Pyrosequencing the salivary transcriptome of Haemadipsa interrupta (Annelida: Clitellata: Haemadipsidae): Anticoagulant diversity and insight into the evolution of anticoagulation capabilities in leeches

Invertebrate Biology

Volumn 133, Issue 1, 2014, Pages 74-98

  Kvist, Sebastian ^a   Brugler, Mercer R ^b   Goh, Thary G ^c   Giribet, Gonzalo ^a   Siddall, Mark E ^b  

^a HARVARD UNIVERSITY   (United States)

^b DIVISION OF INVERTEBRATE ZOOLOGY   (United States)

^c UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

Bioactive proteins; Hematophagy; Hirudinida; Transcriptomics

Indexed keywords

EID: 84896544115     PISSN: 10778306     EISSN: 17447410     Source Type: Journal    
DOI: 10.1111/ivb.12039     Document Type: Article

References (102)

1. Adams SL 1988. The medicinal leech. A page from the annelids of internal medicine. Ann. Intern. Med. 109: 399-405.
2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, & Lipman DJ 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
3. Apakupakul K, Siddall ME, & Burreson EM 1999. Higher level relationships of leeches (Annelida: Clitellata: Euhirudinea) based on morphology and gene sequences. Mol. Phylogenet. Evol. 12: 350-359.
4. Bhatia ML 1975. Land leeches, their adaptation, and responses to external stimuli. Zool. Pol. 25: 31-53.
5. Blankenship DT, Brankamp RG, Manley GD, & Cardin AD 1990. Amino acid sequence of ghilanten: anticoagulant-antimetastatic principle of the South American leech, Haementeria ghilianii. Biochem. Biophys. Res. Commun. 166: 1384-1389.
6. Borda E & Siddall ME 2004. Arhynchobdellida (Annelida: Oligochaeta: Hirudinida): phylogenetic relationships and evolution. Mol. Phylogenet. Evol. 30: 213-225.
7. Borda E & Siddall ME 2011. Insights into the evolutionary history of Indo-Pacific bloodfeeding terrestrial leeches (Hirudinida: Arhynchobdellida: Haemadipsidae). Invertebr. Syst. 24: 456-472.
8. Brankamp RG, Manley GG, Blankenship DT, Bowlin TL, & Cardin AD 1991. Studies in the anticoagulant, antimetastatic and heparin-binding properties of ghilanten-related inhibitors. Blood Coagul. Fibrinolysis 2: 161-166.
9. Chatrenet B & Chang J-Y 1993. The disulphide folding pathway of hirudin elucidated by stop/go folding experiments. J. Biol. Chem. 268: 20988-20996.
10. Chevreux B, Wetter T, & Suhai S 1999. Genome sequence assembly using trace signals and additional sequence information. Sci. Biol. Proc. Ger. Conf. Bioinform. 99: 45-56.
11. Chopin V, Salzet M, Baert J, Vandenbulcke F, Sautiere PE, Kerckaert JP, & Malecha J 2000. Therostasin, a novel clotting factor Xa inhibitor from the rhynchobdellid leech, Theromyzon tessulatum. J. Biol. Chem. 275: 32701-32707.
12. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, & Robles M 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
13. 2+-dependent proteinases (mu-calpain and m-calpain). J. Biol. Chem. 264: 10096-10103.
14. Electricwala A, von Sicard NA, Sawyer RT, & Atkinson T 1992. Biochemical characterization of a pancreatic elastase inhibitor from the leech Hirudinaria manillensis. J. Enzym. Inhib. 6: 293-302.
15. Elliott JM & Kutschera U 2011. Medicinal Leeches: historical use, ecology, genetics and conservation. Freshw. Rev. 4: 21-41.
