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Proteases of Haematophagous Arthropod Vectors Santiago et al. Parasites & Vectors (2017) 10:79 DOI 10.1186/s13071-017-2005-z REVIEW Open Access Proteases of haematophagous arthropod vectors are involved in blood-feeding, yolk formation and immunity - a review Paula Beatriz Santiago1, Carla Nunes de Araújo1,2, Flávia Nader Motta1,2, Yanna Reis Praça1,3, Sébastien Charneau4, Izabela M. Dourado Bastos1 and Jaime M. Santana1* Abstract Ticks, triatomines, mosquitoes and sand flies comprise a large number of haematophagous arthropods considered vectors of human infectious diseases. While consuming blood to obtain the nutrients necessary to carry on life functions, these insects can transmit pathogenic microorganisms to the vertebrate host. Among the molecules related to the blood-feeding habit, proteases play an essential role. In this review, we provide a panorama of proteases from arthropod vectors involved in haematophagy, in digestion, in egg development and in immunity. As these molecules act in central biological processes, proteases from haematophagous vectors of infectious diseases may influence vector competence to transmit pathogens to their prey, and thus could be valuable targets for vectorial control. Keywords: Proteases, Haematophagy, Digestion, Yolk formation, Immunity, Ticks, Triatomines, Mosquitoes Background leishmaniasis, malaria, sleeping sickness, lymphatic filaria- Haematophagous arthropod vectors are spread world- sis and onchocerciasis are all examples of vector-borne wide. They are of medical and veterinary importance diseases with global impact on morbidity and mortality since their blood-feeding habit provides a scenario for (Table 1) since they affect more than one billion individ- the transmission of a variety of pathogens, including uals and cause over one million deaths every year [2]. virus, bacteria, protozoans and helminths [1]. Although Ecological factors are associated with vector dispersion there are clinical differences among the diseases caused to urban areas [3]. Ticks, triatomine bugs, mosquitoes, by these organisms, they share the tendency to coexist sand flies, tsetse and black flies are the main haema- in low and middle-income countries. Additionally, for tophagous arthropod vectors [2], which present different most of the infectious diseases transmitted by inverte- feeding habits. In ticks and triatomines, this habit is seen brate vectors there are neither vaccines nor preventive in both female and male, and in all stages of develop- treatments. Few chemotherapy drugs are available for ment. Changing from one stage to the next requires at the treatment with many serious adverse reactions and least one blood meal. On the other hand, only females of rapid emergence of resistant strains, generating social and mosquitoes and sand flies require a blood meal to fulfil economic losses in those countries. Chikungunya, Mayaro their need to complete the oogenesis process [4]. and Zika virus infections, Crimean-Congo haemorrhagic Vascular damage caused by the haematophagous bite fever, dengue fever, Japanese encephalitis, Rift Valley fever, during the repast triggers physiological defence re- tick-borne encephalitis, West Nile fever, yellow fever, Lyme sponses in the host that are mainly determined by three disease, plague, rickettsiosis, tularaemia, Chagas disease, important events: haemostasis, immunity and inflamma- tion. To accomplish a continued blood flow, a saliva array of pharmacologically active biomolecules, as anti- * Correspondence: [email protected] 1Laboratório de Interação Patógeno-Hospedeiro, Departamento de Biologia haemostatic, anti-inflammatory and immunomodulatory Celular, Instituto de Ciências Biológicas, Universidade de Brasília, Campus compounds, is injected into the bite site [5–9]. Within Universitário Darcy Ribeiro, Asa Norte, 70910-900 Brasília, DF, Brazil this context, different pathogens can be transmitted by Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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. Santiago et al. Parasites & Vectors (2017) 10:79 Page 2 of 20 Table 1 Vector-borne diseases Disease Pathogen Estimated number Major distribution Major vectors Chikungunya Chikungunya virus: 37,480 (Americas, 2015) Africa, the Americas, Asia, Aedes spp. Alphavirus (Togaviridae) Europe Mayaro fever Mayaro virus: Alphavirus 197 cases (2015)a South America Haemagogus (Togaviridae) janthinomys Zika Zika virus: Flavivirus No official WHO reportb Africa and Asia (60s to 80s); Aedes