Hostname: page-component-7c8c6479df-8mjnm Total loading time: 0 Render date: 2024-03-27T16:43:02.269Z Has data issue: false hasContentIssue false

Characterization of hydrophobic-ligand-binding proteins of Taenia solium that are expressed specifically in the adult stage

Published online by Cambridge University Press:  01 June 2012

M. RAHMAN
Affiliation:
Department of Molecular Parasitology, Sungkyunkwan University School of Medicine and Center for Molecular Medicine, Samsung Biomedical Research Institute, Suwon 446-740, Republic of Korea
E.-G. LEE
Affiliation:
Department of Molecular Parasitology, Sungkyunkwan University School of Medicine and Center for Molecular Medicine, Samsung Biomedical Research Institute, Suwon 446-740, Republic of Korea
S.-H. KIM
Affiliation:
Department of Molecular Parasitology, Sungkyunkwan University School of Medicine and Center for Molecular Medicine, Samsung Biomedical Research Institute, Suwon 446-740, Republic of Korea
Y.-A. BAE
Affiliation:
Department of Molecular Parasitology, Sungkyunkwan University School of Medicine and Center for Molecular Medicine, Samsung Biomedical Research Institute, Suwon 446-740, Republic of Korea
H. WANG
Affiliation:
Qinghai Province Institute for Endemic Diseases Prevention and Control, Qinghai Centers for Disease Prevention and Control, Xining, China
Y. YANG
Affiliation:
Parasitology Institute, Guangxi Centers for Disease Prevention and Control, Nanning, China
Y. KONG*
Affiliation:
Department of Molecular Parasitology, Sungkyunkwan University School of Medicine and Center for Molecular Medicine, Samsung Biomedical Research Institute, Suwon 446-740, Republic of Korea
*
*Corresponding author: Department of Molecular Parasitology, Sungkyunkwan University School of Medicine, 300 Cheoncheon-dong, Jangan-gu, Suwon 440-746, Korea. Tel: +82 31 299 6251. Fax: +82 31 299 6269. E-mail: kongy@skku.edu

Summary

Taenia solium, a causative agent of taeniasis and cysticercosis, has evolved a repertoire of lipid uptake mechanisms. Proteome analysis of T. solium excretory-secretory products (TsESP) identified 10 kDa proteins displaying significant sequence identity with cestode hydrophobic-ligand-binding-proteins (HLBPs). Two distinct 362- and 352-bp-long cDNAs encoding 264- and 258-bp-long open reading frames (87 and 85 amino acid polypeptides) were isolated by mining the T. solium expressed sequence tags and a cDNA library screening (TsHLBP1 and TsHLBP2; 94% sequence identity). They clustered into the same clade with those found in Moniezia expansa and Hymenolepis diminuta. Genomic structure analysis revealed that these genes might have originated from a common ancestor. Both the crude TsESP and bacterially expressed recombinant proteins exhibited binding activity toward 1-anilinonaphthalene-8-sulfonic acid (1,8-ANS), which was competitively inhibited by oleic acid. The proteins also bound to cis-parinaric acid (cPnA) and 16-(9-anthroyloxy) palmitic acid (16-AP), but showed no binding activity against 11-[(5-dimethylaminonaphthalene-1-sulfonyl) amino] undecanoic acid (DAUDA) and dansyl-DL-α-aminocaprylic acid (DACA). Unsaturated fatty acids (FAs) showed greater affinity than saturated FAs. The proteins were specifically expressed in adult worms throughout the strobila. The TsHLBPs might be involved in uptake and/or sequestration of hydrophobic molecules provided by their hosts, thus contributing to host-parasite interface interrelationships.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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

