A Lectin from Dioclea violacea Interacts with Midgut Surface of Lutzomyia migonei, Unlike Its Homologues, Cratylia floribunda Lectin and Canavalia gladiata Lectin

Monteiro Tínel, Juliana Montezuma Barbosa; Benevides, Melina Fechine Costa; Frutuoso, Mércia Sindeaux; Rocha, Camila Farias; Arruda, Francisco Vassiliepe Sousa; Vasconcelos, Mayron Alves; Pereira-Junior, Francisco Nascimento; Cajazeiras, João Batista; do Nascimento, Kyria Santiago; Martins, Jorge Luiz; Teixeira, Edson Holanda; Cavada, Benildo Sousa; dos Santos, Ricardo Pires; Lima Pompeu, Margarida Maria

doi:https://doi.org/10.1155/2014/239208

The Scientific World Journal

On this page

Abstract Introduction Materials and Methods Results and Discussion Conclusions Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2014 | Article ID 239208 | https://doi.org/10.1155/2014/239208

A Lectin from Dioclea violacea Interacts with Midgut Surface of Lutzomyia migonei, Unlike Its Homologues, Cratylia floribunda Lectin and Canavalia gladiata Lectin

Juliana Montezuma Barbosa Monteiro Tínel,¹Melina Fechine Costa Benevides,¹Mércia Sindeaux Frutuoso,¹Camila Farias Rocha,¹Francisco Vassiliepe Sousa Arruda,²Mayron Alves Vasconcelos,²Francisco Nascimento Pereira-Junior,³João Batista Cajazeiras,³Kyria Santiago do Nascimento,³Jorge Luiz Martins,⁴Edson Holanda Teixeira,²and Benildo Sousa Cavada³ et al.

Academic Editor: Alberto A. Iglesias

Received30 May 2014

Accepted02 Oct 2014

Published05 Nov 2014

Abstract

Leishmaniasis is a vector-borne disease transmitted by phlebotomine sand fly. Susceptibility and refractoriness to Leishmania depend on the outcome of multiple interactions that take place within the sand fly gut. Promastigote attachment to sand fly midgut epithelium is essential to avoid being excreted together with the digested blood meal. Promastigote and gut sand fly surface glycans are important ligands in this attachment. The purpose of the present study was to evaluate the interaction of three lectins isolated from leguminous seeds (Diocleinae subtribe), D-glucose and D-mannose-binding, with glycans on Lutzomyia migonei midgut. To study this interaction the lectins were labeled with FITC and a fluorescence assay was performed. The results showed that only Dioclea violacea lectin (DVL) was able to interact with midgut glycans, unlike Cratylia floribunda lectin (CFL) and Canavalia gladiata lectin (CGL). Furthermore, when DVL was blocked with D-mannose the interaction was inhibited. Differences of spatial arrangement of residues and volume of carbohydrate recognition domain (CRD) may be the cause of the fine specificity of DVL for glycans in the surface on Lu. migonei midgut. The findings in this study showed the presence of glycans in the midgut with glucose/mannose residues in its composition and these residues may be important in interaction between Lu. migonei midgut and Leishmania.

1. Introduction

Cutaneous leishmaniasis is endemic in the tropics and neotropics. This pathology is often referred to as a group of diseases because of the varied spectrum of clinical manifestations, which range from small cutaneous nodules to gross mucosal tissue destruction [1]. Cutaneous leishmaniasis can be caused by several Leishmania spp. and is transmitted to human beings and animals by sand flies [2].

Lutzomyia migonei is one of the sand flies that transmit the American cutaneous leishmaniasis [3]. Since several sand flies are specific or even permissive to development of different Leishmania parasites, Lu. migonei can also be considered as a possible vector for American visceral leishmaniasis [4, 5]. According to Rangel and Lainson [6], this specie is widely distributed in South America, being found from Argentina to Colombia and living in a variety of habitats.