spp. (Flaviviridae) Americas, Western Pacific Crimean-Congo Crimean-Congo virus: Regional outbreaks Africa, the Balkans, the Middle Hyalomma spp. haemorrhagic fever Nairovirus (Bunyaviridae) East, Asia Dengue Dengue virus, serotypes 3.2 million (Americas, South-East Africa, the Americas, Eastern Aedes aegypti and DEN 1–4: Flavivirus Asia and Western Pacific, 2015) Mediterranean, South-East Aedes albopictus (Flaviviridae) Asia, the Western Pacific (secondary vector) Japanese encephalitis Japanese encephalitis virus: 68,000 (Asia, estimated per year) South-East Asia and Western Culex spp. Flavivirus (Flaviviridae) Pacific regions Rift Valley fever Rift Valley virus: Phlebovirus Regional outbreaks Africa, Arabian Peninsula Aedes spp. (Bunyaviridae) Tick-borne encephalitis Tick-borne encephalitis virus: 10,000–12,000 (estimated per year) Europe, northern China, Ixodidae Flavivirus (Flaviviridae) Mongolia, the Russian Federation West Nile fever West Nile virus: Flavivirus Regional outbreaks Africa, Europe, the Middle East, Culex spp. (Flaviviridae) North America and West Asia Yellow fever Yellow fever virus: Flavivirus 200,000 (estimated per year) Africa, Central and South America Aedes and (Flaviviridae) Haemagogus Lyme disease Borrelia burgdorferi 25,359 (USA, 2014)c Areas of Asia, north-western, Ixodidae (Spirochaetaceae) central and eastern Europe, USA Plague Yersinia pestis 783 (2013) Asia and South America (until 90s); Xenopsylla cheopis (Enterobacteriaceae) Africa Rickettsiosis Species of the genera: Millions of cases annuallyc Americas, Europe, Asia, Africa Ticks, lice and Rickettsia, Orientia, Ehrlichia, fleas Neorickettsia, Neoehrlichia and Anaplasma Tularaemia Francisella tularensis Regional outbreaks North America, eastern Europe, Dermacentor spp., (Francisellaceae) China, Japan, Scandinavia Chrysops spp., Amblyomma americanum American Trypanosoma cruzi 6 to 7 million Central and South America Triatominae trypanosomiasis (Trypanosomatidae) (Chagas disease) African trypanosomiasis Trypanosoma brucei 3,796 (2014) sub-Saharan Africa Glossina spp. (sleeping sickness) (Trypanosomatidae) Leishmaniasis Leishmania spp. 900,000–1.3 million Americas, North Africa-Eurasia, Plebotomine (Trypanosomatidae) (estimated per year) East Africa, South-East Asia, sand flies Mediterranean basin Malaria Plasmodium spp. 214 million (estimated, 2015) sub-Saharan Africa, Asia, Latin Anopheles spp. (Plasmodiidae) America, the Middle East Lymphatic filariasis Wuchereria bancrofti 120 million (2000) Angola, Cameroon, Côte d’Ivoire, Culex spp. (Onchocercidae) Democratic Republic of the Congo, India, Indonesia, Mozambique, Myanmar, Nigeria, the United Republic of Tanzania Onchocerciasis Onchocerca volvulus 25 millionc sub-Saharan Africa, Yemen, Brazil, Simulium spp. (Onchocercidae) Venezuela Babesiosis Babesia spp. 1,762 (USA, 2013)c EUA Ixodidae (Babesiidae) Data from World Health Organization (WHO) web page available in <http://www.who.int/en/>. Accessed on September 15, 2016 aData from Brazilian Health Ministry bRecent outbreak in South and Central America but no official count of the number of people infected was reported by WHO cData from Centers for Disease Control and Prevention (CDC) web page available in <http://www.cdc.gov>. Accessed on September 15, 2016 Santiago et al. Parasites & Vectors (2017) 10:79 Page 3 of 20 vector saliva [10, 11]. Depending on each feeding habit, biological processes, with an emphasis on their roles in after achieving the necessary fluidity, the haematopha- vector biology. gous can consume a large amount of blood in a single meal, and proceed to digestion [4]. Various proteases are The role of arthropod vector proteases in blood involved in the blood meal digestion as a means to ob- dependent processes tain the necessary energy for vital biological processes, Haematophagy guaranteeing the haematophagous arthropods’ survival, Haematophagous arthropod vectors tend to take large biological development and reproduction [11]. blood meals, reducing the number of host visits and en- Proteases are enzymes that hydrolyse (a) peptide suring a supply of nutrients for a long period [4]. The bond(s) in amino acid residue sequences; if such cataly- blood-feeding habit can both occur from haemorrhagic sis occurs in internal peptide bonds of a protein, they pools that accumulate in the tissues following skin lacer- are called endopeptidases. However, when cleavage of a ations (pool feeders, as sand flies and ticks) or directly peptide bond takes place at the N- or C-terminal
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