Recombinant scorpine: A multifunctional antimicrobial peptide with activity against different pathogens

Cellular and Molecular Life Sciences

Volumn 65, Issue 19, 2008, Pages 3081-3092

  Carballar Lejarazu R ^a   Rodriguez M H ^a   De La Cruz Hernandez Hernandez F ^b   Ramos Castaneda J ^a   Possani, L D ^c   Zurita Ortega, M ^c   Reynaud Garza, E ^c   Hernandez Rivas R ^b   Loukeris, T ^d   Lycett, G ^d   Lanz Mendoza, H ^a  

^a INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^d INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

Antimicrobial peptide; Dengue; Malaria; Plasmodium; Recombinant scorpine; Virus

Indexed keywords

POLYPEPTIDE ANTIBIOTIC AGENT; RECOMBINANT SCORPINE; UNCLASSIFIED DRUG;

ANOPHELES GAMBIAE; ANTIBACTERIAL ACTIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACILLUS SUBTILIS; CONTROLLED STUDY; DENGUE VIRUS; DROSOPHILA; HEMOLYMPH; KLEBSIELLA PNEUMONIAE; MOLECULAR CLONING; NONHUMAN; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; PROTEIN EXPRESSION; PROTEIN SECRETION; TRANSGENIC ANIMAL; VIRUS INHIBITION; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANOPHELES GAMBIAE; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BACILLUS SUBTILIS; CELLS, CULTURED; DEFENSINS; DROSOPHILA MELANOGASTER; KLEBSIELLA PNEUMONIAE; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; PLASMODIUM BERGHEI; RECOMBINANT PROTEINS; SCORPION VENOMS;

BACILLUS SUBTILIS; HEXAPODA; KLEBSIELLA PNEUMONIAE; MURINAE; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM;

EID: 53049103246     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-008-8250-8     Document Type: Article

References (78)

