Evolution of vertebrate hemostatic and inflammatory control mechanisms in blood-feeding arthropods

Journal of Innate Immunity

Volumn 3, Issue 1, 2011, Pages 41-51

  Mans, Ben J ^a  

^a ONDERSTEPOORT VETERINARY INSTITUTE   (South Africa)

Author keywords

Coagulation; Evolution; Host defense; Invertebrates; Parasitology

Indexed keywords

SECRETORY PROTEIN; SIALOME; UNCLASSIFIED DRUG;

ARTHROPOD; ARTICLE; CELL LINEAGE; COMPARATIVE STUDY; GENE DUPLICATION; HEMOSTASIS; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SALIVARY GLAND; VERTEBRATE;

ANIMALS; ARTHROPODS; BIOLOGICAL EVOLUTION; BLOOD COAGULATION; EVOLUTION, MOLECULAR; FEEDING BEHAVIOR; HEMOSTASIS; HUMANS; SALIVARY GLANDS; VERTEBRATES;

EID: 78650513994     PISSN: 1662811X     EISSN: 16628128     Source Type: Journal    
DOI: 10.1159/000321599     Document Type: Article

References (94)

1. Doolittle RF, Feng DF: Reconstructing the evolution of vertebrate blood coagulation from a consideration of the amino acid sequences of clotting proteins. Cold Spring Harb Symp Quant Biol 1987;52:869-874.
2. Schofield CJ, Galvão C: Classification, evolution, and species groups within the Triatominae. Acta Trop 2009;110:88-100.
3. Grimaldi D, Engel MS: Evolution of the Insects, ed 1. New York, Cambridge University Press, 2010.
4. Mans BJ, Francischetti IM: Sialomic perspectives on the evolution of blood-feeding behavior in arthropods: future therapeutics by natural design; in Kini RM, Clemetson KJ, Markland FS, McLane MA, Morita T (eds): Toxins and Hemostasis: From Bench to Bed-Side. Berlin, Springer, 2010.
5. Bochkov AV, Connor BM, Wauthy G: Phylogenetic position of the mite family Myobiidae within the infraorder Eleutherengona (Acariformes) and origins of parasitism in eleutherengone mites. Zool Anz 2008;247:15-45.
6. Walter DE, Proctor HC: Mites: Ecology, Evolution and Behaviour, ed 1. Wallingford, CABI, 1999.
7. Radovsky FJ: Adaptive radiation in the parasitic mesostigmata. Acarologia 1969;11:450-483.
8. Mans BJ, Andersen JF, Francischetti IM, Valenzuela JG, Schwan TG, Pham VM, Garfield MK, Hammer CH, Ribeiro JM: Comparative sialomics between hard and soft ticks: implications for the evolution of blood-feeding behavior. Insect Biochem Mol Biol 2008;38:42-58.
9. Mans BJ, Louw AI, Neitz AW: Evolution of hematophagy in ticks: common origins for blood coagulation and platelet aggregation inhibitors from soft ticks of the genus Ornithodoros. Mol Biol Evol 2002;19:1695-1705.
10. Mans BJ, Neitz AW: Adaptation of ticks to a blood-feeding environment: evolution from a functional perspective. Insect Biochem Mol Biol 2004;34:1-17.
11. Mans BJ, Andersen JF, Schwan TG, Ribeiro JM: Characterization of anti-hemostatic factors in the argasid, Argas monolakensis: implications for the evolution of bloodfeeding in the soft tick family. Insect Biochem Mol Biol 2008;38:22-41.
12. de la Fuente J: The fossil record and the origin of ticks (Acari: Parasitiformes: Ixodida). Exp Appl Acarol 2003;29:331-344.
13. Ribeiro JM, Arca B: From sialomes to the sialoverse: an insight into salivary potion of blood-feeding insects. Adv In Insect Physiol 2009;37:59-118.
14. Francischetti IMB, Sa-Nunes A, Mans BJ, Santos IM, Ribeiro JM: The role of saliva in tick feeding. Front Biosci 2009;14:2051-2088.
