Particle and Fibre Toxicology | |
Phlebotomus papatasi SP15: mRNA expression variability and amino acid sequence polymorphisms of field populations | |
Mary Ann McDowell4  Frank H. Collins4  Shaden Kamhawi1  Scott J. Emrich4  Andrew R. Mahon3  Neil F. Lobo4  Jenica Abrudan7  Douglas A. Shoue4  Mariha Wadsworth4  Gwen Stayback4  David F. Hoel6  Mahmoud Abo-Shehada5  Emad El-Din Y. Fawaz9  Shabaan S. El-Hossary9  Hanafi A. Hanafi5  Hussan Dayem5  Rami Mukbel5  Carlos Alberto S. Figueiredo8  Valdir Q. Balbino8  Iliano V. Coutinho-Abreu1  Marcelo Ramalho-Ortigão2  | |
[1] Laboratory of Malaria and Vector Research, NIAID-NIH, 12735 Twinbrook Parkway, Rockville 20852, MD, USA;Department of Entomology, Kansas State University, Manhattan 66506, KS, USA;Department of Biology, Central Michigan University, Mount Pleasant, Detroit 48859, MI, USA;Eck Institute for Global Health, Department of Biological Sciences, University of Notre Dame, Notre Dame 46556, IN, USA;Faculty of Veterinary Medicine, Jordan University of Science and Technology, Irbid 22110, Jordan;Department of Biostatistics, Uniformed Services University of the Health Sciences, Bethesda 20814, MD, USA;Department of Pathology and Laboratory Medicine, The Children’s Hospital of Philadelphia, Philadelphia, USA;Department of Genetics, Universidade Federal de Pernambuco, Recife, PE, Brazil;Vector Biology Research Program, U.S. Naval Medical Research Unit No. 3 (NAMRU-3), Cairo, Egypt | |
关键词: MHC class II epitopes; Expression variability; Vaccine; Leishmaniasis; PpSP15; Saliva; Sand fly; | |
Others : 1224686 DOI : 10.1186/s13071-015-0914-2 |
|
received in 2015-04-11, accepted in 2015-05-22, 发布年份 2015 | |
【 摘 要 】
Background
The Phlebotomus papatasi salivary protein PpSP15 was shown to protect mice against Leishmania major, suggesting that incorporation of salivary molecules in multi-component vaccines may be a viable strategy for anti-Leishmania vaccines.
Methods
Here, we investigated PpSP15 predicted amino acid sequence variability and mRNA profile of P. papatasi field populations from the Middle East. In addition, predicted MHC class II T-cell epitopes were obtained and compared to areas of amino acid sequence variability within the secreted protein.
Results
The analysis of PpSP15 expression from field populations revealed significant intra- and interpopulation variation.. In spite of the variability detected for P. papatasi populations, common epitopes for MHC class II binding are still present and may potentially be used to boost the response against Le. major infections.
Conclusions
Conserved epitopes of PpSP15 could potentially be used in the development of a salivary gland antigen-based vaccine.
【 授权许可】
2015 Ramalho-Ortigão et al.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150912080807566.pdf | 1398KB | download | |
Fig. 5. | 29KB | Image | download |
Fig. 4. | 21KB | Image | download |
Fig. 3. | 41KB | Image | download |
Fig. 2. | 147KB | Image | download |
Fig. 1. | 31KB | Image | download |
【 图 表 】
Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
【 参考文献 】
- [1]Milleron RS, Ribeiro JM, Elnaime D, Soong L, Lanzaro GC. Negative effect of antibodies against maxadilan on the fitness of the sand fly vector of American visceral leishmaniasis. Am J Trop Med Hyg. 2004; 70(3):278-285.
- [2]Wikel SK. Immune responses to arthropods and their products. Annu Rev Entomol. 1982; 27:21-48.
- [3]Alger NE, Cabrera EJ. An increase in death rate of Anopheles stephensi fed on rabbits immunized with mosquito antigen. J Econ Entomol. 1972; 65(1):165-168.