1. Epand, R. and Vogel, H. J. (1999) Diversity of antimicrobial peptides and their mechanism of action. Biochem. Biophys. Acta 1462, 11-28.
2. Friedrich, C. L., Moyles, D., Beveridge, T. J. and Hancock, R. E. (2000) Antibacterial action of structurally diverse cationic peptides on gram-positive bacteria. Antimicrob. Agents Chemother. 44, 2086-2092.
3. Ganz, T. and Lehrer, R. I. (1995) Defensins. Pharmacol. Ther. 66, 191-205.
4. Hancock, R. E. and Scott, M. G. (2000) The role of antimicrobial peptides in animal defences. Proc. Natl. Acad. Sci. USA 97, 8856-8861.
5. Simmaco, M., Mignogna, G. and Barra, D. (1998) Antimicrobial peptides from amphibian skin: what do they tell us? Biopolymers 47, 435-450.
6. Baker, M. A., Maloy, W. L., Zasloff, M. and Jacob, L. S. (1993) Anticancer efficacy of magainin 2 and analogue peptides. Cancer Res. 53, 3052-3057.
7. Chen, Y., Xu, X., Hong, S., Chen, J., Liu, N., Underhill, C. B., Creswell, K. and Zhang, L. (2001) RGD-tachyplesin inhibits tumor growth. Cancer Res. 61, 2434-2438.
8. Hoskin, W.D and Ramamoorthy, A. (2008) Studies on anticancer activities of antimicrobial peptides. BBA Biomembranes 1778, 357-375.
9. Brogden, A. K. (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3, 238-250.
10. Cudic, M. and Otvos, L.Jr. (2002) Intracellular targets of antimicrobial peptides. Curr. Drug Targets 3, 101-106.
11. Lehrer, R. I., Barton, A., Daher, K. A., Harwig, S. S., Ganz, T. and Selsted, M. E. (1989) Interaction of human defensins with Escherichia coli: mechanism of bactericidal activity. J. Clin. Invest. 84, 553-561.
12. Matsuzaki, K. (1999) Why and how are peptide-lipid interactions utilized for self-defense?Magainins and tachyplesins as archetypes. Biochim. Biophys. Acta 1462, 1-10.
13. Otvos, L. Jr., Snyder, C., Condie, B., Bulet, P. and Wade, J. (2005) Chimeric antimicrobial peptides exhibit multiple modes of action. Int. J. Peptide Res. and Ther. 11, 29-42.
14. Park, C. B., Kim, H. S. and Kim, S. C. (1998) Mechanism of action of the antimicrobial peptide buforin II: buforin II kills microorganisms by penetrating the cell membrane and inhibiting cellular functions. Biochem. Biophys. Res. Commun. 244, 253-257.
15. Carlsson, A., Nystrom, T., de Cock, H. and Bennich, H. (1998) Attacin - an insect immune protein - binds LPS and triggers the specific inhibition of bacterial outer-membrane protein synthesis. Microbiology 144, 2179-2188.
16. Boman, H.G., Agerberth, B. and Boman, A. (1993) Mechanisms of action on Escherichia coli of cecropin P1 and PR-39, two antibacterial peptides from pig intestine. Infect. Immun. 61, 2978-2984.
17. Ramamoorthy A., Thennarasu, S., Lee, D., Tan, A. and Maloy, L. (2006) Solid-State NMR investigation of the membrane-disrupting mechanism of antimicrobial peptides MSI-78 and MSI-594 derived from magainin 2 and melittin. Biophys. J. 91, 206-216.
18. Dhople, V., Krukemeyer, A. and Ramamoorthy, A. (2006) The human beta-defensin-3, an antibacterial peptide with multiple biological functions. BBA-Biomembranes 1758, 1499-1512.
19. Gwadz, R., Kaslow, D., Lee, J., Maloy, L., Zasloff, M. and Miller, L. (1989) Effects of magainins and cecropins on the sporogonic development of malaria parasites in mosquitoes. Infect. Immun. 57, 2628-2633.
20. Shahabuddin, M., Fields, I., Bulet, P., Hoffmann, J. A. and Miller, L. H. (1998) Plasmodium gallinaceum: differential killing of some mosquito stages of the parasite by insect defensin. Exp. Parasitol. 89, 103-112.
21. Arrighi, R. B. G., Nakamura, C., Miyake, J., Hurd, H. and Burgess, J. G. (2002) Design and activity of antimicrobial peptides against sporogonic-stage parasites causing murine malaria. Antimicrob. Agents Chemother. 46, 2104-2110.
22. Boisbouvier, J., Prochnicka-Chalufour, A., Nieto, A. R., Torres, J. A., Nanard, N., Rodriguez, M. H., Possani, L. D. and Delepierre, M. (1998) Structural information on a cecropin-like synthetic peptide, shiva-3 toxic to the sporogonic development of Plasmodium berghei. Eur. J. Biochem. 257, 263-273.