15. Sabbatani L: Fermento anticoagulante dell' Ixodes ricinus. Arch Ital Biol 1899;31:37-53.
16. Nuttall GH, Strickland BA: On the presence of an anticoagulin in the salivary glands and intestines of Argas persicus. Parasitology 1909;1:302-310.
17. Cornwall JW, Patton WS: Some observations on the salivary secretion of the commoner blood-sucking insects and ticks. Indian J Med Res 1914;2:569-593.
18. Law J, Ribeiro JM, Wells M: Biochemical insights derived from diversity in insects. Ann Rev Biochem 1992;61:87-112.
19. Ribeiro JM: Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infect Agents Dis 1995;4:143-152.
20. Ribeiro JM, Francischetti IM: Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu Rev Entomol 2003;48:73-88.
21. Andersen JF, Hinnebusch BJ, Lucas DA, Conrads TP, Veenstra TD, Pham VM, Ribeiro JM: An insight into the sialome of the oriental rat flea, Xenopsylla cheopis (Rots). BMC Genomics 2007;8:102.
22. Francischetti IM, Calvo E, Andersen JF, Pham VM, Favreau AJ, Barbian KD, Romero A, Valenzuela JG, Ribeiro JM: Insight into the sialome of the bed bug, Cimex lectularius. J Proteome Res 2010;9:3820-3831.
23. Ribeiro JM, Andersen JF, Silva-Neto MA, Pham VM, Garfield MK, Valenzuela JG: Exploring the sialome of the blood-sucking bug Rhodnius prolixus. Insect Biochem Mol Biol 2004;34:61-79.
24. Santos A, Ribeiro JM, Lehane MJ, Gontijo NF, Veloso AB, Sant'Anna MR, Nascimento Araujo R, Grisard EC, Pereira MH: The sialotranscriptome of the blood-sucking bug Triatoma brasiliensis (Hemiptera, Triatominae). Insect Biochem Mol Biol 2007;37:702-712.
25. Kato H, Jochim RC, Gomez EA, Sakoda R, Iwata H, Valenzuela JG, Hashiguchi Y: A repertoire of the dominant transcripts from the salivary glands of the blood-sucking bug, Triatoma dimidiata, a vector of Chagas disease. Infect Genet Evol 2010;10:184-191.
26. Assumpção TC, Francischetti IM, Andersen JF, Schwarz A, Santana JM, Ribeiro JM: An insight into the sialome of the blood-sucking bug Triatoma infestans, a vector of Chagas disease. Insect Biochem Mol Biol 2008;38:213-232.
27. Van Den Abbeele J, Caljon G, Dierick JF, Moens L, De Ridder K, Coosemans M: The Glossina morsitans tsetse fly saliva: general characteristics and identification of novel salivary proteins. Insect Biochem Mol Biol 2007;37:1075-1085.
28. Alves-Silva J, Ribeiro JM, Van Den Abbeele J, Attardo G, Hao Z, Haines LR, Soares MB, Berriman M, Aksoy S, Lehane MJ: An insight into the sialome of Glossina morsitans morsitans. BMC Genomics 2010;11:213.
29. Wang X, Ribeiro JM, Broce AB, Wilkerson MJ, Kanost MR: An insight into the transcriptome and proteome of the salivary gland of the stable fly, Stomoxys calcitrans. Insect Biochem Mol Biol 2009;39:607-614.
30. Valenzuela JG, Garfield M, Rowton ED, Pham VM: Identification of the most abundant secreted proteins from the salivary glands of the sand fly Lutzomyia longipalpis, vector of Leishmania chagasi. J Exp Biol 2004;207:3717-3729.
31. Hostomská J, Volfová V, Mu J, Garfield M, Rohousová I, Volf P, Valenzuela JG, Jochim RC: Analysis of salivary transcripts and antigens of the sand fly Phlebotomus arabicus. BMC Genomics 2009;10:282.
