Hostname: page-component-76fb5796d-25wd4 Total loading time: 0 Render date: 2024-04-27T02:16:38.264Z Has data issue: false hasContentIssue false

Proline modulates the effect of bisphosphonate on calcium levels and adenosine triphosphate production in cell lines derived from bovine Echinococcus granulosus protoscoleces

Published online by Cambridge University Press:  07 June 2013

A.G. Fuchs*
Affiliation:
Centro de Altos Estudios en Ciencias Humanas y de la Salud (CAECIHS), Universidad Abierta Interamericana (UAI), Avenida Montes de Oca 745, (C127OAAH), Buenos Aires, Argentina
C.I. Echeverría
Affiliation:
Centro de Altos Estudios en Ciencias Humanas y de la Salud (CAECIHS), Universidad Abierta Interamericana (UAI), Avenida Montes de Oca 745, (C127OAAH), Buenos Aires, Argentina
F.G. Pérez Rojo
Affiliation:
Centro de Altos Estudios en Ciencias Humanas y de la Salud (CAECIHS), Universidad Abierta Interamericana (UAI), Avenida Montes de Oca 745, (C127OAAH), Buenos Aires, Argentina
E.A. Prieto González
Affiliation:
Centro de Altos Estudios en Ciencias Humanas y de la Salud (CAECIHS), Universidad Abierta Interamericana (UAI), Avenida Montes de Oca 745, (C127OAAH), Buenos Aires, Argentina
E.J.A. Roldán
Affiliation:
Centro de Altos Estudios en Ciencias Humanas y de la Salud (CAECIHS), Universidad Abierta Interamericana (UAI), Avenida Montes de Oca 745, (C127OAAH), Buenos Aires, Argentina
*
*Fax: (54) 11 4301 5240 extension 2 E-mail: Alicia.Fuchs@uai.edu.ar

Abstract

Bisphosphonates have been proposed as pharmacological agents against parasite and cancer cell growth. The effect of these compounds on helminthic cell viability and acellular compartment morphology, however, has not yet been studied. The effects of different types of bisphosphonates, namely etidronate (EHDP), pamidronate (APD), alendronate (ABP), ibandronate (IB) and olpadronate (OPD), and their interaction with amiloride, 1,25-dihydroxycholecalciferol (D3) and proline were evaluated on a cell line derived from bovine Echinococcus granulousus protoscoleces (EGPE) that forms cystic colonies in agarose. The EGPE cell line allowed testing the effect of bisphosphonates alone and in association with other compounds that could modulate calcium apposition/deposition, and were useful in measuring the impact of these compounds on cell growth, cystic colony formation and calcium storage. Decreased cell growth and cystic colony formation were found with EHDP, IB and OPD, and increased calcium storage with EHDP only. Calcium storage in EGPE cells appeared to be sensitive to the effect of amiloride, D3 and proline. Proline decreased calcium storage and increased colony formation. Changes in calcium storage may be associated with degenerative changes of the cysts, as shown in the in vitro colony model and linked to an adenosine triphosphate (ATP) decrease. In conclusion, bisphosphonates could be suitable tempering drugs to treat cestode infections.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2013 

