Identification and characterization of the fibrinogen-like domain of fibrinogen-related proteins in the mosquito, Anopheles gambiae, and the fruitfly, Drosophila melanogaster, genomes
- 6k Downloads
- 42 Citations
Abstract
Background
The fibrinogen-like (FBG) domain, which consists of approximately 200 amino acid residues, has high sequence similarity to the C-terminal halves of fibrinogen β and γ chains. Fibrinogen-related proteins (FREPs), which contain FBG domains in their C-terminal region, are found universally in vertebrates and invertebrates. In invertebrates, FREPs are involved in immune responses and other aspects of physiology. To understand the complexity of this family in insects, we analyzed FREPs in the mosquito genome and made comparisons to FREPs in the fruitfly genome.
Results
By using the genome data of the mosquito, Anopheles gambiae, 53 FREPs were identified, whereas only 20 members were found in the Drosophila melanogaster genome. Using sequence profile analysis, we found that FBG domains have high sequence similarity and are highly conserved throughout the FBG domain region. By secondary structure analysis and comparison, the FBG domains of FREPs are predicted to function in recognition of carbohydrates and their derivatives on the surface of microorganisms in innate immunity.
Conclusion
Detailed sequence and structural analysis discloses that the FREP family contains FBG domains that have high sequence similarity in the A. gambiae genome. Expansion of the FREP family in mosquitoes during evolutionary history is mainly accounted for by a major expansion of the FBG domain architecture. The characterization of the FBG domains in the FREP family is likely to aid in the experimental analysis of the ability of mosquitoes to recognize parasites in innate immunity and physiologies associated with blood feeding.
Keywords
Protein Data Bank GlcNAc Hemocyte Actual Transcript Human FibrinogenAbbreviations
- FBG domain
fibrinogen-like domain
- FREP
fibrinogen-related protein
- AL-1
aslectin, TL5A, tachylectin 5A
- GlcNAc
N-acetylglucosamine
- MAP
microfibril-associated protein
- aa
amino acid
- BLAST
basic local alignment search tool
- PSI-BLAST
position specific iterative BLAST
- EST
expressed sequence tag
- PDB
protein data bank
- Molmol
molecule analysis and molecule display.
Background
In mammals, fibrinogen, a soluble plasma protein, contains six polypeptide chains, two each of the Aα, Bβ and γ chains, linked by 29 disulfide bonds. Fibrinogen participates in both the cellular phase and the fluid phase of coagulation [1]. The fibrinogen-like (FBG) domain, which consists of approximately 200aa residues and has high similarity to the C-terminal halves of fibrinogen β and γ chains, has been found in a growing number of proteins [2]. Three distinct fibrinogen-related proteins (FREPs) have been identified in human: ficolin, tenascins, and microfibril-associated protein (MAP) [3, 4, 5]. These FREPs all contain a common C-terminal FBG domain with high sequence identity to the C-terminal regions of fibrinogen β and γ chains, but differ in their N-terminal regions. The FBG domain in ficolin can be brought together as clusters of three by collagen O-like triple helices, and is responsible for N-acetylglucosamine (GlcNAc) binding activity [6]. Recent studies have shown that human serum ficolins act as phagocytic receptors on circulating monocytes for microorganism recognition [7]. Tenascins are a family of multifunctional extracellular matrix (ECM) glycoproteins subject to complex spatial and temporal patterns of expression in the course of various organogenetic processes. These proteins mediate cell adhesion and show tissue-specific and cell growth-associated expression [4]. Microfibril-associated protein, another extracellular matrix protein, is a component of connective tissue microfibrils and a candidate for involvement in the etiology of inherited connective tissue diseases, which are associated with the Smith-magenis syndrome, a multiple congenital anomaly/mental retardation syndrome [8].