When the parasites are taken up with the blood meal, they undergo a period of replication and development in the midgut. Then, these parasites differentiate to an infective metacyclic stage, which is adapted for transmission to mammals [7]. The procyclic promastigotes are surrounded by the peritrophic matrix [8], which is constituted by a mixture of chitin, proteins, glycoproteins, and proteoglycans [9]. The next step for the vector infection is the insertion of parasites flagella into midgut microvilli [10]. The interaction between parasite and the vector midgut cells is controlled by species-specific modifications of the major surface glycoconjugate of promastigotes, lipophosphoglycan (LPG), which selectively binds to the midgut galectin receptor [7, 11, 12]. Nevertheless, previous works reported the presence of glycans in the midgut that serve as binding sites for lectins on Leishmania surface [13, 14].

Lectins are a group of widely distributed and structurally heterogeneous (glycol-) proteins that contain at least one noncatalytic domain, which selectively recognizes and reversibly binds to specific carbohydrates or glycoconjugates (glycoproteins and glycolipids) without altering the structure of the ligand [15].

Among plant lectins, those isolated from Diocleinae subtribe are well studied. These lectins have many chemical and physicochemical properties in common, such as the specificity for D-glucose/D-mannose residues [16]. Minor differences in the ratios of dimeric and tetrameric forms of the lectins, together with differences in the relative orientations of the carbohydrate-binding sites in the quaternary structures, have been hypothesized to contribute to the differences in biological activities exhibited by Diocleinae lectins [17]. These interesting properties make these lectins valuable biotechnological tools. Furthermore, Diocleinae lectins provide an excellent system to study the effects of minor changes in the protein structure on their functional properties in biological models [18].

Thus, in the present study three lectins isolated from the seeds of Cratylia floribunda (CFL), Canavalia gladiata (CGL), and Dioclea violacea (DVL) were labeled with fluorescein isothiocyanate (FITC) and evaluated concerning their ability to recognize glycans on Lu. migonei midgut.

2. Materials and Methods

2.1. Lectins Purification

Lectins from Cratylia floribunda (CFL), Dioclea violacea (DVL), and Canavalia gladiata (CGL) were purified as previously reported [19–21]. Briefly, the lectins were extracted from air-dried ground seeds collected in Fortaleza-CE, Brazil, and defatted with n-hexane. The protein extract was obtained by continuous stirring with 0.9% NaCl (1 : 10 w/v) at 20°C for 4 h, followed by centrifugation at 10.000 g for 20 min at 4°C. The supernatant was submitted to affinity chromatography on a Sephadex G-50 column (5 × 25 mm), equilibrated with 0.9% NaCl containing 5 M CaCl₂ and 5 M MnCl₂. Then, the column was washed using the same buffer at a flow rate of 45 mL/h. The bound lectin was eluted with 0.1 M glycine, pH 2.6; dialyzed extensively against distilled water; and lyophilized. The purity of each lectin was monitored by SDS-PAGE, as described by Laemmli [22].

2.2. FITC-Labeled Lectins

FITC-labeled CFL, DVL, and CGL were prepared in inhibition buffer (0.1 M D-mannose in M carbonate-bicarbonate buffer, pH 9.0), conjugation buffer (0.1 M carbonate-bicarbonate buffer, pH 9.0), and washing buffer (phosphate-buffered saline: 0.01 M sodium phosphate buffer, 0.027 M KCl, and 0.15 M NaCl, pH 7.4). Initially, the lectins were dissolved in inhibition buffer and incubated at 37°C for 1 h. Then, 250 μL fluorescein isothiocyanate (FITC) (500 μg/mL in conjugation buffer) was added dropwise. The solution was incubated for 2 h at room temperature under gentle stirring. Subsequently, unconjugated FITC was separated from FITC-lectin by size exclusion chromatography using a Sephadex G-25 column previously equilibrated and eluted with washing buffer. The absorbance of all fractions was determined at 280 nm (protein) and 495 nm (FITC) to verify the chromatographic efficiency. FITC-labeled lectins were then dialyzed against 0.1 M acetic acid for 1 h to remove the inhibitor carbohydrate and were extensively dialyzed against distilled water.

