Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-26T17:10:58.692Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of aliphatic, monocarboxylic, dicarboxylic, heterocyclic and sulphur-containing amino acids on Leishmania spp. chemotaxis

Published online by Cambridge University Press:  23 September 2015

E. DIAZ ,
A. K. ZACARIAS ,
S. PÉREZ ,
O. VANEGAS ,
L. KÖHIDAI ,
M. PADRÓN-NIEVES  and
A. PONTE-SUCRE
E. DIAZ
Affiliation:
Laboratory of Molecular Physiology, Institute of Experimental Medicine, School of Medicine Luis Razetti, Faculty of Medicine, Universidad Central de Venezuela, Caracas, Venezuela
A. K. ZACARIAS
Affiliation:
Laboratory of Molecular Physiology, Institute of Experimental Medicine, School of Medicine Luis Razetti, Faculty of Medicine, Universidad Central de Venezuela, Caracas, Venezuela
S. PÉREZ
Affiliation:
Laboratory of Molecular Physiology, Institute of Experimental Medicine, School of Medicine Luis Razetti, Faculty of Medicine, Universidad Central de Venezuela, Caracas, Venezuela
O. VANEGAS
Affiliation:
Laboratory of Molecular Physiology, Institute of Experimental Medicine, School of Medicine Luis Razetti, Faculty of Medicine, Universidad Central de Venezuela, Caracas, Venezuela
L. KÖHIDAI
Affiliation:
Department of Genetics, Cell and Immunobiology, Semmelweis University, Budapest, Hungary
M. PADRÓN-NIEVES
Affiliation:
Laboratory of Molecular Physiology, Institute of Experimental Medicine, School of Medicine Luis Razetti, Faculty of Medicine, Universidad Central de Venezuela, Caracas, Venezuela
A. PONTE-SUCRE*
Affiliation:
Laboratory of Molecular Physiology, Institute of Experimental Medicine, School of Medicine Luis Razetti, Faculty of Medicine, Universidad Central de Venezuela, Caracas, Venezuela
*
*Corresponding author. Laboratory of Molecular Physiology, Institute of Experimental Medicine, Faculty of Medicine, Universidad Central de Venezuela, Caracas, Venezuela. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In the sand-fly mid gut, Leishmania promastigotes are exposed to acute changes in nutrients, e.g. amino acids (AAs). These metabolites are the main energy sources for the parasite, crucial for its differentiation and motility. We analysed the migratory behaviour and morphological changes produced by aliphatic, monocarboxylic, dicarboxylic, heterocyclic and sulphur-containing AAs in Leishmania amazonensis and Leishmania braziliensis and demonstrated that L-methionine (10−12m), L-tryptophan (10−11m), L-glutamine and L-glutamic acid (10−6m), induced positive chemotactic responses, while L-alanine (10−7m), L-methionine (10−11 and 10−7m), L-tryptophan (10−11m), L-glutamine (10−12m) and L-glutamic acid (10−9m) induced negative chemotactic responses. L-proline and L-cysteine did not change the migratory potential of Leishmania. The flagellum length of L. braziliensis, but not of L. amazonensis, decreased when incubated in hyperosmotic conditions. However, chemo-repellent concentrations of L-alanine (Hypo-/hyper-osmotic conditions) and L-glutamic acid (hypo-osmotic conditions) decreased L. braziliensis flagellum length and L-methionine (10−11m, hypo-/hyper-osmotic conditions) decreased L. amazonensis flagellum length. This chemotactic responsiveness suggests that Leishmania discriminate between slight concentration differences of small and structurally closely related molecules and indicates that besides their metabolic effects, AAs play key roles linked to sensory mechanisms that might determine the parasite's behaviour.