In invertebrates, several FREPs have been reported in various species, such as tachylectins from the horseshoe crab, Tachypleus tridentatus [9], fibrinogen-related proteins (FREP) from the snail, Biomphalaria glabrata [10], ficolins from the solitary ascidian, Halocynthia roretzi [11], tachylectin-related protein in the sponge, Suerites domuncula [12] and aslectin (AL-1) from the mosquito, Armigeres subalbatus [13]. All of these FREPs contain a common C-terminal FBG domain with high sequence identity to that of fibrinogen β and γ chains, but which differs in their N-terminal regions. These FREPs likely play an important role in the innate immune response against parasites [9, 12, 13]. The FBG domain of tachylectin is able to bind GlcNAc [9]. Aslectin, which also binds GlcNAc, is able to bind bacteria, and is likely involved in the antibacterial immune response in mosquitoes [13].
The rapid progress in the development of whole genome and expressed sequence tag (EST) databases provides an abundance of sequence data that greatly facilitates gene function studies. Using bioinformatics, one can mine the information from these databases to acquire an overview of each gene family and assess evolutionary relationships among its members [14]. Although the FREP family in the genomes of Anopheles gambiae and Drosophila melanogaster was briefly compared earlier [15], the FBG domains in this gene family have not been comparatively characterized. In this study, data derived from the genome and EST databases of the mosquito, A. gambiae, and the fruitfly, D. melanogaster, are presented here as an initial, yet exhaustive search for FREPs in both species. Provided is an overview of this protein family, including sequence alignments, patterns of conservation, and phylogenetic relationships. A further comparison between the annotated gene products from the genome sequences and the actual transcripts from the EST database also is made. In summary, these studies provide the first encompassing description of the FREP gene family in insects and establish a foundation for future studies that aim to define the role of these genes.
Results and discussion
Identification of FREP genes and characterization of the FBG domain in the A. gambiae genome
Fibrinogen-related proteins in A. gambiae and D. melanogaster
Gene ID | Length (aa)1 | FBG domain2 | Chromosomal location | Transcription3 | ||
---|---|---|---|---|---|---|
P | M | EST | cDNA library | |||
A. gambiae | ||||||
EAA10385 | 201 | full | 2L 20D | - | ||
EAA10406 | 217 | full | 2L 20D | - | ||
EAA04425 | 186 | full | 2L 26A | + | Hemocyte | |
EAA10466 | 865 | 848 | 3' truncated | 2L 21A | + | Development |
EAA14231 | 226 | full | 3R 35B | + | NAP1 | |
EAA44096 | 190 | full | 2L 23B | + | NAP1,NAH, Blood1,NAFB | |
EAA05203 | 296 | 273 | full | 3L 42B | - | |
EAA05102 | 363 | 341 | full | 3L 42A | + | 4A3A,NAP1,NAH, Blood1,NAFB |
EAA05205 | 308 | full | 3L 42A | - | ||
EAA05224 | 310 | full | 3L 42A | + | 4A3B, NAH, Blood1 | |
EAA43404 | 314 | 292 | full | 3R 33C | - | |
EAA01903 | 236 | full | Unknown | + | NAP1 | |
EAL39348 | 202 | full | 3L 40A | - | ||
EAA10360 | 688 | 660 | full | 2L 21A | - | |
EAA00222 | 173 | full | Unknown | - | ||
EAA13725 | 182 | full | 3L 40A | - | ||
EAA05204 | 543 | 3' truncated | 3L 42A | - | ||
