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 Table of Contents  
Year : 2015  |  Volume : 8  |  Issue : 2  |  Page : 95-100

Heat shock proteins: Part III. Arthropods

Department of Parasitology, Faculty of Medicine, Suez Canal University, Ismailia, Egypt

Date of Submission24-Oct-2015
Date of Acceptance09-Nov-2015
Date of Web Publication27-Jan-2016

Correspondence Address:
Sherif M Abaza
Department of Parasitology, Faculty of Medicine, Suez Canal University, Ismailia
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/1687-7942.175005

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  1. Different aspects of HSPs in arthropods
    1.1. Effects of expression in response to blood meal
    1.2. Effects of expression in response to temperature, water dehydration and hypoxia
    1.3. Effects of expression on developmental stages
    1.4. Effects of expression on oogenesis and embryonic development
  2. Other aspects related to HSPs in arthropods
  3. Applications
    Concluding remarks

Keywords: blood-feeding arthropods, bugs, Drosophila spp., mites, mosquitoes, neurodegenerative diseases, oogenesis, thermotolerance, vector control

How to cite this article:
Abaza SM. Heat shock proteins: Part III. Arthropods. Parasitol United J 2015;8:95-100

How to cite this URL:
Abaza SM. Heat shock proteins: Part III. Arthropods. Parasitol United J [serial online] 2015 [cited 2023 Dec 8];8:95-100. Available from: http://www.new.puj.eg.net/text.asp?2015/8/2/95/175005

  Introduction Top

A search made in old literature revealed a few studies conducted on HSP70 and Drosophila spp. In this fly, the hsp70 genes were found to encode two heat shock proteins (HSPs) (68 and 70) and seven heat cognate proteins (HCPs), which are synthesized at normal temperature, but not induced by heat shock. The investigators also succeeded in localizing the fly's hsp70 genes [1],[2] . Subsequently, several studies utilized the fact that HSP70 is conserved among different creatures, including humans. For example, polyclonal antibodies raised against chicken HSP70 cross-reacted with similar proteins from Drosophila spp., yeast, and humans [3] . At the same time, the response to heat of different cultured cells from unrelated species (Drosophila spp., chicken, and man) was investigated. It was found that the HSP84 expressed in Drosophila spp. has considerable homology with the vertebrate HSP85, whereas a less obvious structural similarity was detected in HSP70. The investigators concluded that both HSPs might play similar roles in all eukaryotic organisms [4] . Since then, investigators used the Drosophila spp. hsp70 gene as a heterologous hybridized probe to isolate and clone human hsp70 gene and have detected several homologous features between the human hsp70 genes and the genes encoding Drosophila spp. HSP68 and HSP70 [5] . In 1990, Perkins and colleagues from USA published a review article summarizing hsp70 gene family and discussed the role of the hcp4 gene in all cells during embryonic development. They indicated that HCP4 is enriched in all cells that required rapid growth and change in their shape [6] . Apart from HSP70, human and Drosophila spp. small HSP27 was also found to share functional similarity. French investigators observed that both HSP27 protected murine fibrosarcoma cells against apoptosis induced by reactive oxygen generated by tumor necrosis factor-α [7] . One year later, the same investigators attributed the mechanism of protection against apoptosis to the ability of HSP27 to increase the concentration of intracellular glutathione [8] . In 1999, researchers studied polyglutamine disease proteins using a Drosophila spp. model and were able to show that HSP70 reduces and suppresses these polyglutamine proteins that cause the majority of human neurodegenerative diseases (HNDDs), and HSP70 was suggested for treatment [9] .

In this respect, there is significant evidence that the pathogenesis of these aging-related diseases is a disturbance of glutathione homeostasis with expansion of polyglutamine proteins through reactive oxygen radicals, leading to mitochondrial dysfunction of the neuronal cells. HNDDs are characterized by the aggregation of abnormal proteins and their deposition as nuclear inclusions in the nervous system. Glutathione protects neuronal tissues against oxidative stress and mitochondrial dysfunction and prevents apoptotic cell death [10] . In two review articles, the authors reviewed the inter-relationship between Drosophila spp. and HNDDs [11],[12] . Since then, Drosophila as a model organism was used extensively in modeling HNDDs to screen for toxicity modifiers because genes associated with HNDDs could be expressed in Drosophila. These clinical studies not only enable the clinicians to understand disease pathogenesis [13],[14],[15] but also enable the pharmacologists to understand HSP70 mechanism(s) of actions [16],[17] , as well as enable investigators to assess the efficacy of geldanamycin as HSP70 inhibitor [18] , or heat shock transcription factor 1 [19] , or HSP90 inhibitor that was used in cancer therapy [20] . Some other studies utilized Drosophila spp. model for human Prion disorders (one of the most noncurable HNDDs); the investigators observed that HSP70 could prevent the accumulation of Prion proteins and it showed therapeutic efficacy for their treatment [21] .