- [4]Nogge G, Giannetti M. Specific antibodies: a potential insecticide. Science. 1980; 209(4460):1028-1029.
- [5]Sutherland GB, Ewen AB. Fecundity decrease in mosquitoes ingesting blood from specifically sensitized mammals. J Insect Physiol. 1974; 20(4):655-660.
- [6]Kemp DH, Agbede RI, Johnston LA, Gough JM. Immunization of cattle against Boophilus microplus using extracts derived from adult female ticks: feeding and survival of the parasite on vaccinated cattle. Int J Parasitol. 1986; 16(2):115-120.
- [7]Chinzei Y, Minoura H. Reduced oviposition in Ornithodoros moubata (Acari: Argasidae) fed on tick-sensitized and vitellin-immunized rabbits. J Med Entomol. 1988; 25(1):26-31.
- [8]Ghosh KN, Mukhopadhyay J. The effect of anti-sandfly saliva antibodies on Phlebotomus argentipes and Leishmania donovani. Int J Parasitol. 1998; 28(2):275-281.
- [9]Ramasamy MS, Sands M, Kay BH, Fanning ID, Lawrence GW, Ramasamy R. Anti-mosquito antibodies reduce the susceptibility of Aedes aegypti to arbovirus infection. Med Vet Entomol. 1990; 4(1):49-55.
- [10]Ramasamy MS, Ramasamy R. Effect of anti-mosquito antibodies on the infectivity of the rodent malaria parasite Plasmodium berghei to Anopheles farauti. Med Vet Entomol. 1990; 4(2):161-166.
- [11]Lal AA, Schriefer ME, Sacci JB, Goldman IF, Louis-Wileman V, Collins WE, Azad AF. Inhibition of malaria parasite development in mosquitoes by anti-mosquito-midgut antibodies. Infect Immun. 1994; 62(1):316-318.
- [12]Kamhawi S, Belkaid Y, Modi G, Rowton E, Sacks D. Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science. 2000; 290(5495):1351-1354.
- [13]Abdeladhim M, Jochim RC, Ben Ahmed M, Zhioua E, Chelbi I, Cherni S, Louzir H, Ribeiro JM, Valenzuela JG. Updating the salivary gland transcriptome of Phlebotomus papatasi (Tunisian strain): the search for sand fly-secreted immunogenic proteins for humans. PloS one. 2012; 7(11):e47347.
- [14]Valenzuela JG, Belkaid Y, Garfield MK, Mendez S, Kamhawi S, Rowton ED, Sacks DL, Ribeiro JM. Toward a defined anti-Leishmania vaccine targeting vector antigens: characterization of a protective salivary protein. J Exp Med. 2001; 194(3):331-342.
- [15]Elnaiem DE, Meneses C, Slotman M, Lanzaro GC. Genetic variation in the sand fly salivary protein, SP-15, a potential vaccine candidate against Leishmania major. Insect Mol Biol. 2005; 14(2):145-150.
- [16]Depaquit J, Lienard E, Verzeaux-Griffon A, Ferte H, Bounamous A, Gantier JC, Hanafi HA, Jacobson RL, Maroli M, Moin-Vaziri V et al.. Molecular homogeneity in diverse geographical populations of Phlebotomus papatasi (Diptera, Psychodidae) inferred from ND4 mtDNA and ITS2 rDNA Epidemiological consequences. Infect Genet Evol. 2008; 8(2):159-170.
- [17]Hamarsheh O, Presber W, Abdeen Z, Sawalha S, Al-Lahem A, Schonian G. Genetic structure of Mediterranean populations of the sandfly Phlebotomus papatasi by mitochondrial cytochrome b haplotype analysis. Med Vet Entomol. 2007; 21(3):270-277.
- [18]Henikoff S, Henikoff JG. Amino acid substitution matrices from protein block. Proc Natl Acad Sci U S A. 1992; 89(22):10915-10919.