Ahnström, J., Faber, K., Axler, O. and Dahlbäck, B. (2007). Hydrophobic ligand binding properties of the human lipocalin apolipoprotein M. Journal of Lipid Research 48, 17541762.Google Scholar
Alvite, G., Canclini, L., Corvo, I. and Esteves, A. (2008). Two novel Mesocestoides vogae fatty acid binding proteins-functional and evolutionary implications. FEBS Journal 275, 107116.Google Scholar
Alvite, G., Di Pietro, S. M., Santomé, J. A., Ehrlich, R. and Esteves, A. (2001). Binding properties of Echinococcus granulosus fatty acid binding protein. Biochimica et Biophysica Acta 1533, 293302.Google Scholar
Bae, Y. A., Xue, Y., Lee, E. G., Kim, S. H. and Kong, Y. (2010). Bioactive molecules of Taenia solium metacestode, a causative agent of neurocysticercosis. Expert Review of Proteomics 7, 691707.Google Scholar
Barrett, J. (2009). Forty years of helminth biochemistry. Parasitology 136, 16331642.Google Scholar
Barrett, J., Saghir, N., Timanova, A., Clarke, K. and Brophy, P. M. (1997). Characterisation and properties of an intracellular lipid-binding protein from the tapeworm Moniezia expansa . European Journal of Biochemistry 250, 269–275.Google Scholar
Basavaraju, S. V., Zhan, B., Kennedy, M. W., Liu, Y., Hawdon, J. and Hotez, P. J. (2003). Ac-FAR-1, a 20 kDa fatty acid- and retinol-binding protein secreted by adult Ancylostoma caninum hookworms: Gene transcription pattern, ligand binding properties and structural characterisation. Molecular and Biochemical Parasitology 126, 6371.Google Scholar
Cabrera, G., Espinoza, I., Kemmerling, U. and Galanti, N. (2010). Mesocestoides corti: Morphological features and glycogen mobilization during in vitro differentiation from larva to adult worm. Parasitology 137, 373384.Google Scholar
Chemale, G., Ferreiraa, H. B., Barrett, J., Brophy, P. M. and Zaha, A. (2005). Echinococcus granulosus antigen B hydrophobic ligand binding properties. Biochimica et Biophysica Acta 1747, 189194.Google Scholar
Chunchob, S., Grams, R., Viyanant, V., Smooker, P. M. and Vichasri-Grams, S. (2010). Comparative analysis of two fatty acid binding proteins from Fasciola gigantica . Parasitology 137, 18051817.Google Scholar
Corsico, B., Liou, H. L. and Storch, J. (2004). The α-helical domain of liver fatty acid binding protein is responsible for the diffusion-mediated transfer of fatty acids to phospholipid membranes. Biochemistry 43, 36003607.Google Scholar
del Brutto, O. H., Sotelo, J. and Roman, G. C. (1998). Neurocysticercosis: A Clinical Handbook. Swets & Zeitlinger Publishers, Lisse, Switzerland.Google Scholar
Espinoza, I., Galindo, M., Bizarro, C. V., Ferreira, H. B., Zaha, A. and Galanti, N. (2005). Early post-larval development of the endoparasitic platyhelminth Mesocestoides corti: Trypsin provokes reversible tegumental damage leading to serum-induced cell proliferation and growth. Journal of Cellular Physiology 205, 211217.Google Scholar
Esquivel, A., Diaz-Otero, F. and Gimenez-Roldan, S. (2005). Growing frequency of neurocysticercosis in Madrid (Spain). Neurologia 20, 1620.Google Scholar
Fairfax, K. C., Vermeirea, J. J., Harrisona, L. M., Bungirod, R. D., Grant, W., Husain, S. Z. and Cappello, M. (2009). Characterization of a fatty acid and retinol binding protein orthologue from the hookworm Ancylostoma ceylanicum . International Journal for Parasitology 39, 15611571.Google Scholar