The impact of other HSPs in Drosophila spp. model related to HNDDs was investigated in few studies. A study conducted in USA utilized the fact that many of the aggregated proteins that deposited as nuclear inclusions in the nervous system used stereotypical amyloid conformation in their aggregated state. The use of HSP104 to resolubilize amyloid and to retain proteins in its native form and function was evaluated. The investigators created novel Drosophila spp. lines augmented with yeast HSP104 as it is absent in metazoa, and they recommended gene therapy using yeast HSP104 in the treatment of one of the HNDDs, spinocerebellar ataxia type-3 [22] .

The present study aims to review different aspects of HSPs in arthropods and to focus on their applications that in turn will be of much benefit to entomologists.

  1. Different aspects of HSPs in arthropods Top

1.1. Effects of expression in response to blood meal

Several hsp genes showed high expression after temperature increase in response to a blood meal in blood-feeding arthropods [23] . HSP70 was the most HSP reported in several arthropods such as A. aegypti [24] , A. gambiae [25] , Culicoides sonorensis [26] , and the American dog tick, Dermacenta orvariabilis [27] . For reduviid bug Triatoma infestans, German scientists identified genes encoding HSP70 that had homologous sequences with the genes highly expressed in the midgut of Triatoma spp. after a blood meal. Meanwhile, the investigators observed another highly homologous gene related to HSP70 in starved bugs, suggesting its role during starvation [28] .

1.2. Effects of expression in response to temperature, water dehydration and hypoxia

An American study was conducted in 2010 to investigate HSPs gene expression on exposure of different stages of A. aegypti (first instar larvae, pupae, and adults) to temperature (23 and 42°C) for different time intervals (0-180 min). The investigators compared hsp26, hsp83, and hsp70 gene expressions at the two temperatures. The results showed that the first two HSPs were significantly elevated, and the investigators concluded that they are essential proteins for the growth and survival of the first instar larvae and pupae [29] . Two years later, another study was also conducted in USA to investigate the expression of HSP70 and HSP83 and other factors such as antimicrobial peptides (cecropin and defensin) and transferrin in A. aegypti larvae (third instars) after exposure for 24 h to different water temperatures (ranging from 10 to 40°C). The investigators found high HSP83 expression at both the lowest and highest water temperatures. The antimicrobial peptides and transferrin were also overexpressed at 36°C, whereas no overexpression of HSP70 was detected on increasing water temperature up to 36°C [30] .

HSPs were also highly expressed in response to water dehydration in a few arthropods, Drosophila melanogaster [31] , Culex pipiens [32] , and Antarctic midge, Belgica antarctica [33] . The investigators documented the impact of HSP70 and HSP90 on these arthropods. Besides, the tolerance of three mosquito species (A. aegypti, A. gambiae, and C. pipiens) to dehydration was studied by an American team of entomologists. They found that the most resistant species to dehydration was A. aegypti. When the investigators suppressed hsp70 and hsp90 genes in A. aegypti, the mosquitoes became less tolerant to water dehydration [34] .

Another American study was conducted to test the tolerance of bed bug, Cimex lectularius, to temperature and hydration. It was found that C. lectularius did not tolerate exposure for 1 h to either −16 or 48°C and died. The bed bugs could not tolerate more than 15% loss of body water. The investigators also found a high expression of both HSPs (70 and 90) during temperature and hydration stress, with more pronounced levels of HSP90 [35] .

In addition, it was found that adult Drosophila spp. can withstand hypoxia for 3-4 h without cell injury. This fact encouraged the scientists to investigate gene expression during constant or intermittent hypoxia. A significant expression of the hsp70 and hsp23 genes was detected during constant hypoxia [36] .

In contrast, a study conducted in the Czech Republic proved that HSP70 has no role in exposure of lime tree bugs, Pyrrhocoris apterus, to cold stress [37] .

1.3. Effects of expression on developmental stages

Synthesis of 12 HSPs was studied in different stages of Anopheles stephensi, the main vector transmitting malaria in India. It was found that two HSPs (62 and 71) were expressed during the larval stages with a sharp decline in the adult stages, whereas three HSPs (31, 33, and 44) were induced during the pupal stages. On the other hand, eight HSPs were induced during the adult stage, but with very little response toward heat shock. The investigators correlated different HSPs synthesis with the various morphological and physiological events occurring during development [38] . German scientists were the first to identify HSP90 as a component of the pericentriolar material in different developmental stages in Drosophila spp. and in cell lines derived from different species of vertebrates. Besides their immunolocalization studies, the investigators used HSP90 inhibitor (geldanamycin) to determine its role in Drosophila spp. life cycle. The results showed that the essential role of HSP90 was for proper centrosome function, as geldanmycin treatment resulted in defects in microtubule organization and chromosome segregation, suggesting improper centrosome functions [39] . In the same year, Canadian investigators identified and localized four HSPs (22, 23, 26, and 27) in D. melanogaster in three different loci. HSP23 and HSP26 proved to be cytosolic, whereas HSP27 was a nuclear protein in the gonads of adult flies. HSP22 was localized in the mitochondria and expressed at different developmental stages. The investigators suggested its expression during aging and recommended further studies to investigate the role of HSP22 in protection against reactive oxygen radicals [40] .

