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Isolation and Characterization of Psalmopeotoxin I and II: Two Novel Antimalarial Peptides from the Venom of the Tarantula Psalmopoeus Cambridgei

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Isolation and Characterization of Psalmopeotoxin I and II: Two Novel Antimalarial Peptides from the Venom of the Tarantula Psalmopoeus Cambridgei FEBS 28663 FEBS Letters 572 (2004) 109–117 Isolation and characterization of Psalmopeotoxin I and II: two novel antimalarial peptides from the venom of the tarantula Psalmopoeus cambridgei Soo-Jin Choia, Romain Parentb,1, Carole Guillaumec, Christiane Deregnaucourtc, Christiane Delarbred, David M. Ojciusd, Jean-Jacques Montagnea, Marie-Louise Celeriere, Aude Phelipotf, Mohamed Amichef, Jordi Molgog, Jean-Michel Camadroa,*, Catherine Guetteb,2 aLaboratoire d’Ingenierie des Proteines et Contro^le Metabolique, Dept. de Biologie des Genomes, Institut Jacques Monod, UMR 7592, CNRS – Universites Paris 6 & 7, 2 place Jussieu, 75251 Paris Cedex 05, France bLaboratoire de Chimie des Substances Naturelles, Museum National d’Histoire Naturelle, 63 rue Buffon, 75231 Paris Cedex 05, France cUSM 0504, Biologie Fonctionnelle des Protozoaires, Museum National d’Histoire Naturelle, 61 rue Buffon, 75231 Paris Cedex 05, France dLaboratoire d’Immunologie Cellulaire, Institut Jacques Monod, UMR 7592, CNRS – Universites Paris 6 & 7, 2 place Jussieu, 75251 Paris Cedex 05, France eLaboratoire d’Ecologie, UMR 7625, CNRS – Universite Pierre et Marie Curie – Paris 6, B^at. A – case 237, 7 Quai Saint-Bernard, 75252 Paris Cedex 05, France fLaboratoire de Bioactivation des Peptides, Institut Jacques Monod, UMR 7592, CNRS – Universites Paris 6 & 7, 2 place Jussieu, 75251 Paris Cedex 05, France gLaboratoire de Neurobiologie Cellulaire et Moleculaire, UPR 9040, CNRS, 1 avenue de laTerrasse, 91198 Gif-sur-Yvette Cedex, France Received 26 May 2004; revised 24 June 2004; accepted 9 July 2004 Available online 21 July 2004 Edited by Felix Wieland 1. Introduction Abstract Two novel peptides that inhibit the intra-erythrocyte stage of Plasmodium falciparum in vitro were identified in the venom of the Trinidad chevron tarantula, Psalmopoeus cambrid- Animal venoms are valuable sources of novel pharmaco- gei. Psalmopeotoxin I (PcFK1) is a 33-residue peptide and logical tools whose specific actions are useful for characterizing Psalmopeotoxin II (PcFK2) has 28-amino acid residues; both their receptors. Hundreds of toxins from snakes, scorpions, have three disulfide bridges and belong to the Inhibitor Cystine spiders and marine invertebrates with a range of pharmaco- Knot superfamily. The cDNAs encoding both peptides were logical activities have all been characterized [1–3]. cloned, and nucleotide sequence analysis showed that the peptides Spider venoms contain a wide spectrum of biologically ac- are synthesized with typical signal peptides and pro-sequences tive substances, which selectively target a variety of vital that are cleaved at a basic doublet before secretion of the mature physiological functions in both insects and mammals (for re- peptides. The IC of PcFK1 for inhibiting P. falciparum growth 5O view, see [4,5]). The spider toxins are ‘‘short’’ polypeptides was 1.59 % 1.15 lM and that of PcFK2 was 1.15 % 0.95 lM. PcFK1 was adsorbed strongly to uninfected erythrocytes, but with molecular mass of 3–8 kDa and a structure that is held PcFK2 was not. Neither peptide has significant hemolytic activity together by several disulfide bonds. There are two main groups at 10 lM. Electrophysiological recordings in isolated frog and of these peptides, the neurotoxins that target neurone recep- mouse neuromuscular preparations revealed that the peptides (at tors, neurone ions channels or presynaptic proteins involved in up to 9.3 lM) do not affect neuromuscular transmission or quantal neurotransmitter release, and the non-neurotoxic peptides, transmitter release. PcFK1 and PcFK2 do not affect the growth or such as necrotic peptides and antimicrobial peptides (for a viability of human epithelial cells, nor do they have any antifungal review, see [6]). Recent studies have characterized the venoms or antibacterial activity at 20 lM. Thus, PcFK1 and PcFK2 seem of the genuses Brachypelma, Pterinochilus and Theraphosa [7– to interact specifically with infected erythrocytes. They could 10]. Several peptides that inhibit atrial fibrillation [11], block therefore be promising tools for antimalaria research and be the the Kv2 and Kv4 subfamilies of voltage-dependent potassium basis for the rational development of antimalarial drugs. Ó 2004 Published by Elsevier B.V. on behalf of the Federation of channels [12,13], or multiple sodium channels [14], and proton- European Biochemical Societies. gated sodium channels [15] have been recently isolated. Al- though spider toxins bind to their receptors with high affinity, Keywords: Tarantula venom; ICK peptide; Malaria; specificity, and selectivity, little is known about them and little Plasmodium falciparum work has been done to develop these toxins for therapeutic use. Malaria is one of the most serious and widespread parasitic * Corresponding author. Fax: +33-1-4427-5716. diseases in the world. There are an estimated 300–500 million E-mail address: [email protected] (J.