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

Cabezón, C., Cabrera, G., Paredes, R., Ferreira, A. & Galanti, N. (2008) Echinococcus granulosus calreticulin: molecular characterization and hydatid cyst localization. Molecular Immunology 45, 14311438.Google Scholar
Casaravilla, C., Brearley, C., Soulé, S., Fontana, C., Veiga, N., Bessio, M.I., Ferreira, F., Kremer, C. & Díaz, A. (2006) Characterization of myo-inositol hexakisphosphate deposits from larval Echinococcus granulosus. The FEBS Journal 273, 31923203.Google Scholar
Chowdhury, N. & Singh, R. (1993) Distribution of some elements in hydatid cysts of Echinococcus granulosus from buffalo (Bubalus bubalis). Journal of Helminthology 67, 112114.Google Scholar
Cukrowski, I., Popović, L., Barnard, W., Paul, S.O., van Rooyen, P.H. & Liles, D.C. (2007) Modeling and spectroscopic studies of bisphosphonate–bone interactions. The Raman, NMR and crystallographic investigations of Ca-HEDP complexes. Bone 41, 668678.Google Scholar
Cumino, A.C., Elisondo, M.C. & Denegri, G.M. (2009) Flubendazole interferes with a wide spectrum of cell homeostatic mechanisms in Echinococcus granulosus protoscoleces. Parasitology International 58, 270277.CrossRefGoogle ScholarPubMed
Cumino, A.C., Lamenza, P. & Denegri, G.M. (2010) Identification of functional FKB protein in Echinococcus granulosus: its involvement in the protoscolicidal action of rapamycin derivates and in calcium homeostasis. International Journal for Parasitology 40, 651661.Google Scholar
Daryani, A., Sharif, M., Amouei, A. & Nasrolahei, M. (2009) Fertility and viability rates of hydatid cysts in slaughtered animals in the Mazandaran Province, Northern Iran. Tropical Animal Health and Production 41, 17011705.Google Scholar
Drake, M.T., Clarke, B.L. & Khosla, S. (2008) Bisphosphonates: mechanism of action and role in clinical practice. Mayo Clinic Proceedings 83, 10321045.Google Scholar
Echeverría, C.I., Isolabella, D.M., Prieto, E.A.G., Leonardelli, A., Prada, L., Perrone, A. & Fuchs, A.G. (2010) Morphological and biological characterization of cell line developed from bovine Echinococcus granulosus. In Vitro Cellular and Development Biology—Animal 46, 781792.Google Scholar
Epping, K. & Brehm, K. (2011) Echinococcus multilocularis: molecular characterization of EmSmadE, a novel BR-Smad involved in TGF-β and BMP signaling. Experimental Parasitology 129, 8594.Google Scholar
Farach-Carson, M.C. & Ridall, A.L. (1998) Dual 1,25-dihydroxyvitamin D3 signal response pathways in osteoblasts: cross-talk between genomic and membrane-initiated pathways. American Journal of Kidney Diseases 31, 729742.Google Scholar
Frayha, G.J. & Haddad, R. (1980) Comparative chemical composition of protoscoleces and hydatid cyst fluid of Echinococcus granulosus (Cestoda). International Journal for Parasitology 10, 359364.CrossRefGoogle Scholar
Giorgio, A., Tarantino, L., Francica, G., Mariniello, N., Aloisio, T., Soscia, E. & Pierri, G. (1992) Unilocular hydatid liver cysts: treatment with US-guided, double percutaneous aspiration and alcohol injection. Radiology 184, 705710.CrossRefGoogle ScholarPubMed
Grosman, C. & Reisin, I.L. (1995) Echinococcus granulosus: partial characterization of the conductive properties of two cation channels from protoscoleces of the ovine strain, reconstituted on planar lipid bilayers. Experimental Parasitology 81, 546555.Google Scholar
Grosman, C. & Reisin, I.L. (1997) Interconverting gating modes of a nonselective cation channel from the tapeworm Echinococcus granulosus reconstituted on planar lipid bilayers. Journal of Membrane Biology 158, 8794.Google Scholar
Guenther, H.L., Guenther, H.E. & Fleisch, H. (1981) The effects of 1-hydroxyethane-1,1-diphosphonate and dichloromethanediphosphonate on collagen synthesis by rabbit articular chondrocytes and rat bone cells. Biochemical Journal 196, 293301.Google Scholar
Guerret, S., Vuitton, D.A., Liance, M., Pater, C. & Carbillet, J.P. (1998) Echinococcus multilocularis: relationship between susceptibility/resistance and liver fibrogenesis in experimental mice. Parasitology Research 84, 657667.CrossRefGoogle ScholarPubMed
Halder, S.K., Goodwin, J.S. & Al-Hendy, A. (2011) 1,25-Dihydroxyvitamin D3 reduces TGF-beta3-induced fibrosis-related gene expression in human uterine leiomyoma cells. Journal of Clinical Endocrinology and Metabolism 96, E754E762.Google Scholar
Heath, D.D., Jensen, O. & Lightowlers, M.W. (2003) Progress in control of hydatidosis using vaccination – a review of formulation and delivery of the vaccine and recommendation for practical use in control programmes. Acta Tropica 85, 133143.Google Scholar
Hemphill, A., Spicher, M., Stadelmann, B., Mueller, J., Naguleswaran, A., Gottstein, B. & Walker, M. (2007) Innovative chemotherapeutical treatment options for alveolar and cystic echinococcosis. Parasitology 134, 16571670.Google Scholar
