Insight into the sialome of the bed bug, cimex lectularius

Journal of Proteome Research

Volumn 9, Issue 8, 2010, Pages 3820-3831

  Francischetti, Ivo M B ^a   Calvo, Eric ^a   Andersen, John F ^a   Pham, Van M ^a   Favreau, Amanda J ^b   Barbian, Kent D ^b   Romero, Alvaro ^c   Valenzuela, Jesus G ^a   Ribeiro, José M C ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

bedbug; saliva; salivary proteome; salivary transcriptome

Indexed keywords

APYRASE; COMPLEMENTARY DNA; ESTERASE; INOSITOL POLYPHOSPHATE; LYSOZYME; MUCIN; SALIVA PROTEIN; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR;

ARTICLE; CIMEX; CIMEX LECTULARIUS; DNA SEQUENCE; GEL ELECTROPHORESIS; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; SALIVA; SALIVARY GLAND; TANDEM MASS SPECTROMETRY; TRANSCRIPTOMICS;

ACETYLCHOLINESTERASE; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BEDBUGS; COMPUTATIONAL BIOLOGY; DNA PRIMERS; ENZYMES; FEEDING BEHAVIOR; FEMALE; GENE LIBRARY; INSECT PROTEINS; MALE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEOMICS; SALIVARY PROTEINS AND PEPTIDES; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TANDEM MASS SPECTROMETRY;

CIMEX LECTULARIUS; CIMICIDAE; HEXAPODA;

EID: 77955434392     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr1000169     Document Type: Article

References (100)

