Cell Biochemistry and Biophysics

, Volume 70, Issue 2, pp 1469–1477 | Cite as

Polar Profile of Antiviral Peptides from AVPpred Database

  • Carlos Polanco
  • José Lino Samaniego
  • Jorge Alberto Castañón-González
  • Thomas Buhse
Original Paper


Diseases of viral origin in humans are among the most serious threats to health and the global economy. As recent history has shown the virus has a high pandemic potential, among other reasons, due to its ability to spread by air, hence the identification, investigation, containment, and treatment of viral diseases should be considered of paramount importance. In this sense, the bioinformatics research has focused on finding fast and efficient algorithms that can identify highly toxic antiviral peptides and to serve as a first filter, so that trials in the laboratory are substantially reduced. The work presented here contributes to this effort through the use of an algorithm already published by this team, called polarity index method, which identifies with high efficiency antiviral peptides from the exhaustive analysis of the polar profile, using the linear sequence of the peptide. The test carried out included all peptides in APD2 Database and 60 antiviral peptides identified by Kumar and co-workers (Nucleic Acids Res 40:W199–204, 2012), to build its AVPpred algorithm. The validity of the method was focused on its discriminating capacity so we included the 15 sub-classifications of both Databases.


Polarity index method Antiviral peptides AVPpred algorithm 



Selective cationic amphipathic antibacterial peptides


Antimicrobial peptide database http://aps.unmc.edu/AP/ [1] accessed December 19, 2012. AVPpred, http://crdd.osdd.net/servers/avppred [2] accessed March 10, 2013


Quantitative structure activity relationships


Support vector machine


Severe acute respiratory syndrome


Human immunodeficiency virus


Amino acid indices, substitution matrices and pair-wise contact potentials database http://www.genome.jp/aaindex/ [3] accessed March 10, 2013



The authors acknowledge the Departamento de Cómputo, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán for support, and the proof-reading of this manuscript by Concepción Celis Juárez.

Conflict of interest

We declare that we do not have any financial and personal interest with other people or organizations that could inappropriately influence (bias) our work.

Supplementary material

12013_2014_84_MOESM1_ESM.gz (3.6 mb)
Supplementary material 1 (GZ 3700 kb)
12013_2014_84_MOESM2_ESM.gz (3.6 mb)
Supplementary material 2 (GZ 3700 kb)


