to be fully explored.

Material and Methods

An extensive search in original and review articles was carried out in this work. The keywords used for this review were Justicia, Acanhaceae and Medicinal Plants. The search was performed accessing SciFinder, ScienceDirect, Web of Science, and Scielo web sites, updated to May 2011. From the literature search, all plants/herbal of Justicia preparations that are used ethnomedically were included in this review. More than 90% of the references obtained were later consulted.

Ethnopharmacological information for the species of Justicia

Several species of Justicia are widely used in folk medicine (as shown in Table 2) for the treatment of respiratory and gastrointestinal diseases (thirteen and ten occurrences, respectively) as well as inflammation (ten occurrences, including applications in rheumatism and arthritis). The plants are also utilized for their effects on the central nervous system as hallucinogens, somniferous agents, sedatives, depressors, and treatments for epilepsy and other mental disorders, with eleven occurrences. Other species are popularly used in the treatment of headache and fever (eight occurrences, which may be associated with their sedative and analgesic properties), cancer (seven occurrences), diabetes (three occurrences), and HIV (two occurrences).

Whole plant and aerial parts are usually used in folk medicine. Extracts made from only the leaves are the most used (nineteen occurrences), followed by those extracts made from only the roots (five occurrences). Some species are used as mixtures (three occurrences). For example, traditional physicians around Kotagiri village near Ootacamund use a mixture of the powdered roots of Cassia occidentalis L., Caesalpineae, Derris brevipes var. coriacea, Papillionaceae, and Justicia simplex D. Don, Acanthaceae, to control fertility. Administration of this mixture for a few days after menstruation prevents conception without any toxic effects. The number of pregnancies among treated women was significantly less than that of the control group. These results indicate the abortifacient nature of the roots of these plants (Badami et al., 2003). The species Justicia pectoralis Jacq. is used as the major component in a mixture to treat various diseases. Moreover, Justicia insularis T. Anderson is used as an infusion mixed with the leaves of Ambrosia maritime L., Compositae.

Pharmacological tests of species of Justicia

Table 3 shows the pharmacological activities of the species of Justicia described in the literature. Some species show antitumoral activity against different cancer cell lines (seven occurrences). An ethanol extract of Justicia neesii Ramamoorthy (Acanthaceae) exhibited anticancer activity against P388 lymphocytic leukemia in mice. A methanol extract of the whole plant of Justicia procumbens L. showed significant inhibitory activity in vivo against P-388 lymphocytic leukemia growth and in vitro cytotoxicity in the 9-KB (human nasopharyngeal carcinoma) cell culture assay (Chen et al., 1995). Some species also showed inhibition of human cancer cell lines, mainly toward human cervical carcinoma (Justicia ciliata Jaqc.), T 47D and HeLa human cell lines (Justicia spicigera Schltdl.), and human ovarian cancer cell line (Justicia rhodoptera Baker), as well as prevention of some tumoral cell growth (Justicia patentiflora Hemsl.). The activity of popularly used whole-plant extracts of J. procumbens and J. nesii and leaf extracts of J. specigera as anticancer agents (Table 2) was confirmed by employing the same parts of the plant, as seen in Table 3. However, the anticancer properties of Justicia adhatoda L. have not yet been confirmed pharmacologically.

The whole-plant extract of J. spicigera contains cytotoxic factors for leukemic cells and has no proliferative activity on normal hematopoietic progenitor cells. The plant extract induces apoptosis in the human leukemia cell line TF-1, but not in the bcl-2 transfectant cell line TB-1. These data suggest a strong correlation between the cytotoxic effect and cell proliferation. The results indicate that the infusion of the aerial parts of J. spicigera does not contain any hematopoietic activity, induces apoptosis inhibited by bcl-2, and is linked to cell proliferation.

Some species show antiviral activity (five occurrences, i.e., Justicia extensa T. Anderson, Justicia gendarussa Burm. f., J. procumbens, Justicia reptans Sw., and Justicia valida Ridl.) against in vitro HIV type 1 reverse transcriptase, HIV replication, and vesicular stomatitis virus (Table 3). However, the species popularly used as antiviral agents, Justicia betonica L. and Justicia flava (Vahl) Vahl (see Table 2), were either not included in pharmacological studies, or were tested but did not show antiviral activity. Crude water extracts of the aerial parts of J. gendarussa proved to be strongly active against in vitro HIV type 1 reverse transcriptase (as shown in Table 3). Based on these observations, this species might be further explored for its antiviral indications.

