Abstract
Infections with parasitic helminths cause severe debilitating and sometimes lethal diseases in humans and domestic animals on a global scale. Unable to synthesize de novo their own fatty acids and sterols, helminth parasites (nematodes, trematodes, cestodes) rely on their hosts for their supply. These organisms produce and secrete a wide range of lipid binding proteins that are, in most cases, structurally different from the ones found in their hosts, placing them as possible novel therapeutic targets. In this sense, a lot of effort has been made towards the structure determination of these proteins, but their precise function is still unknown. In this review, we aim to present the current knowledge on the functions of LBPs present in parasitic helminths as well as novel members of this highly heterogeneous group of proteins.
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References
Alvite G, Esteves A (2012)Lipid binding proteins from parasitic platyhelminthes.Front Physiol 3.https://doi.org/10.3389/FPHYS.2012.00363
Arend AC, Zaha A, Ayala FJ, Haag KL (2004) The Echinococcus granulosus antigen B shows a high degree of genetic variability. Exp Parasitol 108(1–2):76–80. https://doi.org/10.1016/j.exppara.2004.07.009
Bancroft AJ, Levy CW, Jowitt TA, Hayes KS, Thompson S, Mckenzie EA, Ball MD, Dubaissi E, France AP, Bellina B, Sharpe C, Mironov A, Brown SL, Cook PC, MacDonald AS, Thornton DJ, Grencis RK, MacDonald AS, Thornton DJ, Grencis RK (2019) The major secreted protein of the whipworm parasite tethers to matrix and inhibits interleukin-13 function. 10(1):1–11.https://doi.org/10.1038/s41467-019-09996-z
Barf T, Lehmann F, Hammer K, Haile S, Axen E, Medina C, Uppenberg J, Svensson S, Rondahl L, Lundbäck T (2009) N-benzyl-indolo carboxylic acids: design and synthesis of potent and selective adipocyte fatty-acid binding protein (a-FABP) inhibitors. Bioorg Med Chem Lett 19(6):1745–1748. https://doi.org/10.1016/j.bmcl.2009.01.084
Barletta GP, Franchini G, Corsico B, Fernandez-Alberti S (2019) Fatty acid and retinol-binding protein: unusual protein conformational and cavity changes dictated by ligand fluctuations. J Chem Inf Model 59(8):3545–3555. https://doi.org/10.1021/acs.jcim.9b00364
Barrett J (2009) Forty years of helminth biochemistry. Parasitology 136(12):1633–1642. https://doi.org/10.1017/S003118200900568X
Barrett J, Saghir N, Timanova A, Clarke K, Brophy PM (1997) Characterisation and properties of an intracellular lipid-binding protein from the tapeworm Moniezia expansa. Eur J Biochem 250(2):269–275. https://doi.org/10.1111/j.1432-1033.1997.0269a.x
Barrett J (1981) Nutrition and biosynthesis. In: Biochemistry of Parasitic Helminths. Macmillan Education UK, pp 149–244. https://doi.org/10.1007/978-1-349-86119-4_4
Basavaraju S, Zhan B, Kennedy MW, Liu Y, Hawdon J, Hotez PJ (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. Mol Biochem Parasitol 126(1):63–71. https://doi.org/10.1016/S0166-6851(02)00253-0
Becker MM, Kalinna BH, Waine GJ, McManus DP (1994) Gene cloning, overproduction and purification of a functionally active cytoplasmic fatty acid-binding protein (Sj-FABPc) from the human blood fluke Schistosoma japonicum. Gene 148(2):321–325. https://doi.org/10.1016/0378-1119(94)90706-4
Bélgamo JA, Alberca LN, Pórfido JL, Romero FNC, Rodriguez S, Talevi A, Córsico B, Franchini GR (2020) Application of target repositioning and in silico screening to exploit fatty acid binding proteins (FABPs) from Echinococcus multilocularis as possible drug targets. J Comput Aided Mol Des 34(12):1275–1288. https://doi.org/10.1007/s10822-020-00352-8
Blaxter M, Koutsovoulos G (2015) The evolution of parasitism in Nematoda. Parasitology 142(Suppl 1):S26–S39. https://doi.org/10.1017/S0031182014000791
Bradley JE, Nirmalan N, Kläger SL, Faulkner H, Kennedy MW (2001) River blindness: a role for parasite retinoid-binding proteins in the generation of pathology? Trends Parasitol 17(10):471–475. https://doi.org/10.1016/S1471-4922(01)02036-0