1. Grimaldi, D.; Engel, M. Evolution of the insects; Cambridge University Press: New York, 2005; p 772.
2. Schofield, C. J.; Galvao, C. Classification, evolution, and species groups within the Triatominae Acta Trop. 2009, 110 (2-3) 88-100
3. Reinhardt, K.; Siva-Jothy, M. T. Biology of the bed bugs (Cimicidae) Annu. Rev. Entomol. 2007, 52, 351-374
4. Doggett, S. L.; Geary, M. J.; Russell, R. C. The resurgence of bed bugs in Australia: with notes on their ecology and control Environ. Health 2004, 4, 30-38
5. Ter Poorten, M. C.; Prose, N. S. The return of the common bedbug Pediatr. Dermatol. 2005, 22 (3) 183-187
6. Lee, I. Y.; Ree, H. I.; An, S. J.; Linton, J. A.; Yong, T. S. Reemergence of the bedbug Cimex lectularius in Seoul, Korea Korean J. Parasitol. 2008, 46 (4) 269-271
7. Anderson, A. L.; Leffler, K. Bedbug infestations in the news: a picture of an emerging public health problem in the United States J. Environ. Health 2008, 70 (9) 24-27, 52-53
8. Abdel-Naser, M. B.; Lotfy, R. A.; Al-Sherbiny, M. M.; Sayed Ali, N. M. Patients with papular urticaria have IgG antibodies to bedbug (Cimex lectularius) antigens Parasitol. Res. 2006, 98 (6) 550-556
9. Leverkus, M.; Jochim, R. C.; Schad, S.; Brocker, E. B.; Andersen, J. F.; Valenzuela, J. G.; Trautmann, A. Bullous allergic hypersensitivity to bed bug bites mediated by IgE against salivary nitrophorin J. Invest. Dermatol. 2006, 126 (1) 91-96
10. Scarupa, M. D.; Economides, A. Bedbug bites masquerading as urticaria J. Allergy Clin. Immunol. 2006, 117 (6) 1508-1509
11. Stucki, A.; Ludwig, R. Images in clinical medicine. Bedbug bites N. Engl. J. Med. 2008, 359 (10) 1047
12. Reinhardt, K.; Kempke, D.; Naylor, R. A.; Siva-Jothy, M. T. Sensitivity to bites by the bedbug, Cimex lectularius Med. Vet. Entomol. 2009, 23 (2) 163-166
13. Ribeiro, J. M. C.; Arca, B. From sialomes to the sialoverse: An insight into the salivary potion of blood feeding insects Adv. Insect Physiol. 2009, 37, 59-118
14. Ribeiro, J. M.; Francischetti, I. M. Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives Annu. Rev. Entomol. 2003, 48, 73-88
15. Valenzuela, J. G.; Charlab, R.; Galperin, M. Y.; Ribeiro, J. M. Purification, cloning, and expression of an apyrase from the bed bug Cimex lectularius. A new type of nucleotide-binding enzyme J. Biol. Chem. 1998, 273 (46) 30583-30590
16. Valenzuela, J. G.; Chuffe, O. M.; Ribeiro, J. M. C. Apyrase and anti-platelet activities from the salivary glands of the bed bug Cimex lectularius Insect Biochem. Mol. Biol. 1996, 21, 557-562
17. Ribeiro, J. M. C. Blood-feeding arthropods: Live syringes or invertebrate pharmacologists Infect. Agents Dis. 1995, 4, 143-152
18. Valenzuela, J. G.; Guimaraes, J. A.; Ribeiro, J. M. A novel inhibitor of factor X activation from the salivary glands of the bed bug Cimex lectularius Exp. Parasitol. 1996, 83 (2) 184-190
19. Weichsel, A.; Maes, E. M.; Andersen, J. F.; Valenzuela, J. G.; Shokhireva, T.; Walker, F. A.; Montfort, W. R. Heme-assisted S-nitrosation of a proximal thiolate in a nitric oxide transport protein Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (3) 594-599
20. Valenzuela, J. G.; Ribeiro, J. M. Purification and cloning of the salivary nitrophorin from the hemipteran Cimex lectularius J. Exp. Biol. 1998, 201 (Pt 18) 2659-2664
21. Valenzuela, J. G.; Walker, F. A.; Ribeiro, J. M. A salivary nitrophorin (nitric-oxide-carrying hemoprotein) in the bedbug Cimex lectularius J. Exp. Biol. 1995, 198 (Pt 7) 1519-1526
22. Moncada, S.; Palmer, R. M. J.; Higgs, E. A. Nitric oxide: Physiology, pathophysiology, and pharmacology Pharmacol. Rev. 1991, 43, 109-142
23. Champagne, D.; Nussenzveig, R. H.; Ribeiro, J. M. C. Purification, characterization, and cloning of nitric oxide-carrying heme proteins (nitrophorins) from salivary glands of the blood sucking insect Rhodnius prolixus J. Biol. Chem. 1995, 270, 8691-8695