J. pectoralis showed high antibacterial activity against E. coli, E. faecalis, and S. epidermidis. Moreover, this species shows positive antimosquito tests, which were observed on the growth and development of IV-stage larvae of Aedes aegypti mosquitoes. A brief exposure to concentrations of 0.05 to 0.50 mg/mL of the plant extract is required to produce 100% larvicidal activity. The extracts of J. pectoralis were found to be the most toxic larvicide among the species of Justicia extracts tested. Extracts of J. pectoralis have estrogenic, progestagenic, and anti-inflammatory effects, explaining the plant's traditional use in menopause and PMS therapies.

The methanol extract of the whole plant of J. procumbens exhibited 50% inhibitory activity toward the arachidonic acid-induced aggregation of rabbit platelets (Chen et al., 1995; Chen et al., 1996). The antiplatelet aggregation activity can be related to the popular use of extracts obtained from Justicia anselliana (Nees) T. Anderson in the treatment of heart disease (Table 2).

The ethanol extract of the leaves of J. gendarussa showed a higher paw edema inhibition than aspirin-treated rats in the FCA-induced and the collagen-induced arthritic models (Table 3). These pharmacological results align with the popular use of J. gendarussa in the treatment of arthritis and rheumatism (see Table 2). The species J. spicigera is popularly used as an anti-inflammatory agent (Table 2), and this activity was also pharmacologically confirmed (see Table 3).

The popular use of J. pectoralis in the treatment of epilepsy and anxiety (as shown in Table 2) was confirmed with the ethanol extract of the leaves (Table 3). The ethanol extracts of J. pectoralis, Justicia aurea Schltdl., and Justicia albobracteata Leonard were tested in vitro for their ability to inhibit GABA- transaminase (GABA-T) or to bind to the GABAA-benzodiazepine receptor, two principal drug targets in epilepsy and anxiety. A significant positive correlation between GABA-T inhibition and the relative frequency of use for epilepsy was observed. Moreover, an even stronger correlation between GABAA binding and the relative frequency of use for shock was observed. Thus the Q'eqchi' traditional knowledge of J. pectoralis, J. aurea, and J. albobracteata is associated with the plant's antiepileptic and anxiolytic activities.

The pharmacological studies of some species were not based on their use in folk medicine. Extracts of the whole plant of Justicia prostrata Gamble showed antiulcer activity (Table 3). The aqueous extract was more active than the alcoholic extract when tests were made using the aspirin-induced pylorus ligated rat model. The antiulcerogenic activities of both extracts were compared with the drug Rantidine, an H2-receptor antagonist. Alcoholic extracts of J. anselliana showed allelopathic properties (Table 3). The aerial part of the plant produced more significant effects on the growth parameters of the cowpea plant (Vigna unguiculata (L.) Walp., Leguminosae), such as germination, elongation, and the weight, than extracts of the root (Ahanchede et al., 2004). Likewise, the popular use of the leaves of Justicia schimperiana (Hochst. ex Nees) T. Anderson in the treatment of liver disease (Table 2) may be related to the hepatoprotective activity of the leaf extracts of the plant (Table 3). However, the hepatoprotective activity of J. adhatoda (Table 3) was not studied despide its popular use. In addition, some other species, such as J. betonica, Justicia calycina (Nees) V.A.W.Graham, Justicia diffusa Willd., Justicia dumetorum Morong, J. flava, Justicia ghiesbreghtiana Lem., Justicia ideogenes, J. insularis, Justicia plectrantus, Justicia purpurea L., Justicia secunda Vahl, Justicia sericea Ruiz & Pav., and J. simplex, showed a variety of popular uses and have no yet been studied pharmacologically.

Compounds isolated from species of Justicia

A great diversity of chemical classes is found in the species of Justicia, mainly alkaloids, lignans, flavonoids, and terpenoids (iridods, diterpenoids, and triterpenoids). Other chemical classes have been isolated from species of Justicia, such as essential oils, vitamins, fatty acids (docosanoic acid), and salicylic acid (Angonese et al., 1992; Al-Juaid & Abdel-Mojib, 2004). The steroids campesterol, stigmasterol, sitosterol, and sitosterol-D-glucoside were isolated from the leaves and roots of J. flava, J. spicigera, and J. gendarussa (Olaniyi, 1980; Wahi et al., 1974; Domínguez et al., 1990; Amborabé et al., 2002; Deepak et al., 2002; Rajakumar & Shivana, 2009). The literature describes the allelopathy effect of the sterols and triterpenes. Both of the chemical classes isolated from the alcoholic extract of the aerial parts of J. anselliana showed allelopathic effects on cowpea plants (Kpoviessi et al., 2006). The allelopathic effects of the leaf and root extracts of J. anselliana have also been described, as shown in Table 3.

Table 4 shows a coumarin, flavonoids, alkaloids, and triterpenoidal glycosides isolated from the species of Justicia. Only one coumarin, umbeliferone (1), and a small variety of flavonoids (2-5), alkaloids (6-13), and triterpenoidal glycosides (14-21) were identified.