- [19]Hoel DF, Butler JF, Fawaz EY, Watany N, El-Hossary SS, Villinski J. Response of phlebotomine sand flies to light-emitting diode-modified light traps in southern Egypt. J Vector Ecol. 2007; 32(2):302-308.
- [20]Hanafi HA, Fryauff DJ, Modi GB, Ibrahim MO, Main AJ. Bionomics of phlebotomine sandflies at a peacekeeping duty site in the north of Sinai, Egypt. Acta Trop. 2007; 101(2):106-114.
- [21]Morsy TA, Shoukry A, Schnur LF, Sulitzeanu A. Gerbillus pyramidum is a host of Leishmania major in the Sinai Peninsula. Ann Trop Med Parasitol. 1987; 81(6):741-742.
- [22]Saliba EK, Pratlong F, Dedet JP, Saleh N, Khoury SA, Oumeish OY, Batayneh O, Al-Oran R. Identification of Leishmania strains from Jordan. Ann Trop Med Parasitol. 2004; 98(7):677-683.
- [23]Janini R, Saliba E, Khoury S, Oumeish O, Adwan S, Kamhawi S. Incrimination of Phlebotomus papatasi as vector of Leishmania major in the southern Jordan Valley. Med Vet Entomol. 1995; 9(4):420-422.
- [24]Janini R, Saliba E, Kamhawi S. Species composition of sand flies and population dynamics of Phlebotomus papatasi (Diptera: Psychodidae) in the southern Jordan Valley, an endemic focus of cutaneous leishmaniasis. J Med Entomol. 1995; 32(6):822-826.
- [25]Kamhawi S, Arbagi A, Adwan S, Rida M. Environmental manipulation in the control of a zoonotic cutaneous leishmaniasis focus. Arch Inst Pasteur Tunis. 1993; 70(3–4):383-390.
- [26]Schlein Y, Jacobson RL. Linkage between susceptibility of Phlebotomus papatasi to Leishmania major and hunger tolerance. Parasitology. 2002; 125(Pt 4):343-348.
- [27]Kamhawi S, Modi GB, Pimenta PF, Rowton E, Sacks DL. The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan-mediated midgut attachment. Parasitology. 2000; 121(Pt 1):25-33.
- [28]Lane RP. The sandflies of Egypt (Diptera: Phlebotominae). Bull Br Mus. 1986; 52(1):1-35.
- [29]Anez N, Tang Y. Comparison of three methods for age-grading of female neotropical phlebotomine sandflies. Med Vet Entomol. 1997; 11(1):3-7.
- [30]Ramalho-Ortigao M, Jochim RC, Anderson JM, Lawyer PG, Pham VM, Kamhawi S, Valenzuela JG. 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. BioMed Central Full Text
- [31]Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Nat Methods. 2001; 25(4):402-408.
- [32]Coutinho-Abreu IV, Wadsworth M, Stayback G, Ramalho-Ortigao M, McDowell MA. Differential expression of salivary gland genes in the female sand fly Phlebotomus papatasi (Diptera: Psychodidae). J Med Entomol. 2010; 47(6):1146-1155.
- [33]Coutinho-Abreu IV, Mukbel R, Hanafi HA, Fawaz EY, El-Hossary SS, Wadsworth M, Stayback G, Pitts DA, Abo-Shehada M, Hoel DF et al.. Expression plasticity of Phlebotomus papatasi salivary gland genes in distinct ecotopes through the sand fly season. BMC Ecology. 2011; 11:24. BioMed Central Full Text
- [34]Ewing B, Green P. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 1998; 8(186–194):186-194.
- [35]Staden R. The Staden sequence analysis package. Mol Biotechnol. 1996; 5(3):233-241.
- [36]Huang X, Madan A. CAP3: A DNA sequence assembly program. Genome Res. 1999; 9(9):868-877.
- [37]Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22(22):4673-4680.
- [38]Kumar S, Nei M, Dudley J, Tamura K. MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform. 2008; 9(4):299-306.
