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The Unfulfilled Promises of Scorpion Insectotoxins Ernesto Ortiz* and Lourival D Possani

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The Unfulfilled Promises of Scorpion Insectotoxins Ernesto Ortiz* and Lourival D Possani Ortiz and Possani Journal of Venomous Animals and Toxins including Tropical Diseases (2015) 21:16 DOI 10.1186/s40409-015-0019-6 REVIEW Open Access The unfulfilled promises of scorpion insectotoxins Ernesto Ortiz* and Lourival D Possani Abstract Since the description and biochemical characterization of the first insect-specific neurotoxins from scorpion venoms, almost all contributions have highlighted their potential application as leads for the development of potent bioinsecticides. Their practical use, however, has been hindered by different factors, some of which are intrinsically related to the toxins and other external determinants. Recent developments in the understanding of the action mechanisms of the scorpion insectotoxins and their bioactive surfaces, coupled with the exploration of novel bioinsecticide delivery systems have renewed the expectations that the scorpion insectotoxins could find their way into commercial applications in agriculture, as part of integrated pest control strategies. Herein, we review the current arsenal of available scorpion neurotoxins with a degree of specificity for insects, the progress made with alternative delivery methods, and the drawbacks that still preclude their practical use. Keywords: Bioinsecticides, Insectotoxins, Scorpion venom Introduction thousand persons every year. Onchocerciasis, or river Insects are the most diverse class of animals living on blindness, is carried by blackflies. About 17 to 25 million Earth, with more than one million described species. people are nowadays infected with river blindness, mostly They are highly adaptable and successful, easily outnum- in sub-Saharan Africa, with approximately 0.8 million hav- bering any other animal category [1]. ing some amount of loss of vision. Plague, the deadly in- Documents distributed by the World Health Organization fectious disease propagated by fleas that has decimated report many cases of insects that are disease-transmit- the human population through history, is still endemic in ting vectors and represent a great menace to human some parts of the world [2]. Other insects that constitute populations [2]. Mosquitoes are the most relevant, disease agents for humans include lice and bed bugs. since they can transmit malaria, dengue and yellow The direct damage caused by insect pests to agriculture fever. Together these three illnesses account for hun- has been estimated by various authors to be responsible for dreds of millions of cases and several million deaths the loss of over 15 % of the global food production [3–5]. every year. Mosquitoes also spread lymphatic filariasis This number does not consider the secondary losses and Japanese encephalitis. Other parasites are carried caused by plant diseases transmitted by insects. The threat by different insects. The tsetse fly transmits the African of insect damage to agriculture is expected to increase as trypanosomiasis or sleeping sickness that causes around the planet warms and high-yielding varieties expand into 9 thousand deaths per year. The American trypanosom- less suitable regions, replacing well-adapted and more re- iasis, more commonly known as Chagas’ disease, is sistant local varieties [5]. According to the most recent spread mostly by blood-sucking insects known as Tria- United Nations 2012 Revision of the World Population tominae or kissing bugs. At least 16 million people in Prospects [6], the world population will reach 9 billion Latin America are infected with Chagas’ disease, and around 2040 and will continue to grow until it stabilizes at more than 10 thousand patients die of Chagas’ every just above 10 billion persons. In order to feed that popula- year. Leishmaniasis is spread by the bite of certain types tion, the crop yields must increase by at least 40 %. This of sandflies. It causes the death of between 20 and 50 cannot be achieved without a rational and integrated pest/ crop management, including crop protection through bio- logical and chemical measures [4]. * Correspondence: [email protected] The use of synthetic insecticides dates back to the Departamento de Medicina Molecular y Bioprocesos, Instituto de Biotecnología, Universidad Nacional Autonóma de México, Avenida introduction of dichlorodiphenyltrichloroethane (DDT) Universidad 2001, Cuernavaca 62210, Mexico © 2015 Ortiz and Possani; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Ortiz and Possani Journal of Venomous Animals and Toxins