EAA13743 | 187 | full | 3L 40A | - | ||
EAA01418 | 362 | 337 | 3' truncated | 2R 10A | - | |
EAA05160 | 216 | 3' truncated | 3L 42B | + | NAH, IRB, Blood1 | |
EAA04072 | 280 | 258 | full | 2L 26B | + | NAH, blood1 |
EAL39349 | 262 | 3' truncated | 3L 40A | - | ||
EAA05042 | 777 | 756 | full | 3L 42A | + | Blood1, cDNA1 |
EAA03931 | 178 | full | 2L 26D | + | Blood1, cDNA1, NAH | |
EAA02818 | 144 | 3' truncated | Unknown | + | NAP1 | |
EAA09906 | 171 | 5' truncated | 3L 39A | + | NAH, NAFB, Blood1 | |
EAL39350 | 330 | 308 | full | 3L 40A | - | |
EAL39343 | 284 | 3' truncated | 3L 40A | - | ||
EAA13689 | 178 | 3' truncated | 3L 40A | - | ||
EAA04169 | 234 | 3' truncated | 2L 26A | - | ||
EAL41889 | 339 | full | 2L 26D | - | ||
EAA05087 | 211 | 3' truncated | 3L 42A | - | ||
EAA06922 | 323 | 267 | 3' truncated | X 5A | + | NAH, NAFB, Blood1 |
EAA01294 | 185 | full | 2R 8C | - | ||
EAA15009 | 183 | 5' truncated | 3R 33B | + | NAP1 | |
EAL39347 | 242 | 3' truncated | 3L 40A | - | ||
EAA13749 | 180 | 3' truncated | 3L 40A | - | ||
EAA05439 | 266 | 3' truncated | 3L 40B | - | ||
EAA05095 | 259 | 230 | 3' truncated | 3L 42A | - | |
AAR01125 | 268 | 3' truncated | Unknown | - | ||
EAA13688 | 1020 | 3' truncated | 3L 40A | + | cDNA1 | |
EAA05097 | 166 | 3' truncated | 3L 42A | - | ||
EAL39030 | 81 | 3' truncated | 3R 33B | + | NAP1 | |
EAA05065 | 116 | 3' truncated | 3L 42A | - | ||
EAL40630 | 94 | 3' truncated | Unknown | - | ||
EAA13692 | 441 | Full | 3L | + | NAP1 | |
EAA02970 | 321 | 300 | Full | Unknown | - | |
EAA13755 | 596 | Full | 3L | - | ||
EAA13691 | 231 | Full | 3L 40A | - | ||
EAA13726 | 212 | Full | 3L 40A | + | NAFB | |
EAA13760 | 271 | Full | 3L | + | cDNA1 | |
EAA10480 | 284 | 265 | Full | 2L | - | |
EAA05069 | 227 | 204 | 3' truncated | 3L | + | NAP1 |
D. melanogaster | ||||||
AAM68209 | 291 | 271 | Full | 2R 58B9 | + | GH |
AAF57948 | 246 | 225 | Full | 2R 53D1 | + | RE |
AAF44911 | 187 | 167 | 3' truncated | 2L 34C4 | - | |
AAF59068 | 347 | Full | 2R 44D4 | - | ||
AAF52372 | 176 | 5' truncated | 2L 26C3 | - | ||
AAF48780 | 358 | 335 | Full | X 16F1 | + | LP |
AAM52597 | 195 | Full | X 9A3 | + | RE, GH | |
AAF46536 | 332 | 310 | Full | X 9A3 | + | RH, GH, EK |
AAN09619 | 241 | Full | X 9A3 | + | RH, GH, EK | |
AAL48972 | 198 | 177 | 3' truncated | 2R 53D1 | + | RE |
AAF47782 | 459 | 436 | Full | 3L 63E5 | + | RE, GM, EK,LP,CA |
AAF58455 | 799 | 758 | Full | 2R 49D3 | + | RE, SD,RE,EK,LP |
AAF55227 | 363 | Full | 3R 89A5 | + | ||
AAF49079 | 422 | Full | 3L 76E1 | + | RE, GM, EK, EC | |
AAN11645 | 406 | Full | 3L 76E1 | + | EK, GM | |
AAM11109 | 154 | 5' truncated | 3L 76E1 | + | EK, GM | |
AAF46535 | 334 | 315 | Full | X 9A3 | + | RE, GH |
AAN09447 | 251 | Full | X 16F1 | + | LP | |
AAF46801 | 157 | 5' truncated | 2R 58B8 | - | ||
AAA28880 | 774 | 752 | Full | 2R 49D3 | + | RE, SD,RE,EK,LP |
Multiple sequence alignment of a representative set of the FBG domains of the FREP family in A. gambiae . Multiple sequence alignment was constructed using T-Coffee program. The 100% consensus sequence was boxed with black in the alignment. The PHD secondary structure is shown above the alignment with H representing an α-helix and E representing a β-strand. The sequences are denoted by their gene names in GenBank.