1.4. Effects of expression on oogenesis and embryonic development

Because the role of cyclin B during mitosis was found to be a conserved process in all organisms, British investigators studied the role of HSP90 during mitosis in Drosophila spp. embryo extracts. Cyclin B, the dynamic molecule or the key regulator for mitosis, is concentrated in the centrosome and microtubules, and the mechanism by which it associates with microtubules was investigated. The results revealed that HSP90 is indirectly essential for efficient localization and association of cyclin B in centrosomes and microtubules. The investigators suggested that HSP90 might improve, through protein folding, the function of a specific domain of cyclin B that is essential for its proper localization on centrosomes and microtubules [41] .

The role of HSP70 in Drosophila spp. oogenesis was investigated in a study conducted in Spain. The results revealed that HSP70 is one of the factors that regulate the migration of border cell in egg chamber, which represents the first step in embryogenesis. Deletion of genes encoding HSP70 in Drosophila spp. results in delay in border cell migration, which causes defects in reorganizing their actin cytoskeleton. In addition, the investigators showed that overexpression of DnaJ-1 (homologous to human HSP40) also caused defects in migration of border cells. They suggested a role of HSP40/HSP70 partnership in the process of Drosophila spp. embryogenesis [42] . One year later, another study was conducted in Italy to elucidate the role of HSP90 during Drosophila spp. oogenesis, as this HSP enhances female germ-line development through gene translational level. When the investigators isolated hsp83 gene from Drosophila spp., there were alterations in the early stages of oogenesis [43] .

  2. Other aspects related to HSPs in arthropods Top

One of the early HSP facts that was detected in relation to arthropods is adaptive cross-protection - i.e., induction of a stress condition induces adaptive protection against another stress condition. Indian investigators found that pre-exposure of the 4 th instar mosquitoes larvae of Anopheles stephensi and A. aegypti to sub-lethal temperature or sub-lethal dose of carbamate insecticide (propoxur) induced adaptive cross-tolerance to the insecticide or thermo-tolerance, respectively [44] .

Determination of the hsp70 gene locus allowed Brazilian investigators to study chromosomal pattern and mutation that occur among Anopheles darlingi mosquitoes, the main vector for malaria in two endemic locations in Brazil. The investigators found that its localization could be used as a marker to assess chromosomal evolution among A. darlingi populations [45] .

To investigate whether 14-3-3 protein could act as a stress protein to prevent protein aggregation and denaturation, Japanese scientists investigated its role under heat stress conditions in Drosophila spp. It was found that one of the components of Drosophila spp. 14-3-3 protein (zeta) is normally expressed under normal conditions. However, exposure of Drosophila spp. to heat led to increased expression through transcriptional activation of its genes. Because of the role played by 14-3-3 zeta protein under stress conditions, the investigators placed it as a stress tolerance factor [46] .

In addition, HSP20 expression was detected by French investigators in the proteomic analysis of the head of P. berghei-infected A. gambiae mosquitoes. The investigators concluded that HSP20 should have an essential role in the capability of sporozoites to penetrate and migrate into the mosquito's salivary gland [47] .

Finally, on reviewing the published articles, no single article on medically important mites was found. All published articles were only on agricultural mites. HSP70 was the most investigated HSP in these articles. Its expression was significantly higher in lead-treated moss mites [48] . Expression levels of HCP70 as a member in HSP70 family were higher during starvation than during heat or cold stress in agricultural Tetranychus urticae mites [49] . Three isoforms of HSP70 were isolated from the same mites, Tetranychus cinnabarinus, and their molecular structure was characterized; the investigators observed higher levels of HSP70-1 and HSP70-3 on exposure of mites to cold and heat stress [50] . The three HSP70 isoforms were also isolated from Panonychus citri, the citrus red mite, and the investigators identified their molecular characters and their sites of expression. HSP70-1 and HSP70-2 were expressed in the cytosol, whereas the third isoform was expressed in the endoplasmic reticulum. It was found that the three isoforms have an essential role in mites' tolerance to heat than to cold stress [51] . HSP70 was also studied in T. urticae and Phytoseiulus persimilis (the predatory mite), and similar results were obtained [52] . On the other hand, hsp90 gene was molecularly characterized from T. cinnabarinus, and the investigators concluded the significant role of HSP90 in extreme temperature tolerance [53] .