2.3. FITC-Labeled Lectins Blocked with D-Mannose

The same FITC-labeled lectins were blocked with D-mannose. Briefly, the FITC-lectins were incubated with 0.1 M D-mannose at 37°C for 30 min to block the CRD. The solutions were then filtered through a 0.22 μm cellulose filter and stored for later use.

2.4. Sand Fly Capture, Culture Maintenance, and Midgut Dissection

The sand flies were collected in Baturité, a city located in the northern region of Ceará state, Brazil, which is endemic for cutaneous leishmaniasis. A colony of Lu. migonei was reared and maintained in the lab as described by Modi and Tesh [23]. Adult flies were maintained at 23°C and 95% relative humidity and had free access to a 10% sucrose solution on a cotton pad. Three-day-old females were fed once a week with a blood meal from an anaesthetized hamster. Experiments were performed with 3–10-day-old females that had not taken a blood meal. Sand flies (5-6 per group) were quickly immobilized at −20°C and individually dissected in drops of 0.1 M PBS, pH 7.4, under a stereoscopic microscope.

2.5. Midgut-Binding Assays

Midguts were transferred to cold PBS and fixed in a 4% paraformaldehyde/PBS solution at 4°C for 1 hour. The abdominal segments of the fixed midguts were opened using a fine needle. The midguts were then transferred to wells of fluorescence slides and washed 3 times with 5% BSA in PBS for 5 min. Then, they were separately incubated with blocked and unblocked FITC-lectins (100 µg/mL) and maintained at 37°C for 40 min in a dark humid chamber. The negative control was performed with 5% BSA in PBS containing 0.5% of FITC. The midguts were then washed 3 times with PBS and transferred to fluorescence slides and observed in a fluorescence microscope.

2.6. Fluorescence Microscopy

Fluorescence images of midguts were obtained using a Nikon Eclipse 80i microscope, fitted with a 100 W mercury lamp, and a fluorescein dichroic cube filter (excitation 490 nm and emission 520 nm). Each image was taken using an objective of ×4 and ocular of ×10 (magnification of ×40). An Evolution MP 5.0 cooled camera (Media Cybernetics, Silver Spring, MD, USA) was used to acquire the images at 7.5 s of exposition. The negative control was used for the subtraction of effects of natural fluorescence of midguts and residual fluorescence of FITC. The same images were acquired in bright field for comparison with fluorescence images. The images were saved in tagged image file format (TIFF).

2.7. Fluorescence Intensity

Ten midguts treated with each lectin (blocked and unblocked) were evaluated to determine the mean fluorescence intensity. Fluorescence intensity was quantified through the arithmetic mean of the distribution of gray values within a given midgut image area, which was determined according to the following formula: where is the gray value (0–255) of the pixel of coordinates and is the number of pixels within a given midgut area. With TIFF images, the gray value is calculated by converting each pixel to gray scale using the formula [24]: where , , and are red, green, and blue values (0–255) of the pixel of coordinates. ImageJ 1.32J software was used for fluorescence intensity calculation [25].

2.8. Statistical Analysis

Statistical data analysis was based on the descriptive statistic-mean value; standard deviation ; margin of error ; the Shapiro-Wilk test, to determine whether or not a random sample of values follows a normal distribution; and hypothesis test, to determine the significance of differences between groups. The margin of error is the maximum likely difference between the observed sample mean and the true value of the population mean. When the population mean is unknown, is determined according to following formula: where is the significance level, is the number of samples, and is Student’s -distribution parameter. The significance level used was 0.05. The software Statistica 10 (Statsoft Inc. 2011) was used in all statistical analysis.

3. Results and Discussion

In the present study three different lectins (CFL, CGL, and DVL), isolated from seeds of leguminous, were stained with FITC and evaluated regarding their ability to interact with glycans disposed on the surface of midgut cells of Lu. migonei.

The midguts were disposed in fluorescent slides and observed in bright field microscopy for the comparison with fluorescence images. The bright field images are showed in Figures 1(a), 2(a), 2(c), 3(a), 3(c), 4(a), and 4(c). Regarding the control samples (midguts without treatment with lectins), the images showed weak intrinsic fluorescence (Figure 1(b)).