16. Fang G, Bhardwaj N, Robilotto R, & Gerstein MB 2010. Getting started in gene orthology and functional analysis. PLoS Comput. Biol. 6: e1000703.
17. Fink E, Rehm H, Gippner C, Bode W, Eulitz M, Machleidt W, & Fritz H 1986. The primary structure of bdellin B-3 from the leech Hirudo medicinalis. Bdellin B-3 is a compact proteinase inhibitor of a 'non-classical' Kazal type. It is present in the leech in a high molecular mass form. Biol. Chem. Hoppe-Seyler 367: 1235-1242.
18. Fogden SLC & Proctor J 1985. Notes on the feeding of land leeches (Haemadipsa zeylanica Moore and H. picta Moore) in Gunung Mulu National Park, Sarawak. Biotropica 17: 172-174.
19. Fritz H, Gebhardt M, Meister R, & Fink E 1971. Trypsin-plasmin inhibitors from leeches - isolation, amino acid composition, inhibitory characteristics. In: Proceedings of the International Research Conference on Proteinase Inhibitors. Fritz H & Tschesche H, eds., pp. 271-280. Walter de Gruyter, Berlin, Germany.
20. Ge F, Wang L-S, & Kim J 2005. The cobweb of life revealed by genome-scale estimates of horizontal gene transfer. PLoS Biol. 3: 1709-1718.
21. Goloboff PA, Farris JS, & Nixon KC 2008. TNT, a free program for phylogenetic analysis. Cladistics 24: 774-786.
22. Graf J, Kikuchi Y, & Rio RVM 2006. Leeches and their microbiota: naturally simple symbiosis models. Trends Microbiol. 14: 365-371.
23. Gronwald W, Bomke J, Maurer T, Domogalla B, Huber F, Schumann F, Kremer W, Fink F, Rysiok T, Frech M, & Kalbitzer HR 2008. Structure of the leech protein saratin and characterization o fits binding to collagen. J. Mol. Biol. 381: 913-927.
24. Hale MC, McCormick CR, Jackson JR, & DeWoody JA 2009. Next-generation pyrosequencing of gonad transcriptomes in the polyploid lake sturgeon (Acipenser fulvescens): the relative merits of normalization and rarefaction in gene discovery. BMC Genomics 10: 203.
25. Han JH, Law SW, Keller PM, Kniskern PJ, Silberklang M, Tung JS, Gasic TB, Gasic GJ, Friedman PA, & Ellis RW 1989. Cloning and expression of cDNA encoding antistasin, a leech-derived protein having anti-coagulant and anti-metastatic properties. Gene 75: 47-57.
26. Hirabayashi J, Dutta SK, & Kasai K-I 1998. Novel galactose-binding proteins in Annelida. Characterization of 29-kDa tandem repeat-type lectins from the earthworm Lumbricus terrestris. J. Biol. Chem. 273: 14450-14460.
27. Hu Z-L, Bao J, & Reecy JM 2008. CateGOrizer: a web-based program to batch analyze gene ontology classification categories. Online J. Bioinform. 9: 108-112.
28. Jia LG, Shimokawa K, Bjarnason JB, & Fox JW 1996. Snake venom metalloproteinases: structure, function and relationship to the ADAMs family of proteins. Toxicon 34: 1269-1276.
29. Joo SS, Won TJ, Kim JS, Yoo YM, Tak ES, Park SY, Hwang KW, Park SC, & Lee DI 2009. Inhibition of coagulation activation and inflammation by a novel factor Xa inhibitor synthesized from the earthworm Eisenia andrei. Biol. Pharm. Bull. 32: 253-258.
30. Jung HI, Kim SI, Ha KS, Joe CO, & Kang KW 1995. Isolation and characterization of guamerin, a new human leukocyte elastase inhibitor from Hirudo nipponia. J. Biol. Chem. 270: 13879-13884.