Keywords

Amino acidschemotaxisflagellum lengthLeishmania braziliensisLeishmania amazonensisparasite's motilityosmotic stress
Type
Research Article
Information
Parasitology , Volume 142 , Issue 13 , November 2015 , pp. 1621 - 1630
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Atías, A. (1998). Parasitología Médica: Leishmaniasis, 2nd Edn. Publicaciones Técnicas Mediterráneo, Santiago de Chile.Google Scholar
Barros, V., Gontijo, N., Melo, M. and Oliveira, J. (2006). Leishmania amazonensis: chemotaxic and osmotaxic responses in promastigotes and their probable role in development in the phlebotomine gut. Experimental Parasitology 112, 152–157.Google Scholar
Bates, P. (2008). Leishmania sand fly interaction: progress and challenges. Current Opinion Microbiology 11, 340–344.Google Scholar
Bengs, F., Scholz, A., Kuhn, D. and Wiese, M. (2005). LmxMPK9, a mitogen-activated protein kinase homologue affects flagellar length in Leishmania mexicana . Molecular Microbiology 55, 1606–1615.Google Scholar
Blaineau, C., Tessier, M., Dubessay, P., Tasse, L., Crobu, L., Page's, M. and Bastien, P. (2007). A novel microtubule-depolymerizing Kinesin involved in length control of a Eukaryotic Flagellum. Current Biology 17, 778–782.Google Scholar
Botero, D. and Restrepo, M. (2003). Parasitosis humanas, 4th Edn. Corporación para Investigaciones Biológicas, Bogotá, Colombia.Google Scholar
Burrows, C. and Blum, J. (1991). Effect of hyper-osmotic stress on alanine content of Leishmania major promastigotes. Journal of Protozoology 38, 47–52.Google Scholar
Darling, T. and Blum, J. (1990). Changes in the shape of Leishmania major promastigotes in response to hexoses, proline, and hypo-osmotic stress. Journal of Protozoology 37, 267–272.Google Scholar
Diaz, E., Köhidai, L., Ponte-Sucre, A., Ríos, A. and Vanegas, O. (2011). Ensayos de quimiotaxis in vitro en Leishmania spp. Evaluación de la técnica de los capilares-dos cámaras en promastigotes. Revista de la Facultad de Farmacia-UCV 74, 31–39.Google Scholar
Diaz, E., Köhidai, L., Ríos, A., Vanegas, O., Silva, A., Szabó, R., Mezo, G., Hudecz, F. and Ponte-Sucre, A. (2013) Leishmania braziliensis: cytotoxic, cytostatic and chemotactic effects of poly-lysine-Methotrexate-conjugates. Experimental Parasitology 135, 134–141.Google Scholar
Dillon, R. J., Ivens, A. C., Churcher, C., Holroyd, N., Quail, M. A., Rogers, M. E., Soares, M. B., Bonaldo, M. F., Casavant, T. L., Lehane, M. J. and Bates, P. A. (2006). Analysis of ESTs from Lutzomyia longipalpis sand flies and their contribution toward understanding the insect-parasite relationship. Genomics 88, 831–840.Google Scholar
Dostálová, A. and Volf, P. (2012). Leishmania development in sand flies: parasite vector interactions overview. Parasites and Vectors 5, 276. Google Scholar
Erdmann, M., Scholz, A., Melzer, I., Schmetz, C. and Wiese, M.(2006). Interacting protein kinases involved in the regulation of Flagellar length. Molecular Biology of the Cell 17, 2035–2045.Google Scholar
Forestier, C., Machu, M., Loussert, C., Pascale, P. and Spath, F. (2011). Imaging host cell-Leishmania interaction dynamics implicates parasite motility, lysosome recruitment, and host cell wounding in the infection process. Cell Host and Microbe 9, 319–330.Google Scholar
Gadelha, C., Wickstead, B. and Gull, K. (2007). Flagellar and ciliary beating in trypanosomome motility. Cell Motility and the Cytoskeleton 64, 629–643.Google Scholar
Handman, E., Goding, J., Papenfuss, A. and Speed, T. (2008). Leishmania surface proteins. In Leishmania, after the Genome (ed. Fasel, N. and Myler, P.), pp. 177–204. Caister Academic Press, England.Google Scholar
Hart, D. T. and Coombs, G. H. (1982). Leishmania mexicana: energy metabolism of amastigotes and promastigotes. Experimental Parasitology 54, 397–409.Google Scholar
Inbar, E., Schlisselber, D., Suter Grotemeyer, M., Rentsch, D. and Zilberstein, D. (2013). A versatile proline/alanine transporter in the unicellular pathogen Leishmania donovani regulates amino acid homoeostasis and osmotic stress responses. Biochemical Journal 449, 555–566.Google Scholar
Jagušić, M., Forčić, D., Brgles, M., Kutle, L., Šantak, M., Jergović, M., Kotarski, L., Bendelja, K. and Halassy, B. (2015). Stability of minimum essential medium functionality despite L-glutamine decomposition. Cytotechnology [Epub ahead of print] doi:10.1007/s10616-015-9875-8.Google Scholar