Conserved structure of the FBG domain in the FREP family and variation in some members
Distribution of multiple FBG domains in the members of FREP family in A. gambiae . The protein is represented by a line with the number above corresponding to amino acids which start from the N-terminus of each protein. The identified domains are shown under the line. FReD represents FBG domain. ZnMc represents Zinc-dependent metalloprotease domain. The sequences are denoted by their gene name in GenBank.
Ribbon representation of the core structure of the FBG domain of tachylectin 5A (PDB: 1JC9) and recombinant human γ-fibrinogen carboxyl terminal fragment (PDB: 2FIB). A. Ribbon plot of the FBG domain of TL5A. The domain shown here is a cartoon representation from the crystal structure. Main α-helices and β-sheets were shown in the figure. The residues forming the ligand-binding packet are depicted in the stick format and labeled in red. B. Superposition of the crystal structure of the FBG domain of TL5A (grey) and human γ-fibrinogen carboxyl terminal fragment (golden). By aligning TL5A and the γ chain fragment, the region composed of 178aa residues at the C-terminal regions of both proteins was used to generate superposition ribbon plot. Loop P-1 and P-3 in fibrinogen γ chain fragment are represented in green.
Topology diagram showing the arrangement of secondary-structure elements in the FBG domains of TL 5A. Domains named in analogy to human fibrinogen γ chain fragment. α-helix is represented in green and β-sheet is represented in brown. Domain B and domain P are separated by a red line. Starting position of amino acid in each secondary structure is shown in the figure with single letter. The disulfide bridge (Cys-206-Cys-219) in the domain P is represented by a dot line.
Recombinant human γ-fibrinogen carboxyl terminal fragment (A) and surface of electrostatic potential of tachylectin 5A (B). A. Negative charged patch was outlined in circle. B. Hydrophobic groove was outlined in circle. The orientation is the same in both A and B. Red is for negative charge, blue is for positive charge and grey is non-polar areas.
Phylogenetic relationships of the FBG domains in A. gambiae
Genomic distribution of FREP family members in A. gambiae . Chromosomes are represented with a line and chromosomal numbers are shown on the top of each chromosome. Chromosomal loci of the FREP genes are shown with their name. The proteins are denoted by their gene name in GenBank.
Phylogenetic tree of the FBG domains of the FREP family in A. gambiae . Phylogenetic relationships of the FBG domains are shown. The seed alignment used for constructing the tree was the multiple alignment sequences shown in Fig. 1. Maximum-likelihood approach was used to construct the tree with the proml program of the PHYLIP package, which uses the Jones-Taylor-Thornton model of change between amino acids and a Hidden Markov Model (HMM) method of inferring different rates of evolution at different amino acid positions. The FBG domains of each FREP are denoted by their gene name in GenBank.
ESTs for FREPs in mosquitoes
Description of EST libraries from A. gambiae and D. melanogaster
Name | Description | Supplier |
---|---|---|
A. gambiae | ||
NAP1 | mix developmental stages | European Molecular Biology |
NAFB | Normalized Fat Body Library | University of Notre Dame |
cDNA1 | Adult cDNA1 | Celera Genomics |
4A3B | cDNA libraries derived from immune-responsive hemocyte-like cell lines | |
blood1 | Adult with blood-fed cDNA | Celera Genomics |
NAH | Normalized Anopheles Head | University of Notre Dame |
IRB | Infected Rat Blood-fed 30 hr Abdomen, Female adult 5–7 days post eclosion | University of Notre Dame |
D. melanogaster | ||
GH | Adult male and female head | |
RE | normalized Embryo from male and female, 0–24 hours mixed stage embryonic | Lawrence Berkeley National lab |
LP | Whole body Larval-early pupal from male and female | |
RH | Adult male and female normalized Head pFlc-1 | Lawrence Berkeley National lab |
EK | Mixed stage embryos, imaginal disks and adult head | Lawrence Berkeley National lab |
GM | Ovary, newly eclosed females, germarium-stage 6, female. | |
SD | Schneider L2 cell culture pOT2, cell line | British Columbia Cancer A |
CA | Male and female salivary gland, 16, 18, 20, 22, and 24 hrs after puparium formation | |
EC | Fat body-3rd instar larva | Lawrence Berkeley National lab |
Fibrinogen-related proteins in D. melanogaster
Multiple sequence alignment of a representative set of the FBG domains of FREP in D. melanogaster . Multiple sequence alignment was constructed using T-Coffee program. The 100% consensus sequence was boxed with black in the alignment. The PHD secondary structure is shown above the alignment with H representing an α-helix and E representing a β-strand. The sequences are denoted by their gene name in GenBank.