  1. 1.
    Wang, G., Li, X., & Wang, Z. (2009). APD2: The updated antimicrobial peptide database and its application in peptide design. Nucleic Acids Research, 37, D933–D937.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Thakur, N., Qureshi, A., & Kumar, M. (40). AVPpred: Collection and prediction of highly effective antiviral peptides. Nucleic Acids Research, 2012, W199–W204.Google Scholar
  3. 3.
    Kawashima, S., & Kanehisa, M. (2000). AAindex: Amino acid index database. Nucleic Acids Research, 28, 374.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Haagmans, B. L., Andeweg, A. C., & Osterhaus, A. (2009). The application of genomics to emerging zoonotic viral diseases. PLoS Pathogens, 2009, 5.Google Scholar
  5. 5.
    De Clercq, E. (2004). Antivirals and antiviral strategies. Nature Reviews Microbiology, 2, 704–720.PubMedCrossRefGoogle Scholar
  6. 6.
    Rerks-Ngarm, S., Pitisuttithum, P., Nitayaphan, S., Kaewkungwal, J., Chiu, J., Paris, R., et al. (2009). Investigators, M.-T. vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. New England Journal of Medicine, 361, 2209–2220.PubMedCrossRefGoogle Scholar
  7. 7.
    Wedemeyer, H., Schuller, E., Schlaphoff, V., Stauber, R. E., Wiegand, J., Schiefke, I., et al. (2009). Therapeutic vaccine IC41 as late add-on to standard treatment in patients with chronic hepatitis C. Vaccine, 27, 5142–5151.PubMedCrossRefGoogle Scholar
  8. 8.
    Dykxhoorn, D. M., & Lieberman, J. (2006). Silencing viral infection. PLOS Medicine, 3, e242.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Kricka, L. J., & Fortina, P. (2009). Analytical ancestry: “Firsts” in fluorescent labeling of nucleosides, nucleotides, and nucleic acids. Clinical Chemistry, 55, 670–683.PubMedCrossRefGoogle Scholar
  10. 10.
    Bharti, A. C., Shukla, S., Mahata, S., Hedau, S., & Das, B. C. (2009). Anti-human papillomavirus therapeutics: Facts & future. Indian Journal of Medical Research, 130, 296–310.PubMedGoogle Scholar
  11. 11.
    McKeegan, K. S., Borges-Walmsley, M. I., & Walmsley, A. R. (2002). Microbial and viral drug resistance mechanisms. Trends in Microbiology, 10, S8–S14.PubMedCrossRefGoogle Scholar
  12. 12.
    Polanco González, C., Nuño Maganda, M. A., Arias-Estrada, M., & del Rio, G. (2011). An FPGA implementation to detect selective cationic antibacterial peptides. PLoS ONE, 6(6), e21399.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Polanco, C., & Samaniego, J. L. (2009). Detection of selective cationic amphipathic antibacterial peptides by Hidden Markov models. Acta Biochimica Polonica, 56, 167–176.PubMedGoogle Scholar
  14. 14.
    Polanco, C., Samaniego, J. L., Buhse, T., Mosqueira, F. G., Negron-Mendoza, A., Ramos-Bernal, S., et al. (2012). Characterization of selective antibacterial peptides by polarity index. International Journal of Peptide, 2012, 585027.Google Scholar
  15. 15.
    del Rio, G., Castro-Obregon, S., Rao, R., Ellerby, H. M., & Bredesen, D. E. (2001). APAP, a sequence-pattern recognition approach identifies substance P as a potential apoptotic peptide. FEBS Letters, 3, 213–219.Google Scholar
  16. 16.
    Polanco, C., Buhse, T., Samaniego, J. L., & Castañón-González, J. A. (2013). A toy model of prebiotic peptide evolution: The possible role of relative amino acid abundances. Acta Biochimica Polonica, 60, 175–182.Google Scholar
  17. 17.
    Polanco, C., Samaniego, J. L., Castañón-González, J. A., Buhse, T., Sordo, M. L. (2013). Characterization of a possible uptake mechanism of selective antibacterial peptides. Acta Biochimica Polonica, 60, 629–633.Google Scholar
  18. 18.
    Beghin, F., & Dirkx, J. (1975). Proceedings: A simple statistical method to predict protein conformations. International Archives of Physiology and Biochemistry, 83, 167–168.Google Scholar
  19. 19.
    Bull, H. B., & Breese, K. (1974). Surface tension of amino acid solutions: A hydrophobicity scale of the amino acid residues. Archives of Biochemistry and Biophysics, 161, 665–670.PubMedCrossRefGoogle Scholar
  20. 20.