  3. Applications Top

Almost all published studies focused on applying HSPs as a new strategy for vector control. After the blood meal taken by the female A. aegypti for egg production, Benoit et al. [54] documented that HSP70 has an essential role in egg production. The investigators suppressed HSP70 expression and recorded its levels in the midgut of suppressed and control mosquitoes. In the control group, HSP70 increased eight-fold within 1 h, and then reduced to two-fold higher than the prefeeding level for the next 12 h. Besides, HSP70 suppression induced impairment of blood digestion in the midgut of A. aegypti, with 25% reduction in egg production, indicating the critical role played by HSP70 to protect the response of the midgut to increased temperatures after a blood meal. It was concluded that HSP70 could be used as a new strategy in control programs to decrease A. aegypti population using HSP70 suppressants.

Insecticidal crystal toxins (Cry) excreted by Bacillus thuringiensis are a safe material for use in insect control programs in agriculture. However, it was found that some insects expressed some sort of defensive mechanism against Cry intoxication. Using proteomic analysis, investigators identified several protein-spots that showed significant expression levels the majority of which proved to be involved in three main functions; 1) protein turnover and folding, 2) energy production and 3) cytoskeleton maintenance. The investigators selected three proteins, each corresponding to one of these functions (HSP90, ATP synthase subunit β, and actin, respectively) and subjected them for systematic analysis. Using gene silencing analyses, the investigators proposed the mechanism(s) by which the midgut of A. aegypti larvae respond against Cry toxins, and the involvement of these three proteins in the defensive response. They concluded that identification of the molecular mechanism(s) provided by the midgut of A. aegypti larvae might facilitate improvement in using Cry toxins in insect control programs [55] .

Another group of scientists identified three isoforms of heat shock factors (HSFs) in A. gambiae, one of them with binding sites to the accessory gland proteins, which are secreted from the male to transfer sperms into the female reproductive tract. The investigators found that silencing HSF1, HSF2, and HSF3 showed downregulation of a large fraction of genes encoding accessory gland proteins, leading to a decrease in mating outcome, anomalies in egg production, ovulation, and sperm storage, with a significant reduction in mosquito populations [56] .

On the other hand, it was found that HSP70 is one of proteins that were down-regulated with mosquitoes' aging. The study was conducted in Australia to find out proteins with proteomic changes during aging of Anopheles spp. transmitting malaria in Australia, gambiae and stephensi. The investigators searched for proteins expressed in Anopheles spp. as they aged. They also assessed the expression changes in these proteins using molecular techniques. They concluded that HSP70 could be used to control malaria transmission through controlling mosquitoes' aging [57] .

  Concluding remarks Top

  1. Drosophila spp. was used extensively in modeling HNDDs because genes encoding HSPs, which are associated with this group of human diseases, could be expressed in Drosophila spp. The conducted studies enabled the clinicians to understand disease pathogenesis and HSPs mechanism(s) of actions and to develop drug targets. Furthermore, several small HSPs were also investigated in Drosophila spp. as a model for human diseases and for their role during aging, with special emphasis on HSP22.
  2. Genes encoding HSPs showed high expression after increased temperature following blood meals in blood-feeding arthropods.
  3. It was found that HSP83 has an essential role in mosquitoes' survival in response to increased temperatures, whereas HSP70 and HSP90 are documented for their survival in response to water dehydration. In C. lectularius, a high expression of both HSPs occurred during temperature and hydration stress, with production of pronounced levels of HSP90. HSP70 and HSP23 were elevated in response of Drosophila spp. to constant hypoxia.
  4. In mosquitoes, different HSPs were documented to impact several morphological and physiological events occurring during their development. In addition, HSP20 was found to improve sporozoite capability in penetration and migration into mosquitoes' salivary gland, and the impact of HSP70 and HSP90 in oogenesis and embryonic development was reported. Gene encoding HSP70 was used to determine mutation among Anopheles mosquitoes.
  5. The only application of HSPs in arthropods is their use as a new strategy in vector control. In blood-feeding arthropods, HSP70 suppression decreased the response of the midgut to increased temperatures following blood meals, leading to decreased capability to digest blood required for egg production. HSP70 was also found to be downregulated with mosquitoes' aging.
  6. Suppression of HSP90 was also found to have a role in vector control. It is considered as one of the factors that improves the response of larvae midgut to insecticidal crystal toxins.
  7. Suppression of HSFs was also suggested to control mosquitoes due to their impact in sperm storage, ovulation, and egg production.

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Conflicts of interest

There are no conflicts of interest.

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