Genomic distribution of FREP family members in D. melanogaster . Alternative spliced transcripts from the same gene are represented with [. The others are as detailed in Figure 6.
Phylogenitic tree of the FBG domains from A. gambiae and D. melanogaster . The seed alignment used for constructing the tree was the multiple alignment sequences of representative set of the FBG domains of FREP families in A. gambiae and D. melanogaster. The phylogenetic tree was constructed as described in methods and detailed in Fig. 5. The FBG domains of each FREP are denoted by their gene name in GenBank. The name of the FREP from A. gambiae start with E, and the name of the FREP from D. melanogaster start with A.
Compared with the D. melanogaster FREP gene family, the massive expansion of the FREP gene family in mosquitoes probably is associated with particular aspects of the mosquito's biology, possibly hematophagy and exposure to parasites [15]. The blood meal imposes challenges associated with proliferation of the microbial flora in the gut and coagulation of ingested blood and penetration of the midgut by blood-born pathogens. A FREP protein (e.g AL-1) in the mosquito Ar. subalbatus has bacteria binding properties, and it has been suggested that FREP may be important in controlling bacteria infections in mosquitoes [13]. However, mosquitoes may use a number of FREP proteins as anticoagulants, for instance, as competitive inhibitors preventing polymerization of blood [15]. Some mosquito FREP genes are up-regulated by invading malaria parasites [20, 21], suggesting a possible role in an antimalarial defense system.
Conclusion
The detailed sequence and structural analyses disclose that the FREP family contains highly similar FBG domains in the A. gambiae genome. FBG domains are predicted to recognize carbohydrates and their derivatives. The sequence divergence seen in the binding domains of FBG domains makes it possible to recognize a wide range of carbohydrate derivatives. This suggests that the FREP family may play an important role in innate immunity. Expansion of the family during evolutionary history is mainly accounted for by a major expansion of the FBG domain architectures. Further analysis of the chromosomal locations and phyletic patterns of the FBG domains suggest that they have been acquired by tandem duplication and shuffling. Compared with D. melanogaster, the massive expansion of the FREP family in A. gambiae probably is associated with particular aspects of the mosquito's biology, such as exposure to parasites and hematophagy. Experimental investigations of these proteins are likely to be of interest in understanding insect innate immunity and physiology.
Methods
Database searching and sequence retrieving for fibrinogen-related protein
A PSI-BLAST search [22] of the A. gambiae and D. melanogaster genome database at the National Center for Biotechnology Information (NCBI) [23] was performed using AL-1 as a query. To obtain the recent progress of FREP in A. gambiae genome, the A. gambiae database at Ensembl [24] was also searched. Following accumulation of the complete list of accession numbers, the corresponding protein sequence was retrieved from GenBank at NCBI and Ensembl.
Signal peptide prediction
Signal peptides were predicted using the SignalPv3.0 [25, 26].