    Charton, M. (1981). Protein folding and the genetic code: An alternative quantitative model. Journal of Theoretical Biology, 1981(91), 115–123.CrossRefGoogle Scholar
  21. 21.
    Chou, P. Y., & Fasman, G. D. (1978). Prediction of the secondary structure of proteins from their amino acid sequence. Advances in Enzymology and Related Areas of Molecular Biology, 47, 145–148.Google Scholar
  22. 22.
    Cohn, E. J., & Edsall, J. T. (1943). Proteins amino acids and peptides as ions and dipolar ions. New York: Reinhold.Google Scholar
  23. 23.
    Fasman, G. D. (1976). Handbook of biochemistry and molecular biology, section D: Physical and Chemical Data. London: Taylor & Francis.Google Scholar
  24. 24.
    Fauchère, J. L., Charton, M., Kier, L. B., Verloop, A., & Pliska, V. (1988). Amino acid side chain parameters for correlation studies in biology and pharmacology. International Journal of Peptide and Protein Research, 32, 269–278.PubMedCrossRefGoogle Scholar
  25. 25.
    Finkelstein, A. V., Ptitsyn, O. B., & Kozitsyn, S. A. (1977). Theory of protein molecule self-organization. II. A comparison of calculated thermodynamic parameters of local secondary structures with experiments. Biopolymers, 16, 497–524.PubMedCrossRefGoogle Scholar
  26. 26.
    Finkelstein, A. V., Badretdinov, A. Y., & Ptitsyn, O. B. (1991). Physical reasons for secondary structure stability: Alpha-helices in short peptides. Proteins, 10, 287–299.PubMedCrossRefGoogle Scholar
  27. 27.
    Geisow, M. J., & Roberts, R. D. (1980). Amino acid preferences for secondary structure vary with protein class. International Journal of Biological Macromolecules, 2, 387–389.CrossRefGoogle Scholar
  28. 28.
    Karplus, P., & Schulz, G. (1985). Prediction of chain flexibility in proteins. A tool for the selection of peptide antigens. Naturwissenschaften, 72, 212–213.CrossRefGoogle Scholar
  29. 29.
    Aurora, R., & Rose, G. D. (1998). Helix capping. Protein Science, 7, 21–38.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Avbelj, F. (2000). Amino acid conformational preferences and solvation of polar backbone atoms in peptides and proteins. Journal of Molecular Biology, 300, 1335–1359.PubMedCrossRefGoogle Scholar
  31. 31.
    George, R. A., & Heringa, J. (2002). An analysis of protein domain linkers: Their classification and role in protein folding. Protein Engineering, 15, 871–879.PubMedCrossRefGoogle Scholar
  32. 32.
    Kidera, A., Konishi, Y., Oka, M., Ooi, T., & Scheraga, A. (1985). Statistical analysis of the physical properties of the 20 naturally occuring amino acids. Journal of Protein Chemistry, 4, 23–55.CrossRefGoogle Scholar
  33. 33.
    Guy, H. R. (1985). Amino acid side-chain partition energies and distribution of residues in soluble proteins. Biophysical Journal, 1985(47), 61–70.CrossRefGoogle Scholar
  34. 34.
    Casari, G., & Sippl, M. J. (1992). Structure-derived hydrophobic potential. Hydrophobic potential derived from X-ray structures of globular proteins is able to identify native folds. Journal of Molecular Biology, 224, 725–732.PubMedCrossRefGoogle Scholar
  35. 35.
    Richardson, C., Hull, D., Greer, P., Hasel, K., Berkovich, A., Englund, G., et al. (1986). The nucleotide sequence of the mRNA encoding the fusion protein of measles virus (Edmonston strain): A comparison of fusion proteins from several different paramyxoviruses. Virology, 155, 508–523.PubMedCrossRefGoogle Scholar
  36. 36.
    Collins, P. L., Huang, Y. T., & Wertz, G. W. (1984). Nucleotide sequence of the gene encoding the fusion (F) glycoprotein of human respiratory syncytial virus. Proceedings of National Academy of Science USA, 1984, 7683–7687.CrossRefGoogle Scholar
  37. 37.
    Kestler, H. W, 3rd, Li, Y., Naidu, Y. M., Butler, C. V., Ochs, M. F., Jaenel, G., et al. (1988). Comparison of simian immunodeficiency virus isolates. Nature, 1988(331), 619–622.CrossRefGoogle Scholar
  38. 38.
    Verschoor, E. J., Hulskotte, E. G., Ederveen, J., Koolen, M. J., Horzinek, M. C., & Rottier, P. J. (1993). Post-translational processing of the feline immunodeficiency virus envelope precursor protein. Virology, 193, 433–438.PubMedCrossRefGoogle Scholar
