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Rhipicephalus Haemaphysaloides by the Suppression Subtractive Hybridization Approach

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Rhipicephalus Haemaphysaloides by the Suppression Subtractive Hybridization Approach Journal of Integrative Agriculture 2012, 11(9): 1528-1536 September 2012 RESEARCH ARTICLE Identification of Differentially Expressed Genes in the Salivary Gand of Rhipicephalus haemaphysaloides by the Suppression Subtractive Hybridization Approach XIANG Fei-yu, ZHOU Yong-zhi and ZHOU Jin-lin Key Laboratory of Animal Parasitology, Ministry of Agriculture/Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Shanghai 200241, P.R.China Abstract For the purpose of screening and analyzing the differentially expressed genes from the salivary gland of Rhipicephalus haemaphysaloides, two salivary gland-subtracted cDNA libraries of partially fed female ticks and fed male ticks were constructed using suppression subtractive hybridization (SSH). A total of 247 female expression sequence tags (ESTs) and 168 male ESTs were obtained from the two SSH cDNA libraries. It is predicted that 25 female ESTs and 44 female ESTs contain the 5´ and 3´ ends, respectively, and that 53 male ESTs and 74 male ESTs contain the 5´ and 3´ ends, respectively. To identify the subtraction rate of the two SSH cDNA libraries, the RT-PCR method was used to test 24 female ESTs and 21 male ESTs selected randomly but not repeatedly. The results showed that there were 13 upregulated or differentially expressed genes in the partially fed salivary gland of the female R. haemaphysaloides and that the differentially expressed rate was 54%. In addition, they indicated that there were 9 upregulated or differently expressed genes in the fed salivary gland of the male R. haemaphysaloides and that the differentially expressed rate was 43%. Putative translations of 141 (57%) female ESTs and 125 (74%) male ESTs had similarity to GenBank sequences, and 32 (23%) female ESTs and 29 (23%) male ESTs exhibited similarity to tick proteins, which showed that most of the proteins in the libraries were mainly related to the feeding blood physiology of the ticks. Key words: Rhipicephalus haemaphysaloides, salivary gland, suppression subtractive hybridization (SSH), cDNA library, expression sequence tag (EST) Organization 1984). The three-host tick Rhipiceph- INTRODUCTION alus haemaphysaloides is a widely distributed ixodid species in China, India, and other South Asian coun- Ticks rank first as arthropod vectors of fungi, protozoa, tries (Zhou et al. 2006). This tick is a major vector of rickettsiae, bacteria, and viruses, causing diseases in bovine babesiosis in China (Yin et al. 1997) and can non-human vertebrates, and rank second only to mos- also transmit the Kyasanur Forest disease virus, as quitoes as vectors of pathogens to humans (Bior et al. shown by animal experiments (Bhat et al. 1978). The 2002). Tick-borne diseases are particularly devastat- tick-disease complex of R. haemaphysaloides is an im- ing to livestock, especially cattle, with costs estimated portant agriculturally related complex, causing severe to be about $7 billion per annum (Food and Agricultural economic losses in milk and beef production and re- Received 6 June, 2011 Accepted 10 October, 2011 XIANG Fei-yu, Mobile: 13996999752, E-mail: [email protected]; Correspondence ZHOU Jin-lin, Tel: +86-21-34293411, Fax: +86-21-54081818, E-mail: [email protected] © 2012, CAAS. All rights reserved. Published by Elsevier Ltd. Identification of Differentially Expressed Genes in the Salivary Gand of Rhipicephalus haemaphysaloides 1529 striction in the traffic of livestock. abundance transcripts and differentially expressed genes Blood-feeding organisms, including ticks, secrete with high subtraction efficiency. For the purpose of bioactive substances that exhibit a range of pharma- screening and analyzing differentially expressed genes cological properties to thwart the host defense mecha- from the salivary gland of R. haemaphysaloides, two nisms in response to attachment (Oaks et al. 1991; salivary gland-subtracted cDNA libraries of female par- Bowman et al. 1997). A large proportion of these tially fed and male fed ticks were constructed using SSH. substances are produced in the salivary glands and secreted into the host during blood feeding. During RESULTS this period, the salivary gland plays a key role that helps the tick feed on blood. The salivary glands of ixodid females undergo remarkable growth and dif- Suppression subtractive hybridization PCR ferentiation during tick feeding as their cells become competent to transport fluid. The mass and protein After 2 rounds of hybridization, the products were am- content of the salivary glands increase about 25-fold, plified by PCR-select with primer pairs and nested primer but the number of cells does not increase (Sauer et al. pairs, and the subtractive cDNA fragments were then 2000). It has been observed that, during the blood obtained. The size and abundance of the PCR products meal, new mRNAs are induced in the salivary glands, were examined by agarose