Anti-inflammatory activity of alkaloids: a twenty-century review

Barbosa-Filho, José M.; Piuvezam, Márcia R.; Moura, Marcelo D.; Silva, Marcelo S.; Lima, Karla V. Batista; da-Cunha, Emídio V. Leitão; Fechine, Ivana M.; Takemura, Orlando S.

doi:10.1590/S0102-695X2006000100020

Abstracts

Many substances which interfere with the inflammatory response have been isolated from plants. This review shows some alkaloids of vegetal origin which in the period of 1907 to 2000 were evaluated regarding a possible anti-inflammatory activity. The alkaloids were classified in sub-groups in accordance with their chemical structures and the pharmacological data were obtained from different experimental models. Of the 171 evaluated alkaloids, 137 presented anti-inflammatory activity, and among those, the isoquinoline type was the most studied. The Carrageenin-induced paw edema was the most used model for evaluating the anti-inflammatory activity. In this review, 174 references were cited.

Alkaloids; anti-inflammatory activity; inflammation; experimental models

Muitas substâncias que interferem na resposta inflamatória têm sido isoladas de plantas. Esta revisão mostra alguns alcalóides de origem vegetal que no período de 1907-2000 foram avaliados quanto a uma possível atividade anti-inflamatória. Os alcalóides foram classificados em subgrupos de acordo com suas estruturas químicas e os dados farmacológicos foram obtidos de diferentes modelos experimentais. Dos 171 alcalóides avaliados, 137 apresentaram atividade anti-inflamatória, e, entre eles, os alcalóides do tipo isoquinolínicos foram os mais estudados. O modelo de edema de pata induzido por carragenina foi o mais empregado para avaliação da atividade anti-inflamatória. Nesta revisão 174 referências foram consultadas.

Alcalóides; atividade anti-inflamatória; inflamação; modelos experimentais

REVISÃO

Anti-inflammatory activity of alkaloids: a twenty-century review

Atividade anti-inflamatória de alkalóides: uma revisão do século XX

José M. Barbosa-FilhoI, ^* * E-mail address: jbarbosa@ltf.ufpb.br, Tel/Fax: + 55-83-32167364 ; Márcia R. Piuvezam^I; Marcelo D. Moura^I; Marcelo S. Silva^I; Karla V. Batista Lima^I; Emídio V. Leitão da-Cunha^{I, II}; Ivana M. Fechine^III, Orlando S. Takemura^IV

^ILaboratório de Tecnologia Farmacêutica Delby Fernandes de Medeiros, Universidade Federal da Paraíba, Caixa Postal 5009, 58051-970, João Pessoa, PB, Brazil

^IIDepartamento de Farmácia, Universidade Estadual da Paraíba, CCBN, 58100-000, Campina Grande, PB, Brasil

^IIIDepartamento de Química, Universidade Estadual da Paraíba, CCEN, 58100-000, Campina Grande, PB, Brasil

^IVLaboratorio de Farmacologia, Universidade Paranaense, Caixa-Postal 224, Centro, 87502-210, Umuarama, PR, Brasil

ABSTRACT

Many substances which interfere with the inflammatory response have been isolated from plants. This review shows some alkaloids of vegetal origin which in the period of 1907 to 2000 were evaluated regarding a possible anti-inflammatory activity. The alkaloids were classified in sub-groups in accordance with their chemical structures and the pharmacological data were obtained from different experimental models. Of the 171 evaluated alkaloids, 137 presented anti-inflammatory activity, and among those, the isoquinoline type was the most studied. The Carrageenin-induced paw edema was the most used model for evaluating the anti-inflammatory activity. In this review, 174 references were cited.

Keywords: Alkaloids, anti-inflammatory activity, inflammation, experimental models.

RESUMO

Muitas substâncias que interferem na resposta inflamatória têm sido isoladas de plantas. Esta revisão mostra alguns alcalóides de origem vegetal que no período de 1907-2000 foram avaliados quanto a uma possível atividade anti-inflamatória. Os alcalóides foram classificados em subgrupos de acordo com suas estruturas químicas e os dados farmacológicos foram obtidos de diferentes modelos experimentais. Dos 171 alcalóides avaliados, 137 apresentaram atividade anti-inflamatória, e, entre eles, os alcalóides do tipo isoquinolínicos foram os mais estudados. O modelo de edema de pata induzido por carragenina foi o mais empregado para avaliação da atividade anti-inflamatória. Nesta revisão 174 referências foram consultadas.

Unitermos: Alcalóides, atividade anti-inflamatória, inflamação, modelos experimentais.