Leaf extracts from J. reptans display a clear virucidal effect on HIV, which was attributed to two glycosylated flavonoids that have not yet been identified (Bedoya, 2008). Compounds of this chemical class have been previously reported to display anti-HIV properties including reverse transcriptase or integrase inhibition, but this is the first time that they are described as virucides (Kumar et al., 2005). Pharmacological tests using the ethanol extract from J. reptans indicated inhibition of HIV replication (Table 3).

A large variety of lignans has been isolated from species of Justicia (Table 5). Lignans are a large group of natural products that show diverse biological effects. Lignans may serve as lead compounds for the development of new therapeutic agents with cytotoxic activity (Fukamiya & Lee, 1986; Hui et al., 1986). For example, lignans obtained from J. pectoralis are cytotoxic to leukemia and solid tumor cell lines (Hui et al., 1986).

Lignans also show antiangiogenic, antileishmanial, antifungal, hypolipidemic, antiasthmatic (Vasilev & Ionkova, 2005), antiviral (Asano et al., 1996), antineoplastic (Gordaliza et al., 2000), antifeedant (Bedoya et al., 2008), insecticidal, cardiotonic, antidepressant (Ghosal et al., 1979), analgesic, antiplatelet (Chen et al., 1996), and anti-inflammatory (Navarro et al., 2004) indications, as well as activity as lipid peroxidation inhibitors. Potent anti-inflammatory activities were described for lignan glycosides isolated from J. ciliata (Day et al., 2000) and phenolic compounds isolated from J. prostrata (Sanmugapriya et al., 2005b).

Many lignans contain an arylnaphthalide skeleton (22-54) and are found in relatively high proportions (Rajasekhar & Subbaraju, 2000). For example, jusmicranthin (22) was isolated from a chloroform extract of J. neesii, giving a mass yield of 0.025%. The dry leaves of J. extensa contain approximately 1% of justicidin P (47), which exists at 25 ºC as two rotamers (Wang & Ripka, 1983). Some arylnaphthalide lignans are glycosylated derivatives (32-37, 39, 42, and 49). Other miscellaneous-type lignans are also found in species of Justicia (55-63).

Biological activity of compounds isolated from species of Justicia

Some compounds show biological activities related to those observed in the species from which they are isolated. Coumarin umbeliferone (1), isolated from hydroalcoholic extract of the leaves of J. pectoralis (Table 4), showed anti-inflammatory, antinociceptive, and bronchodilator activities, which are related to the estrogenic, progestogenic, and anti-inflammatory activities of this species (Table 3) and its popular use in the treatment of bronchitis (Table 2). This species is also popularly used in the treatment of respiratory diseases (Table 2). The vasodilator activity of the flavonoid 2 is related to the anti-hypertensive activity of the Justicia cataractae Leonard, as shown in Table 3. Apigenin (3) has been reported to exert anti-inflammatory effects such as lowering oxidative stress and forestalling the expression of several inflammatory factors (Sawatzky et al., 2006). The flavonoid vitexin (5) is a potent anti-inflammatory agent, inhibiting the 5-lipoxygenase pathway, which, together with the COX-2 pathway, is very important in producing and maintaining inflammation (Sridhar et al., 2006). Compounds 3 and 5 were isolated from the ethanol extract of J. gendarussa, which is used in the treatment of inflammation, rheumatism, and arthritis in folk medicine (see Table 2). The antimicrobial and anti-inflammatory activities of flavonoid 4 (Table 4), as well as its effects on macrophage regulation and reduction in blood glucose levels are related to the popular uses of J. spicigera in giardicidal, anti-inflammatory, anticancer, and antidiabetes therapies (Tables 2 and 3). Alkaloid 11, also isolated from J. spicigera, is used as an anti-inflammatory agent (Table 2).

Alkaloids 9, 10, and 13 show bronchodilator activity (Table 4) and were isolated from J. adhatoda, which is popularly used in the treatment of bronchitis (Table 2). The antifertility activity of triterpenoidal glycoside 21 (Table 4) is related to the popular use of J. simplex as an abortifacient and to control fertility (Table 2). Alkaloids 7 and 8 show antitumor activity (Table 4) and were isolated from J. betonica, however, this species is popularly used in the treatment of diarrhea, inflammations, and HIV/AIDS (Table 2), not toward cancer.