Britton C, Moore J, Gilleard JS, Kennedy MW (1995) Extensive diversity in repeat unit sequences of the cDNA encoding the polyprotein antigen/allergen from the bovine lungworm Dictyocaulus viviparus. Mol Biochem Parasitol 72(1–2):77–88. https://doi.org/10.1016/0166-6851(95)00088-I
Britton C, Roberts B, Marks ND (2016) Functional genomics tools for Haemonchus contortus and lessons from other Helminths. Adv Parasitol 93:599–623. https://doi.org/10.1016/bs.apar.2016.02.017
Burbelo PD, Leahy HP, Iadarola MJ, Nutman TB (2009) A four-antigen mixture for rapid assessment of Onchocerca volvulus infection. PLoS Negl Trop Dis 3(5):e438. https://doi.org/10.1371/journal.pntd.0000438
Cardona ÁJ, González TM, Álvarez PJ (2010) Otitis bovina por Rhabditis bovis en Córdoba, Colombia. Reporte de dos casos. Rev MVZ Cordoba 15(3):2240–2244. https://doi.org/10.21897/rmvz.311
Ceol CJ, Horvitz HR (2004) A new class of C. elegans synMuv genes implicates a Tip60/NuA4-like HAT complex as a negative regulator of Ras signaling. Dev Cell 6(4):563–576. https://doi.org/10.1016/S1534-5807(04)00065-6
Chemale G, Haag KL, Ferreira HB, Zaha A (2001) Echinococcus granulosus antigen B is encoded by a gene family. Mol Biochem Parasitol 116(2):233–237. https://doi.org/10.1016/S0166-6851(01)00316-4
Cheng X, Xiang Y, Xie H, Xu CL, Xie TF, Zhang C, Li Y (2013) Molecular characterization and functions of fatty acid and retinoid binding protein gene (Ab-far-1) in Aphelenchoides besseyi. PLoS ONE 8(6):e66011. https://doi.org/10.1371/journal.pone.0066011
Curran SP, Ruvkun G (2007) Lifespan regulation by evolutionarily conserved genes essential for viability. PLoS Genet 3(4):0479–0487. https://doi.org/10.1371/journal.pgen.0030056
Dutta TK, Banakar P, Rao U (2015) The status of RNAi-based transgenic research in plant nematology. Front Microbiol 0(DEC):760. https://doi.org/10.3389/FMICB.2014.00760
Eiras J, Zhu XQ, Yurlova N, Pedrassani D, Yoshikawa M, Nawa Y (2021) Dioctophyme renale (Goeze, 1782) (Nematoda, Dioctophymidae) parasitic in mammals other than humans: a comprehensive review. Parasitol Int 81:102269. https://doi.org/10.1016/j.parint.2020.102269
Esteves A, Ehrlich R (2006) Invertebrate intracellular fatty acid binding proteins. Comp Biochem Physiol C: Toxicol Pharmacol 142(3–4):262–274. https://doi.org/10.1016/j.cbpc.2005.11.006
Esteves A, Dallagiovanna B, Ehrlich R (1993) A developmentally regulated gene of Echinococcus granulosus codes for a 15.5-kilodalton polypeptide related to fatty acid binding proteins. Mol Biochem Parasitol 58(2):215–222. https://doi.org/10.1016/0166-6851(93)90043-W
Estuningsih SE, Smooker PM, Wiedosari E, Widjajanti S, Vaiano S, Partoutomo S, Spithill TW (1997) Evaluation of antigens of Fasciola gigantica as vaccines against tropical fasciolosis in cattle. Int J Parasitol 27(11):1419–1428. https://doi.org/10.1016/S0020-7519(97)00096-9
Fairfax KC, Vermeire JJ, Harrison LM, Bungiro RD, Grant W, Husain SZ, Cappello M (2009) Characterisation of a fatty acid and retinol binding protein orthologue from the hookworm Ancylostoma ceylanicum. Int J Parasitol 39(14):1561–1571. https://doi.org/10.1016/j.ijpara.2009.06.005
Fernández V, Ferreira HB, Fernández C, Zaha A, Nieto A (1996) Molecular characterisation of a novel 8-kDa subunit of Echinococcus granulosus antigen B. Mol Biochem Parasitol 77(2):247–250. https://doi.org/10.1016/0166-6851(96)02602-3
Frayha GJ, Smyth JD (1983) Lipid metabolism in parasitic helminths. Adv Parasitol 22(C):309–387. https://doi.org/10.1016/S0065-308X(08)60465-0
Frosch P, Hartmann M, Mühlschlegel F, Frosch M (1994) Sequence heterogeneity of the echinococcal antigen B. Mol Biochem Parasitol 64(1):171–175. https://doi.org/10.1016/0166-6851(94)90145-7
Furuhashi M, Tuncman G, Görgün CZ, Makowski L, Atsumi G, Vaillancourt E, Kono K, Babaev VR, Fazio S, Linton MF, Sulsky R, Robl JA, Parker RA, Hotamisligil GS (2007) Treatment of diabetes and atherosclerosis by inhibiting fatty-acid-binding protein aP2. Nature 447(7147):959–965. https://doi.org/10.1038/nature05844