  39. 39.
    Lohmann, V., Körner, F., Koch, J., Herian, U., Theilmann, L., & Bartenschlager, R. (1999). Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science, 285, 110–113.PubMedCrossRefGoogle Scholar
  40. 40.
    Choo, Q. L., Richman, K. H., Han, J. H., Berger, K., Lee, C., Dong, C., et al. (1991). Genetic organization and diversity of the hepatitis C virus. Proceedings of National Academy of Science USA, 88, 2451–2455.CrossRefGoogle Scholar
  41. 41.
    Penin, F., Brass, V., Appel, N., Ramboarina, S., Montserret, R., Ficheux, D., et al. (2004). Structure and function of the membrane anchor domain of hepatitis C virus nonstructural protein 5A. Journal of Biological Chemistry, 2004(279), 40835–40843.CrossRefGoogle Scholar
  42. 42.
    Chamberlain, R. W., Adams, N. J., Taylor, L. A., Simmonds, P., & Elliott, R. M. (1997). The complete coding sequence of hepatitis C virus genotype 5a, the predominant genotype in South Africa. Biochemical and Biophysical Research Communications, 236, 44–49.PubMedCrossRefGoogle Scholar
  43. 43.
    Gould, A. R. (1996). Comparison of the deduced matrix and fusion protein sequences of equine morbillivirus with cognate genes of the Paramyxoviridae. Virus Research, 1996(43), 17–31.CrossRefGoogle Scholar
  44. 44.
    Spriggs, M. K., Olmsted, R. A., Venkatesan, S., Coligan, J. E., & Collins, P. L. (1986). Fusion glycoprotein of human parainfluenza virus type 3: Nucleotide sequence of the gene, direct identification of the cleavage-activation site, and comparison with other paramyxoviruses. Virology, 152, 241–251.PubMedCrossRefGoogle Scholar
  45. 45.
    Wang, H., & Ng, T. B. (2000). Ginkbilobin, a novel antifungal protein from Ginkgo biloba seeds with sequence similarity to embryo-abundant protein. Biochemical and Biophysical Research Communications, 279, 407–411.PubMedCrossRefGoogle Scholar
  46. 46.
    Stevenson, M., Haggerty, S., Lamonica, C., Mann, A. M., Meier, C., & Wasiak, A. (1990). Cloning and characterization of human immunodeficiency virus type 1 variants diminished in the ability to induce syncytium-independent cytolysis. Journal of Virology, 64, 3792–3803.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Belanger, F. C., & Kriz, A. L. (1989). Molecular characterization of the major maize embryo globulin encoded by the glb1 gene. Plant Physiology, 91, 636–643.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Mulvenna, J. P., Sando, L., & Craik, D. J. (2005). Processing of a 22 kDa precursor protein to produce the circular protein tricyclon A. Structure, 13, 691–701.PubMedCrossRefGoogle Scholar
  49. 49.
    Harris, J. D., Hibler, D. W., Fontenot, G. K., Hsu, K. T., Yurewicz, E. C., & Sacco, A. G. (1994). Cloning and characterization of zona pellucida genes and cDNAs from a variety of mammalian species: The ZPA, ZPB and ZPC gene families. DNA Sequence, 4, 361–393.PubMedGoogle Scholar
  50. 50.
    Hauser, L. J., Land, M. L., Brown, S. D., Larimer, F., Keller, K. L., Rapp-Giles, B. J., et al. (2011). Complete genome sequence and updated annotation of Desulfovibrio alaskensis G20. Journal of Bacteriology, 193, 4268–4269.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Agerberth, B., Gunne, H., Odeberg, J., Kogner, P., Boman, H. G., & Gudmundsson, G. H. (1995). FALL-39, a putative human peptide antibiotic, is cysteine-free and expressed in bone marrow and testis. Proceedings of the National Academy of Sciences USA, 92, 195–199.CrossRefGoogle Scholar
  52. 52.
    Ireland, D. C., Colgrave, M. L., & Craik, D. J. (2006). A novel suite of cyclotides from Viola odorata: Sequence variation and the implications for structure, function and stability. Biochemical Journal, 400, 1–12.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Tang, Y. Q., Yuan, J., Osapay, G., Osapay, K., Tran, D., Miller, C. J., et al. (1999). A cyclic antimicrobial peptide produced in primate leukocytes by the ligation of two truncated alpha-defensins. Science, 286, 498–502.PubMedCrossRefGoogle Scholar