31. Katoh K, Kuma K-I, Toh H, & Miyata T 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33: 511-518.
32. Keegan HL, Toshioka S, & Suzuki H 1968. Blood sucking Asian leeches of families Hirudinidae and Haemadipsidae. Biomedical Reports of The 406 Medical Laboratory No. 16. U.S. Army Medical Command, Japan.
33. Keller PM, Schultz LD, Condra C, Karczewski J, & Connolly TM 1992. An inhibitor of collagen-stimulated platelet activation from the salivary glands of the Haementeria officinalis leech. II. Cloning of the cDNA and expression. J. Biol. Chem. 267: 6899-6904.
34. Kikuchi Y & Fukatsu T 2002. Endosymbiotic bacteria in the esophageal organ of glossiphoniid leeches. Appl. Environ. Microbiol. 68: 4637-4641.
35. Kim DR & Kang KW 1998. Amino acid sequence of piguamerin, an antistasin-type protease inhibitor from the blood sucking leech Hirudo nipponia. Eur. J. Biochem. 254: 692-697.
36. Kini RM & Evans HJ 1992. Structural domains in venom proteins: evidence that metalloproteinases and nonenzymatic platelet aggregation inhibitors (disintegrins) from snake venoms are derived by proteolysis from a common precursor. Toxicon 30: 265-293.
37. Knecht R, Seemuller U, Liersch M, Fritz H, Braun DG, & Chang JY 1983. Sequence determination of eglin C using combined microtechniques of amino acid analysis, peptide isolation, and automatic Edman degradation. Anal. Biochem. 130: 65-71.
38. Kutschera U, Pfeiffer I, & Ebermann E 2007. The European land leech: biology and DNA-based taxonomy of a rare species that is threatened by climate warming. Naturwissenschaften 94: 967-974.
39. Kvist S & Siddall ME 2013. Phylogenomics of Annelida revisited: a cladistics approach using genome-wide expressed sequence tag data mining and examining the effects of missing data. Cladistics 29: 435-448.
40. Kvist S, Sarkar IN, & Siddall ME 2011a. Genome-wide search for leech antiplatelet proteins in the non-bloodfeeding leech Helobdella robusta (Rhyncobdellida: Glossiphoniidae) reveals evidence of secreted anticoagulants. Invertebr. Biol. 130: 344-350.
41. Kvist S, Narechania A, Oceguera-Figueroa A, Fuks B, & Siddall ME 2011b. Phylogenomics of Reichenowia parasitica, an alphaproteobacterial endosymbiont of the freshwater leech Placobdella parasitica. PLoS ONE 6: e28192.
42. Kvist S, Min G-S, & Siddall ME 2013. Diversity and selective pressures of anticoagulants in three medicinal leeches (Hirudinida: Hirudinidae, Macrobdellidae). Ecol. Evol. 3: 918-933.
43. Lee MS, Tak ES, Park SK, Cho SJ, Hahn Y, Joo SS, Lee DI, Ahn CH, & Park SC 2010. Eisenstasin, new antistasin family inhibitor from the earthworm. Biologia 65: 284-288.
44. Lefebvre C, Cocquerelle C, Vandenbulcke F, Hot D, Huot L, Lemoine Y, & Salzet M 2004. Transcriptomic analysis in the leech Theromyzon tessulatum: involvement of cystatin B in innate immunity. Biochem. J. 380: 617-625.
45. Light JE & Siddall ME 1999. Phylogeny of the leech family Glossiphoniidae based on mitochondrial gene sequences and morphological data. J. Parasitol. 85: 815-823.
46. Ludwig HC, Lottspeich F, Henschen A, Ladenstein R, & Bacher A 1987. Heavy riboflavin synthase of Bacillus subtilis. Primary structure of the beta subunit. J. Biol. Chem. 262: 1016-1021.