Garofalo A, Kläger SL, Rowlinson MC, Nirmalan N, Klion A, Allen JE, Kennedy MW, Bradley JE (2002) The FAR proteins of filarial nematodes: secretion, glycosylation and lipid binding characteristics. Mol Biochem Parasitol 122(2):161–170. https://doi.org/10.1016/S0166-6851(02)00097-X
Giorello AN, Kennedy MW, Butti MJ, Radman NE, Córsico B, Franchini GR (2017) Identification and characterization of the major pseudocoelomic proteins of the giant kidney worm, Dioctophyme Renale. Parasites Vectors 10(1):446. https://doi.org/10.1186/s13071-017-2388-x
González G, Nieto A, Fernández C, Örn A, Wernstedt C, Hellman U (1996) Two different 8 kDa monomers are involved in the oligomeric organization of the native Echinococcus granulosus antigen B. Parasite Immunol 18(12):587–596. https://doi.org/10.1046/j.1365-3024.1996.d01-38.x
Guidi A, Mansour NR, Paveley RA, Carruthers IM, Besnard J, Hopkins AL, Gilbert IH, Bickle QD (2015) Application of RNAi to genomic drug target validation in schistosomes. PLoS Negl Trop Dis 9(5):e0003801. https://doi.org/10.1371/JOURNAL.PNTD.0003801
Haag KL, Ayala FJ, Kamenetzky L, Gutierrez AM, Rosenzvit M (2004) Livestock trade history, geography, and parasite strains: the mitochondrial genetic structure of Echinococcus granulosus in Argentina. J Parasitol 90(2):234–239. https://doi.org/10.1645/GE-173R
Haunerland NH, Chisholm JM (1990) Fatty acid binding protein in flight muscle of the locust, Schistocerca gregaria. Biochim Biophys Acta (BBA)/Lipids Lipid Metab 1047(3):233–238. https://doi.org/10.1016/0005-2760(90)90521-X
Haunerland NH, Spener F (2004) Fatty acid-binding proteins - Insights from genetic manipulations. Prog Lipid Res 43(4):328–349. https://doi.org/10.1016/j.plipres.2004.05.001
Hewitson JP, Grainger JR, Maizels RM (2009) Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol Biochem Parasitol 167(1):1–11. https://doi.org/10.1016/j.molbiopara.2009.04.008
Hiepe T, Lucius R, Gottstein B (2006) Allgemeine Parasitologie mit Grundzügen der Immunologie, Diagnostik und Bekämpfung. Schweizer Archiv Für Tierheilkunde 103(10):A-615. https://doi.org/10.1024/0036-7281.148.6.317a
Huang F, Dang Z, Suzuki Y, Horiuchi T, Yagi K, Kouguchi H, Irie T, Kim K, Oku Y (2016) Analysis on gene expression profile in oncospheres and early stage metacestodes from echinococcus multilocularis. PLoS Negl Trop Dis 10(4):e0004634. https://doi.org/10.1371/JOURNAL.PNTD.0004634
Ibáñez-Shimabukuro M, Florencia Rey-Burusco M, Gabrielsen M, Franchini GR, Riboldi-Tunnicliffe A, Roe AJ, Griffiths K, Cooper A, Córsico B, Kennedy MW, Smith BO (2019) Structure and ligand binding of As-p18, an extracellular fatty acid binding protein from the eggs of a parasitic nematode. Biosci Rep 39(7). https://doi.org/10.1042/BSR20191292
Iberkleid I, Vieira P, de Almeida Engler J, Firester K, Spiegel Y, Horowitz SB (2013) Fatty acid-and retinol-binding protein, Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes. PLoS ONE 8(5):e64586. https://doi.org/10.1371/journal.pone.0064586
Iberkleid I, Sela N, Brown Miyara S (2015) Meloidogyne javanica fatty acid- and retinol-binding protein (Mj-FAR-1) regulates expression of lipid-, cell wall-, stress- and phenylpropanoid-related genes during nematode infection of tomato. BMC Genomics 16(1):1–26. https://doi.org/10.1186/s12864-015-1426-3
Jia WZ, Yan HB, Lou ZZ, Ni XW, Liu HX, Li HM, Guo AJ, Fu BQ (2011) Genetic variation of the 8-kDa glycoprotein family from echinococcus granulosus, taenia multiceps and taenia hydatigena. Chin Med J 124(18):2849–2856. https://doi.org/10.3760/cma.j.issn.0366-6999.2011.18.010
Jian X, Shu-Hua X, Hui-Qing Q, Sen L, Hotez P, Bing-Gui S, Hai-Chou X, Tie-Hua L, Bin Z (2003) Necator americanus: maintenance through one hundred generations in golden hamsters (Mesocricetus auratus). II. Morphological development of the adult and its comparison with humans. Exp Parasitol 105(3–4):192–200. https://doi.org/10.1016/j.exppara.2003.12.016