32. Oliveira F, Kamhawi S, Seitz AE, Pham VM, Guigal PM, Fischer L, Ward J, Valenzuela JG: From transcriptome to immunome: identification of DTH inducing proteins from a Phlebotomus ariasi salivary gland cDNA library. Vaccine 2006;24:374-390.
33. Anderson JM, Oliveira F, Kamhawi S, Mans BJ, Reynoso D, Seitz AE, Lawyer P, Garfield M, Pham M, Valenzuela JG: Comparative salivary gland transcriptomics of sandfly vectors of visceral leishmaniasis. BMC Genomics 2006;7:52.
34. Kato H, Anderson JM, Kamhawi S, Oliveira F, Lawyer PG, Pham VM, Sangare CS, Samake S, Sissoko I, Garfield M, Sigutova L, Volf P, Doumbia S, Valenzuela JG: High degree of conservancy among secreted salivary gland proteins from two geographically distant Phlebotomus duboscqi sandfly populations (Mali and Kenya). BMC Genomics 2006;7:226.
35. Valenzuela JG, Pham VM, Garfield MK, Francischetti IM, Ribeiro JM: Toward a description of the sialome of the adult female mosquito Aedes aegypti. Insect Biochem Mol Biol 2002;32:1101-1122.
36. Ribeiro JM, Arcà B, Lombardo F, Calvo E, Pham VM, Chandra PK, Wikel SK: An annotated catalogue of salivary gland transcripts in the adult female mosquito, Aedes aegypti. BMC Genomics 2007;8:6.
37. Arcà B, Lombardo F, Francischetti IM, Pham VM, Mestres-Simon M, Andersen JF, Ribeiro JM: An insight into the sialome of the adult female mosquito Aedes albopictus. Insect Biochem Mol Biol 2007;37:107-127.
38. Calvo E, Andersen J, Francischetti IM, del Capurro M, de Bianchi AG, James AA, Ribeiro JM, Marinotti O: The transcriptome of adult female Anopheles darlingi salivary glands. Insect Mol Biol 2004;13:73-88.
39. Calvo E, Pham VM, Marinotti O, Andersen JF, Ribeiro JM: The salivary gland transcriptome of the neotropical malaria vector Anopheles darlingi reveals accelerated evolution of genes relevant to hematophagy. BMC Genomics 2009;10:57.
40. Calvo E, Dao A, Pham VM, Ribeiro JM: An insight into the sialome of Anopheles funestus reveals an emerging pattern in anopheline salivary protein families. Insect Biochem Mol Biol 2007;37:164-175.
41. Francischetti IM, Valenzuela JG, Pham VM, Garfield MK, Ribeiro JM: Toward a catalog for the transcripts and proteins (sialome) from the salivary gland of the malaria vector Anopheles gambiae. J Exp Biol 2002;205:2429-2451.
42. Arcà B, Lombardo F, Valenzuela JG, Francischetti IM, Marinotti O, Coluzzi M, Ribeiro JM: An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae. J Exp Biol 2005:208:3971-3986.
43. Valenzuela JG, Francischetti IM, Pham VM, Garfield MK, Ribeiro JM: Exploring the salivary gland transcriptome and proteome of the Anopheles stephensi mosquito. Insect Biochem Mol Biol 2003;33:717-732.
44. Ribeiro JM, Charlab R, Pham VM, Garfield M, Valenzuela JG: An insight into the salivary transcriptome and proteome of the adult female mosquito Culex pipiens quinquefasciatus. Insect Biochem Mol Biol 2004;34:543-563.
45. Calvo E, Sanchez-Vargas I, Favreau AJ, Barbian KD, Pham VM, Olson KE, Ribeiro JM: An insight into the sialotranscriptome of the West Nile mosquito vector, Culex tarsalis. BMC Genomics 2010;11:51.
46. Calvo E, Sanchez-Vargas I, Kotsyfakis M, Favreau AJ, Barbian KD, Pham VM, Olson KE, Ribeiro JM: The salivary gland transcriptome of the eastern tree hole mosquito, Ochlerotatus triseriatus. J Med Entomol 2010;47:376-386.
