PHYTOTHERAPY RESEARCH
Phytother. Res. 17, 512 – 519 (2003)
Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/ptr.1314
Copyright © 2003 John Wiley & Sons, Ltd.
Revised 18 April 2002
Accepted 25 July 2002
John Wiley & Sons, Ltd.
Carpobrotus edulis Methanol Extract Inhibits
the MDR Efflux Pumps, Enhances Killing
of Phagocytosed S. aureus and Promotes
Immune Modulation
CARPOBROTUS EDULIS INHIBITS MDR EFFLUX PUMPS
Diane Ordway
1
, Judit Hohmann
2
, Miguel Viveiros
1
, Antonio Viveiros
3
, Joseph Molnar
4
,
Clara Leandro
1
, Maria Jorge Arroz
5
, Maria Amelia Gracio
6
and Leonard Amaral
1
*
1
Unit of Mycobacteriology, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Rua da Junqueira 96, 1349-008
Lisboa, Portugal
2
Institute of Pharmacognosy, Faculty of Medicine, University of Szeged, Dóm tér 10/11,6720 Szeged, Hungary
3
Departamento de Biologia Vegetal, Faculdade de Ciências da Universidade de Lisboa, Edificio C3, Campo Grande, 1749-016
Lisboa, Portugal
4
Institute of Medical Microbiology, Albert-Szent Gyorgyi School of Medicine, Dóm tér 10/11,6720 Szeged, Hungary
5
Flow Cytometry Unit, Hospital de Egas Moniz, Rua da Junqueira 126, 1349-019 Lisboa & Faculdade de Ciências Médicas de
Lisboa/UNL, Campo Mártires da Pátria 130, 1169-056 Lisboa, Portugal
6
Unit of Helmintology & UPMM, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Rua da Junqueira 96,
1349-019 Lisboa, Portugal
Although alkaloids from the family Aizoaceae have anticancer activity, species of this family have received
little attention. Because these alkaloids also exhibit properties normally associated with compounds that
have activity at the level of the plasma membrane, a methanol extract of Carpobrotus edulis, a common
plant found along the Portuguese coast, was studied for properties normally associated with plasma mem-
brane active compounds. The results of this study show that the extract is non-toxic at concentrations that
inhibit a verapamil sensitive efflux pump of L5178 mouse T cell lymphoma cell line thereby rendering these
multi-drug resistant cells susceptible to anticancer drugs. These non-toxic concentrations also prime THP-1
human monocyte-derived macrophages to kill ingested Staphylococcus aureus and to promote the release of
lymphokines associated with cellular immune functions. The extract also induces the proliferation of THP-1
cells within 1 day of exposure to quantities normally associated with phytohaemagglutinin. The potential role
of the compound(s) isolated from this plant in cancer biology is intriguing and is currently under investiga-
tion. It is supposed that the resistance modifier and immunomodulatory effect of this plant extract can be
exploited in the experimental chemotherapy of cancer and bacterial or viral infections. Copyright © 2003
John Wiley & Sons, Ltd.
Keywords: Carpobrotus edulis; immune-modulator; efflux pump inhibitor.
INTRODUCTION
Members of the plant family Aizoaceae contain alka-
loids known to have narcotic-anxiolytic properties and
strong synergism with psychomimetics (Smith et al.,
1996). These properties are consistent with those pre-
sented by other neuro-active compounds whose activities
reside primarily at the level of the plasma mem-
brane (Williams et al., 2001). Although some of these
alkaloids have been reported to have anticancer proper-
ties as well (Smith et al., 1996) they have received
little attention, perhaps due to their reported toxicity.
Along the coast of Portugal one may find a member
of the Aizoaceae family that is so prolific that it is
considered a nuisance. This plant Carpobrotus edulis
captured the attention of Professor J. Molnar during his
visit to this laboratory (L. Amaral). Subsequent to the
plant’s identification, it became reasonably clear that
the properties reported for members of this family may
also be present in this nuisance plant. Furthermore,
inasmuch as some inhibitors of efflux pumps responsible
for antibiotic resistance in eukaryotic and prokarytic
cells have activities on other plasma membrane func-
tions (Molnar et al., 1997; Nacsa et al., 1998), this
plant was of mutual interest and thus became a subject
of mutual study that evaluated any anticancer activity
that an extract of this plant might have. This report pro-
vides evidence that the methanol extract of Carpobrotus
edulis inhibits the MDR1-efflux pump of a chemo-
therapeutic resistant lymphoma cell line, primes a
human monocyte-macrophage cell line (THP-1) to
kill intracellular Staphylococcus aureus, induces these
latter cells to secrete those lymphokines associated with
cellular immune activity as well induces proliferation
of these cells within 24 h. These activities are conducted
with concentrations in the extract that are non-toxic
and non-apoptotic to the THP-1 cells, human mono-
cytes derived from peripheral blood, sub-populations
of human T cells or mouse T cell lymphoma cells.
* Correspondence to: Dr L. Amaral, Unit of Mycobacteriology, Instituto
de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Rua
Junqueira 96, 1349-008 Lisboa, Portugal.
E-mail: lamaral@ihmt.unl.pt
Contract/grant sponsor: Scientific Council of the Institute of Hygiene
and Tropical Medicine of Lisbon.