(a)

(b)

(a)

(b)

(c)

(d)

(a)

(b)

(c)

(d)

(a)

(b)

(c)

(d)

Similar fluorescence intensity was achieved when the midguts were treated with CFL and CGL without D-mannose (Figures 2(b) and 3(b), resp.). Interestingly, unlike CFL and CGL, in the treatment with DVL a strong fluorescence was observed (Figure 4(b)). In order to verify if the lectins interact with midgut cells through the CRD, all lectins were blocked with D-mannose and new images were acquired. No differences were observed in the fluorescence pattern of blocked and unblocked CFL and CGL (Figures 2(d) and 3(d), resp.). On the other hand, when the midguts were treated with blocked DVL, a remarkable decrease in the fluorescence pattern was achieved (Figure 4(d)).

Moreover, data from mean fluorescence intensity of midguts were collected for control, blocked, and unblocked lectins. The mean fluorescence intensity (arbitrary units (AU)) of the control was 7.62 ± 1.29. Concerning FITC-lectins, CFL, CGL and DVL, showed, respectively, 8.17 ± 0.94, 8.50 ± 0.69, and 51.95 ± 5.76. The fluorescence intensities exhibited by the same lectins blocked with D-mannose were 8.20 ± 0.85, 8.43 ± 1.35, and 34.618 ± 2.42 (Figure 5).

A statistical analysis using Shapiro-Wilk test resulted in normal distributions for all experimental groups. Moreover, the ANOVA test (with Tukey post hoc) was used to verify significant statistical differences among the means. In this analysis, it was observed that blocked and unblocked DVL showed significant statistical differences when compared to the control. In addition, statistically significant differences were achieved among themselves (Figure 5).

Plant lectins have been used as biotechnological tools in different areas. These areas include cancer detection [26], effects on bacterial and yeasts growth as well as their biofilms [27, 28], anti-inflammatory and antinociceptive effect [29], anti-HIV action [30], antidepressant-like effect on nervous cells [31], larvicidal activity of Aedes aegypti [32], antineoplastic agents [33], prohealing effect [34], immunization against Leishmania infection [35], carbohydrate identification on Leishmania promastigotes [36], among others.

Since the interaction between lectins and carbohydrates is very specific, they can be used as tools to identify carbohydrates on the cell surface and thus decipher the glycocode of cell receptors. Therefore, in the present work three different lectins were assayed concerning their ability to identify glucose/mannose motifs on glycans from the epithelial surface of Lu. migonei midgut.

The recognition of host epithelia surfaces is an important step for infection by pathogens [37]. In many cases, proteins such as lectins are the mediators of adhesion events [7, 11, 12]. Despite the importance in elucidating the glycans that participate with the interaction between pathogen and vector midgut epitelia, only few studies describe the vector glycans that are involved in the interaction with adhesins of pathogens. On the other hand, many studies are focused on the role of LPG as the major adhesin responsible for midgut binding in all Leishmania species [38, 39]. Myskova and colleagues [14] using Helix pomatia lectin and Concanavalin A to detect glycoproteins in midgut lysates suggested a new modality of interaction between vector midgut and Leishmania pathogen.

According to the present study, only DVL interacted with glycans (glycoproteins or glycolipids) disposed on the midgut epithelial cell surface, suggesting the presence of glucose/mannose residues. Probably, glucose/mannose residues are important for the occurrence of the interaction between the vector and pathogen.

The lectins used in this study were isolated from members of Diocleinae subtribe and share a high degree of structural similarity between them [16]. However, only DVL was able to interact with midgut glycans of Lu. migonei, suggesting that minor changes in the structure of CRD are responsible for the basis of interaction between lectin and ligand. These changes include differences in the distance exhibited by specific amino acid residues that compose the primary CRD or/and alterations on the volume of this site [18].

4. Conclusions

In summary, both CFL and CGL were not able to interact with Lu. migonei midgut glycans. On the other hand, DVL established interactions with glycans as evidenced by fluorescence images. The interaction was inhibited when the lectin was blocked with D-mannose, suggesting the presence of terminal mannose residues on high mannose-, hybrids-, and complex-type of N-linked glycans on Lu. migonei midgut surface. Therefore, the present study corroborates with the literature about the composition of glycans involved in the interaction between Leishmania parasites and vectors. Future studies should propose the role of DVL as a biotechnological tool to inhibit specific interactions between Leishmania and digestive tract of the sand fly.