23. Rodríguez, M. C., Zamudio, F., Torres, J. A., González- Cerón, L., Posanni, L. D. and Rodríguez, M. H. (1995) Effect of a cecropin-like synthetic peptide (Shiva-3) on the sporogonic development of Plasmodium berghei. Exp. Parasitol. 80, 596-604.
24. Buck, C., Day, P., Thompson, C., Lubkowski, J., Lu, W., Lowry, D. and Schiller, J. (2006) Human α-defensins block papillomavirus infection. Proc. Natl. Acad. Sci. USA 103, 1516-1521.
25. Albiol, M. V. and Castilla, V. (2004) Antiviral activity of antimicrobial cationic peptides against Junin virus and herpes simplex virus. Int. J. Antimicrob. Agents 23, 382-389.
26. Sinha, S., Cheshenko, N., Lehrer, R. and Herold, B. (2003) NP-1, a rabbit α-defensin, prevents the Eetry and intercellular spread of herpes simplex virus type 2. Antimicrob. Agents Chemother. 47, 494-500.
27. Yasin, B., Wang, W., Pang, M., Cheshenko, N., Hong, T., Waring, A. J., Herold, B. C., Wagar, E. A. and Lehrer, R. R. (2004) Theta defensins protect cells from infection by herpes simplex virus by inhibiting viral adhesion and entry. J. Virol. 78, 5147-5156.
28. Daher, K. A., Selsted, M. E. and Lehrer, R. I. (1986) Direct inactivation of viruses by human granulocyte defensins. J. Virol. 60, 1068-1074.
29. Cole, A. M. and Lehrer, R. I. (2003) Minidefensins: antimicrobial peptides with activity against HIV-1. Curr. Pharm. Des. 9, 1463-1473.
30. Munk, C., Wei, G., Yang, O. O., Waring, A. J., Wang, W., Hong, T., Lehrer, R. I., Landau, N. R. and Cole, A. M. (2003) The theta-defensin, retrocyclin, inhibits HIV-1 entry. AIDS Res. Hum. Retroviruses 19, 875-881.
31. Quinones-Mateu, M. E., Lederman, M. M., Feng, Z., Chakraborty, B., Weber, J., Rangel, H. R., Marotta, M. L., Mirza, M., Jiang, B., Kiser, P., Medvik, K., Sieg, S. F. and Weinberg, A. (2003) Human epithelial beta-defensins 2 and 3 inhibit HIV-1 replication. AIDS 17, F39-48.
32. Robinson, W. E. Jr., McDougall, B., Tran, D. and Selsted, M. E. (1998) Anti-HIV-1 activity of indolicidin, an antimicrobial peptide from neutrophils. J. Leukoc. Biol. 63, 94-100.
33. VanCompernolle, S. E., Taylor, R. J., Oswald-Richter, K., Jiang, J., Youree, B. E., Bowie, J. H., Tyler, M. J., Conlon, J. M., Wade, D., Aiken, C., Dermody, T. S., KewalRamani, V. N., Rollins-Smith, L. A. and Unutmaz, D. (2005) Antimicrobial peptides from amphibian skin potently inhibit human immunodeficiency virus infection and transfer of virus from dendritic cells to T cells. J. Virol. 79, 11598-11606.
34. Wachinger, M., Kleinschmidt, A., Winder, D., von Pechmann, N., Ludvigsen, A., Neumann, M., Holle, R., Salmons, B., Erfle, V. and Brack-Werner, R. (1998) Antimicrobial peptides melittin and cecropin inhibit replication of human immunodeficiency virus 1 by suppressing viral gene expression. J. Gen. Virol. 79, 731-740.
35. Ramamoorthy, A., Thennarasu, S., Tan, A., Gottipati, K., Sreekumar, S., Heyl, D. L., An, F. Y. P., and Shelburne, C. E. (2006) Deletion of all cysteines in tachyplesin I abolish hemolytic activity and retain antimicrobial activity and lipopolysaccharide selective binding. Biochemistry 45, 6529-6540.
36. Powers, J. P. S., Tan, A., Ramamoorthy, A and Hancock, R. E. W. (2005) Solution structure and interaction of the antimicrobial polyphemusins with lipid membranes, Biochemistry 44, 15504-15513.
37. Tamamura, H., Otaka, A., Murakami, T., Ishihara, T., Ibuka, T., Waki, M., Matsumoto, A., Yamamoto, N. and Fujii, N. (1996) Interaction of an anti-HIV peptide, T22, with gp120 and CD4. Biochem. Biophys. Res. Commun. 219, 555-559.
38. Leikina, E., Delanoe-Ayari, H., Melikov, K., Cho, M. S., Chen, A., Waring, A. J., Wang, W., Xie, Y., Loo, J. A., Lehrer, R. I. and Chernomordik, L. V. (2005) Carbohydrate-binding molecules inhibit viral fusion and entry by crosslinking membrane glycoproteins. Nat. Immunol. 6, 995-1001.
39. Hultmark, D., Steiner, H., Rasmuson, T. and Boman, H. G. (1980) Insect immunity. Purification and properties of three inducible bactericidal proteins from hemolymph of immunized pupae of Hyalophora cecropia. Eur. J. Biochem. 127, 207-217.