gel electrophoresis. The re- leading to the synthesis of a wide range of new pro- sults showed that the sizes of the subtractive cDNA frag- teins (Leboulle et al. 2000). In contrast to females, ments mainly ranged between 500 and 750 bp (Fig. 1). very little is known about the physiological, biochemical, and molecular changes in the salivary glands of male ticks before or after male attachment to the host. While female ticks imbibe large volumes of blood over 2 wk, male ixodid ticks are intermittent feeders with relatively low blood intake. The mass of the salivary glands of male A. americanum increases about 1.6-fold during feeding (Shipley et al. 1993). The type IV acinus, re- stricted to males, is thought to have a reproductive role, possibly in sperm transfer (Feldman-Muhsam et al. 1970). Wang and Nuttall (1998) provided evidence for male-specific immunoglobulin-G-binding proteins that are hypothesized to be important in protecting the mate during attachment and feeding by nearby females (Wang et al. 1998). It is believed that several these induced genes are essential for the completion of the tick feed- ing process and the transmission of pathogens. Therefore, to screen the differentially expressed genes of the salivary gland, we can identify the dynamic changes occurring at the bioactive molecular level dur- ing male and female tick feeding and obtain valuable functional molecular information. A PCR- select cDNA subtraction method (suppression subtractive hybridization, SSH) was de- veloped by Clontech, USA. Because it includes a nor- Fig. 1 Gel electrophoresis of the subtraction PCR-select products from the salivary gland cDNA of the female (A) and male (B) malization step to equalize the abundance of cDNAs R. haemaphysaloides. Lane 1, subtraction result; lane 2, within the target population, this method can detect low- unsubtraction control; M, DL2000 marker. © 2012, CAAS. All rights reserved. Published by Elsevier Ltd. 1530 XIANG Fei-yu et al. Characterization of select clones and sequences regulation, energy metabolism, and antioxidization of the 2 subtractive cDNA libraries (Tables 3 and 4). After screening the 2 subtractive cDNA libraries with DISCUSSION nested primer 1 and primer 2R, all positive clones in the libraries were sequenced. By searching the primer 1 SSH is a highly efficient method to screen and isolate and primer 2R in the sequences with the software differentially expressed genes. We successfully applied DNAMAN (v4.0), 247 female ESTs and 168 male ESTs SSH in this test and isolated some valuable genes re- were obtained. Based on the characteristic sequence lated to tick feeding. One potential disadvantage of the ACGCGGG and the poly(A) sequence, it was predicted SSH technique first reported by Diatechenko (1996) is that 25 female ESTs and 44 female ESTs would con- the fact that a few micrograms of poly(A) RNA and tain the 5´ and 3´ ends, respectively, and that 53 male some low-redundancy RNA may be difficult to obtain. ESTs and 74 male ESTs would contain the 5´ and 3´ To resolve this problem, an amplification step for both ends, respectively (Table 1). the driver and tester cDNAs was incorporated to gen- erate sufficient quantities of both cDNA samples be- Confirmation of differential expression of genes fore initiating the SSH procedure. In our protocol, we solved this problem with LD-PCR by use of the After the subtracted cDNA library was obtained, it was CLONTECH Super SMART PCR cDNA Synthesis Kit, important to confirm that individual clones did indeed USA. In the typical SSH protocol, the lowest quantity represent differentially expressed genes. This was ac- of RNA is 2 µg. However, for the SMART method, the complished by RT-PCR with randomly selected minimum amount of starting material for standard cDNA sequences. Therefore, 24 female and 21 male se- is 2 ng of the total RNA. In our experiment, the differ- quences were selected randomly but not repeatedly. entially expressed rate was high, and some valuable The primers were designed using DNAMAN (v4.0) genes were isolated. software. The length of all primers was about 20 bp, The present results demonstrate that new gene ex- and all amplified products were about 250 bp, includ- pression occurs in the salivary glands of male and fe- ing the control. The results showed that there were 13 male R. haemaphysaloides. These salivary gland upregulated or differentially expressed genes in the proteins, which play an important role in tick biology, pa r t i a l l y fe d s a l i v a r y gl a nd o f t he fema l e e.g. as histamine binding and immunoglobulin binding R. haemaphysaloides and that the differenti al ly ex- proteins and serine proteinase inhibitors, have been de- pressed rate was 54%. In addition, they indicated that scribed previously (Waxman et al. 1990; Wang et al. there were 9 upregulated or differently expressed genes 1995; Sangamnatdej et al. 2002). Considering the di- in the fed salivary gland of the male R. haemaphysaloides verse roles of putative secreted proteins in blood feeding, and that the differentially expressed rate was 43%.
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