  54. 54.
    Wong, J. H., & Ng, T. B. (2005). Sesquin, a potent defensin-like antimicrobial peptide from ground beans with inhibitory activities toward tumor cells and HIV-1 reverse transcriptase. Peptides, 26, 1120–1126.PubMedCrossRefGoogle Scholar
  55. 55.
    Kurachi, K., Chandra, T., Degen, S. J., White, T. T., Marchioro, T. L., Woo, S. L., et al. (1981). Cloning and sequence of cDNA coding for alpha 1-antitrypsin. Proceedings of the National Academy of Sciences, 78, 6826–6830.CrossRefGoogle Scholar
  56. 56.
    Nishimura, Y., Miyazawa, T., Ikeda, Y., Izumiya, Y., Nakamura, K., Cai, J. S., et al. (1998). Molecular cloning and sequencing of feline stromal cell-derived factor-1 alpha and beta. European Journal of Immunogenetics, 25, 303–305.PubMedCrossRefGoogle Scholar
  57. 57.
    Collman, R., Balliet, J. W., Gregory, S. A., Friedman, H., Kolson, D. L., Nathanson, N., et al. (1992). An infectious molecular clone of an unusual macrophage-tropic and highly cytopathic strain of human immunodeficiency virus type 1. Journal of Virology, 66, 7517–7521.PubMedPubMedCentralGoogle Scholar
  58. 58.
    Taylor, G. R., Lagosky, P. A., Storms, R. K., & Haynes, R. H. (1987). Molecular characterization of the cell cycle-regulated thymidylate synthase gene of Saccharomyces cerevisiae. Journal of Biological Chemistry, 262, 5298–5307.PubMedGoogle Scholar
  59. 59.
    Church, D. M., Goodstadt, L., Hillier, L. W., Zody, M. C., Goldstein, S., She, X., et al. (2009). Mouse genome sequencing consortium. Lineage-specific biology revealed by a finished genome assembly of the mouse. PLOS Biology, 7, e1000112.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Ousley, A., Zafarullah, K., Chen, Y., Emerson, M., Hickman, L., & Sehgal, A. (1998). Conserved regions of the timeless (tim) clock gene in Drosophila analyzed through phylogenetic and functional studies. Genetics, 148, 815–825.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Ratner, L., Haseltine, W., Patarca, R., Livak, K. J., Starcich, B., Josephs, S. F., et al. (1985). Complete nucleotide sequence of the AIDS virus, HTLV-III. Nature, 313, 277–284.PubMedCrossRefGoogle Scholar
  62. 62.
    Ratner, L., Fisher, A., Jagodzinski, L. L., Mitsuya, H., Liou, R. S., Gallo, R. C., et al. (1987). Complete nucleotide sequences of functional clones of the AIDS virus. AIDS Research and Human Retroviruses, 3, 57–69.PubMedCrossRefGoogle Scholar
  63. 63.
    Steinborner, S. T., Currie, G. J., Bowie, J. H., Wallace, J. C., & Tyler, M. J. (1998). New antibiotic caerin 1 peptides from the skin secretion of the Australian tree frog Litoria chloris. Comparison of the activities of the caerin 1 peptides from the genus Litoria. Journal of Peptide Research, 51, 121–126.PubMedCrossRefGoogle Scholar
  64. 64.
    Reitz, M. S, Jr, Hall, L., Robert-Guroff, M., Lautenberger, J., Hahn, B. M., Shaw, G. M., et al. (1994). Viral variability and serum antibody response in a laboratory worker infected with HIV type 1 (HTLV type IIIB). AIDS Research and Human Retroviruses, 10, 1143–1155.PubMedCrossRefGoogle Scholar
  65. 65.
    Goraya, J., Knoop, F. C., & Conlon, J. M. (1998). Ranatuerins: Antimicrobial peptides isolated from the skin of the American bullfrog, Rana catesbeiana. Biochemical and Biophysical Research Communications, 250, 589–592.PubMedCrossRefGoogle Scholar
  66. 66.
    Rozek, T., Wegener, K. L., Bowie, J. H., Olver, I. N., Carver, J. A., Wallace, J. C., et al. (2000). The antibiotic and anticancer active aurein peptides from the Australian Bell Frogs Litoria aurea and Litoria raniformis the solution structure of aurein 1.2. European Journal of Biochemistry, 267, 5330–5341.PubMedCrossRefGoogle Scholar
  67. 67.
    Tamas, I., Klasson, L., Canbäck, B., Näslund, A. K., Eriksson, A. S., Wernegreen, J. J., et al. (2002). 50 million years of genomic stasis in endosymbiotic bacteria. Science, 296, 2376–2379.PubMedCrossRefGoogle Scholar
  68. 68.