Conflict of Interests

All the authors contributed to and approved this paper and there is no conflict of interests to declare regarding this paper.

Acknowledgments

The present study was supported by Grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP).

References

R. Reithinger, J.-C. Dujardin, H. Louzir, C. Pirmez, B. Alexander, and S. Brooker, “Cutaneous leishmaniasis,” The Lancet Infectious Diseases, vol. 7, no. 9, pp. 581–596, 2007.
View at: Publisher Site | Google Scholar
M. Yaghoobi-Ershadi, “Phlebotomine sand flies (Diptera: Psychodidae) in Iran and their role on Leishmania transmission,” Journal of Arthropod-Borne Diseases, vol. 6, no. 1, pp. 1–17, 2012.
View at: Google Scholar
F. M. Vigoder, N. A. Souza, and A. A. Peixoto, “Copulatory courtship song in Lutzomyia migonei (Diptera: Psychodidae),” Memorias do Instituto Oswaldo Cruz, vol. 105, no. 8, pp. 1065–1067, 2010.
View at: Publisher Site | Google Scholar
O. D. Salomón, M. G. Quintana, G. Bezzi, M. L. Morán, E. Betbeder, and D. V. Valdéz, “Lutzomyia migonei as putative vector of visceral leishmaniasis in La Banda, Argentina,” Acta Tropica, vol. 113, no. 1, pp. 84–87, 2010.
View at: Publisher Site | Google Scholar
A. Svárovská, T. H. Ant, V. Seblová, L. Jecná, S. M. Beverley, and P. Volf, “Leishmania major glycosylation mutants require phosphoglycans $({l p g 2}^{-})$ but not lipophosphoglycan $({l p g 1}^{-})$ for survival in permissive sand fly vectors,” PLoS Neglected Tropical Diseases, vol. 4, no. 1, article 580, 2010.
View at: Publisher Site | Google Scholar
E. F. Rangel and R. Lainson, “Proven and putative vectors of American cutaneous leishmaniasis in Brazil: aspects of their biology and vectorial competence,” Memorias do Instituto Oswaldo Cruz, vol. 104, no. 7, pp. 937–954, 2009.
View at: Publisher Site | Google Scholar
S. Kamhawi, “Phlebotomine sand flies and Leishmania parasites: friends or foes?” Trends in Parasitology, vol. 22, no. 9, pp. 439–445, 2006.
View at: Publisher Site | Google Scholar
D. L. Sacks, G. Modi, E. Rowton et al., “The role of phosphoglycans in Leishmania-sand fly interactions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 1, pp. 406–411, 2000.
View at: Publisher Site | Google Scholar
M. J. Lehane, “Peritrophic matrix structure and function,” Annual Review of Entomology, vol. 42, pp. 525–550, 1997.
View at: Publisher Site | Google Scholar
A. Warburg, R. B. Tesh, and D. McMahon-Pratt, “Studies on the attachment of Leishmania flagella to sand fly midgut epithelium,” Journal of Protozoology, vol. 36, no. 6, pp. 613–617, 1989.
View at: Publisher Site | Google Scholar
S. Kamhawi, M. Ramalho-Ortigao, S. Kumar et al., “A role for insect galectins in parasite survival,” Cell, vol. 119, no. 3, pp. 329–341, 2004.
View at: Publisher Site | Google Scholar
P. F. Pimenta, S. J. Turco, M. J. McConville, P. G. Lawyer, P. V. Perkins, and D. L. Sacks, “Stage-specific adhesion of Leishmania promastigotes to the sandfly midgut,” Science, vol. 256, no. 5065, pp. 1812–1815, 1992.
View at: Publisher Site | Google Scholar
L. G. Evangelista and A. C. R. Leite, “Histochemical localization of N-acetyl-galactosamine in the midgut of Lutzomyia longipalpis (Diptera: Psychodidae),” Journal of Medical Entomology, vol. 39, no. 3, pp. 432–439, 2002.
View at: Publisher Site | Google Scholar