40. Simard, M. J. and Watt, D. D. (2004) Venoms and toxins. The Biology of Scorpions, in: Polis G. A. (ed.), New York: Stanford University Press, 1990, p. 414-444.
41. Ehret-Sabatier, L., Loew, D., Goyffon, M., Fehlbaum, P., Hoffmann, J. A., van Dorsselaer, A. and Bulet, P. (1996) Characterization of novel cysteine-rich antimicrobial peptides from scorpion blood. J. Biol. Chem. 271, 29537-29544.
42. Hetru, C., Letellier, L., Oren, Z., Hoffmann, J. A. and Shai, Y. (2000) Androctonin, a hydrophilic disulphide-bridged non-haemolytic anti-microbial peptide: a plausible mode of action. Biochem. J. 345, 653-664.
43. Torres-Larios, A., Gurrola, G. B., Zamudio, F. Z. and Posanni, L. D. (2000) Hadrurin, a new antimicrobial peptide from the venom of the scorpion Hadrurus aztecus. Eur. J. Biochem. 267, 5023-5031.
44. Verdonck F. (2000) A novel class of pore-forming peptides in the venom of Parabuthus schlechteri Purcell (Scorpions: Buthidae) Cimbebasia 16, 247-60.
45. Moerman, L., Bosteels, S., Noppe, W., Willems, J., Clynen, E., Schoofs, L., Thevissen, K., Tytgat, J., Van Eldere, J., Van Der Walt, J. and Verdonck. F. (2002) Antibacterial and antifungal properties of alpha-helical, cationic peptides in the venom of scorpions from southern Africa. Eur. J. Biochem. 269, 4799-4810.
46. Corzo, G., Escoubas, P., Villegas, E., Barnham, K., He, W., Norton, R. and Nakajima, T. (2001) Characterization of unique amphipatic antimicrobial peptides from venom of the scorpion Pandinus imperator. Biochem. J. 359, 35-45.
47. Conde, R., Zamudio, F.Z., Rodríguez, M.H. and Possani, L.D. (2000) Scorpine, an anti-malaria and anti-bacterial agent purified from scorpion venom. FEBS Lett. 471, 165-168.
48. Lycett, G. J., Kafatos F. C. and Loukeris, T. G. (2004) Conditional expression in the malaria mosquito Anopheles stephensi with Tet-On and Tet-Off systems. Genetics 167, 1781-1790.
49. Catteruccia, F., Nolan, T., Loukeris, T. G., Blass, C., Savakis, C., Kafatos, F. C. and Crisanti, A. (2000) Stable germline transformation of the malaria mosquito Anopheles stephensi. Nature 405, 959-962.
50. Fleming, H. P., Walter, W. M. and Etchells, J. L. (1973) Antimicrobial properties of oleuropein and products of its hydrolysis from green olives. Appl. Environ. Microbiol. 26, 777-782.
51. Hoffman, D., Hultmark, D. and Boman, H.G. (1981) Insect immunity: Galleria mellonella and other Lepidoptera have cecropia-P9-like factors active against gram negative bacteria. Insect Biochem. 11, 537-548.
52. Trager, W. and Jensen, J. B. (1976) Human malaria parasites in continuous culture. Science 193, 673-675.
53. Schneider, D. and Shahabuddin, M. (2000) Malaria parasite development in a Drosophila model. Science 2888, 2376-2379.
54. Possani, L. D., Corona, M., Zurita, M. and Rodríguez, M. H. (2002) From noxiustoxin to scorpine and posible transgenic mosquitoes resistant to malaria. Arch. Med. Res. 33, 398-404.
55. Spradling, A. C. P. (1986) P-element-mediated transformation. In. Drosophila, a Practical Approach, pp 175-191, Roberts, D. B. (ed.), IRL Press, Oxford.
56. Schlesinger, R. W. Dengue Viruses (1977), vol. 16, 2nd ed., pp. 75-84, Virology Monographs, ed. Gard, S. and Hallauer, C. (eds.), Springer, New York, 75-84.
57. Cociancich, S., Goyffon, M., Bontems, F., Bulet, P., Bouet, F., Menez, A. and Hoffmann, J. (1993) Purification and characterization of a scorpion defensin, a 4 kDa antibacterial peptide presenting structural similarities with insect defensins and scorpion toxins. Biochem. Biophys. Res. Commun. 194, 17-22.
58. Revest, J. M., DeMoerlooze, L. and Dickson, C. (2000) Fibroblast growth factor 9 secretion is mediated by a noncleaved amino-terminal signal sequence. J. Biol. Chem. 275, 8083-8090.
59. Bellovino, D., Marimoto, T., Mengheri, E., Perozzi, G., Garaquso, I., Nobili, F. and Gaetani, S. (2001) Unique biochemical nature of carp retinol-binding protein. N-linked glycosylation and uncleaable NH2-terminal signal peptide. J. Biol. Chem. 276, 13949-13956.
