Biochemical Characterization of Anopheles gambiae SRPN6, a Malaria Parasite Invasion Marker in Mosquitoes

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  An, Chunju ^a,b   Hiromasa, Yasuaki ^a   Zhang, Xin ^a   Lovell, Scott ^c   Zolkiewski, Michal ^a   Tomich, John M ^a   Michel, Kristin ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

^c UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMOLYMPH PROTEIN 6; INSECT PROTEIN; KALLIKREIN; PROPHENOLOXIDASE ACTIVATING PROTEINASE 1; PROPHENOLOXIDASE ACTIVATING PROTEINASE 3; RECOMBINANT PROTEIN; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR; SERINE PROTEINASE INHIBITOR 6; TRYPSIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANOPHELES GAMBIAE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; COMPLEX FORMATION; CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; ENZYME SPECIFICITY; ESCHERICHIA COLI; IN VITRO STUDY; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRECIPITATION; PROTEIN AGGREGATION; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; SEQUENCE ANALYSIS; SPECIES INVASION; STRUCTURE ANALYSIS; TEMPERATURE SENSITIVITY;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; KALLIKREINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SERINE ENDOPEPTIDASES; SERINE PROTEINASE INHIBITORS; SERPINS;

ANOPHELES GAMBIAE; BOVINAE; ESCHERICHIA COLI; MANDUCA SEXTA; SUS;

EID: 84869077676     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048689     Document Type: Article

References (64)

1. Huff CG, (1927) Studies on the infectivity of plasmodia of birds for mosquitoes, with special reference to the problem of immunity in the mosquito. The American Journal of Hygiene 7: 706-734.
2. Alavi Y, Arai M, Mendoza J, Tufet-Bayona M, Sinha R, et al. (2003) The dynamics of interactions between Plasmodium and the mosquito: a study of the infectivity of Plasmodium berghei and Plasmodium gallinaceum, and their transmission by Anopheles stephensi, Anopheles gambiae and Aedes aegypti. Int J Parasitol 33: 933-943.
3. Gouagna LC, Mulder B, Noubissi E, Tchuinkam T, Verhave JP, et al. (1998) The early sporogonic cycle of Plasmodium falciparum in laboratory-infected Anopheles gambiae: an estimation of parasite efficacy. Trop Med Int Health 3: 21-28.
4. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116: 661-670.
5. Osta MA, Christophides GK, Kafatos FC, (2004) Effects of mosquito genes on Plasmodium development. Science 303: 2030-2032.
6. Garver LS, Dong Y, Dimopoulos G, (2009) Caspar controls resistance to Plasmodium falciparum in diverse anopheline species. PLoS Pathog 5: e1000335.
7. Mitri C, Jacques JC, Thiery I, Riehle MM, Xu J, et al. (2009) Fine pathogen discrimination within the APL1 gene family protects Anopheles gambiae against human and rodent malaria species. PLoS Pathog 5: e1000576.
8. Rodrigues J, Oliveira GA, Kotsyfakis M, Dixit R, Molina-Cruz A, et al. (2012) An epithelial serine protease, AgESP, is required for Plasmodium invasion in the mosquito Anopheles gambiae. PLoS ONE 7: e35210.
9. Dong Y, Das S, Cirimotich C, Souza-Neto JA, McLean KJ, et al. (2011) Engineered anopheles immunity to Plasmodium infection. PLoS Pathog 7: e1002458.
10. Iwanaga S, Kawabata S, Muta T, (1998) New types of clotting factors and defense molecules found in horseshoe crab hemolymph: their structures and functions. J Biochem (Tokyo) 123: 1-15.
11. Levashina EA, Langley E, Green C, Gubb D, Ashburner M, et al. (1999) Constitutive activation of toll-mediated antifungal defense in serpin-deficient Drosophila. Science 285: 1917-1919.