24. Ribeiro, J. M. C.; Walker, F. A. High affinity histamine-binding and anti-histaminic activity of the salivary NO-carrying heme protein (Nitrophorin) of Rhodnius prolixus J. Exp. Med. 1994, 180, 2251-2257
25. Andersen, J. F.; Francischetti, I. M.; Valenzuela, J. G.; Schuck, P.; Ribeiro, J. M. Inhibition of hemostasis by a high affinity biogenic amine-binding protein from the saliva of a blood-feeding insect J. Biol. Chem. 2003, 278 (7) 4611-4617
26. Francischetti, I. M.; Andersen, J. F.; Ribeiro, J. M. Biochemical and functional characterization of recombinant Rhodnius prolixus platelet aggregation inhibitor 1 as a novel lipocalin with high affinity for adenosine diphosphate and other adenine nucleotides Biochemistry 2002, 41 (11) 3810-3818
27. Francischetti, I. M.; Ribeiro, J. M.; Champagne, D.; Andersen, J. Purification, cloning, expression, and mechanism of action of a novel platelet aggregation inhibitor from the salivary gland of the blood- sucking bug, Rhodnius prolixus J. Biol. Chem. 2000, 275 (17) 12639-12650
28. Gudderra, N. P.; Ribeiro, J. M.; Andersen, J. F. Structural determinants of factor IX(a) binding in nitrophorin 2, a lipocalin inhibitor of the intrinsic coagulation pathway J. Biol. Chem. 2005, 280 (26) 25022-25028
29. Zhang, Y.; Ribeiro, J. M.; Guimaraes, J. A.; Walsh, P. N. Nitrophorin-2: a novel mixed-type reversible specific inhibitor of the intrinsic factor-X activating complex Biochemistry 1998, 37 (30) 10681-10690
30. Ribeiro, J. M. C.; Schneider, M.; Guimaraes, J. A. Purification and characterization of Prolixin S (Nitrophorin 2), the salivary anticoagulant of the blood sucking bug, Rhodnius prolixus Biochem. J. 1995, 308, 243-249
31. Bartley, J. D.; Harlan, H. J. Bed bug infestation: its control and management Military Medic 1974, 884-886
32. Montes, C.; Cuadrillero, C.; Vilella, D. Maintenance of a laboratory colony of Cimex lectularius (Hemiptera: Cimicidae) using an artificial feeding technique J. Med. Entomol. 2002, 39 (4) 675-679
33. Guo, Y.; Ribeiro, J. M.; Anderson, J. M.; Bour, S. dCAS: a desktop application for cDNA sequence annotation Bioinformatics 2009, 25 (9) 1195-1196
34. Huang, X.; Madan, A. CAP3: A DNA sequence assembly program Genome Res. 1999, 9 (9) 868-877
35. Altschul, S. F.; Gish, W.; Miller, W.; Myers, E. W.; Lipman, D. J. Basic local alignment search tool J. Mol. Biol. 1990, 215 (3) 403-410
36. Thompson, J. D.; Gibson, T. J.; Plewniak, F.; Jeanmougin, F.; Higgins, D. G. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res. 1997, 25 (24) 4876-4882
37. Page, R. D. TreeView: an application to display phylogenetic trees on personal computers Comput. Appl. Biosci. 1996, 12 (4) 357-358
38. Kumar, S.; Tamura, K.; Nei, M. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment Brief. Bioinform. 2004, 5 (2) 150-163
39. Altschul, S. F.; Madden, T. L.; Schaffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 1997, 25 (17) 3389-3402
40. Ashburner, M.; Ball, C. A.; Blake, J. A.; Botstein, D.; Butler, H.; Cherry, J. M.; Davis, A. P.; Dolinski, K.; Dwight, S. S.; Eppig, J. T.; Harris, M. A.; Hill, D. P.; Issel-Tarver, L.; Kasarskis, A.; Lewis, S.; Matese, J. C.; Richardson, J. E.; Ringwald, M.; Rubin, G. M.; Sherlock, G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium Nat. Genet. 2000, 25 (1) 25-29
41. Bateman, A.; Birney, E.; Durbin, R.; Eddy, S. R.; Howe, K. L.; Sonnhammer, E. L. The Pfam protein families database Nucleic Acids Res. 2000, 28 (1) 263-266
42. Schultz, J.; Copley, R. R.; Doerks, T.; Ponting, C. P.; Bork, P. SMART: a web-based tool for the study of genetically mobile domains Nucleic Acids Res. 2000, 28 (1) 231-234
43. Tatusov, R. L.; Fedorova, N. D.; Jackson, J. D.; Jacobs, A. R.; Kiryutin, B.; Koonin, E. V.; Krylov, D. M.; Mazumder, R.; Mekhedov, S. L.; Nikolskaya, A. N.; Rao, B. S.; Smirnov, S.; Sverdlov, A. V.; Vasudevan, S.; Wolf, Y. I.; Yin, J. J.; Natale, D. A. The COG database: an updated version includes eukaryotes BMC Bioinform. 2003, 4 (1) 41
