Venoms of Heteropteran Insects: A Treasure Trove of Diverse Pharmacological Toolkits
Abstract
:1. Evolution of Venom Systems in Heteroptera
1.1. Introduction: Are Heteropterans Venomous Animals?
1.2. Evolution of the Heteropteran Venom Apparatus
1.3. Diversification of Trophic Strategies in the Heteropteran Radiation
2. Diversification of Venom Pharmacology in the Evolution of Heteroptera
2.1. Aquatic and Semi-Aquatic Hunters: Nepomorpha, Gerromorpha and Leptopodomorpha
2.1.1. Habitat and Prey Range
2.1.2. Activity and Composition of Nepomorphan Venoms
2.2. Assassin’s Creed: Terrestrial Predators in Cimicomorpha and Pentatomomorpha
2.2.1. Efficient Predation through Envenomation, Prey-Capture Organs and Dietary Specialisation
2.2.2. Physiological Effect of Venoms of Terrestrial Predaceous Heteropterans
Effects of venom on invertebrates
Effects of venom on vertebrates
2.2.3. Composition of Venoms from Terrestrial Predators.
2.3. The Blood Feeders
2.3.1. Convergent Evolution of Blood-Feeding in Heteroptera
2.3.2. Venoms of Haematophagous Heteroptera
3. Future Directions
4. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Infraorder | Family | Species | Feeding Strategy a | Phospholipase A2 | Hyaluronidase | Protease | Lipase | Esterase | Invertase | Nuclease | Acid phosphatase | Alkaline phosphatase | Amylase | Pectinase | Refs. | |||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Trypsin-like | Chymotrypsin-like | Aminopeptidase | Carboxypeptidase | |||||||||||||||
Nepo-morpha | Belostomatidae | Lethocerus sp.b | P | yes | yes | yes | yes | yes | yes | yes | yes | no | [39,71] | |||||
Belostomatidae | Belostoma sp.b | P | yes | yes | yes | yes | ? | no | yes | yes | ? | [39,68,72] | ||||||
Nepidae | Ranatra elongata | P | yes | no | no | yes | no | [72] | ||||||||||
Cimicomorpha | Reduviidae | Platymeris rhadamanthus | P | yes | yes | yes | no | no | [6,42] | |||||||||
Reduviidae | Zelus renardii | P | strong | strong | yes | weak | weak | weak | [31,84,85] | |||||||||
Reduviidae | Sinea confusa | P | strong | strong | weak | [31,85] | ||||||||||||
Reduviidae | Rhynocoris marginatusc | P | yes | yes | strong | weak | yes | yes | yes | yes | yes | yes | [86,87,88] | |||||
Reduviidae | Catamiarus brevipennis | P | yes | yes | yes | yes | [87] | |||||||||||
Anthocoridae | Orius insidiosus | P | yes | yes | [89] | |||||||||||||
Nabidae | Nabis alternatus | P,(H) | yes | yes | ? | [31,85] | ||||||||||||
Miridae | Deraeocoris sp. | P | yes | yes | yes | ? | [85,90] | |||||||||||
Miridae | Lygus sp. | H,(P) | ? | no | yes | yes | strong | yes | [85,91,92,93,94] | |||||||||
Miridae | Creontiades dilutus | H,(P) | weak | yes | yes | [95,96] | ||||||||||||
Pentatom-omorpha | Pentatomidae | Podisus sp.d | P | ? | yes | yes | yes | [31,85,97,98,99] | ||||||||||
Pentatomidae | Andrallus spinidens | P | yes | yes | yes | yes | [100] | |||||||||||
Geocoridae | Geocoris punctipes | P,(H) | yes | yes | yes | ? | [31,85,92] |
Molecule | Protein Family/Molecule Class | Species | Physiological Function a | Molecular Target | Reference |
---|---|---|---|---|---|
Nitric oxide | Gas | R. prolixus, C. lectularius | V, PAI | Activates guanylate cyclase | [193,194] |
Lysophosphatidylcholine | Lipid | Rhodnius prolixus | PAI, other | Unknown | [195] |
Nitrophorins 1–4 | Lipocalin | Rhodnius prolixus | V, PAI, AI | NO donor, also binds histamine | [159,193,196,197,198,199,200,201,202] |
Nitrophorin-2 (Prolixin) | Lipocalin | Rhodnius prolixus | AC, V, PAI, AI | Additionally inhibits Tenase complex | [186,203,204,205,206,207] |
Nitrophorin-7 | Lipocalin | Rhodnius prolixus | AC, V, PAI, AI | Additionally binds anionic phospholipids to prevent activation of clotting factors and platelets | [208,209,210,211,212] |
Amine Binding Protein | Lipocalin | Rhodnius prolixus | V | Binds serotonin and norepinephrine | [213,214] |
Triabin | Lipocalin | Triatoma pallidipennis | AC | Inhibits activation of thrombin | [185,215,216] |
Palladipin | Lipocalin | Triatoma pallidipennis | PAI | Collagen-induced PAI, mechanism unknown | [181,217,218] |
Rhodnius Platelet Aggregation Inhibitor 1 | Lipocalin | Rhodnius prolixus | PAI | ADP-induced PAI by binding to ADP | [219,220] |
Triplatin | Lipocalin | Triatoma infestans | V, anti-NET | Binds thromboxane A2 and prostaglandin F2α | [221,222,223] |
Triafestin-1, -2 | Lipocalin | Triatoma infestans | AC | Inhibits reciprocal activation of Factor XII, prekallikrein | [224] |
Dipetalodipin | Lipocalin | Dipetalogaster maxima | V, anti-NET | Binds thromboxane A2 and various eicosanoids | [180,222] |
Dimiconin | Lipocalin | Triatoma dimidiata | AC | Inhibits activation of Factor XII | [225] |
Antigen-5 | Antigen-5 | D. maxima, T. infestans | PAI | Collagen-induced PAI by scavenging free radicals | [226] |
Apyrase (Triatomine type) | 5′ Nucleotidase | Triatoma infestans | PAI | Degrades ADP | [227,228] |
Trialysin | Trialysin | Triatoma infestans | Antimicrobial | Pore formation | [229,230,231] |
Protease | Trypsin-like | T. infestans, Panstrongylus megistus | AC, unknown | Degrades fibrin nets, other unknown function? | [232,233] |
Inositol Phosphatase | Inositol phosphatase | Rhodnius prolixus | Unknown | Phosphatidylinositol | [234] |
Procalin | Lipocalin | Triatoma protracta | Allergen | Unknown | [235] |
Nitrophorin (Cimex type) | Inositol phosphatase | Cimex lectularius | V, PAI | NO donor | [236,237] |
Apyrase (Cimex type) | Apyrase (Cimex type) | Cimex lectularius | PAI | Degrades ADP | [183,238] |
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Walker, A.A.; Weirauch, C.; Fry, B.G.; King, G.F. Venoms of Heteropteran Insects: A Treasure Trove of Diverse Pharmacological Toolkits. Toxins 2016, 8, 43. https://doi.org/10.3390/toxins8020043
Walker AA, Weirauch C, Fry BG, King GF. Venoms of Heteropteran Insects: A Treasure Trove of Diverse Pharmacological Toolkits. Toxins. 2016; 8(2):43. https://doi.org/10.3390/toxins8020043
Chicago/Turabian StyleWalker, Andrew A., Christiane Weirauch, Bryan G. Fry, and Glenn F. King. 2016. "Venoms of Heteropteran Insects: A Treasure Trove of Diverse Pharmacological Toolkits" Toxins 8, no. 2: 43. https://doi.org/10.3390/toxins8020043