Jordanova R, Groves MR, Kostova E, Woltersdorf C, Liebau E, Tucker PA (2009) Fatty acid- and retinoid-binding proteins have distinct binding pockets for the two types of cargo. J Biol Chem 284(51):35818–35826. https://doi.org/10.1074/jbc.M109.022731
Kamenetzky L, Muzulin PM, Gutierrez AM, Angel SO, Zaha A, Guarnera EA, Rosenzvit MC (2005) High polymorphism in genes encoding antigen B from human infecting strains of Echinococcus granulosus. Parasitology 131(6):805–815. https://doi.org/10.1017/S0031182005008474
Kennedy MW (2011) The polyprotein allergens of nematodes (NPAs) - structure at last, but still mysterious. Exp Parasitol 129(2):81–84. https://doi.org/10.1016/j.exppara.2011.06.007
Kennedy MW, Tomlinson LA, Fraser EM, Christie JF (1990) The specificity of the antibody response to internal antigens of Ascaris: heterogeneity in infected humans, and MHC (H-2) control of the repertoire in mice. Clin Exp Immunol 80(2):219–224. https://doi.org/10.1111/j.1365-2249.1990.tb05237.x
Kennedy MW, Britton C, Price NC, Kelly SM, Cooper A (1995) The DvA-1 polyprotein of the parasitic nematode Dictyocaulus viviparus. A small helix-rich lipid-binding protein. J Biol Chem 270(33):19277–19281. https://doi.org/10.1074/jbc.270.33.19277
Kennedy MW, Garside LH, Goodrick LE, McDermott L, Brass A, Price NC, Kelly SM, Cooper A, Bradley JE (1997) The Ov20 protein of the parasitic nematode Onchocerca volvulus. A structurally novel class of small helix-rich retinol-binding proteins. J Biol Chem 272(47):29442–29448. https://doi.org/10.1074/jbc.272.47.29442
Kimber MJ, McKinney S, McMaster S, Day TA, Fleming CC, Maule AG (2007) flp gene disruption in a parasitic nematode reveals motor dysfunction and unusual neuronal sensitivity to RNA interference. FASEB J 21(4):1233–1243. https://doi.org/10.1096/fj.06-7343com
Kiontke K, Sudhaus W (2006) Ecology of Caenorhabditis species. In: WormBook : the online review of C. elegans biology. pp 1–14. https://doi.org/10.1895/wormbook.1.37.1
Kuang L, Colgrave ML, Bagnall NH, Knox MR, Qian M, Wijffels G (2009) The complexity of the secreted NPA and FAR lipid-binding protein families of Haemonchus contortus revealed by an iterative proteomics-bioinformatics approach. Mol Biochem Parasitol 168(1):84–94. https://doi.org/10.1016/j.molbiopara.2009.07.001
Le X, Wang X, Guan T, Ju Y, Li H (2016) Isolation and characterization of a fatty acid- and retinoid-binding protein from the cereal cyst nematode Heterodera avenae. Exp Parasitol 167:94–102. https://doi.org/10.1016/j.exppara.2016.05.009
Lee E-G, Kim S-H, Bae Y-A, Chung J-Y, Suh M, Na B-K, Kim T-S, Kang I, Ma L, 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(21):4016–4030. https://doi.org/10.1002/PMIC.200700332
Li BW, Rush AC, Tan J, Weil GJ (2004) Quantitative analysis of gender-regulated transcripts in the filarial nematode Brugia malayi by real-time RT-PCR. Mol Biochem Parasitol 137(2):329–337. https://doi.org/10.1016/j.molbiopara.2004.07.002
Lightowlers MW, Liu D, Haralambous A, Rickard MD (1989) Subunit composition and specificity of the major cyst fluid antigens of Echinococcus granulosus. Mol Biochem Parasitol 37(2):171–182. https://doi.org/10.1016/0166-6851(89)90149-7
Lilley CJ, Davies LJ, Urwin PE (2012) RNA interference in plant parasitic nematodes: a summary of the current status. Parasitology 139(5):630–640. https://doi.org/10.1017/S0031182011002071
Liu RZ, Li X, Godbout R (2008) A novel fatty acid-binding protein (FABP) gene resulting from tandem gene duplication in mammals: transcription in rat retina and testis. Genomics 92(6):436–445. https://doi.org/10.1016/j.ygeno.2008.08.003
Logan J, Pearson MS, Manda SS, Choi Y-J, Field M, Eichenberger RM, Mulvenna J, Nagaraj SH, Fujiwara RT, Gazzinelli-Guimaraes P, Bueno L, Mati V, Bethony JM, Mitreva M, Sotillo J, Loukas A (2020) Comprehensive analysis of the secreted proteome of adult Necator americanus hookworms. PLoS Negl Trop Dis 14(5):1–30. https://doi.org/10.1371/JOURNAL.PNTD.0008237