Köhidai, L. and Csaba, G. (2003). Chemotactic range fitting of amino acids and its correlations to physicochemical parameters in Tetrahymena pyriformis evolutionary consequences. Cellular and Molecular Biology 49, 487–495.Google Scholar
Köhidai, L., Csaba, G. and Lemberkovics, E. (1995). Molecule dependent chemotactic responses of Tetrahymena pyriformis elicited by volatile oils. Acta Protozoologica 34, 181–185.Google Scholar
Köhidai, L., Bösze, S., Hudecz, F., Illyés, E., Lang, O., Mák, M., Sebestyen, F. and Sóos, P. (2003). Chemotactic activity of oligopeptides containing and EWS motif on Tetrahymena pyriformis: the effect of amidation of the C-terminal residue. Cell Biochemistry Function 21, 113–120.Google Scholar
LeFurgey, A., Blum, J. and Ingram, P. (2000). Compartmental responses to acute osmotic stress in Leishmania major result in rapid loss of Na+ and Cl− . Comparative Biochemistry and Physiology. Part A: Molecular & Integrative Physiology 128, 385–393.Google Scholar
Leslie, G., Barret, M. and Burchmore, R. (2002). Leishmania mexicana: promastigotes migrate through osmotic gradients. Experimental Parasitology 102, 117–120.Google Scholar
Motulsky, H. (1995). Intuitive Biostatistics. Oxford University Press, New York, USA.Google Scholar
Opperdoes, F. and Michels, P. (2008). The metabolic repertoire of Leishmania and implication for drug discovery. In Leishmania, after the Genome (ed. Fasel, N. and Myler, P.), pp. 123–158. Caister Academic Press, England.Google Scholar
Paes, L., Daliry, A., Floeter-Winter, L., Galvez, R. and Ramírez, M. (2008). Active transport of Glutamate in Leishmania amazonensis . Journal of Eukaryotic Microbiology 55, 382–387.Google Scholar
Pajouhesh, H. and Lenz, G. (2005) Medicinal chemical properties of successful central nervous system drugs. Neurotherapeutics 2, 541–553.Google Scholar
Peters, E., Ansel, J., Ericson, M., Hordinsky, M., Hosoi, J., Paus, R., Scholzen, T. and Seiffert, K. (2006). Neuropeptide control mechanisms in cutaneous biology; physiological and clinical significance. Journal of Investigative Dermatology 126, 1937–1947.Google Scholar
Pozzo, L. Y., Fontes, A., de Thomaz, A. A., Santos, B. S., Farias, P. M., Ayres, D. C., Giorgio, S. and Cesar, C. L. (2009) Studying taxis in real time using optical tweezers: applications for Leishmania amazonensis parasites. Micron 40, 617–620.Google Scholar
Rotureau, B., Bastin, P., Morales, M. and Spath, G. (2009). The flagellum mitogen activated protein kinase connection in Trypanosomatids: a key sensory role in parasite signaling and development. Cell Microbiology 11, 710–718.Google Scholar
Santos, V. C., Araujo, R. N., Machado, L. A., Pereira, M. H. and Gontijo, N. F. (2008). The physiology of the midgut of Lutzomyia longipalpis (Lutz and Neiva 1912): pH in different physiological conditions and mechanisms involved in its control. Journal of Experimental Biology 211 (Pt 17), 2792–2798.Google Scholar
Santos, V. C., Nunes, C. A., Pereira, M. H. and Gontijo, N. F. (2011). Mechanisms of pH control in the midgut of Lutzomyia longipalpis: roles for ingested molecules and hormones. Journal of Experimental Biology 214 (Pt 9), 1411–1418.Google Scholar
Santos, V. C., Vale, V. F., Silva, S. M., Nascimento, A. A., Saab, N. A., Soares, R. P., Michalick, M. S., Araujo, R. N., Pereira, M. H., Fujiwara, R. T. and Gontijo, N. F. (2014). Host modulation by a parasite: how Leishmania infantum modifies the intestinal environment of Lutzomyia longipalpis to favor its development. PLoS ONE 9, e111241. eCollection 2014.Google Scholar
Szemes, Á., Lajkó, E., Láng, O. and Kőhidai, L. (2015). Chemotactic effect of mono and disaccharides on the unicellular Tetrahymena pyriformis . Carbohydrate Research 407, 158–165.Google Scholar
Vieira, L., Lafuente, E., Gamarro, F. and Cabantchik, Z. (1996). An amino acid channel activated by hypotonically induced swelling of Leishmania major promastigotes. The Biochemical Journal 319, 691–697.Google Scholar
Voet, D., Voet, J. and Pratt, C. (2007). Fundamentos de Bioquímica, Aminoácidos, 2nd edición. Editorial Médica Panamericana, Argentina.Google Scholar