- [39]Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C et al.. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012; 28(12):1647-1649.
- [40]Coutinho-Abreu IV, Sonoda IV, Fonseca JA, Melo MA, Balbino VQ, Ramalho-Ortigao M. Lutzomyia longipalpis s.l. in Brazil and the impact of the Sao Francisco River in the speciation of this sand fly vector. Parasites & vectors. 2008; 1(1):16. BioMed Central Full Text
- [41]Hudson RR, Boos DD, Kaplan NL. A statistical test for detecting population subdivision. Mol Biol Evol. 1992; 9:138-151.
- [42]Hudson RR, Slatkin M, Maddison WP. Estimation of levels of gene flow from DNA sequence data. Genetics. 1992; 132:583-589.
- [43]Nei M. Analysis of gene diversity in subdivided populations. ProcNatl Acad Sci USA. 1973; 70:3321-3323.
- [44]Lynch M, Crease TJ. The analysis of population survey data on DNA sequence variation. Mol Biol Evol. 1990; 7:377-394.
- [45]Jukes TH, Cantor CR. Evolution of protein molecules. In: Mammalian Protein Metabolism. Munro HN, editor. Academic, New York; 1969: p.21-132.
- [46]Kimura M. Evolutionary rate at the molecular level. Nature. 1968; 217:624-626.
- [47]Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989; 123(3):585-595.
- [48]Fu Y-X, Li W-H. Statistical tests of neutrality of mutations. Genetics. 1993; 133:693-709.
- [49]Fu YX. Statistical tests of neutrality of mutations against population growth hitchhiking and background selection. Genetics. 1997; 147(2):915-925.
- [50]Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009; 25(11):1451-1452.
- [51]Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res. 2004; 14:1188-1190.
- [52]Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999; 41:95-98.
- [53]Bian H, Hammer J. Discovery of promiscuous HLA-II-restricted T cell epitopes with TEPITOPE. Methods. 2004; 34(4):468-475.
- [54]Singh H, Raghava GPS. ProPred: Prediction of HLA-DR binding sites. Bioinformatics. 2001; 17(12):1236-1237.
- [55]Lanzaro GC, Lopes AH, Ribeiro JM, Shoemaker CB, Warburg A, Soares M, Titus RG. Variation in the salivary peptide, maxadilan, from species in the Lutzomyia longipalpis complex. Insect Mol Biol. 1999; 8(2):267-275.
- [56]Laurenti MD, da Matta VL, Pernichelli T, Secundino NF, Pinto LC, Corbett CE, Pimenta PP. Effects of salivary gland homogenate from wild-caught and laboratory-reared Lutzomyia longipalpis on the evolution and immunomodulation of Leishmania (Leishmania) amazonensis infection. Scand J Immunol. 2009; 70(4):389-395.
- [57]Laurenti MD, Silveira VM, Secundino NF, Corbett CE, Pimenta PP. Saliva of laboratory-reared Lutzomyia longipalpis exacerbates Leishmania (Leishmania) amazonensis infection more potently than saliva of wild-caught Lutzomyia longipalpis. Parasitol International. 2009; 58:220-226.
- [58]Ben Hadj Ahmed S, Chelbi I, Kaabi B, Cherni S, Derbali M, Zhioua E. Differences in the salivary effects of wild-caught versus colonized Phlebotomus papatasi (Diptera: Psychodidae) on the development of zoonotic cutaneous leishmaniasis in BALB/c mice. J Med Entomol. 2010; 47(1):74-79.
- [59]Kato H, Anderson JM, Kamhawi S, Oliveira F, Lawyer PG, Pham VM, Sangare CS, Samake S, Sissoko I, Garfield M et al.. High degree of conservancy among secreted salivary gland proteins from two geographically distant Phlebotomus duboscqi sandflies populations (Mali and Kenya). BMC genomics. 2006; 7:226. BioMed Central Full Text
- [60]Prates DB, Santos LD, Miranda JC, Souza AP, Palma MS, Barral-Netto M, Barral A. Changes in amounts of total salivary gland proteins of Lutzomyia longipallpis (Diptera: Psychodidae) according to age and diet. J Med Entomol. 2008; 45(3):409-413.