Flisser, A., Rodriguez-Canul, R. and Willingham, A. L. (2006). Control of the taeniosis/cysticercosis complex: Future developments. Veterinary Parasitology 139, 283292.Google Scholar
Fusco, A. C., Salafsky, B. and Kevin, M. B. (1985). Schistosoma mansoni: Eicosanoid production by cercariae. Experimental Parasitology 59, 4450.CrossRefGoogle ScholarPubMed
Garcia, H. H., Gilman, R. H., Gonzalez, A. E., Rodriguez, S., Gavidia, C., Tsang, V. C., Falcon, N., Lescano, A. G., Moulton, L. H., Bernal, T., Tovar, M. and Cysticercosis Working Group in Perú. (2003). Hyperendemic human and porcine Taenia solium infection in Perú. American Journal of Tropical Medicine and Hygiene 68, 268725.Google Scholar
Garofalo, A., Rowlinson, M. C., Amambua, N. A., Hughes, J. M., Kelly, S. M., Price, N. C., Cooper, A., Watson, D. G., Kennedy, M. W. and Bradley, J. E. (2003). The FAR protein family of the nematode Caenorhabditis elegans: Differential lipid binding properties, structural characteristics, and developmental regulation. Journal of Biological Chemistry 278, 80658074.Google Scholar
Gilman, R. H., del Brutto, O. H., Garcia, H. H., Martinez, M. and Cysrticercosis Working Group in Perú. (2000). Prevalence of taeniosis among patients with neurocysticercosis is related to severity of infection. Neurology 55, 1062.Google Scholar
Glatz, J. F. and van der Vusse, G. J. (1996). Cellular fatty acid-binding proteins: Their function and physiological significance. Progress in Lipid Research 35, 243282.Google Scholar
Jacobsen, N. S. and Fairbarin, D. (1967). Lipid metabolism in helminth parasites III. Biosynthesis and interconversion of fatty acids by Hymenolepis diminuta (Cestoda). Journal of Parasitology 53, 355361.Google Scholar
Janssen, D. and Barrett, J. (1995). A novel lipid-binding protein from the cestode Moniezia expansa . The Biochemical Journal 311, 4957.Google Scholar
Jeon, H. K., Chai, J. Y., Kong, Y., Waikagul, J., Insisiengmay, B., Rim, H. J. and Eom, K. S. (2009). Differential diagnosis of Taenia asiatica using multiplex PCR. Experimental Parasitology 121, 151156.Google Scholar
Kennedy, M. W. (2000). The nematode polyprotein allergen/antigens. Parasitology Today 16, 373380.Google Scholar
Kennedy, M. W., Brass, A., McCruden, A. B., Price, N. C., Kelly, S. M. and Cooper, A. (1995). The ABA-1 allergen of the parasitic nematode Ascaris suum: Fatty acid and retinoid binding function and structural characterization. Biochemistry 34, 67006710.Google Scholar
Kennedy, M. W., Garside, L. H., Goodrick, L. E., McDermott, L., Brass, A., Price, N. C., Kelly, S. M., Cooper, A. and Bradley, J. E. (1997). The Ov20 protein of the parasitic nematode Onchocerca volvulus: A structurally novel class of small helix-rich retinol-binding proteins. Journal of Biological Chemistry 272, 2944229448.CrossRefGoogle ScholarPubMed
Kim, S. H., Bae, Y. A., Yang, Y., Hong, S. T. and Kong, Y. (2011). Paralogous proteins comprising the 150 kDa hydrophobic-ligand-binding-protein complex of the Taenia solium metacestode have evolved non-overlapped binding affinities toward fatty acid analogs. International Journal for Parasitology 41, 12071215.Google Scholar
Lee, E. G., Bae, Y. A., Jeong, Y. T., Chung, J. Y., Je, E. Y., Kim, S. H., Na, B. K., Ju, J. W., Kim, T. S., Ma, L., Cho, S. Y. and Kong, Y. (2005). Proteomic analysis of a 120 kDa protein complex in cyst fluid of Taenia solium metacestode and preliminary evaluation of its value for the serodiagnosis of neurocysticercosis. Parasitology 131, 867879.Google Scholar