Ibarra, C. & Reisin, I.L. (1994) Echinococcus granulosus: characterization of the electrical potential of the syncytial tegument of protoscoleces incubated in vitro – effect of inhibitors. Experimental Parasitology 78, 400409.Google Scholar
Irigoin, F., Casaravilla, C., Iborra, F., Sim, R.B., Ferreira, F. & Díaz, A. (2004) Unique precipitation and exocytosis of a calcium salt of myo-inositol hexakisphosphate in larval Echinococcus granulosus. Journal of Cellular Biochemistry 93, 12721281.CrossRefGoogle ScholarPubMed
Kavanagh, K.L., Guo, K., Dunford, J.E., Wu, X., Knapp, S., Ebetino, F.H., Rogers, M.J., Russell, R.G.G. & Oppermann, U. (2006) The molecular mechanism of nitrogen-containing bisphosphonates as antiosteoporosis drugs. Proceedings of the National Academy of Science of the United States of America 103, 78297834.Google Scholar
Kusters, J.M.A.M., Dernison, M.M., van Meerwijk, W.P.M., Ypey, D.L., Theuvenet, A.P.R. & Gielen, C.C.A.M. (2005) Stabilizing role of calcium store-dependent plasma membrane calcium channels in action-potential firing and intracellular calcium oscillations. Biophysical Journal 89, 37413756.Google Scholar
Lidor, C., Meyer, M.S., Wasserman, R.H. & Edelstein, S. (1987) The effect of disodium ethane-1-hydroxy-1,1-diphosphonate on the metabolism of calcitriol in chicks. Biochemical Journal 243, 7578.Google Scholar
Mahmoud, L.H. & el-Garhy, M.F. (2002) A histochemical study on the hydatid cyst and electron microscopy of the hydatid sand of Echinococcus granulosus. Journal of the Egyptian Society of Parasitology 32, 647656(Abstract).Google Scholar
Masud, T., Mulcahy, B., Thompson, A.V., Donnelly, S., Keen, R.W., Doyle, D.V. & Spector, T.D. (1998) Effects of cyclical etidronate combined with calcitriol versus cyclical etidronate alone on spine and femoral neck bone mineral density in postmenopausal osteoporotic women. Annals of the Rheumatic Diseases 57, 346349.Google Scholar
Moro, P. & Schantz, P.M. (2006) Cystic echinococcosis in the Americas. Parasitology International 55, s181s186.Google Scholar
Ortiz-Gómez, A., Jiménez, C., Estévez, A.M., Carrero-Lérida, J., Ruiz-Pérez, L.M. & González-Pacanowska, D. (2006) Farnesyl diphosphate synthase is a cytosolic enzyme in Leishmania major promastigotes and its overexpression confers resistance to risedronate. Eukaryotic Cell 5, 10571064.Google Scholar
Panda, D.K., Miao, D., Bolivar, I., Li, J., Huo, R., Hendy, G.N. & Goltzman, D. (2004) Inactivation of the 25-hydroxyvitamin D 1α-hydroxylase and vitamin D receptor demonstrates independent and interdependent effects of calcium and vitamin D on skeletal and mineral homeostasis. Journal of Biological Chemistry 279, 1675416766.CrossRefGoogle Scholar
Phang, J.M., Liu, W., Hancock, C. & Christian, K.J. (2012) The proline regulatory axis and cancer. Frontiers in Oncology 2, 60.Google Scholar
Sanz-Rodriguez, C.E., Concepción, J.L., Pekerar, S., Oldfield, E. & Urbina, J.A. (2007) Bisphosphonates as inhibitors of Trypanosoma cruzi kexokinase: kinetic and metabolic studies. Journal of Biological Chemistry 282, 1237712387.Google Scholar
Sato, M., Grasser, W., Endo, N., Akins, R., Simmons, H., Thompson, D.D., Golub, E. & Rodan, G.A. (1991) Bisphosphonate action. Alendronate localization in rat bone and effects on osteoclast ultrastructure. Journal of Clinical Investigation 88, 20952105.Google Scholar
Shao, W., Orlando, R.C. & Awayda, M.S. (2005) Bisphosphonates stimulate an endogenous nonselective cation channel in Xenopus oocytes: potential mechanism of action. American Journal of Physiology – Cell Physiology 289, C248C256.Google Scholar
Smith, S.A. & Richards, K.S. (1993) Ultrastructure and microanalyses of the calcareous corpuscles of the protoscoleces of Echinococcus granulosus. Parasitology Research 79, 245250.Google Scholar
Spillotis, M. & Brehm, K. (2004) Echinocuccus multilocularis: identification and molecular characterization of a Ral-like small GTP-binding protein. Experimental Parasitology 107, 163172.Google Scholar
Vazquez, G., Santillan, G., Boland, R., Roldán, E. & Pérez-Lloret, A. (2003) Modulation of cytosolic calcium levels in osteoblast-like osteosarcoma cells by olpadronate and its amino-derivative IG-9402. Calcified Tissue International 72, 215221.Google Scholar
Vidor, E., Piens, M.A., Abbas, M. & Petavy, A.F. (1986) Hydatid cyst fluid (Echinococcus granulosus) biochemistry. Influence of site on cyst permeability. Annales de Parasitologie Humaine et Comparee 61, 333340(Abstract).Google Scholar
Zurabian, R., Carrero, J.C., Rodríguez-Contreras, D., Willms, K. & Laclette, J.P. (2005) Antigenic proteins associated with calcareous corpuscules of Taenia solium; partial characterization of a calcium-binding protein. Archives of Medical Research 36, 49.Google Scholar