12. Zou Z, Jiang H, (2005) Manduca sexta serpin-6 regulates immune serine proteinases PAP-3 and HP8. cDNA cloning, protein expression, inhibition kinetics, and function elucidation. J Biol Chem 280: 14341-14348.
13. Mulenga A, Khumthong R, Chalaire KC, (2009) Ixodes scapularis tick serine proteinase inhibitor (serpin) gene family; annotation and transcriptional analysis. BMC Genomics 10: 217.
14. Jiang R, Kim EH, Gong JH, Kwon HM, Kim CH, et al. (2009) Three pairs of protease-serpin complexes cooperatively regulate the insect innate immune responses. The Journal of biological chemistry 284: 35652.
15. Marinotti O, Nguyen QK, Calvo E, James AA, Ribeiro JMC, (2005) Microarray analysis of genes showing variable expression following a blood meal in Anopheles gambiae. Insect Molecular Biology 14: 365-373.
16. De Gregorio E, Han SJ, Lee WJ, Baek MJ, Osaki T, et al. (2002) An immune-responsive Serpin regulates the melanization cascade in Drosophila. Dev Cell 3: 581-592.
17. Ligoxygakis P, Pelte N, Ji C, Leclerc V, Duvic B, et al. (2002) A serpin mutant links Toll activation to melanization in the host defence of Drosophila. Embo J 21: 6330-6337.
18. Jiang H, Wang Y, Yu XQ, Zhu Y, Kanost M, (2003) Prophenoloxidase-activating proteinase-3 (PAP-3) from Manduca sexta hemolymph: a clip-domain serine proteinase regulated by serpin-1J and serine proteinase homologs. Insect Biochem Mol Biol 33: 1049-1060.
19. Tong Y, Kanost MR, (2005) Manduca sexta serpin-4 and serpin-5 inhibit the prophenol oxidase activation pathway: cDNA cloning, protein expression, and characterization. J Biol Chem 280: 14923-14931.
20. Tang H, Kambris Z, Lemaitre B, Hashimoto C, (2006) Two proteases defining a melanization cascade in the immune system of Drosophila. The Journal of biological chemistry 281: 28097.
21. Scherfer C, Tang H, Kambris Z, Lhocine N, Hashimoto C, et al. (2008) Drosophila Serpin-28D regulates hemolymph phenoloxidase activity and adult pigmentation. Dev Biol 323: 189-196.
22. Michel K, Budd A, Pinto S, Gibson TJ, Kafatos FC, (2005) Anopheles gambiae SRPN2 facilitates midgut invasion by the malaria parasite Plasmodium berghei. EMBO Rep 6: 891-897.
23. Michel K, Suwanchaichinda C, Morlais I, Lambrechts L, Cohuet A, et al. (2006) Increased melanizing activity in Anopheles gambiae does not affect development of Plasmodium falciparum. Proc Natl Acad Sci U S A 103: 16858-16863.
24. An C, Budd A, Kanost MR, Michel K, (2010) Characterization of a regulatory unit that controls melanization and affects longevity of mosquitoes. Cell Mol Life Sci.
25. Zou Z, Shin SW, Alvarez KS, Kokoza V, Raikhel AS, (2010) Distinct Melanization Pathways in the Mosquito Aedes aegypti. Immunity 32: 41-53.
26. Calvo E, Mizurini DM, Sa-Nunes A, Ribeiro JMC, Andersen JF, et al. (2011) Alboserpin, a Factor Xa Inhibitor from the Mosquito Vector of Yellow Fever, Binds Heparin and Membrane Phospholipids and Exhibits Antithrombotic Activity. Journal of Biological Chemistry 286: 27998-28010.
27. Kambris Z, Blagborough AM, Pinto SB, Blagrove MS, Godfray HC, et al. (2010) Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae. PLoS Pathog 6: e1001143.