Lee, E. G., Kim, S. H., Bae, Y. A., Chung, J. Y., Suh, M., Na, B. K., Kim, T. S., Kang, I., Ma, L. and Kong, Y. (2007). A hydrophobic ligand-binding protein of the Taenia solium metacestode mediates uptake of the host lipid: Implication for the maintenance of parasitic cellular homeostasis. Proteomics 7, 40164030.Google Scholar
Lescano, A. G., Garcia, H. H., Gilman, R. H., Gavidia, C. M., Tsang, V. C., Rodriguez, S., Moulton, L. H., Villaran, M. V., Montan, S. M. and Gonzalezet, A. E. (2009). Taenia solium cysticercosis hotspots surrounding tapeworm carriers: Clustering on human seroprevalence but not on seizures. PLoS Neglected Tropical Diseases 3, e371.CrossRefGoogle Scholar
McDermott, L., Cooper, A. and Kennedy, M. W. (1999). Novel classes of fatty acid and retinol binding protein from nematodes. Molecular and Cellular Biochemistry 192, 6975.Google Scholar
Meenan, N. A., Ball, G., Bromek, K., Uhrín, D., Cooper, A., Kennedy, M. W. and Smith, B. O. (2011). Solution structure of a repeated unit of the ABA-1 nematode polyprotein allergen of Ascaris reveals a novel fold and two discrete lipid-binding sites. PLoS Neglected Tropical Diseases 5, e1040.Google Scholar
Pastukhov, A. V. and Ropson, I. J. (2003). Fluorescent dyes as probes to study lipid-binding proteins. Proteins 53, 607615.Google Scholar
Patthy, L. (1999). Genome evolution and the evolution of exon-shuffling-a review. Gene 238, 103114.Google Scholar
Rabiela, M. T., Hornelas, Y., Garcia-Allan, C., Rodríguez-del Rosal, E. and Flisser, A. (2000). Evagination of Taenia solium cysticerci: A histologic and electron microscopy study. Archives of Medical Research 31, 605607.Google Scholar
Saghir, N., Conde, P. J., Brophy, P. M. and Barrett, J. (2001). Biochemical characterisation of a hydrophobic ligand binding protein from the tapeworm Hymenolepis diminuta . International Journal for Parasitology 31, 653660.Google Scholar
Smyth, J. D. and McManus, D. P. (1989). The Physiology and Biochemistry of Cestodes. Cambridge University Press, Cambridge, UK.Google Scholar
Solovyova, A. S., Meenan, N., McDermott, L., Garofalo, A., Bradley, J. E., Kennedy, M. W. and Byron, O. (2003). The polyprotein and FAR lipid binding proteins of nematodes: Shape and monomer/dimer states in ligand-free and bound forms. European Biophysical Journal 32, 465476.Google Scholar
Sorvillo, F., Wilkins, P., Shafir, S. and Eberhard, M. (2011). Public health implications of cysticercosis acquired in the United States. Emerging Infectious Diseases 17, 16.CrossRefGoogle ScholarPubMed
Veerkamp, J. H., van Moerkerk, H. T. B., Prinsen, C. F. M. and van Kuppevelt, T. H. (1999). Structural and functional studies on different human FABP types. Molecular and Cellular Biochemistry 192, 137142.Google Scholar
Zhang, W., Li, J., Jones, M. K., Zhang, Z., Zhao, L., Blair, D. and McManus, D. P. (2010). The Echinococcus granulosus antigen B gene family comprises at least 10 unique genes in five subclasses which are differentially expressed. PLoS Neglected Tropical Diseases 4, e784.CrossRefGoogle ScholarPubMed
Supplementary material: File

M. RAHMAN, E.-G. LEE, S.-H. KIM, Y.-A. BAE, H. WANG, Y. YANG and Y. KONG

Legends for supplementary figures

Download M. RAHMAN, E.-G. LEE, S.-H. KIM, Y.-A. BAE, H. WANG, Y. YANG and Y. KONG(File)
File 12.4 KB