47. Russell CL, Heesom KJ, Arthur CJ, Helps CR, Mellor PS, Day MJ, Torsteinsdottir S, Björnsdóttir TS, Wilson AD: Identification and isolation of cDNA clones encoding the abundant secreted proteins in the saliva proteome of Culicoides nubeculosus. Insect Mol Biol 2009;18:383-393.
48. Campbell CL, Vandyke KA, Letchworth GJ, Drolet BS, Hanekamp T, Wilson WC: Midgut and salivary gland transcriptomes of the arbovirus vector Culicoides sonorensis (Diptera: Ceratopogonidae). Insect Mol Biol 2005;14:121-136.
49. Ribeiro JM, Valenzuela JG, Pham VM, Kleeman L, Barbian KD, Favreau AJ, Eaton DP, Aoki V, Hans-Filho G, Rivitti EA, Diaz LA: An insight into the sialotranscriptome of Simulium nigrimanum, a black fly associated with fogo selvagem in South America. Am J Trop Med Hyg 2010;82:1060-1075.
50. Andersen JF, Pham VM, Meng Z, Champagne DE, Ribeiro JM: Insight into the sialome of the black fly, Simulium vittatum. J Proteome Res 2009;8:1474-1488.
51. Francischetti IM, Meng Z, Mans BJ, Gudderra N, Hall M, Veenstra TD, Pham VM, Kotsyfakis M, Ribeiro JM: An insight into the salivary transcriptome and proteome of the soft tick and vector of epizootic bovine abortion, Ornithodoros coriaceus. J Proteomics 2008;71:493-512.
52. Francischetti IM, Mans BJ, Meng Z, Gudderra N, Veenstra TD, Pham VM, Ribeiro JM: An insight into the sialome of the soft tick, Ornithodorus parkeri. Insect Biochem Mol Biol 2008;38:1-21.
53. Francischetti IM, My Pham V, Mans BJ, Andersen JF, Mather TN, Lane RS, Ribeiro JM: The transcriptome of the salivary glands of the female western black-legged tick Ixodes pacificus (Acari: Ixodidae). Insect Biochem Mol Biol 2005;35:1142-1161.
54. Chmelar J, Anderson JM, Mu J, Jochim RC, Valenzuela JG, Kopecký J: Insight into the sialome of the castor bean tick, Ixodes ricinus. BMC Genomics 2008;9:233.
55. Valenzuela JG, Francischetti IM, Pham VM, Garfield MK, Mather TN, Ribeiro JM: Exploring the sialome of the tick Ixodes scapularis. J Exp Biol 2002;205:2843-2864.
56. Ribeiro JM, Alarcon-Chaidez F, Francischetti IM, Mans BJ, Mather TN, Valenzuela JG, Wikel SK: An annotated catalog of salivary gland transcripts from Ixodes scapularis ticks. Insect Biochem Mol Biol 2006;36:111-129.
57. Aljamali MN, Hern L, Kupfer D, Downard S, So S, Roe BA, Sauer JR, Essenberg RC: Transcriptome analysis of the salivary glands of the female tick Amblyomma americanum (Acari: Ixodidae). Insect Mol Biol 2009;18:129-154.
58. Batista IF, Chudzinski-Tavassi AM, Faria F, Simons SM, Barros-Batestti DM, Labruna MB, Leão LI, Ho PL, Junqueira-de-Azevedo IL: Expressed sequence tags (ESTs) from the salivary glands of the tick Amblyomma cajennense (Acari: Ixodidae). Toxicon 2008;51:823-834.
59. Nene V, Lee D, Quackenbush J, Skilton R, Mwaura S, Gardner MJ, Bishop R: AvGI, an index of genes transcribed in the salivary glands of the ixodid tick Amblyomma variegatum. Int J Parasitol 2002;32:1447-1456.
60. Nakajima C, da Silva Vaz I Jr, Imamura S, Konnai S, Ohashi K, Onuma M: Random sequencing of cDNA library derived from partiallyfed adult female Haemaphysalis longicornis salivary gland. J Vet Med Sci 2005;67:1127-1131.
61. Alarcon-Chaidez FJ, Sun J, Wikel SK: Transcriptome analysis of the salivary glands of Dermacentor andersoni Stiles (Acari: Ixodidae). Insect Biochem Mol Biol 2007;37:48-71.