J. Myskova, M. Svobodova, S. M. Beverley, and P. Volf, “A lipophosphoglycan-independent development of Leishmania in permissive sand flies,” Microbes and Infection, vol. 9, no. 3, pp. 317–324, 2007.
View at: Publisher Site | Google Scholar
E. J. M. van Damme, W. J. Peumans, A. Barre, and P. Rougé, “Plant lectins: a composite of several distinct families of structurally and evolutionary related proteins with diverse biological roles,” Critical Reviews in Plant Sciences, vol. 17, no. 6, pp. 575–692, 1998.
View at: Publisher Site | Google Scholar
B. S. Cavada, T. Barbosa, S. Arruda, T. B. Grangeiro, and M. Barral-Netto, “Revisiting proteus: do minor changes in lectin structure matter in biological activity? Lessons from and potential biotechnological uses of the diocleinae subtribe lectins,” Current Protein & Peptide Science, vol. 2, no. 2, pp. 123–135, 2001.
View at: Publisher Site | Google Scholar
J. L. A. Correia, A. S. F. Do Nascimento, J. B. Cajazeiras et al., “Molecular characterization and tandem mass spectrometry of the lectin extracted from the seeds of Dioclea sclerocarpa ducke,” Molecules, vol. 16, no. 11, pp. 9077–9089, 2011.
View at: Publisher Site | Google Scholar
E. H. S. Bezerra, B. A. M. Rocha, C. S. Nagano et al., “Structural analysis of ConBr reveals molecular correlation between the carbohydrate recognition domain and endothelial NO synthase activation,” Biochemical and Biophysical Research Communications, vol. 408, no. 4, pp. 566–570, 2011.
View at: Publisher Site | Google Scholar
J. T. A. Oliveira, B. S. Cavada, and R. A. Moreira, “Isolation and partial characterization of a lectin from Cratylia floribunda Mart. Seeds,” Brazilian Journal of Botany, vol. 14, pp. 63–68, 1991.
View at: Google Scholar
R. A. Moreira, E. F. Cordeiro, M. V. Ramos et al., “Isolation and partial characterization of a lectin from seeds of Dioclea violacea,” Revista Brasileira de Fisiologia Vegetal, vol. 8, no. 1, pp. 23–29, 1996.
View at: Google Scholar
F. B. M. B. Moreno, P. Delatorre, B. T. Freitas et al., “Crystallization and preliminary X-ray diffraction analysis of the lectin from Canavalia gladiata seeds,” Acta Crystallographica D: Biological Crystallography, vol. 60, no. 8, pp. 1493–1495, 2004.
View at: Publisher Site | Google Scholar
U. K. Laemmli, “Cleavage of structural proteins during the assembly of the head of bacteriophage T4,” Nature, vol. 227, no. 5259, pp. 680–685, 1970.
View at: Publisher Site | Google Scholar
G. B. Modi and R. B. Tesh, “A simple technique for mass rearing Lutzomyia longipalpis and Phlebotomus papatasi (Diptera: Psychodidae) in the laboratory,” Journal of Medical Entomology, vol. 20, no. 5, pp. 568–569, 1983.
View at: Google Scholar
R. C. Gonzalez and P. A. Wintz, Digital Image Processing, Addison-Wesley, Reading, Mass, USA, 2nd edition, 1987.
C. A. Schneider, W. S. Rasband, and K. W. Eliceiri, “NIH Image to ImageJ: 25 years of image analysis,” Nature Methods, vol. 9, no. 7, pp. 671–675, 2012.
View at: Publisher Site | Google Scholar
Y. H. Ahn, P. M. Shin, N. R. Oh, G. W. Park, H. Kim, and J. S. Yoo, “A lectin-coupled, targeted proteomic mass spectrometry (MRM MS) platform for identification of multiple liver cancer biomarkers in human plasma,” Journal of Proteomics, vol. 75, no. 17, pp. 5507–5515, 2012.
View at: Publisher Site | Google Scholar
G. B. Klafke, G. M. S. G. Moreira, L. G. Monte et al., “Assessment of plant lectin antifungal potential against yeasts of major importance in medical mycology,” Mycopathologia, vol. 175, no. 1-2, pp. 147–151, 2013.