INTRODUCTION

Inflammation can be defined as a generalized, nonspecific but beneficial response of tissues to injury. It comprises a complex array of adaptive responses to tissue injury which are both local and systemic. The local responses result in recruitment of phagocytic cells and removal of endogenous or foreign material. The systemic responses may alter the milieu interior to allow these processes to occur more efficiently (Denko, 1992; Henson; Murphy, 1989). The cellular processes of inflammation fall into four major groups: changes in blood flow caused by changes in smooth muscle cell function causing vasodilatation, alterations in vascular permeability engendered by cytoskeletal contraction in endothelial cells, migration of phagocytic leukocytes to the site of inflammation, and phagocytosis (Denko, 1992; Evans; Whicher, 1992).

The main pathophysiological pathways for drug targeting at present are: arachidonic acid metabolism; the complement cascade; phagocytosis and other cell functions; auto-immune processes; protein kinase C and others enzymes involved in second messenger systems (Willianson, 1996). Early inflammation changes in damaged tissues are now known to involve the release of various biologically active materials from polymorph nuclear leukocytes, lysossomal enzymes and others. The vascular effects are primarily mediated by kinins, prostaglandins and vaso-active amines (e.g. histamine, released by mast cells), which cause increased vascular permeability leading to plasma exudation.

The inflammatory process involves a complex interplay between cells of the blood, the blood vessels themselves and the cells of the involved tissue. The process can be seen as a coordinated response of a large number of cells to an initial stimulus (Henson; Murphy, 1989).

The immigrating cells themselves exert little effect by their presence alone, but initiate all the complex reaction of inflammation as a consequence of the materials that they secrete or release to the extra cellular environment. Such materials include molecules that exacerbate the response by attracting further inflammatory cells, inhibitors that serve to reduce the severity of the reactions, histotoxic agents such as proteases, oxygen metabolites and cations, as well as signals to the surrounding inflammatory and tissue cells to implement some or all of the complex reactions which they are capable (Henson; Murphy, 1989).

Uncontrolled inflammation is undesirable. The reversible features such as pain redness, heat and swelling are joined by a fifth and less transient feature, namely, loss of function of involved organs. Therefore control of inflammation is sought to protect the body function (Denko, 1992; Parnham, 1991).

In the field of inflammation research, several experimental models have been used to evaluate the inflammation. The usual methods of determining whether compounds have anti-inflammatory activity are to test them against animal and biochemical models of inflammation. There is no experimental model of inflammation that covers all aspects of inflammation (Lewis, 1989).

The experimental models can be divided into two broad classes: (1) acute inflammatory models and (2) chronic inflammatory models. Acute models are designed to test drugs that modulate blood flow (erythema), changes in vascular permeability, leukocyte migration and chemotaxis, phagocytosis - PMNLs and other phagocytic cells, measurement of local pain, antipyretic activity, local analgesic action and rat paw edema. Chronic models are designed to find drugs that may modulate the disease process and these include sponge and pellet implants and granuloma pouches which deposit granulation tissue, adjuvant induced arthritis and rabbit monoarticular arthritis which have an immune etiology (Lewis, 1989). Experimental inflammation in whole animal is the usual starting point for anti-inflammatory testing. These experiments are varied and widely used, specially the rat paw edema test. It can be adapted in numerous ways using different inflammatory agents in attempt to mimic pathological inflammation and arthritis (Willianson, 1996).

It has been demonstrated numerous physiological changes that find a parallel in human disorders such as different forms of arthritis and acute inflammation. These responses to inflammation include variation in temperature, leukocyte counting, sedimentation rate.

Natural products have long been recognized as an important source of therapeutically effective medicines. Of the 520 new drugs approved between 1983 and 1994, 39% were natural products or derived from natural products and 6080% of antibacterial and anticancer drugs were also derived from natural products (Cragg et al., 1997). Plants offer a vast source of compounds that present different effects in human.

The alkaloids comprise the largest single class of secondary plant substances. They have a remarkable range of pharmacological activity. The term alkaloids generally include those basic substances that contain one or more nitrogen atoms, usually in combination as part of a ciclic system (Harborne, 1991). They are often toxic to man and many have dramatic physiological activities.

Different approaches used to analyze the anti-inflammatory potential of plant and plant-derived compounds have been developed in the past years (Mascolo, 1987; Alcaraz; Jiménez, 1988; Handa et al., 1992; Gorzalczany et al., 1996, Falcão et al., 2005). In this work we review specially the alkaloids isolated and identified from the plants, previously demonstrated to have an anti-inflammatory activity. These compounds have been selected, classified in appropriate subgroups and the data are reported based on their pharmacological activity in different experimental models.