62. Nene V, Lee D, Kang'a S, Skilton R, Shah T, de Villiers E, Mwaura S, Taylor D, Quackenbush J, Bishop R: Genes transcribed in the salivary glands of female Rhipicephalus appendiculatus ticks infected with Theileria parva. Insect Biochem Mol Biol 2004;34:1117-1128.
63. Carvalho WA, Maruyama SR, Franzin AM, Abatepaulo AR, Anderson JM, Ferreira BR, Ribeiro JM, Moré DD, Augusto Mendes Maia A, Valenzuela JG, Garcia GR, de Miranda Santos IK: Rhipicephalus (Boophilus) microplus: clotting time in tick-infested skin varies according to local inflammation and gene expression patterns in tick salivary glands. Exp Parasitol 2010;124:428-435.
64. Anatriello E, Ribeiro JM, de Miranda-Santos IK, Brandão LG, Anderson JM, Valenzuela JG, Maruyama SR, Silva JS, Ferreira BR: An insight into the sialotranscriptome of the brown dog tick, Rhipicephalus sanguineus. BMC Genomics 2010;11:450.
65. Binnington KC: Sequenctial changes in salivary gland structure during attachment and feeding of the cattle tick, Boophilus microplus. Int J Parasitol 1978;8:97-115.
66. Binnington KC, Stone BF: Developmental changes in morphology and toxin content of the salivary gland of the Australian paralysis tick Ixodes holocyclus. Int J Parasitol 1981;11:343-351.
67. Madden RD, Sauer JR, Dillwith JW: A proteomics approach to characterizing tick salivary secretions. Exp Appl Acarol 2002;28:77-87.
68. Lehane M: The biology of blood-sucking in insects, ed 1. New York, Cambridge University Press, 2005.
69. Waage, JK: The evolution of insect/vertebrate associations. Biol J Linn Soc 1979;12:187-224.
70. Francischetti IM, Lopes AH, Dias FA, Pham VM, Ribeiro JM: An insight into the sialotranscriptome of the seed-feeding bug, Oncopeltus fasciatus. Insect Biochem Mol Biol 2007;37:903-910.
71. Fry BG, Roelants K, Champagne DE, Scheib H, Tyndall JD, King GF, Nevalainen TJ, Norman JA, Lewis RJ, Norton RS, Renjifo C, de la Vega RC: The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet 2009;10:23.1-23.29.
72. Ribeiro JM, Mans BJ, Arcà B: An insight into the sialome of blood feeding Nematocera. Insect Biochem Mol Biol 2010;40:767-784.
73. Andersen JF: Structure and mechanism in salivary proteins from blood-feeding arthropods. Toxicon 2010;56:1120-1129.
74. Weichsel A, Maes EM, Andersen JF, Valenzuela JG, Shokhireva T, Walker FA, Montfort WR: Heme-assisted S-nitrosation of a proximal thiolate in a nitric oxide transport protein. Proc Natl Acad Sci USA 2005;102:594-599.
75. Andersen JF, Ribeiro JM: A secreted salivary inositol polyphosphate 5-phosphatase from a blood-feeding insect: allosteric activation by soluble phosphoinositides and phosphatidylserine. Biochemistry 2006;45:5450-5457.
76. Mans BJ, Calvo E, Ribeiro JMC, Andersen JF: The crystal structure of D7r4, a salivary biogenic amine-binding protein from the malaria mosquito Anopheles gambiae. J Biol Chem 2007;282:36626-36633.
77. Valenzuela JG, Charlab R, Gonzalez EC, de Miranda-Santos IK, Marinotti O, Francischetti IM, Ribeiro JM: The D7 family of salivary proteins in blood sucking diptera. Insect Mol Biol 2002;11:149-155.
78. Mans BJ, Ribeiro JM, Andersen JF: Structure, function, and evolution of biogenic amine-binding proteins in soft ticks. J Biol Chem 2008;283:18721-18733.