47. Markwardt F 1985. Pharmacology of hirudin: one hundred years after the first report of the anticoagulant agent in medicinal leeches. Biomed. Biochim. Acta 44: 1007-1013.
48. Mason TA, McIlroy PJ, & Shain DH 2004. A cysteine-rich protein in the Theromyzon (Annelida: Hirudinea) cocoon membrane. FEBS Lett. 561: 167-172.
49. Mazur P, Dennis MS, Seymour JL, & Lazarus RA 1993. Expression, purification, and characterization of recombinant ornatin E, a potent glycoprotein IIb-IIIa antagonist. Protein Expression Purif. 4: 282-289.
50. McLane MA, Sanchez EE, Wong A, Paquette-Straub C, & Perez JC 2004. Disintegrins. Curr. Drug Targets Cardiovasc. Haematol. Disord. 4: 327-355.
51. Min G-S, Sarkar IN, & Siddall ME 2010. Salivary transcriptome of the North American medicinal leech, Macrobdella decora. J. Parasitol. 96: 1211-1221.
52. Moore JP 1927. The segmentation (metamerism and annulation) of the Hirudinea; Arhynchobdellae. In: The Fauna of British India Hirudinea. Harding WA & Moore JP, eds., pp. 97-302. Taylor & Francis, London.
53. Nesemann H & Sharma S 1996. Contribution to the knowledge of the leeches of Nepal (Annelida: Hirudinea). Acta Zool. Acad. Sci. Hung. 42: 231-249.
54. Nesemann H & Sharma S 2001. Leeches of the suborder Hirudiniformes (Hirudinea: Haemopidae, Hirudinidae, Haemadipsidae) from the Ganga watershed (Nepal, India: Bihar). Ann. Naturhist. Mus. Wien (B Bot. Zool.) 103B: 77-88.
55. Nybelin O 1943. Nesophilaemon n. g. fur Philaemon skottsbergi L. Johansson aus den Juan Fernandez Inseln. Zool. Anz. 142: 249-250.
56. Perkins SL, Budinoff RB, & Siddall ME 2005. New Gammaproteobacteria associated with blood-feeding leeches and a broad phylogenetic analysis of leech endosymbionts. Appl. Environ. Microbiol. 71: 5219-5224.
57. Petersen TN, Brunak S, von Heijne G, & Nielsen H 2011. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8: 785-786.
58. Phillips AJ & Siddall ME 2009. Poly-paraphyly of Hirudinidae: many lineages of medicinal leeches. BMC Evol. Biol. 9: 246.
59. Prussin C & Metcalfe DD 2003. IgE, mast cells, basophils, and eosinophils. J. Allergy Clin. Immunol. 111(Suppl. 2): S486-S494.
60. Reverter D, Vendrell J, Canals F, Horstmann J, Avilés FX, Fritz H, & Sommerhoff CP 1998. A carboxypeptidase inhibitor from the medical leech Hirudo medicinalis isolation, sequence analysis, cDNA cloning, recombinant expression, and characterization. J. Biol. Chem. 273: 32927-32933.
61. Ribeiro JM 2003. A catalogue of Anopheles gambiae transcripts significantly more or less expressed following a blood meal. Insect Biochem. Mol. Biol. 33: 865-882.
62. Rice P, Longden I, & Bleasby A 2000. EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 16: 276-277.
63. Richardson LR 1975. A contribution to the general zoology of the land-leeches (Hirudinea: Haemadipsoidea superfam. nov.). Acta Zool. Acad. Sci. Hung. 21: 119-152.
64. Richardson LR 1978. On the zoological nature of land leeches in the Seychelles Islands, and a consequential revision of the status of land leeches in Madagascar (Hirudinea: Haemadipsoidea). Rev. Zool. Afr. 92: 837-866.