    Lamberty, M., Zachary, D., Lanot, R., Bordereau, C., Robert, A., Hoffmann, J. A., et al. (2001). Insect immunity. Constitutive expression of a cysteine-rich antifungal and a linear antibacterial peptide in a termite insect. Journal of Biological Chemistry, 276, 4085–4092.PubMedCrossRefGoogle Scholar
  69. 69.
    McGeoch, D. J., & Davison, A. J. (1986). DNA sequence of the herpes simplex virus type 1 gene encoding glycoprotein gH, and identification of homologues in the genomes of varicella-zoster virus and Epstein-Barr virus. Nucleic Acids Research, 14, 4281–4292.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Mushahwar, I. K., Erker, J. C., Muerhoff, A. S., Leary, T. P., Simons, J. N., Birkenmeyer, L. G., et al. (1999). Molecular and biophysical characterization of TT virus: Evidence for a new virus family infecting humans. Proceedings of National Academy of Science USA, 96, 3177–3182.CrossRefGoogle Scholar
  71. 71.
    Giménez-Bonafé, P., Soler, F. M., Buesa, C., Sautière, P. E., Ausió, J., Kouach, M., et al. (2004). Chromatin organization during spermiogenesis in Octopus vulgaris. II: DNA-interacting proteins. Molecular Reproduction and Development, 68, 232–239.PubMedCrossRefGoogle Scholar
  72. 72.
    Hammond, J., & Hammond, R. W. (2003). The complete nucleotide sequence of isolate BYMV-GDD of Bean yellow mosaic virus, and comparison to other potyviruses. Archives of Virology, 148, 2461–2470.PubMedCrossRefGoogle Scholar
  73. 73.
    Yoshida, T., Miyagawa, K., Odagiri, H., Sakamoto, H., Little, P. F., Terada, M., et al. (1987). Genomic sequence of hst, a transforming gene encoding a protein homologous to fibroblast growth factors and the int-2-encoded protein. Proceedings of National Academy of Science USA, 84, 7305–7309.CrossRefGoogle Scholar
  74. 74.
    Gombart, A. F., Blissard, G. W., & Rohrmann, G. F. (1989). Characterization of the genetic organization of the HindIII M region of the multicapsid nuclear polyhedrosis virus of Orgyia pseudotsugata reveals major differences among baculoviruses. Journal of General Virology, 70, 1815–1828.PubMedCrossRefGoogle Scholar
  75. 75.
    Suerbaum, S., Josenhans, C., Sterzenbach, T., Drescher, B., Brandt, P., Bell, M., et al. (2003). The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proceedings National Academy of Science USA, 100, 7901–7906.CrossRefGoogle Scholar
  76. 76.
    Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., et al. (1998). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature, 393, 537–544.PubMedCrossRefGoogle Scholar
  77. 77.
    Collins, P. L., Huang, Y. T., & Wertz, G. W. (1984). Nucleotide sequence of the gene encoding the fusion (F) glycoprotein of human respiratory syncytial virus. Proceedings of National Academy of Science USA, 81, 7683–7687.CrossRefGoogle Scholar
  78. 78.
    Terry, A. S., Poulter, L., Williams, D. H., Nutkins, J. C., Giovannini, M. G., Moore, C. H., et al. (1988). The cDNA sequence coding for prepro-PGS (prepro-magainins) and aspects of the processing of this prepro-polypeptide. Journal of Biological Chemistry, 263, 5745–5751.PubMedGoogle Scholar
  79. 79.
    Gil, R., Silva, F. J., Zientz, E., Delmotte, F., González-Candelas, F., Latorre, A., et al. (2003). The genome sequence of Blochmannia floridanus: Comparative analysis of reduced genomes. Proceedings of National Academy of Science USA, 100, 9388–9393.CrossRefGoogle Scholar
  80. 80.
    Gettner, S. N., Kenyon, C., & Reichardt, L. F. (1995). Characterization of beta pat-3 heterodimers, a family of essential integrin receptors in C. elegans. Journal of Cell Biology, 129, 1127–1141.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Carlos Polanco
    • 1
    • 2
  • José Lino Samaniego
    • 1
    • 2
  • Jorge Alberto Castañón-González
    • 1
  • Thomas Buhse
    • 3
  1. 1.Facultad de Ciencias de la SaludUniversidad AnáhuacHuixquilucanMexico
  2. 2.Departamento de Matemáticas, Facultad de CienciasUniversidad Nacional Autónoma de MéxicoMexicoMexico
  3. 3.Centro de Investigaciones QuímicasUniversidad Autónoma del Estado de MorelosCuernavacaMexico

Personalised recommendations