Searching for ESTs database
To determine the actual transcripts for individual FREP genes, BLAST search of an EST database at Berkeley Drosophila Genome Project and TIGR A. gambiae Gene Index (AgGI) was performed [27, 28]. The annotated cDNA sequences encoding FREPs identified in the PSI-BLAST search were used as queries for individual BLAST search in these EST database. The availability of EST was determined based on sequence similarity with the query: a 97% or greater identity was considered to be an EST corresponding to a specific gene. To get information about FREP transcripts in the mosquito, Ar. Subalbatus and Ae. aegypti, hemocyte EST databases at ASAP in both species were searched using AL-1 as a seed [18, 29].
Multiple sequence alignment and phylogenetic analysis
Multiple sequence alignment was performed using the T-Coffee program [30, 31]. Phylogenetic analysis was carried out with the maximum-likelihood algorithm [32]. The package used for phylogenetic analysis was proml program from PHYLIP [33], and the unrooted tree was draw using drawtree program in this package.
View of DNA sequence annotation
To verify the annotation of truncated genes, the corresponding genomic sequences was scanned by Artemis [34].
Secondary structure prediction
Secondary structure prediction was produced with the PHD program [35], with multiple alignment of individual FBG domains of FREP family. The structure data of TL5A and recombinant human γ-fibrinogen carboxyl terminal fragment were obtained from protein data bank (PBD) [36] and the ribbon diagrams were constructed with Molmol program [37].
Chromosomal location and alternative splice transcripts
The chromosomal location of the FREP genes in A. gambiae genome was retrieved at Ensembl [24]. The chromosomal location of the FREP genes in D. melanogaster was retrieved at NCBI [23]. To identify alternative spliced transcripts for each gene, spidey, a cDNA-to-genomic alignment program, was used to align spliced sequences to genomic sequences, using local alignment algorithms and heuristics to put together a global spliced alignment [38].
Notes
Acknowledgements
We thank Thomas A. Rocheleau and George Mayhew for critically reading the manuscript and useful discussion. We are grateful to Anthony Nappy for assistance with graphics. This study was supported by NIH grant AI 19769.
Supplementary material
References
- 1.Gorkun OV, Veklich YI, Weisel JW, Lord ST: The conversion of fibrinogen to fibrin: recombinant fibrinogen typifies plasma fibrinogen. Blood. 1997, 89: 4407-14.PubMedGoogle Scholar
- 2.Lu J, Le Y: Ficolins and the fibrinogen-like domain. Immunobiology. 1998, 199: 190-199.PubMedCrossRefGoogle Scholar
- 3.Matsushita M, Fujita T: The role of ficolins in innate immunity. Immunobiology. 2002, 205: 490-497. 10.1078/0171-2985-00149.PubMedCrossRefGoogle Scholar
- 4.Erickson HP: Tenascin-C, tenascin-R and tenascin-X: a family of talented proteins in search of functions. Curr Opin Cell Biol. 1993, 5: 869-76. 10.1016/0955-0674(93)90037-Q.PubMedCrossRefGoogle Scholar
- 5.Kobayashi R, Mizutani A, Hidaka H: Isolation and characterization of a 36-kDa microfibril-associated glycoprotein by the newly synthesized isoquinolinesulfonamide affinity chromatography. Biochem Biophys Res Commun. 1994, 198: 1262-6. 10.1006/bbrc.1994.1178.PubMedCrossRefGoogle Scholar