MacDonald K, Buxton S, Kimber MJ, Day TA, Robertson AP, Ribeiro P (2014) Functional characterization of a novel family of acetylcholine-gated chloride channels in Schistosoma mansoni. PLoS Pathog 10(6):e1004181. https://doi.org/10.1371/journal.ppat.1004181
Marcelino AMC, Smock RG, Gierasch LM (2006) Evolutionary coupling of structural and functional sequence information in the intracellular lipid-binding protein family. Proteins: Struct Funct Genet 63(2):373–384. https://doi.org/10.1002/prot.20860
McDermott L, Kennedy MW, McManus DP, Bradley JE, Cooper A, Storch J (2002) How helminth lipid-binding proteins offload their Ligands to membranes: differential mechanisms of fatty acid transfer by the ABA-1 Polyprotein Allergen and Ov-FAR-1 Proteins of Nematodes and Sj-FABPc of Schistosomes. Biochemistry 41(21):6706–6713. https://doi.org/10.1021/bi0159635
Meenan NAG, Ball G, Bromek K, Uhrín D, Cooper A, Kennedy MW, Smith BO (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 Negl Trop Dis 5(4):e1040. https://doi.org/10.1371/journal.pntd.0001040
Mei B, Kennedy MW, Beauchamp J, Komuniecki PR, Komuniecki R (1997) Secretion of a novel, developmentally regulated fatty acid-binding protein into the perivitelline fluid of the parasitic nematode, Ascaris suum. J Biol Chem 272(15):9933–9941. https://doi.org/10.1074/jbc.272.15.9933
Michalski ML, Weil GJ (1999) Gender-specific gene expression in Brugia malayi. Mol Biochem Parasitol 104(2):247–257. https://doi.org/10.1016/S0166-6851(99)00149-8
Michalski ML, Monsey JD, Cistola DP, Weil GJ (2002) An embryo-associated fatty acid-binding protein in the filarial nematode Brugia malayi. Mol Biochem Parasitol 124(1–2):1–10. https://doi.org/10.1016/S0166-6851(02)00081-6
Moore J, Mcdermott L, Price NC, Kelly SM, Cooper A, Kennedy MW (1999) Sequence-divergent units of the ABA-1 polyprotein array of the nematode Ascaris suum have similar fatty-acid- and retinol-binding properties but different binding-site environments. Biochem J 340(1):337–343. https://doi.org/10.1042/bj3400337
Morphew RM, Wilkinson TJ, MacKintosh N, Jahndel V, Paterson S, McVeigh P, Abbas Abidi SM, Saifullah K, Raman M, Ravikumar G, Lacourse J, Maule A, Brophy PM (2016) Exploring and expanding the fatty-acid-binding protein superfamily in Fasciola species. J Proteome Res 15(9):3308–3321. https://doi.org/10.1021/acs.jproteome.6b00331
Moser D, Tendler M, Griffiths G, Klinkert MQ (1991) A 14-kDa Schistosoma mansoni polypeptide is homologous to a gene family of fatty acid binding proteins. J Biol Chem 266(13):8447–8454. https://doi.org/10.1016/s0021-9258(18)92995-9
Muzulin PM, Kamenetzky L, Gutierrez AM, Guarnera EA, Rosenzvit MC (2008) Echinococcus granulosus antigen B gene family: further studies of strain polymorphism at the genomic and transcriptional levels. Exp Parasitol 118(2):156–164. https://doi.org/10.1016/j.exppara.2007.07.004
Nirmalan N, Cordeiro NJV, Kläger SL, Bradley JE, Allen JE (1999) Comparative analysis of glycosylated and nonglycosylated filarial homologues of the 20-kilodalton retinol binding protein from Onchocerca volvulus (Ov20). Infect Immun 67(12):6329–6334. https://doi.org/10.1128/iai.67.12.6329-6334.1999
Obal G, Ramos AL, Silva V, Lima A, Batthyany C, Bessio MI, Ferreira F, Salinas G, Ferreira AM (2012) Characterisation of the native lipid moiety of echinococcus granulosus antigen B. PLoS Negl Trop Dis 6(5):e1642. https://doi.org/10.1371/journal.pntd.0001642
Oriol R, Williams JF, Pérez Esandi MV, Oriol C (1971) Purification of lipoprotein antigens of Echinococcus granulosus from sheep hydatid fluid. Am J Trop Med Hyg 20(4):569–574. https://doi.org/10.4269/ajtmh.1971.20.569
Paras KL, Miller L, Verocai GG (2018) Ectopic infection by Dioctophyme renale in a dog from Georgia, USA, and a review of cases of ectopic dioctophymosis in companion animals in the Americas. Vet Parasitol: Reg Stud Rep 14:111–116. https://doi.org/10.1016/j.vprsr.2018.09.008