60. Ye, R. D., Wun, T. C. and Sadler, J. E. (1988) Mammalian protein secretion without signal peptide removal. Biosynthesis of plasminogen activator inhibitor-2 in U-937 cells. J. Biol. Chem. 263, 4869-4875.
61. Efron, L., Dagan, A., Gaidukov, L., Ginsburg, H. and Mor, A. (2002) Direct interaction of Dermaseptin S4 aminoheptanoyl derivative with intraerythrocytic malaria parasite leading to increased specific antiparasitic activity in culture. J. Biol. Chem. 277, 24067-24072.
62. Oren, Z., Lerman, J. C., Gudmundsson G. H., Agerberth B. and Shai, Y. (1999) Structure and organization of the human antimicrobial peptide LL-37 in phospholipid membranes: relevance to the molecular basis for its non-cell-selective activity. Biochem. J. 341, 501-513.
63. Numao, N., Hirota, Y., Iwahori, A., Kidokoro, S., Sasatsu, M., Kondo, I., Itoh, S., Itoh, E., Katoh, T., Shimozono, N., Yamazaki, A., Takao, K., Kobayashi, S. (1999) Biological activities of 1,1,6-trisubstituted indanes: beyond magainin 2. Biol. Pharm. Bull. 22,73-76.
64. Diego-Garcia, E., Abdel-Mottaleb, Y., Schwartz, E. F., de la Vega, R. C. and Posanni, L. D. (2007) Cytolytic and K(+) channel blocking activities of beta-KTx and scorpine-like peptides purified from scorpion venoms. Cell. Mol. Life Sci.
65. Peschel, A., Otto, M., Jack, R. W., Kalbacher, H., Jung, G. and Gotz, F. (1999) Inactivation of the dlt operon in Staphylococcus aureus confers sensitivity to defensins, protegrins, and other antimicrobial peptides. J. Biol. Chem. 274, 8405-8410.
66. Shai, Y. (1999) Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell nonselective membrane-lytic peptides. Biochim. Biophys. Acta 1462, 55-70.
67. Yang, L., Harroun, T. A., Weiss, T. M., Ding, L. and Huang, H. W. (2001) Barrel-stave model or toroidal model? A case study on melittin pores. Biophys. J. 81, 1475-1485.
68. Yang, L., Weiss, T. M., Lehrer, R. I. and Huang, H. W. (2000) Crystallization of antimicrobial pores in membranes:magainin and protegrin. Biophys. J. 79, 2002-2009.
69. Westerhoff, H. V., Juretic, D., Hendler, R. W. and Zasloff, M. (1989) Magainins and the disruption of membrane-linked free-energy transduction. Proc. Natl. Acad. Sci. USA 86, 6597-6601.
70. Bierbaum, G. and Sahl, H. G. (1985) Induction of autolysis of staphylococci by the basic peptide antibiotics Pep 5 and nisin and their influence on the activity of autolytic enzymes. Arch. Microbiol. 141, 249-254.
71. Castle, M., Nazarian, A., Yi, S. S. and Tempst, P. (1999) Lethal effects of apidaecin on Escherichia coli involve sequential molecular interactions with diverse targets. J. Biol. Chem. 274, 32555-32564.
72. Xiong, Y., Yeaman, M. R. and Bayer, A,S. (1999) In vitro antibacterial activities of platelet microbicidal protein and neutrophil defensin against Staphylococcus aureus are influenced by antibiotics differing in mechanism of action. Antimicrob. Agents Chemother. 43, 1111-1117.
73. Mukhopadhyay, S., Kuhn, R. J. and Rossmann, M. G. (2006)A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3, 13 -22.
74. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms. Nature 415, 389-395.
75. Reyes-Del Valle, J., Chávez-Salinas, S., Medina, F. and Del Angel, R. M. (2005) Heat shock protein 90 and heat shock protein 70 are components of dengue virus receptor complex in human cells. J. Virol. 79, 4557-4567.
76. Li, J., Zhang, C., Xu, X., Wang, J., Yu, H., Lai, R. and Gong, W. (2007) Trypsin inhibitory loop is an excellent lead structure to design serine protease inhibitors and antimicrobial peptides. FASEB J. 21, 2466-2473.
77. Dürr, U. H. N., Sudheendra, U. S. and Ramamoorthy, A. (2006) LL-37, the only human member of the cathelicidin family of antimicrobial peptides. BBA-Biomembranes 1758, 1408-1425.
78. Moon, J. Y., Henzler-Wildman, K. A. and Ramamoorthy, A, (2006) Expression and purification of a recombinant LL-37 from Escherichia coli. Biochim. Biophys. Acta 1758, 1351-1358.