28. Danielli A, Barillas-Mury C, Kumar S, Kafatos FC, Loukeris TG, (2005) Overexpression and altered nucleocytoplasmic distribution of Anopheles ovalbumin-like SRPN10 serpins in Plasmodium-infected midgut cells. Cell Microbiol 7: 181-190.
29. Abraham EG, Pinto SB, Ghosh A, Vanlandingham DL, Budd A, et al. (2005) An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proc Natl Acad Sci U S A 102: 16327-16332.
30. Pinto SB, Kafatos FC, Michel K, (2008) The parasite invasion marker SRPN6 reduces sporozoite numbers in salivary glands of Anopheles gambiae. Cell Microbiol 10: 891-898.
31. Olson ST, Gettins PG, (2011) Regulation of proteases by protein inhibitors of the serpin superfamily. Prog Mol Biol Transl Sci 99: 185-240.
32. Huber R, Carrell RW, (1989) Implications of the three-dimensional structure of alpha 1-antitrypsin for structure and function of serpins. Biochemistry 28: 8951-8966.
33. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599.
34. Schick C, Kamachi Y, Bartuski AJ, Cataltepe S, Schechter NM, et al. (1997) Squamous cell carcinoma antigen 2 is a novel serpin that inhibits the chymotrypsin-like proteinases cathepsin G and mast cell chymase. The Journal of biological chemistry 272: 1849.
35. Ulvila J, Vanha-Aho LM, Ramet M, (2011) Drosophila phagocytosis- still many unknowns under the surface. APMIS 119: 651-662.
36. Flink IL, Bailey TJ, Gustafson TA, Markham BE, Morkin E, (1986) Complete amino acid sequence of human thyroxine-binding globulin deduced from cloned DNA: close homology to the serine antiproteases. Proc Natl Acad Sci U S A 83: 7708-7712.
37. Valenzuela JG, Pham VM, Garfield MK, Francischetti IMB, Ribeiro JMC, (2002) Toward a description of the sialome of the adult female mosquito Aedes aegypti. Insect Biochemistry and Molecular Biology 32: 1101-1122.
38. Hunt LT, Dayhoff MO, (1980) A surprising new protein superfamily containing ovalbumin, antithrombin-III, and alpha 1-proteinase inhibitor. Biochem Biophys Res Commun 95: 864-871.
39. Dissanayake SN, Marinotti O, Ribeiro JM, James AA, (2006) angaGEDUCI: Anopheles gambiae gene expression database with integrated comparative algorithms for identifying conserved DNA motifs in promoter sequences. BMC Genomics 7: 116.
40. An C, Lovell S, Kanost MR, Battaile KP, Michel K, (2011) Crystal structure of native Anopheles gambiae serpin-2, a negative regulator of melanization in mosquitoes. Proteins 79: 1999-2003.
41. Baglin TP, Carrell RW, Church FC, Esmon CT, Huntington JA, (2002) Crystal structures of native and thrombin-complexed heparin cofactor II reveal a multistep allosteric mechanism. Proc Natl Acad Sci U S A 99: 11079-11084.
42. Huntington JA, Olson ST, Fan B, Gettins PG, (1996) Mechanism of heparin activation of antithrombin. Evidence for reactive center loop preinsertion with expulsion upon heparin binding. Biochemistry 35: 8495-8503.
43. Jin L, Abrahams JP, Skinner R, Petitou M, Pike RN, et al. (1997) The anticoagulant activation of antithrombin by heparin. Proc Natl Acad Sci U S A 94: 14683-14688.
44. Roy A, Kucukural A, Zhang Y, (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738.
45. Zhang Y, (2007) Template-based modeling and free modeling by I-TASSER in CASP7. Proteins 69 (Suppl 8):: 108-117.
46. Zhu Y, Wang Y, Gorman MJ, Jiang H, Kanost MR, (2003) Manduca sexta serpin-3 regulates prophenoloxidase activation in response to infection by inhibiting prophenoloxidase-activating proteinases. J Biol Chem 278: 46556-46564.