Parks SC, Nguyen C, Nasrolahi S, Juncaj D, Lu D, Ramaswamy R, Dhillon H, Buchman A, Akbari OS, Yamanaka N, Boulanger MJ, Dillman AR (2021) Parasitic nematode fatty acid- and retinol-binding proteins compromise host immunity by interfering with host lipid signaling pathways. BioRxiv, 2021.03.25.436866. https://doi.org/10.1101/2021.03.25.436866
Pérez MG, Spiliotis M, Rego N, Macchiaroli N, Kamenetzky L, Holroyd N, Cucher MA, Brehm K, Rosenzvit MC (2019) Deciphering the role of miR-71 in echinococcus multilocularis early development in vitro. PLoS Negl Trop Dis 13(12):1–21. https://doi.org/10.1371/JOURNAL.PNTD.0007932
Phani V, Shivakumara TN, Davies KG, Rao U (2017) Meloidogyne incognita fatty acid- and retinol- binding protein (Mi-FAR-1) affects nematode infection of plant roots and the attachment of pasteuria penetrans endospores. Front Microbiol 8(NOV). https://doi.org/10.3389/FMICB.2017.02122
Plenefisch J, Xiao H, Mei B, Geng J, Komuniecki PR, Komuniecki R (2000) Secretion of a novel class of iFABPs in nematodes: coordinate use of the Ascaris/Caenorhabditis model systems. Mol Biochem Parasitol 105(2):223–236. https://doi.org/10.1016/S0166-6851(99)00179-6
Poole CB, Hornstra LJ, Benner JS, Fink JR, McReynolds LA (1996) Carboxy-terminal sequence divergence and processing of the polyprotein antigen from Dirofilaria immitis. Mol Biochem Parasitol 82(1):51–65. https://doi.org/10.1016/0166-6851(96)02721-1
Pórfido JL, Herz M, Kiss F, Kamenetzky L, Brehm K, Rosenzvit MC, Córsico B, Franchini GR (2020) Fatty acid-binding proteins in Echinococcus spp.: the family has grown. Parasitol Res 119(4):1401–1408. https://doi.org/10.1007/s00436-020-06631-5
Prior A, Jones JT, Blok VC, Beauchamp J, McDermott L, Cooper A, Kennedy MW (2001) A surface-associated retinol- and fatty acid-binding protein (GP-FAR-1) from the potato cyst nematode Globodera pallida: lipid binding activities, structural analysis and expression pattern. Biochem J 356(2):387–394. https://doi.org/10.1042/0264-6021:3560387
Radoslavov G, Jordanova R, Teofanova D, Georgieva K, Hristov P, Salomone-Stagni M, Liebau E, Bankov I (2010) A novel secretory poly-cysteine and histidine-tailed metalloprotein (Ts-PCHTP) from Trichinella spiralis (Nematoda). PLoS ONE 5(10):e13343. https://doi.org/10.1371/JOURNAL.PONE.0013343
Rey Burusco M Fl (2014) Estudio biofísico y estructural de Na-FAR-1, miembro de una nueva familia de proteínas de nematodos que unen ácidos grasos y retinol [Universidad Nacional de La Plata]. https://doi.org/10.35537/10915/34308
Rey-Burusco MF, Ibáñez-Shimabukuro M, Gabrielsen M, Franchini GR, Roe AJ, Griffiths K, Zhan B, Cooper A, Kennedy MW, Córsico B, Smith BO (2015) Diversity in the structures and ligand-binding sites of nematode fatty acid and retinol-binding proteins revealed by Na-FAR-1 from Necator americanus. Biochem J 471(3):403–414. https://doi.org/10.1042/BJ20150068
Rodríguez-Pérez J, Rodrǵuez-Medina JR, García-Blanco MA, Hillyer GV (1992) Fasciola hepatica: molecular cloning, nucleotide sequence, and expression of a gene encoding a polypeptide homologous to a Schistosoma mansoni fatty acid-binding protein. Exp Parasitol 74(4):400–407. https://doi.org/10.1016/0014-4894(92)90202-L
Saghir N, Conde PJ, Brophy PM, Barrett J (2001) Biochemical characterisation of a hydrophobic ligand binding protein from the tapeworm Hymenolepis diminuta. Int J Parasitol 31(7):653–660. https://doi.org/10.1016/S0020-7519(01)00135-7
Sako Y, Nakao M, Ikejima T, Piao XZ, Nakaya K, Ito A (2000) Molecular characterization and diagnostic value of Taenia solium low-molecular-weight antigen genes. J Clin Microbiol 38(12):4439–4444. https://doi.org/10.1128/jcm.38.12.4439-4444.2000
Sanchez F, March F, Mercader M, Coll P, Muñoz C, Prats G (1991) Immunochemical localization of major hydatid fluid antigens in protoscoleces and cysts of Echinococcus granulosus from human origin. Parasite Immunol 13(6):583–592. https://doi.org/10.1111/j.1365-3024.1991.tb00554.x