including Tropical Diseases (2015) 21:16 Page 2 of 7 at the end of World War II. Different generations of syn- the gating mechanism of voltage-gated sodium (Nav)chan- thetic insecticides have helped mankind to control the nels [12]. Short-chain toxins (28 to 46 amino acids) primar- burden of insect pests, although not without conse- ily block potassium channels [12]. Based on the quences for the environment [7]. Their indiscriminate physiological effect that the long-chain toxins elicit on Nav use and the high frequency with which insecticides have channels, they are further classified as alpha (α-NaScTxs) been applied have led to the emergence of insect strains or beta (β-NaScTxs). The α-NaScTxs target the receptor resistant to their active principles [8, 9]. There is no site 3 of Nav channels and inhibit the channel’srapidin- other way to prevent or at least delay the emergence of activation process, thereby prolonging the action potential resistance other than the alternated use of substances [13]. The β-NaScTxs bind to receptor site 4 and shift the with different mechanisms of action, combined with in- channel activation to more negative potentials [14]. tegrated pest control strategies, including the protection Only a few α-NaScTxs exhibit high activity in insects. of beneficial organisms and the pest’s natural antago- Examples include LqhαIT from Leiurus quinquestriatus nists. It is in this context that scorpion venom insect- hebraeus [15] (currently denominated L. hebraeus [16]), specific toxins (insectotoxins), with particular modes of Lqq3 from L. q. quinquestriatus [17] (currently named L. action, have become attractive candidates for the devel- quinquestriatus [16]), BotIT1 from Buthus occitanus tune- opment of novel insecticides. tanus [18] (currently denominated B. tunetanus [19]) and Scorpions constitute a very well adapted order of preda- BjαIT from Buthotus judaicus (now known as Hottentotta tory animals. They have inhabited the planet for well over judaicus) [20]. These toxins are highly active on insects 400 million years, being among the first complex animals but are weak on mice (as tested by intracerebroventricular to make the transition from sea to land [10]. They are so injection), and bind with high affinity to insect neuronal successful that their morphology has changed little over preparations but weakly to rat brain synaptosomes [21]. this long timespan. Meanwhile, they have diversified to These properties are in sharp contrast with the effects comprise more than 1700 species that have been de- produced by the majority of the reported “classical” scribed to date [11]. The key to their success is the pro- α-NaScTxs, which are very potent on mammalian Nav duction of potent and complex venoms that they use channels, bind with high affinity to rat brain synapto- primarily to kill or paralyze their prey and to deter pos- somes, and show strong toxicity to mammals while pre- sible competitors and predators. Insects constitute an im- senting very weak toxicity when injected to insects. portant food source for most scorpion species, and Scorpion α-insectotoxins and the classical α-NaScTxs therefore, potent peptidic insectotoxins have been isolated share the same cysteine-stabilized αß scaffold, while their from the venoms of different scorpion species. three-dimensional structures are very similar in spite of These toxins are valuable as leads for the development their sequence diversity. Their pharmacological differ- of insecticides. Their practical application, however, has ences seem to be related to small structural differences in been hindered by problems mainly associated with their limited regions of the toxins and slight alterations in their natural mechanism of delivery. Scorpions inject venom surface topology [21, 22]. Small differences in the receptor into their prey with a stinger, so the toxins did not natur- site 3 in the homologous yet non-identical insect and ally evolve to be resistant to the harsh conditions of the mammalian Nav channels might be selectively discrimi- insect’s digestive system. Therefore, alternatives to feeding, nated by the different α-NaScTxs. Unfortunately, detailed or other variants with enhanced cuticle or gut mucosa ab- structural studies comparing receptor site 3 between in- sorption have to be devised. The other problem that has sects and mammals are not available. Moreover, due to to be circumvented is their potential broad range of tar- the flexibility displayed by protein-protein interactions, it gets, which may include other beneficial insects or even is possible that rearrangements occur after toxin-to- mammals. It is highly relevant to accurately
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