79. Beaufays J, Adam B, Menten-Dedoyart C, Fievez L, Grosjean A, Decrem Y, Prévôt PP, Santini S, Brasseur R, Brossard M, Vanhaeverbeek M, Bureau F, Heinen E, Lins L, Vanhamme L, Godfroid E: Ir-LBP, an Ixodes ricinus tick salivary LTB4-binding lipocalin, interferes with host neutrophil function. PLoS One 2008;3: e3987.
80. Beaufays J, Adam B, Decrem Y, Prévôt PP, Santini S, Brasseur R, Brossard M, Lins L, Vanhamme L, Godfroid E: Ixodes ricinus tick lipocalins: identification, cloning, phylogenetic analysis and biochemical characterization. PLoS One 2008;3: e3941.
81. Mans BJ, Ribeiro JM: Function, mechanism and evolution of the moubatin-clade of soft tick lipocalins. Insect Biochem Mol Biol 2008;38:841-852.
82. Corral-Rodrýguez CA, Macedo-Ribeiro S, Pereira PJ, Fuentes-Prior P: Tick-derived Kunitz-type inhibitors as antihemostatic factors. Insect Biochem Mol Biol 2009;39:579-595.
83. Macedo-Ribeiro S, Almeida C, Calisto BM, Friedrich T, Mentele R, Sturzebecher J, Fuentes-Prior P, Pereira PJ: Isolation, cloning and structural characterisation of boophilin, a multifunctional Kunitz-type proteinase inhibitor from the cattle tick. PLoS One 2008;3:1-17.
84. Calvo E, Mans BJ, Andersen JF, Ribeiro JM: Function and evolution of a mosquito salivary protein family. J Biol Chem 2006;281:1935-1942.
85. Hilger C, Bessot JC, Hutt N, Grigioni F, De Blay F, Pauli G, Hentges F: IgE-mediated anaphylaxis caused by bites of the pigeon tick Argas reflexus: cloning and expression of the major allergen Arg r 1. J Allergy Clin Immunol 2005;115:617-622.
86. Oleaga A, Escudero-Población A, Camafeita E, Pérez- Sánchez R: A proteomic approach to the identification of salivary proteins from the argasid ticks Ornithodoros moubata and Ornithodoros erraticus. Insect Biochem Mol Biol 2007;37:1149-1159.
87. Peng Z, Simons FE: Cross-reactivity of skin and serum specific IgE responses and allergen analysis for three mosquito species with worldwide distribution. J Allergy Clin Immunol 1997;100:192-198.
88. Kushnir-Sukhov NM, Brown JM, Wu Y, Kirshenbaum A, Metcalfe DD: Human mast cells are capable of serotonin synthesis and release. J Allergy Clin Immunol 2007;119:498-499.
89. Humprey JH, Jaques R: The histamine and serotonin content of the platelets and polymorphonuclear leucocytes of various species. J Physiol 1954;124:305-310.
90. Brown SJ, Askenase PW: Cutaneous basophil responses and immune resistance of guinea pigs to ticks: passive transfer with peritoneal exudade cells or serum. J Immunol 1981;127:2163-2167.
91. Giribet G, Edgecombe GD, Wheeler WC, Babbitt C: Phylogeny and systematic position of Opiliones: a combined analysis of chelicerate relationships using morphological and molecular data. Cladistics 2002;18:5-70.
92. Klompen H, Lekveishvili M, Black WC: Phylogeny of parasitiform mites (Acari) based on rRNA. Mol Phylogenet Evol 2007;43:936-951.
93. Barker SC, Murrell A: Systematics and evolution of ticks with a list of valid genus and species names. Parasitology 2004;129: S15-S36.
94. Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Pena A, Horak IG, Shao R, Barker SC: The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names. Zootaxa 2010;2528:1-28.