44. Marchler-Bauer, A.; Panchenko, A. R.; Shoemaker, B. A.; Thiessen, P. A.; Geer, L. Y.; Bryant, S. H. CDD: a database of conserved domain alignments with links to domain three-dimensional structure Nucleic Acids Res. 2002, 30 (1) 281-283
45. Hulo, N.; Bairoch, A.; Bulliard, V.; Cerutti, L.; De Castro, E.; Langendijk-Genevaux, P. S.; Pagni, M.; Sigrist, C. J. The PROSITE database Nucleic Acids Res. 2006, 34 (Database issue) D227-D230
46. Nielsen, H.; Engelbrecht, J.; Brunak, S.; von Heijne, G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites Protein Eng. 1997, 10 (1) 1-6
47. Hansen, J. E.; Lund, O.; Tolstrup, N.; Gooley, A. A.; Williams, K. L.; Brunak, S. NetOglyc: prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility Glycoconj. J. 1998, 15 (2) 115-130
48. Arca, B.; Lombardo, F.; Valenzuela, J. G.; Francischetti, I. M.; Marinotti, O.; Coluzzi, M.; Ribeiro, J. M. An updated catalogue of salivary gland transcripts in the adult female mosquito, Anopheles gambiae J. Exp. Biol. 2005, 208 (Pt 20) 3971-3986
49. Francischetti, I. M.; Valenzuela, J. G.; Pham, V. M.; Garfield, M. K.; Ribeiro, J. M. Toward a catalog for the transcripts and proteins (sialome) from the salivary gland of the malaria vector Anopheles gambiae J. Exp. Biol. 2002, 205 (Pt 16) 2429-2451
50. Ribeiro, J. M.; Andersen, J.; Silva-Neto, M. A.; Pham, V. M.; Garfield, M. K.; Valenzuela, J. G. Exploring the sialome of the blood-sucking bug Rhodnius prolixus Insect Biochem. Mol. Biol. 2004, 34 (1) 61-79
51. Ribeiro, J. M.; Charlab, R.; Pham, V. M.; Garfield, M.; Valenzuela, J. G. An insight into the salivary transcriptome and proteome of the adult female mosquito Culex pipiens quinquefasciatus Insect Biochem. Mol. Biol. 2004, 34 (6) 543-563
52. Galperin, M. Y.; Koonin, E. V. Conserved hypothetical' proteins: prioritization of targets for experimental study Nucleic Acids Res. 2004, 32 (18) 5452-5463
53. Kashiwada, M.; Lu, P.; Rothman, P. B. PIP3 pathway in regulatory T cells and autoimmunity Immunol. Res. 2007, 39 (1-3) 194-224
54. Harris, S. J.; Parry, R. V.; Westwick, J.; Ward, S. G. Phosphoinositide lipid phosphatases: natural regulators of phosphoinositide 3-kinase signaling in T lymphocytes J. Biol. Chem. 2008, 283 (5) 2465-2469
55. Santos, A.; Ribeiro, J. M.; Lehane, M. J.; Gontijo, N. F.; Veloso, A. B.; Sant'Anna, M. R.; Nascimento Araujo, R.; Grisard, E. C.; Pereira, M. H. The sialotranscriptome of the blood-sucking bug Triatoma brasiliensis (Hemiptera, Triatominae) Insect Biochem. Mol. Biol. 2007, 37 (7) 702-712
56. Assumpcao, T. C.; Francischetti, I. M.; Andersen, J. F.; Schwarz, A.; Santana, J. M.; Ribeiro, J. M. An insight into the sialome of the blood-sucking bug Triatoma infestans, a vector of Chagas' disease Insect Biochem. Mol. Biol. 2008, 38 (2) 213-232
57. Andersen, J. F.; Ribeiro, J. M. A secreted salivary inositol polyphosphate 5-phosphatase from a blood-feeding insect: allosteric activation by soluble phosphoinositides and phosphatidylserine Biochemistry 2006, 45 (17) 5450-5457
58. Valenzuela, J. G.; Charlab, R.; Galperin, M. Y.; Ribeiro, J. M. Purification, cloning, and expression of an apyrase from the bed bug Cimex lectularius. A new type of nucleotide-binding enzyme J. Biol. Chem. 1998, 273 (46) 30583-30590
59. Kisselev, L. L.; Justesen, J.; Wolfson, A. D.; Frolova, L. Y. Diadenosine oligophosphates (Ap(n)A), a novel class of signalling molecules FEBS Lett. 1998, 427 (2) 157-163
60. Schluter, H.; Tepel, M.; Zidek, W. Vascular actions of diadenosine phosphates J. Auton. Pharmacol. 1996, 16 (6) 357-362
61. Stavrou, B. M. Diadenosine polyphosphates: postulated mechanisms mediating the cardiac effects Curr. Med. Chem. Cardiovasc. Hematol. Agents 2003, 1 (2) 151-169