- [61]Jacobson RL, Studentsky L, Schlein Y. Glycolytic and chitinolytic activities of Phlebotomus papatasi (Diptera: Psychodidae) from diverse ecological habitats. Folia Parasitol (Praha). 2007; 54(4):301-309.
- [62]Schlein Y, Jacobson RL. Mortality of Leishmania major in Phlebotomus papatasi caused by plant feeding of the sand flies. Am J Trop Med Hyg. 1994; 50(1):20-27.
- [63]Schlein Y, Jacobson RL. Photosynthesis modulates the plant feeding of Phlebotomus papatasi (Diptera: Psychodidae). J Med Entomol. 2000; 37(3):319-324.
- [64]Coutinho-Abreu IV, Wadsworth M, Stayback G, Ramalho-Ortigao M, McDowell MA: Differential expression of salivary gland-encoding genes in the female sand fly Phlebotomus papatasi. J Med Entomol. 2010, In print.
- [65]Berzofsky JA. Features of T-cell recognition and antigen structure useful in the design of vaccines to elicit T-cell immunity. Vaccine. 1988; 6(2):89-93.
- [66]Berzofsky JA, Cease KB, Cornette JL, Spouge JL, Margalit H, Berkower IJ, Good MF, Miller LH, DeLisi C. Protein antigenic structures recognized by T cells: potential applications to vaccine design. Immunol Review. 1987; 98:9-52.
- [67]Belkaid Y, Valenzuela JG, Kamhawi S, Rowton E, Sacks DL, Ribeiro JM. Delayed-type hypersensitivity to Phlebotomus papatasi sand fly bite: An adaptive response induced by the fly? Proc Natl Acad Sci U S A. 2000; 97(12):6704-6709.
- [68]Borbulevych OY, Insaidoo FK, Baxter T, Powell DJJ, Johnson LA, Restifo NP, Baker BM. Structures of MART-126/27-35 Peptide/HLA-A2 complexes reveal a remarkable disconnect between antigen structural homology and T cell recognition. J Mol Biol. 2007; 372(5):1123-1136.
- [69]Collin N, Gomes R, Teixeira C, Cheng L, Laughinghouse A, Ward J, Elnaiem D, Fischer L, Valenzuela J, Kamhawi S. Sand fly salivary proteins induce strong cellular immunity in a natural reservoir of visceral leishmaniasis with adverse consequences for Leishmania. PLoS Pathog. 2009; 5:e1000441.
- [70]Gomes R, Teixeira C, Teixeira M, Oliveira F, Menezes M, Silva C, de Oliveira C, Miranda J, Elnaiem D, Kamhawi S et al.. Immunity to a salivary protein of a sand fly vector protects against the fatal outcome of visceral leishmaniasis in a hamster model. Proc Natl Acad Sci U S A. 2008; 105:7845-7850.
- [71]Oliveira F, Lawyer P, Kamhawi S, Valenzuela J. Immunity to distinct sand fly salivary proteins primes the anti-Leishmania immune response towards protection or exacerbation of disease. PLoS Negl Trop Dis. 2008; 2:e226.
- [72]Yin H, Norris DE, Lanzaro GC. Sibling species in the Lutzomyia longipalpis complex differ in levels of mRNA expression for the salivary peptide, maxadilan. Insect Mol Biol. 2000; 9(3):309-314.
- [73]Clement M, Posada D, Crandall KA. TCS: a computer program to estimate gene genealogies. Molecular Ecology. 2000; 9(10):1657-1659.
- [74]Crandall KA, Templeton AR, Sing CF. Intraspecific phylogenetics: problems and solutions. In: Models in phylogeny reconstruction systematics association specias. Scotland RW, Siebert JD, Williams DM, editors. Claredon Press, Oxford; 1994: p.273-297.