65. Richter G, Fischer M, Krieger C, Eberhardt S, Lüttgen H, Gerstenschläger I, & Bacher A 1997. Biosynthesis of riboflavin: characterization of the bifunctional deaminase-reductase of Escherichia coli and Bacillus subtilis. J. Bacteriol. 179: 2022-2028.
66. Rousset V, Pleijel F, Rouse GW, Erséus C, & Siddall ME 2007. A molecular phylogeny of annelids. Cladistics 23: 41-63.
67. Salzet M 2001. Anticoagulants and inhibitors of platelet aggregation derived from leeches. FEBS Lett. 429: 187-192.
68. Salzet M, Chopin V, Baert J, Matias I, & Malecha J 2000. Theromin, a novel leech thrombin inhibitor. J. Biol. Chem. 275: 30774-30780.
69. Sawyer RT 1981. Why we need to save the medicinal leech. Oryx 16: 165-168.
70. Sawyer RT 1986. Leech Biology and Behavior. Clarendon Press, Oxford, UK. 1065 pp.
71. Scacheri E, Nitti G, Valsasina B, Orsini G, Visco C, Ferrera M, Sawyer RT, & Sarmientos P 1993. Novel hirudin variants from the leech Hirudinaria manillensis. Amino acid sequence, cDNA cloning and genomic organization. Eur. J. Biochem. 214: 295-304.
72. Scharf M, Engels J, & Tripier D 1989. Primary structures of new "iso-hirudins". FEBS Lett. 255: 105-110.
73. Schnell IB, Thomsen PF, Wilkinson N, Rasmussen M, Jensen LRD, Willerslev E, Berteksen MF, & Gilbert MTP 2012. Screening mammal biodiversity using DNA from leeches. Curr. Biol. 22: R262-R263.
74. Seagrave GS & Salsman LV 1946. Burma surgeon returns. Am. J. Nurs. 46: 724.
75. Seymour JL, Henzel WJ, Nevins B, Stults JT, & Lazarus RA 1990. Decorins. A potent gycoprotein IIb-IIIa antagonist and platelet aggregation inhibitor from the leech Macrobdella decora. J. Biol. Chem. 265: 10143-10147.
76. Shain DH 2009. Annelids in Modern Biology. John Wiley, Sons, New York, NY.
77. Siddall ME & Burreson EM 1995. Phylogeny of the Euhirudinea: independent evolution of blood feeding by leeches? Can. J. Zool. 73: 1048-1064.
78. Siddall ME & Burreson EM 1996. Leeches (Oligochaeta?: Euhirudinea), their phylogeny and the evolution of life history strategies. Hydrobiologia 334: 277-285.
79. Siddall ME & Burreson EM 1998. Phylogeny of leeches (Hirudinea) based on mitochondrial cytochrome c oxidase subunit I. Mol. Phylogenet. Evol. 9: 156-162.
80. Siddall ME, Apakupakul K, Burreson EM, Coates KA, Erséus C, Gelder SR, Källersjö M, & Trapido-Rosenthal H 2001. Validating Livanow: molecular data agree that leeches, branchiobdellidans, and Acanthobdella peledina form a monophyletic group of oligochaetes. Mol. Phylogenet. Evol. 21: 346-351.
81. Siddall ME, Perkins SL, & Desser SS 2004. Leech mycetome endosymbionts are a new lineage of alphaproteobacteria related to the Rhizobiaceae. Mol. Phylogenet. Evol. 30: 178-186.
82. Siddall ME, Trontelj P, Utevsky SY, Nkamany M, & Macdonald KS III 2007. Diverse molecular data demonstrate that commercially available medicinal leeches are not Hirudo medicinalis. Proc. R. Soc. Lond. B 274: 1481-1487.
83. Siddall ME, Min G-S, Fontanella FM, Phillips AJ, & Watson SC 2011. Bacterial symbiont and salivary peptide evolution in the context of leech phylogeny. Parasitology 138: 1815-1827.
84. Söllner C, Mentele R, Eckerskorn C, Fritz H, & Sommerhoff CP 1994. Isolation and characterization of hirustasin, an antistasin-type serine-protease inhibitor from the medicinal leech Hirudo medicinalis. Eur. J. Biochem. 219: 937-943.