62. Harel, M.; Kryger, G.; Rosenberry, T. L.; Mallender, W. D.; Lewis, T.; Fletcher, R. J.; Guss, J. M.; Silman, I.; Sussman, J. L. Three-dimensional structures of Drosophila melanogaster acetylcholinesterase and of its complexes with two potent inhibitors Protein Sci. 2000, 9 (6) 1063-1072
63. Bourne, Y.; Taylor, P.; Bougis, P. E.; Marchot, P. Crystal structure of mouse acetylcholinesterase. A peripheral site-occluding loop in a tetrameric assembly J. Biol. Chem. 1999, 274 (5) 2963-2970
64. Sussman, J. L.; Harel, M.; Frolow, F.; Oefner, C.; Goldman, A.; Toker, L.; Silman, I. Atomic structure of acetylcholinesterase from Torpedo californica: a prototypic acetylcholine-binding protein Science 1991, 253 (5022) 872-879
65. Bennett-Lovsey, R. M.; Herbert, A. D.; Sternberg, M. J.; Kelley, L. A. Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre Proteins 2008, 70 (3) 611-625
66. Colletier, J. P.; Fournier, D.; Greenblatt, H. M.; Stojan, J.; Sussman, J. L.; Zaccai, G.; Silman, I.; Weik, M. Structural insights into substrate traffic and inhibition in acetylcholinesterase Embo J. 2006, 25 (12) 2746-2756
67. Ma, D.; Wang, Y.; Yang, H.; Wu, J.; An, S.; Gao, L.; Xu, X.; Lai, R. Anti-thrombosis repertoire of blood-feeding horsefly salivary glands Mol. Cell. Proteomics 2009, 8, 2071-2079
68. Rau, J. C.; Beaulieu, L. M.; Huntington, J. A.; Church, F. C. Serpins in thrombosis, hemostasis and fibrinolysis J. Thromb. Haemost. 2007, 5, 102-115
69. Kanost, M. R. Serine proteinase inhibitors in arthropod immunity Dev. Comp. Immunol. 1999, 23 (4-5) 291-301
70. Stark, K. R.; James, A. A. Isolation and characterization of the gene encoding a novel factor Xa-directed anticoagulant from the yellow fever mosquito, Aedes aegypti J. Biol. Chem. 1998, 273 (33) 20802-20809
71. Megraw, T.; Kaufman, T. C.; Kovalick, G. E. Sequence and expression of Drosophila Antigen 5-related 2, a new member of the CAP gene family Gene 1998, 222 (2) 297-304
72. Milne, T. J.; Abbenante, G.; Tyndall, J. D.; Halliday, J.; Lewis, R. J. Isolation and characterization of a cone snail protease with homology to CRISP proteins of the pathogenesis-related protein superfamily J. Biol. Chem. 2003, 278 (33) 31105-31110
73. Yamazaki, Y.; Hyodo, F.; Morita, T. Wide distribution of cysteine-rich secretory proteins in snake venoms: isolation and cloning of novel snake venom cysteine-rich secretory proteins Arch. Biochem. Biophys. 2003, 412 (1) 133-141
74. Yamazaki, Y.; Morita, T. Structure and function of snake venom cysteine-rich secretory proteins Toxicon 2004, 44 (3) 227-231
75. Mochca-Morales, J.; Martin, B. M.; Possani, L. D. Isolation and characterization of helothermine, a novel toxin from Heloderma horridum horridum (Mexican beaded lizard) venom Toxicon 1990, 28 (3) 299-309
76. Ameri, M.; Wang, X.; Wilkerson, M. J.; Kanost, M. R.; Broce, A. B. An immunoglobulin binding protein (antigen 5) of the stable fly (Diptera: Muscidae) salivary gland stimulates bovine immune responses J. Med. Entomol. 2008, 45 (1) 94-101
77. Xu, X.; Yang, H.; Ma, D.; Wu, J.; Wang, Y.; Song, Y.; Wang, X.; Lu, Y.; Yang, J.; Lai, R. Toward an understanding of the molecular mechanism for successful blood feeding by coupling proteomics analysis with pharmacological testing of horsefly salivary glands Mol. Cell. Proteomics 2008, 7 (3) 582-590
78. Scarborough, R. M.; Naughton, M. A.; Teng, W.; Rose, J. W.; Phillips, D. R.; Nannizzi, L.; Arfsten, A.; Campbell, A. M.; Charo, I. F. Design of potent and specific integrin antagonists. Peptide antagonists with high specificity for glycoprotein IIb-IIIa J. Biol. Chem. 1993, 268 (2) 1066-1073
79. Hekmat-Scafe, D. S.; Dorit, R. L.; Carlson, J. R. Molecular evolution of odorant-binding protein genes OS-E and OS-F in Drosophila Genetics 2000, 155 (1) 117-127
80. Valenzuela, J. G.; Charlab, R.; Gonzalez, E. C.; de Miranda-Santos, I. K.; Marinotti, O.; Francischetti, I. M.; Ribeiro, J. M. The D7 family of salivary proteins in blood sucking diptera Insect Mol. Biol. 2002, 11 (2) 149-155