MATERIAL AND METHODS

The keywords used for this review were anti-inflammatory activity plus alkaloids. The search was done using Chemical Abstracts, Biological Abstracts and in the data bank of University of Illinois in Chicago NAPRALERT (Acronym for NAtural PRoducts ALERT), updated until December 2000. The references found in the search were later consulted.

RESULTS AND DISCUSSION

Alkaloids are most common in flowering plants, and usually in the Papaveraceae (poppies), Papilonaceae (lupins), Ranunculaceae (aconites), and Solanaceae (tobacco and potatoes). They are also found in lower plants, insects, marine organisms, microorganisms and animals (Lewis, 1989).

The pharmacological studies in alkaloids have been largely concerned with the effect of alkaloids on physiological processes other than inflammation.

Only one alkaloid, colchicine is an established clinical agent for arthritic disease and leukocytoclastic vasculitis (Sais et al., 1995). The alkaloid is present in corns and seeds of crocuslike plants. Colchicine is best known for its preventive action against gout, but it also reduces pain and swelling in degenerative and immunological inflammatory disease (Malkinson, 1982).

Isoquinoline, indole and diterpene alkaloids were the most studied about their activities on inflammation. Aconitine and others alkaloids from Aconitum genus were screened for anti-inflammatory activity. They were effective on different assays including carrageenin-induced paw o edema, adjuvant-induced arthritis and acetic acid induced vascular permeability tests (Benn; Jacyno, 1983; Luo et al., 1991; Zhang et al., 1982; Hikino et al., 1982; Saito et al., 1982). There are about 500 species of Aconitum and the species has been intensively investigated for the pharmacological activity of their alkaloids. Since anti-rheumatic properties have been associated with this plant, some attention has been made to the anti-inflammatory activity of alkaloids in Aconitum (Lewis, 1989).

Several isoquinoline alkaloids (berbamine, berberine, cepharanthine and tetrandine) were examined for anti-inflammatory activity. They showed to be active in different assays as reported by different authors (Wong et al., 1992; Yasukawa et al., 1993; Ono, 1994; Hikino et al., 1980). For instance, tetrandrine, a bisbenzylisoquinoline alkaloid extracted from the root of the creeper Stephania tetrandra S. Moore (Menispermaceae) has been shown to inhibit neutrophil and monocyte functions, including adherence, locomotion and superoxide generation (Seow et al., 1986; Seow et al., 1988) and the plant has been used for the treatment of rheumatic diseases, silicosis and other chronic inflammatory disease (Binggi et al., 1983). Several studies showed that the alkaloid suppress antigen and mitogen-induced lymphocyte proliferation, natural-Killer cell cytotoxicity, histamine release by mast cells, interleukin-1 (IL-1) secretion by human monocytes and the action of PAF on platelets (Seow et al., 1989). Teh et al. (1989 and 1990) showed that tetrandine and its natural analogue, berbamine inhibit prostaglandin and leukotriene generation by human monocytes and neutrophils in dose-dependent manner.

Berbarine is a major compound present in Phellodendri cortex and Coptidis rhizomaand the plant has been used for the treatment of diarrhea and other gastrointestinal disease in Japan and some Eastern countries. Ivanovsk; Philipov (1996) and Yasukawa et al. (1991) showed berbarine had an inhibitory effect on the ear TPA-induced inflammation indicating that this alkaloid may have important activity in chronic inflammation.

The alkaloids tend to be rather toxic, although the toxicity appears to be well below the therapeutic levels. The alkaloids appear to offer the considerable promise for further investigation as anti-inflammatory compounds, and some appears to be remarkably active.

Of the 171 evaluated alkaloids, 137 presented anti-inflammatory activity, and among those, the isoquinoline type was the most studied. The Carrageenin-induced pedal edema was the most used model for evaluating the anti-inflammatory activity. In this review, 174 references were cited.

ACKNOWLEDGEMENTS

The authors wish to express their sincere thanks to College of Pharmacy, The University of Illinois at Chicago, Chicago, Illinois 60612-7231, U.S.A., for helping with the computer aided NAPRALERT search of antiinflammatory activity.

Received 09/29/05

Accepted 01/25/06

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*

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Publication Dates

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26 Feb 2008
Date of issue
Mar 2006

History

Received
29 Sept 2005
Accepted
25 Jan 2006

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