View at: Publisher Site | Google Scholar
M. A. Vasconcelos, F. V. S. Arruda, V. A. Carneiro et al., “Effect of algae and plant lectins on planktonic growth and biofilm formation in clinically relevant bacteria and yeasts,” BioMed Research International, vol. 2014, Article ID 365272, 9 pages, 2014.
View at: Publisher Site | Google Scholar
J. F. M. Leite, A. M. S. Assreuy, M. R. L. Mota et al., “Antinociceptive and anti-inflammatory effects of a lectin-like substance from Clitoria fairchildiana R. Howard seeds,” Molecules, vol. 17, no. 3, pp. 3277–3290, 2012.
View at: Publisher Site | Google Scholar
M. D. Swanson, H. C. Winter, I. J. Goldstein, and D. M. Markovitz, “A lectin isolated from bananas is a potent inhibitor of HIV replication,” The Journal of Biological Chemistry, vol. 285, no. 12, pp. 8646–8655, 2010.
View at: Publisher Site | Google Scholar
S. C. Barauna, M. P. Kaster, B. T. Heckert et al., “Antidepressant-like effect of lectin from Canavalia brasiliensis (ConBr) administered centrally in mice,” Pharmacology Biochemistry and Behavior, vol. 85, no. 1, pp. 160–169, 2006.
View at: Publisher Site | Google Scholar
R. A. Sá, N. D. D. L. Santos, C. S. B. D. Silva et al., “Larvicidal activity of lectins from Myracrodruon urundeuva on Aedes aegypti,” Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, vol. 149, no. 3, pp. 300–306, 2009.
View at: Publisher Site | Google Scholar
J. Chen, B. Liu, N. Ji et al., “A novel sialic acid-specific lectin from Phaseolus coccineus seeds with potent antineoplastic and antifungal activities,” Phytomedicine, vol. 16, no. 4, pp. 352–360, 2009.
View at: Publisher Site | Google Scholar
L. G. do Nascimento Neto, L. da Silva Pinto, R. M. Bastos et al., “Effect of the lectin of Bauhinia variegata and its recombinant isoform on surgically induced skin wounds in a murine model,” Molecules, vol. 16, no. 11, pp. 9298–9315, 2011.
View at: Publisher Site | Google Scholar
C. R. Teixeira, K. A. Cavassani, R. B. Gomes et al., “Potential of KM lectin in immunization against Leishmania amazonensis infection,” Vaccine, vol. 24, no. 15, pp. 3001–3008, 2006.
View at: Publisher Site | Google Scholar
A. F. B. Andrade and E. M. B. Saraiva, “Lectin-binding properties of different Leishmania species,” Parasitology Research, vol. 85, no. 7, pp. 576–581, 1999.
View at: Publisher Site | Google Scholar
A. Imberty and A. Varrot, “Microbial recognition of human cell surface glycoconjugates,” Current Opinion in Structural Biology, vol. 18, no. 5, pp. 567–576, 2008.
View at: Publisher Site | Google Scholar
P. F. P. Pimenta, E. M. B. Saraiva, E. Rowton et al., “Evidence that the vectorial competence of phlebotomine sand flies for different species of Leishmania is controlled by structural polymorphisms in the surface lipophosphoglycan,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 19, pp. 9155–9159, 1994.
View at: Publisher Site | Google Scholar
S. Kamhawi, G. B. Modi, P. F. P. Pimenta, E. Rowton, and D. L. Sacks, “The vectorial competence of Phlebotomus sergenti is specific for Leishmania tropica and is controlled by species-specific, lipophosphoglycan-mediated midgut attachment,” Parasitology, vol. 121, no. 1, pp. 25–33, 2000.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2014 Juliana Montezuma Barbosa Monteiro Tínel et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies

Views

1389

Downloads

943

Citations