81. Ribeiro, J. M.; Arca, B.; Lombardo, F.; Calvo, E.; Phan, V. M.; Chandra, P. K.; Wikel, S. K. An annotated catalogue of salivary gland transcripts in the adult female mosquito, Aedes aegypti BMC Genomics 2007, 8 (1) 6
82. Mans, B. J.; Calvo, E.; Ribeiro, J. M.; Andersen, J. F. The crystal structure of D7r4, a salivary biogenic amine-binding protein from the malaria mosquito Anopheles gambiae. J. Biol. Chem. 2007, 282 (50) 36626-36633
83. Calvo, E.; Mans, B. J.; Ribeiro, J. M.; Andersen, J. F. Multifunctionality and mechanism of ligand binding in a mosquito antiinflammatory protein Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (10) 3728-3733
84. Otti, O.; Naylor, R. A.; Siva-Jothy, M. T.; Reinhardt, K. Bacteriolytic activity in the ejaculate of an insect Am. Nat. 2009, 174 (2) 292-295
85. Hang, H. C.; Bertozzi, C. R. The chemistry and biology of mucin-type O-linked glycosylation Bioorg. Med. Chem. 2005, 13 (17) 5021-5034
86. Fukuda, M. Roles of mucin-type O-glycans in cell adhesion Biochim. Biophys. Acta 2002, 1573 (3) 394-405
87. Jochim, R. C.; Teixeira, C. R.; Laughinghouse, A.; Mu, J.; Oliveira, F.; Gomes, R. B.; Elnaiem, D. E.; Valenzuela, J. G. The midgut transcriptome of Lutzomyia longipalpis: comparative analysis of cDNA libraries from sugar-fed, blood-fed, post-digested and Leishmania infantum chagasi-infected sand flies BMC Genomics 2008, 9, 15
88. Ramalho-Ortigao, M.; Jochim, R. C.; Anderson, J. M.; Lawyer, P. G.; Pham, V. M.; Kamhawi, S.; Valenzuela, J. G. Exploring the midgut transcriptome of Phlebotomus papatasi: comparative analysis of expression profiles of sugar-fed, blood-fed and Leishmania-major-infected sandflies BMC Genomics 2007, 8, 300
89. Friedman, R.; Hughes, A. L. Codon volatility as an indicator of positive selection: data from eukaryotic genome comparisons Mol. Biol. Evol. 2005, 22 (3) 542-546
90. Pillai, S. K.; Kosakovsky Pond, S. L.; Woelk, C. H.; Richman, D. D.; Smith, D. M. Codon volatility does not reflect selective pressure on the HIV-1 genome Virology 2005, 336 (2) 137-143
91. Chen, Y.; Emerson, J. J.; Martin, T. M. Evolutionary genomics: codon volatility does not detect selection Nature 2005, 433 (7023) E6-E7, discussion E7-E8
92. Sharp, P. M. Gene "volatility" is most unlikely to reveal adaptation Mol. Biol. Evol. 2005, 22 (4) 807-809
93. Archetti, M. Genetic robustness at the codon level as a measure of selection Gene 2009, 443 (1-2) 64-69
94. Plotkin, J. B.; Dushoff, J.; Desai, M. M.; Fraser, H. B. Codon usage and selection on proteins J. Mol. Evol. 2006, 63 (5) 635-653
95. Krzywinski, J.; Grushko, O. G.; Besansky, N. J. Analysis of the complete mitochondrial DNA from Anopheles funestus: an improved dipteran mitochondrial genome annotation and a temporal dimension of mosquito evolution Mol. Phylogenet. Evol. 2006, 39 (2) 417-423
96. Valenzuela, J. G.; Belkaid, Y.; Rowton, E.; Ribeiro, J. M. The salivary apyrase of the blood-sucking sand fly Phlebotomus papatasi belongs to the novel Cimex family of apyrases J. Exp. Biol. 2001, 204 (Pt 2) 229-237
97. Valenzuela, J. G.; Garfield, M.; Rowton, E. D.; Pham, V. M. 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 (Pt 21) 3717-3729
98. Andersen, J. F.; Pham, V. M.; Meng, Z.; Champagne, D. E.; Ribeiro, J. M. Insight into the sialome of the Black Fly Simulium vittatum J. Proteome Res. 2009, 8 (3) 1474-1488
99. Kondrashov, F. A.; Koonin, E. V. A common framework for understanding the origin of genetic dominance and evolutionary fates of gene duplications Trends Genet 2004, 20 (7) 287-290
100. Smadja, C.; Shi, P.; Butlin, R. K.; Robertson, H. M. Large gene family expansions and adaptive evolution for odorant and gustatory receptors in the pea aphid, Acyrthosiphon pisum Mol. Biol. Evol. 2009, 26 (9) 2073-2086