- 6.Lu J, Teh C, Kishore U, Reid KB: Collectins and ficolins: sugar pattern recognition molecules of the mammalian innate immune system. Biochim Biophys Acta. 2002, 1572: 387-400.PubMedCrossRefGoogle Scholar
- 7.Teh C, Le Y, Lee SH, Lu J: M-ficolin is expressed on monocytes and is a lectin binding to N-acetyl-D-glucosamine and mediates monocyte adhesion and phagocytosis of Escherichia coli. Immunology. 2000, 101: 225-32. 10.1046/j.1365-2567.2000.00099.x.PubMedPubMedCentralCrossRefGoogle Scholar
- 8.Zhao Z, Lee CC, Jiralerspong S, Juyal RC, Lu F, Baldini A, Greenberg F, Caskey CT, Patel PI: The gene for a human microfibril-associated glycoprotein is commonly deleted in Smith-Magenis syndrome patients. Hum Mol Genet. 1995, 4: 589-97.PubMedCrossRefGoogle Scholar
- 9.Gokudan S, Muta T, Tsuda R, Koori K, Kawahara T, Seki N, Mizunoe Y, Wai SN, Iwanaga S, Kawabata S: Horseshoe crab acetyl group-recognizing lectins involved in innate immunity are structurally related to fibrinogen. Proc Natl Acad Sci USA. 1999, 96: 10086-10091. 10.1073/pnas.96.18.10086.PubMedPubMedCentralCrossRefGoogle Scholar
- 10.Adema CM, Hertel LA, Miller RD, Loker ES: A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc Natl Acad Sci USA. 1997, 94: 8691-8696. 10.1073/pnas.94.16.8691.PubMedPubMedCentralCrossRefGoogle Scholar
- 11.Kenjo A, Takahashi M, Matsushita M, Endo Y, Nakata M, Mizuochi T, Fujita T: Cloning and characterization of novel ficolins from the solitary ascidian, Halocynthia roretzi. J Biol Chem. 2001, 276: 19959-19965. 10.1074/jbc.M011723200.PubMedCrossRefGoogle Scholar
- 12.Schroder HC, Ushijima H, Krasko A, Gamulin V, Thakur NL, Diehl-Seifert B, Muller IM, Muller WE: Emergence and disappearance of an immune molecule, an antimicrobial lectin, in basal metazoa. A tachylectin-related protein in the sponge Suberites domuncula. J Biol Chem. 2003, 278: 32810-7. 10.1074/jbc.M304116200.PubMedCrossRefGoogle Scholar
- 13.Wang X, Rocheleau TA, Fuchs JF, Hillyer JF, Chen CC, Christensen BM: A novel lectin with a fibrinogen-like domain and its potential involvement in the innate immune response of Armigeres subalbatus against bacteria. Insect Mol Biol. 2004, 13: 273-82. 10.1111/j.0962-1075.2004.00484.x.PubMedCrossRefGoogle Scholar
- 14.Redfern O, Grant A, Maibaum M, Orengo C: Survey of current protein family databases and their application in comparative, structural and functional genomics. J Chromatogr B Analyt Technol Biomed Life Sci. 2005, 815: 97-107.PubMedCrossRefGoogle Scholar
- 15.Zdobnov EM, von Mering C, Letunic I, Torrents D, Suyama M, Copley RR, Christophides GK, Thomasova D, Holt RA, Subramanian GM, Mueller HM, Dimopoulos G, Law JH, Wells MA, Birney E, Charlab R, Halpern AL, Kokoza E, Kraft CL, Lai Z, Lewis S, Louis C, Barillas-Mury C, Nusskern D, Rubin GM, Salzberg SL, Sutton GG, Topalis P, Wides R, Wincker P, Yandell M, Collins FH, Ribeiro J, Gelbart WM, Kafatos FC, Bork P: Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science. 2002, 298: 149-59. 10.1126/science.1077061.PubMedCrossRefGoogle Scholar
- 16.Kairies N, Beisel HG, Fuentes-Prior P, Tsuda R, Muta T, Iwanaga S, Bode W, Huber R, Kawabata S: The 2.0-A crystal structure of tachylectin 5A provides evidence for the common origin of the innate immunity and the blood coagulation systems. Proc Natl Acad Sci USA. 2001, 98: 13519-24. 10.1073/pnas.201523798.PubMedPubMedCentralCrossRefGoogle Scholar