Sanchez F, Garcia J, March F, Cardeñosa N, Coll P, Muñoz C, Auladell C, Prats G (1993) Ultrastructural localization of major hydatid fluid antigens in brood capsules and protoscoleces of Echinococcus granulosus of human origin. Parasite Immunol 15(8):441–447. https://doi.org/10.1111/j.1365-3024.1993.tb00629.x
Scapin G, Gordon JI, Sacchettini JC (1992) Refinement of the structure of recombinant rat intestinal fatty acid-binding apoprotein at 1.2-A resolution. J Biol Chem 267(6):4253–4269. https://doi.org/10.1016/S0021-9258(19)50654-8
Schaap FG, Van der Vusse GJ, Glatz JFC (2002) Evolution of the family of intracellular lipid binding proteins in vertebrates. Mol Cell Biochem 239(1):69–77. https://doi.org/10.1023/A:1020519011939
Selkirk ME, Gregory WF, Jenkins RE, Maizels RM (1993) Localization, turnover and conservation of gp 15/400 in different stages of Brugia malayi. Parasitology 107(4):449–457. https://doi.org/10.1017/S0031182000067810
Silva-Álvarez V, Folle AM, Ramos AL, Zamarreño F, Costabel MD, García-Zepeda E, Salinas G, Córsico B, Ferreira AM (2015) Echinococcus granulosus antigen B: A Hydrophobic Ligand Binding Protein at the host-parasite interface. Prostaglandins Leukot Essent Fatty Acids 93:17–23. https://doi.org/10.1016/j.plefa.2014.09.008
Silva-Álvarez V, Folle AM, Ramos AL, Kitano ES, Iwai LK, Corraliza I, Córsico B, Ferreira AM (2016) Echinococcus granulosus antigen B binds to monocytes and macrophages modulating cell response to inflammation. Parasit Vectors 9(1):1–17. https://doi.org/10.1186/S13071-016-1350-7
Silva-Álvarez V, Ramos AL, Folle AM, Lagos S, Dee VM, Ferreira AM (2018) Antigen B from Echinococcus granulosus is a novel ligand for C-reactive protein. Parasit Immunol 40(9):e12575. https://doi.org/10.1111/pim.12575
Siracusano A, Riganò R, Ortona E, Profumo E, Margutti P, Buttari B, Delunardo F, Teggi A (2008) Immunomodulatory mechanisms during Echinococcus granulosus infection. Exp Parasitol 119(4):483–489. https://doi.org/10.1016/j.exppara.2008.01.016
Smathers RL, Petersen DR (2011) The human fatty acid-binding protein family: Evolutionary divergences and functions. Hum Genomics 5(3):170–191. https://doi.org/10.1186/1479-7364-5-3-170
Solovyova AS, Meenan N, McDermott L, Garofalo A, Bradley JE, Kennedy MW, Byron O (2003) The polyprotein and FAR lipid binding proteins of nematodes: shape and monomer/dimer states in ligand-free and bound forms. Eur Biophys J 32(5):465–476. https://doi.org/10.1007/s00249-003-0297-8
Spiliotis M, Brehm K (2009) Axenic in vitro cultivation of Echinococcus multilocularis metacestode vesicles and the generation of primary cell cultures. Methods Mol Biol 470:245–262. https://doi.org/10.1007/978-1-59745-204-5_17
Stevens L, Rooke S, Falzon LC, Machuka EM, Momanyi K, Murungi MK, Njoroge SM, Odinga CO, Ogendo A, Ogola J, Fèvre EM, Blaxter M (2020) The Genome of Caenorhabditis bovis. Curr Biol 30(6):1023-1031.e4. https://doi.org/10.1016/j.cub.2020.01.074
Storch J, Corsico B (2008) The emerging functions and mechanisms of mammalian fatty acid–binding Proteins. Annu Rev Nutr 28:73–95. https://doi.org/10.1146/ANNUREV.NUTR.27.061406.093710
Storch J, McDermott L (2009) Structural and functional analysis of fatty acid-binding proteins. J Lipid Res 50(SUPPL.):S126–S131. https://doi.org/10.1194/jlr.R800084-JLR200
Tomlinson LA, Christie JF, Fraser EM, McLaughlin D, McIntosh AE, Kennedy MW (1989) MHC restriction of the antibody repertoire to secretory antigens, and a major allergen, of the nematode parasite Ascaris. J Immunol 143(7):2349–2356 (http://www.ncbi.nlm.nih.gov/pubmed/2778320)
Tree TIM, Gillespie AJ, Shepley KJ, Blaxter ML, Tuan RS, Bradley JE (1995) Characterisation of an immunodominant glycoprotein antigen of Onchocerca volvulus with homologues in other filarial nematodes and Caenorhabditis elegans. Mol Biochem Parasitol 69(2):185–195. https://doi.org/10.1016/0166-6851(94)00204-Z