47. An C, Ishibashi J, Ragan EJ, Jiang H, Kanost MR, (2009) Functions of Manduca sexta Hemolymph Proteinases HP6 and HP8 in Two Innate Immune Pathways. The Journal of biological chemistry 284: 19716.
48. Philo JS, (2000) A method for directly fitting the time derivative of sedimentation velocity data and an alternative algorithm for calculating sedimentation coefficient distribution functions. Anal Biochem 279: 151-163.
49. Jiang H, Wang Y, Kanost MR, (1998) Pro-phenol oxidase activating proteinase from an insect, Manduca sexta: a bacteria-inducible protein similar to Drosophila easter. Proc Natl Acad Sci U S A 95: 12220-12225.
50. Jiang H, Wang Y, Gu Y, Guo X, Zou Z, et al. (2005) Molecular identification of a bevy of serine proteinases in Manduca sexta hemolymph. Insect Biochem Mol Biol 35: 931-943.
51. Li J, Wang Z, Canagarajah B, Jiang H, Kanost M, et al. (1999) The structure of active serpin 1K from Manduca sexta. Structure Fold Des 7: 103-109.
52. Park SH, Jiang R, Piao S, Zhang B, Kim EH, et al. (2010) Structural and functional characterization of a highly specific serpin in the insect innate immunity. J Biol Chem.
53. Suwanchaichinda C, Kanost MR, (2009) The serpin gene family in Anopheles gambiae. Gene 442: 47.
54. Pelte N, Robertson AS, Zou Z, Belorgey D, Dafforn TR, et al. (2006) Immune challenge induces N-terminal cleavage of the Drosophila serpin Necrotic. Insect Biochem Mol Biol 36: 37-46.
55. Lomas DA, Evans DL, Finch JT, Carrell RW, (1992) The mechanism of Z alpha 1-antitrypsin accumulation in the liver. Nature 357: 605-607.
56. Davis RL, Shrimpton AE, Holohan PD, Bradshaw C, Feiglin D, et al. (1999) Familial dementia caused by polymerization of mutant neuroserpin. Nature 401: 376-379.
57. Saklatvala J, Wood GC, White DD, (1976) Isolation and characterization of human plasma alpha 1-proteinase inhibitor and a conformational study of its interaction with proteinases. Biochem J 157: 339-351.
58. Nordenman B, Nystrom C, Bjork I, (1977) The size and shape of human and bovine antithrombin III. Eur J Biochem 78: 195-203.
59. Takahara H, Shibata S, Sinohara H, (1984) Conformational differences between mouse contrapsin and alpha-1-antitrypsin as studied by ultraviolet absorption and circular dichroism spectroscopy. Tohoku J Exp Med 142: 261-273.
60. Pearce FG, Mackintosh SH, Gerrard JA, (2007) Formation of amyloid-like fibrils by ovalbumin and related proteins under conditions relevant to food processing. J Agric Food Chem 55: 318-322.
61. Stark KR, James AA, (1995) A factor Xa-directed anticoagulant from the salivary glands of the yellow fever mosquito Aedes aegypti. Exp Parasitol 81: 321-331.
62. Irving JA, Pike RN, Lesk AM, Whisstock JC, (2000) Phylogeny of the serpin superfamily: implications of patterns of amino acid conservation for structure and function. Genome Res 10: 1845-1864.
63. Tong Y, Jiang H, Kanost MR, (2005) Identification of plasma proteases inhibited by Manduca sexta serpin-4 and serpin-5 and their association with components of the prophenol oxidase activation pathway. J Biol Chem 280: 14932-14942.
64. Muller HM, Dimopoulos G, Blass C, Kafatos FC, (1999) A hemocyte-like cell line established from the malaria vector Anopheles gambiae expresses six prophenoloxidase genes. J Biol Chem 274: 11727-11735.