85. Sommerhoff CP, Söllner C, Mentele R, Piechottka GP, Auerswald EA, & Fritz H 1994. A Kazal-type inhibitor of human mast cell tryptase: isolation from the medical leech Hirudo medicinalis, characterization, and sequence analysis. Biol. Chem. Hoppe-Seyler 375: 685-694.
86. Stammers FMG 1950. Observations on the behavior of land-leeches (genus Haemadipsa). Parasitology 40: 237-246.
87. Stange R, Moser C, Hopfenmueller W, Mansmann U, Buehring M, & Uehleke B 2012. Randomised controlled trial with medical leeches for osteoarthritis of the knee. Complement Ther. Med. 20: 1-7.
88. Strube KH, Kroger B, Bialojan S, Otte M, & Dodt J 1993. Isolation, sequence analysis, and cloning of haemadin. An anticoagulant peptide from the Indian leech. J. Biol. Chem. 268: 8590-8595.
89. Struck TH, Paul C, Hill N, Hartmann S, Hösel C, Kube M, Lieb B, Meyer A, Tiedemann R, Purschke G, & Bleidorn C 2011. Phylogenomic analyses unravel annelid evolution. Nature 471: 95-98.
90. Swadesh JK, Huang IY, & Budzynski AZ 1990. Purification and characterization of hementin, a fibrinogenolytic protease from the leech Haementeria ghilianii. J. Chromatogr. 502: 359-369.
91. Trontelj P & Utevsky SY 2005. Celebrity with a neglected taxonomy: molecular systematics of the medicinal leech (genus Hirudo). Mol. Phylogenet. Evol. 34: 616-624.
92. Trontelj P, Sket B, & Steinbrück G 1999. Molecular phylogeny of leeches: congruence of nuclear and mitochondrial rDNA data sets and the origin of bloodsucking. J. Zool. Syst. Evol. Res. 37: 141-147.
93. Tulinsky A & Qiu X 1993. Active site and exosite binding of alpha-thrombin. Blood Coagul. Fibrinolysis 4: 305-312.
94. Vankhede GN, Gomase VS, Deshmukh SV, & Chikhale NJ 2005. Prediction of antigenic epitope of hirudin from Poecilobdella viridis. J. Comp. Toxicol. Physiol. 2: 110-118.
95. Von Heijne G 1990. The signal peptide. J. Membr. Biol. 115: 195-201.
96. Waterhouse AM, Procter JB, Martin DMA, Clamp M, & Barton GJ 2009. Jalview version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
97. Wells MD, Manktelow RT, Boyd JB, & Bowen V 1993. The medical leech: an old treatment revisited. Microsurgery 14: 183-186.
98. Whitaker IS, Izadi D, Oliver DW, Monteath GM, & Butler PE 2004. Hirudo Medicinalis and the plastic surgeon. Br. J. Plast. Surg. 57: 348-353.
99. Wilkinson M, McInerney JO, Hirt RP, Foster PG, & Embley TM 2007. Of clades and clans: terms for phylogenetic relationships in unrooted trees. Trends Ecol. Evol. 22: 114-115.
100. Xu Q, Wu X-F, Xia Q-C, & Wang K-Y 1999. Cloning of a galactose-binding lectin from the venom of Trimeresurus stejnegeri. Biochem. J. 341: 733-737.
101. Zavalova L, Lukyanov S, Baskova I, Snezhkov E, Akopov S, Berezhnoy S, Bogdanova E, Basova E, & Sverdlov ED 1996. Genes from the medicinal leech (Hirudo medicinalis) coding for unusual enzymes that specifically cleave endo-epsilon (gamma-Glu)-Lys isopeptide bonds and help dissolve blood clots. Mol. Gen. Genet. 253: 20-25.
102. Zrzavý J, Říha P, Piálek L, & Janouškovec J 2009. Phylogeny of Annelida (Lophotrochozoa): total-evidence analysis of morphology and six genes. BMC Evol. Biol. 9: 189.