Tritten L, Tam M, Vargas M, Jardim A, Stevenson MM, Keiser J, Geary TG (2017) Excretory/secretory products from the gastrointestinal nematode Trichuris muris. Exp Parasitol 178:30–36. https://doi.org/10.1016/j.exppara.2017.05.003
Tsai IJ, Zarowiecki M, Holroyd N, Garciarrubio A, Sanchez-Flores A, Brooks KL, Tracey A, Bobes RJ, Fragoso G, Sciutto E, Aslett M, Beasley H, Bennett HM, Cai J, Camicia F, Clark R, Cucher M, De Silva N, Day TA, … Valdes V (2013) The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496(7443):57–63. https://doi.org/10.1038/nature12031
Vieira P, Eves-Van Den Akker S, Verma R, Wantoch S, Eisenback JD, Kamo K (2015) The pratylenchus penetrans transcriptome as a source for the development of alternative control strategies: Mining for putative genes involved in parasitism and evaluation of in planta RNAi. PLoS ONE 10(12):e0144674. https://doi.org/10.1371/journal.pone.0144674
Wang YT, Liu CH, Zhu HL (2016) Fatty acid binding protein (FABP) inhibitors: a patent review (2012–2015). Expert Opin Ther Pat 26(7):767–776. https://doi.org/10.1080/13543776.2016.1182500. Taylor & Francis
Wang DW, Xu CL, Ding SW, Huang X, Cheng X, Zhang C, Chen C, Xie H (2018) Identification and function of FAR protein family genes from a transcriptome analysis of Aphelenchoides besseyi. Bioinformatics 34(17):2936–2943. https://doi.org/10.1093/bioinformatics/bty209
Xia Y, Spence HJ, Moore J, Heaney N, McDermott L, Cooper A, Watson DG, Mei B, Komuniecki R, Kennedy MW (2000) The ABA-1 allergen of Ascaris lumbricoides: Sequence polymorphism, stage and tissue-specific expression, lipid binding function, and protein biophysical properties. Parasitology 120(2):211–224. https://doi.org/10.1017/S0031182099005363
Xu M, Joo HJ, Paik YK (2011) Novel functions of lipid-binding protein 5 in Caenorhabditis elegans fat metabolism. J Biol Chem 286(32):28111–28118. https://doi.org/10.1074/jbc.M111.227165
Zarlenga DS, Rhoads ML, A1-Yaman FM (1994) A Taenia crassiceps cDNA sequence encoding a putative immunodiagnostic antigen for bovine cysticercosis. Mol Biochem Parasitol 67(2):215–223. https://doi.org/10.1016/0166-6851(94)00132-4
Zhang W, Li J, Jones MK, Zhang Z, Zhao L, Blair D, McManus DP (2010) The Echinococcus granulosus antigen B gene family comprises at least 10 unique genes in five subclasses which are differentially expressed. PLoS Negl Trop Dis 4(8):e784. https://doi.org/10.1371/journal.pntd.0000784
Zhang C, Xie H, Cheng X, Wang DW, Li Y, Xu CL, Huang X (2015) Molecular identification and functional characterization of the fatty acid- and retinoid-binding protein gene Rs-far-1 in the burrowing nematode Radopholus similis (Tylenchida: Pratylenchidae). PLoS ONE 10(3):e0118414. https://doi.org/10.1371/journal.pone.0118414
Zheng H, Zhang W, Zhang L, Zhang Z, Li J, Lu G, Zhu Y, Wang Y, Huang Y, Liu J, Kang H, Chen J, Wang L, Chen A, Yu S, Gao Z, Jin L, Gu W, Wang Z, … Wang S (2013a) The genome of the hydatid tapeworm Echinococcus granulosus. Nat Genet 45(10):1168–1175. https://doi.org/10.1038/ng.2757
Zheng Y, Blair D, Bradley JE (2013b) Phyletic distribution of fatty acid-binding protein genes. PLoS ONE 8(10):e77636. https://doi.org/10.1371/journal.pone.0077636
Zhou L, Chen F, Pan H, Ye J, Dong X, Li C, Lin F (2016) Identifying virulence-associated genes using transcriptomic and proteomic association analyses of the plant parasitic nematode Bursaphelenchus mucronatus. Int J Mol Sci 17(9):1492. https://doi.org/10.3390/ijms17091492
Zimmerman AW, Veerkamp JH (2002) New insights into the structure and function of fatty acid-binding proteins. Cell Mol Life Sci 59(7):1096–1116. https://doi.org/10.1007/S00018-002-8490-Y
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Lombardo, J.F., Pórfido, J.L., Sisti, M.S. et al. Function of lipid binding proteins of parasitic helminths: still a long road. Parasitol Res 121, 1117–1129 (2022). https://doi.org/10.1007/s00436-022-07463-1
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DOI: https://doi.org/10.1007/s00436-022-07463-1