-M. Camadro). clinical cases each year, and 1–1.5 million people die each year due to malaria, mainly young children (for a review, see [16]). 1 Present address: INSERM U271, 151 cours Albert Thomas, 69424 The causative agent of malaria, an intracellular protozoan of Lyon Cedex 03, France. 2 Present address: USM 0505, Ecosystemes et Interactions toxiques, the genus Plasmodium, spends much of its life cycle within the Museum National d’Histoire Naturelle, 12 rue Buffon, 75231 Paris host erythrocyte. Plasmodium falciparum is the most virulent Cedex 05, France. of the four species of Plasmodium that infect humans. The 0014-5793/$22.00 Ó 2004 Published by Elsevier B.V. on behalf of the Federation of European Biochemical Societies. doi:10.1016/j.febslet.2004.07.019 110 S.-J. Choi et al. / FEBS Letters 572 (2004) 109–117 increasing resistance of the parasite to classical antimalarial 2.4. Cloning drugs means that new chemotherapeutic approaches are ur- Total RNAs were extracted from P. cambridgei venom glands frozen gently needed [17]. Classical strategies are based on modifying in liquid nitrogen, powdered and homogenized, as described by Chomczynski and Sacchi [23]. Poly(A)þ RNAs were purified using the known antimalarial drugs, while others that seek new biolog- Invitrogen Micro-FastTrack kit, and a cDNA library was constructed ical targets require a better understanding of the Plasmodium [24], using a standard procedure with a NotI adaptor in the cDNA biology, life cycle and interaction with its host [18]. Various synthesis step and a SalI adaptor for cloning into the pSPORT1 vector plant and animal substances have emerged recently as inter- (Life Technologies, Inc.). Recombinant plasmids were prepared by transformation of JM109 competent Escherichia coli cells. The quality esting tools for exploring new potential antimalarial targets of the cDNA library was estimated by determining the size of the inserts [19–22]. in a random sample of 20 plasmids linearized by digestion with MluI. As part of a general screening for antimalarial drugs, we A combination of 30-RACE (Rapid Amplification of cDNA End) investigated the potential of toxins from Psalmopoeus cam- and nested-PCR steps was used to screen the cDNA library for se- bridgei, the Trinidad chevron tarantula. This report describes quences encoding PcFK. The reaction was performed using an anti- sense universal primer (primer UP: 50-TAAAACGACGGCCAGT-30) two novel peptides (PcFK1 and PcFK2, Psalmopoeus cam- and a sense degenerated primer corresponding to the amino acids bridgei F alciparum killer) that possess great antiplasmodial HDNCVYV of PcFK1 (primer PSA-I: 50-CAYGAYAAYTGYG- activity against the intra-erythrocyte stage of P. falciparum TKTAYGT-30) and the amino acids PAGKTCV of PcFK2 (primer 0 0 in vitro, but do not lyse erythrocytes or nucleated mammalian PSA-II: 5 -CCKGCKGGRAARACKTGYGT-3 ) under the following conditions: 94 °C for 240 s, followed by 30 cycles of 94 °C for 40 s, 56 cells and do not inhibit neuromuscular function, despite their °C for 30 s, and 72 °C for 60 s. An aliquot of the first round of PCR structural similarity to known neurotoxins. was used as template for nested-PCR, using an antisense universal primer and a sense degenerated primer corresponding to the amino acids YVPAQNPC of PcFK1 (primer Nest-PSA-I: 50-TAY- GTKCCKGCKCARAAYCCKTGY-30) and the amino acids TCVRGPMR of PcFK2 (primer 2: 50-TGYGTTKMGKGGKCCK- 2. Materials and methods ATGMG-30) under the following conditions: 94 °C for 240 s, followed by 25 cycles of 94 °C for 40 s, 52 °C for 30 s, and 72 °C for 60 s. At the 2.1. Venom and toxin purification end of the last cycle, the sample was incubated at 72 °C for a further 5 Psalmopoeus cambridgei (Araneae theraphosidae) venom was ob- min and separated by electrophoresis in 1.2% agarose gels. DNA tained by electrical stimulation of venom glands. The crude venom was fragments were excised from the gel and purified using the Qiaquick gel centrifuged (5000 Â g,4°C, 20 min), filtered through 0.45-lm micro- extraction kit (Qiagen). The PCR product was cloned in the pGEMT- filters (SJHVL04NS, 4-mm diameter, Millipore) and stored at )20 °C. Easy vector system (Promega). Nucleotide sequences were analyzed by It was then diluted twofold in 10% acetic acid and fractionated by the dideoxy chain termination technique in a double-stranded reverse-phase high pressure liquid chromatography (RP-HPLC) on a pGEMT-Easy vector using the BigDye fluorescent labeling kit and an C18 column (Supelcosil, 5 lm, 4.6 Â 250 mm, Supelco) eluted with a ABI 377 automatic sequencer. We used an antisense T7 primer (primer linear 0–60% gradient of acetonitrile in 0.1% aqueous trifluoroacetic T7: 50-TAATACGACTCACTATAGGGA-30) and a 30 sense gene- acid (TFA) for 70 min (flow rate: 0.75 ml/min). Fractions (0.75 ml) specific primer deducted from the 50 cDNA of PcFK1 (primer 3: were collected and freeze-dried. The peptides were dissolved in RPMI 50-TTTCTGTGCTTTTGTTGCT-30) or PcFK2 (primer 4: 50-CTCA- 1640 (Life Technologies, Inc.) and screened for antiplasmodial activity. TTAACTTCGTTTCATCAGGTAC-30) to determine the sequences of The peptides in active fractions were further purified by RP-HPLC on the 50-end of the Psalmopeotoxins.
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