- 17.Yee VC, Pratt KP, Cote HC, Trong IL, Chung DW, Davie EW, Stenkamp RE, Teller DC: Crystal structure of a 30 kDa C-terminal fragment from the gamma chain of human fibrinogen. Structure. 1997, 5: 125-38. 10.1016/S0969-2126(97)00171-8.PubMedCrossRefGoogle Scholar
- 18.Glasner JD, Liss P, Plunkett G, Darling A, Prasad T, Rusch M, Byrnes A, Gilson M, Biehl B, Blattner FR, Perna NT: ASAP, a systematic annotation package for community analysis of genomes. Nucleic Acids Res. 2003, 31: 147-51. 10.1093/nar/gkg125.PubMedPubMedCentralCrossRefGoogle Scholar
- 19.Bartholomay LC, Cho WL, Rocheleau TA, Boyle JP, Beck ET, Fuchs JF, Liss P, Rusch M, Butler KM, Wu RC, Lin SP, Kuo HY, Tsao IY, Huang CY, Liu TT, Hsiao KJ, Tsai SF, Yang UC, Nappi AJ, Perna NT, Chen CC, Christensen BM: Description of the transcriptomes of immune response-activated hemocytes from the mosquito vectors Aedes aegypti and Armigeres subalbatus. Infect Immun. 2004, 72: 4114-26. 10.1128/IAI.72.7.4114-4126.2004.PubMedPubMedCentralCrossRefGoogle Scholar
- 20.Dimopoulos G, Christophides GK, Meister S, Schultz J, White KP, Barillas-Mury C, Kafatos FC: Genome expression analysis of Anopheles gambiae : responses to injury, bacterial challenge, and malaria infection. Proc Natl Acad Sci USA. 2002, 99: 8814-9. 10.1073/pnas.092274999.PubMedPubMedCentralCrossRefGoogle Scholar
- 21.Srinivasan P, Abraham EG, Ghosh AK, Valenzuela J, Ribeiro JM, Dimopoulos G, Kafatos FC, Adams JH, Fujioka H, Jacobs-Lorena M: Analysis of the Plasmodium and Anopheles transcriptomes during oocyst differentiation. J Biol Chem. 2004, 279: 5581-7. 10.1074/jbc.M307587200.PubMedPubMedCentralCrossRefGoogle Scholar
- 22.Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25: 3389-402. 10.1093/nar/25.17.3389.PubMedPubMedCentralCrossRefGoogle Scholar
- 23.The National Center for Biotechnology Information (NCBI). [http://www.ncbi.nlm.nih.gov.]
- 24.The A. gambiae database at Ensembl. [http://www.ensembl.org/Anopheles_gambiae/]
- 25.Nielsen H, Engelbrecht J, Brunak S, von Heijne G: Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering. 1997, 10: 1-6. 10.1093/protein/10.1.1.PubMedCrossRefGoogle Scholar
- 26.The SignalPv3.0. [http://www.cbs.dtu.dk/services/SignalP/]
- 27.Berkeley Drosophila Genome Project. [http://www.fruitfly.org/EST/]
- 28.TIGR A. gambiae Gene Index (AgGI). [http://www.tigr.org/tdb/tgi/aggi/]
- 29.The mosquito, Ar. Subalbatus and Ae. aegypti, hemocyte EST databases at ASAP. [https://asap.ahabs.wisc.edu/annotation/php/logon.php.]
- 30.Notredame C, Higgins DG, Heringa J: T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol. 2000, 302: 205-17. 10.1006/jmbi.2000.4042.PubMedCrossRefGoogle Scholar
- 31.The T-Coffee program. [http://igs-server.cnrs-mrs.fr/Tcoffee/]
- 32.Felsenstein J: Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. Methods Enzymol. 1996, 266: 418-27.PubMedCrossRefGoogle Scholar
- 33.
- 34.Artemis. [http://www.sanger.ac.uk/Software/Artemis/]
- 35.Rost B, Sander C: Prediction of protein secondary structure at better than 70% accuracy. J Mol Biol. 1993, 232: 584-99. 10.1006/jmbi.1993.1413.PubMedCrossRefGoogle Scholar
- 36.Guex N, Peitsch MC: SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis. 1997, 18: 2714-23. 10.1002/elps.1150181505.PubMedCrossRefGoogle Scholar
- 37.Koradi R, Billeter M, Wuthrich K: MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph. 1996, 14: 51-5. 10.1016/0263-7855(96)00009-4.PubMedCrossRefGoogle Scholar
- 38.
Copyright information
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.