Elenoside (42), isolated from Justicia hyssopifolia L., is the most pharmacologically studied arylnaphthalene lignan in the genus Justicia. This compound shows sedative, muscle relaxant, cytotoxic, antiviral, insecticidal, cardiotonic, analgesic, lipid peroxidation inhibitory, anti-inflammatory, and stimulant activities and exhibits significant central nervous system depressant properties in rats. Its anxiolytic action, inducing sedation and muscle relaxation (Navarro et al., 2001a), is similar to other tranquilizer drugs (Irwin, 1968) such as the action of sedative-hypnotic barbiturates (Navarro et al., 2004). The cytotoxic activity of 42 was verified in human cancer cell lines in a range of concentrations from 10^-5 to 10^-4 M, with an LD50 of 305 mg/kg in mice and central depressive properties at doses of 25, 50, and 100 mg/kg. No lethality was observed for five days following administration of this compound (Alonso et al., 1997). As a consequence, this compound behaves as a sedative with broad-spectrum cytotoxicity (Navarro et al., 2001b), also showing cytotoxic effects toward leukemia cell lines (Navarro et al., 2001a).

Other lignans isolated from species of Justicia show a smaller spectrum of biological activity. The antiplatelet aggregation activity of lignans 25, 26, 28, 29, 38, 40, and 52 are related to the pharmacological tests of the methanol extract of J. procumbens (Table 3). Lignans 29, 30, 31, 53, and 54 showed strong antiviral activity against vesicular stomatitis virus and low cytotoxicity against cultured rabbit lung cells (RL-33) (Asano et al., 1996). Lignans 29 and 43 showed inhibition of secondary aggregation induced by adrenaline (Wu et al., 2007). Moreover, these compounds showed an inhibitory effect on cyclooxygenase-1 (COX-1), with an antiplatelet effect partially due to the suppression of COX-1 activity and reduced thromboxane formation.

Lignan 24 inhibits human hepatitis B viral replication. This compound is isolated from J. flava, which is popularly used in the treatment of HIV/AIDS in Uganda. Lignans 29, 30, 31, 44, 45, 46, 53, and 54 show antiviral activities. These compounds were isolated from J. extensa, J. betonica, and J. procumbens, and also show the same biological activities (Tables 2 and 3). Conversely, lignans 29, 30, 31, 35, 36, and 42 show antiviral activity, but were isolated from species that did not show this activity (Tables 2 and 3). A larger investigation of the extracts of these species is required to explore their antiviral activities.

The antitumor activity of lignans 25, 27, 29, 30, 31, 35, 36, 37, 50, 51, 53, and 54 are related to the popular uses of J. procumbens, J. ciliata, J. rhodoptera, and J. patentiflora as anticancer therapies (Tables 2 and 3). Lignans 30, 31, and 37, isolated from J. ciliata, showed significant citotoxic effects toward a number of cancer cell types (human hepatomacellular carcinoma, human cervical carcinoma, human colorectal adenocarcinoma, human colorectal carcinoma, and human breast cancer) (Day et al., 2002). Lignan 31 also displayed potent cytotoxic effects against T-24, CaSki, SiHa, HT-3, PLC/PRF/5, and 212 cells in vitro (Day et al., 1999). Lignan 60 exhibited low cytotoxicity against three human tumor cell lines: A-549 (human lung carcinoma), MCF-7 (human breast carcinoma), and HT-29 (human colon adenocarcinoma) (Subbaraju et al., 1991). Lignan 62 is included in a wide variety of cancer chemotherapy protocols and was used as a precursor for the semi-synthesis of anticancer therapeutics (Canel et al., 2000). Lignans 24, 26, 29, 30, 31, 32, 37, 42, 51, 60, 61, and 62 show antitumoral activity, but they were isolated from species that did not show this activity (see Tables 2, 3, and 5). The data warrant a larger exploration of the extracts of these species for their anticancer properties.

Conclusion

Although the genus Justicia contains only a few species that have been chemically and biologically studied, a broad range of biological applications was observed. Lignans are the major components of the active extracts of the species of Justicia, exhibiting important pharmacological properties, such as antiviral, antitumoral, anti-inflamatory, and antiplatelet aggregations activities, which warrant further exploration. The chemical and pharmacological data shown in the present work should inspire additional study of the species of Justicia for their use in therapeutics.

Acknowledgements

The authors thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM) for their financial support.

Instituto de Ciências Exatas e Tecnologia, Universidade Federal do Amazonas

69100-000 Itacoatiara- AM, Brazil

[e-mail]

Received 7 Jun 2011

Accepted 15 Jul 2011

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Correspondence

Geone M. Corrêa

Departamento de Química, ICEx, Universidade Federal de Minas Gerais

31270-901 Belo Horizonte- MG, Brazil

Publication Dates

• Publication in this collection
  01 Nov 2011
• Date of issue
  Feb 2012

History

• Received
  07 June 2011
• Accepted
  15 July 2011