Expression of acyl-CoA-binding protein 5 from Rhodnius prolixus and its inhibition by RNA interference

English version

Autoři: Muriel G. M. D. Almeida ^aff001; Daniela S. Arêdes ^aff001; David Majerowicz ^aff002; Nils J. Færgeman ^aff002; Jens Knudsen ^aff002; Katia C. Gondim ^aff001
Působiště autorů: Instituto de Bioquímica Médica Leopoldo de Meis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil ^aff001; Institut for Biokemi og Molekylær Biologi, Syddansk Universitet, Odense, Denmark ^aff002; Faculdade de Farmácia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil ^aff003
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227685

Souhrn

The acyl-CoA-binding proteins (ACBP) act by regulating the availability of acyl-CoA in the cytoplasm and must have essential functions in lipid metabolism. The genome of the kissing-bug Rhodnius prolixus encodes five proteins of this family, but little is known about them. In this study we investigated the expression and function of RpACBP-5. Feeding induced RpACBP-5 gene expression in the posterior midgut, and an increase of about four times was observed two days after the blood meal. However, the amount of protein, which was only detected in this organ, did not change during digestion. The RpACBP-5 gene was also highly expressed in pre-vitellogenic and vitellogenic oocytes. Recombinant RpACBP-5 was shown to bind to acyl-CoA of different lengths, and it exhibited nanomolar affinity to lauroyl-CoA in an isothermal titration assay, indicating that RpACBP-5 is a functional ACBP. RpACBP-5 knockdown by RNA interference did not affect digestion, egg laying and hatching, survival, or accumulation of triacylglycerol in the fat body and oocytes. Similarly, double knockdown of RpACBP-1 and RpACBP-5 did not alter egg laying and hatching, survival, accumulation of triacylglycerol in the fat body and oocytes, or the neutral lipid composition of the posterior midgut or hemolymph. These results show that RpACBP-5 is a functional ACBP but indicate that the lack of a detectable phenotype in the knockdown insects may be a consequence of functional overlap of the proteins of the ACBP family found in the insect.

Klíčová slova:

Blood – Fats – Gene expression – Insects – Lipids – Oocytes – Ovaries – Recombinant proteins

Zdroje

1. Neess D, Bek S, Engelsby H, Gallego SF, Færgeman NJ. Long-chain acyl-CoA esters in metabolism and signaling: Role of acyl-CoA binding proteins. Prog Lipid Res. Elsevier Ltd; 2015;59: 1–25. doi: 10.1016/j.plipres.2015.04.001 25898985

2. Faergeman NJ, Knudsen J. Role of long-chain fatty acyl-CoA esters in the regulation of metabolism and in cell signalling. Biochem J. 1997;323: 1–12. doi: 10.1042/bj3230001 9173866

3. Neess D, Kiilerich P, Sandberg MB, Helledie T, Nielsen R, Mandrup S. ACBP—A PPAR and SREBP modulated housekeeping gene. Mol Cell Biochem. 2006;284: 149–157. doi: 10.1007/s11010-005-9039-9 16411019

4. Vock C, Biedasek K, Boomgaarden I, Heins A, Nitz I, Döring F. ACBP knockdown leads to down-regulation of genes encoding rate-limiting enzymes in cholesterol and fatty acid metabolism. Cell Physiol Biochem. 2010;25: 675–686. doi: 10.1159/000315087 20511713

5. Gaigg B, Neergaard TB, Schneiter R, Hansen JK, Faergeman NJ, Jensen NA, et al. Depletion of acyl-coenzyme A-binding protein affects sphingolipid synthesis and causes vesicle accumulation and membrane defects in Saccharomyces cerevisiae. Mol Biol Cell. 2001;12: 1147–60. doi: 10.1091/mbc.12.4.1147 11294913

6. Larsen MK, Tuck S, Faergeman NJ, Knudsen J. MAA-1, a Novel Acyl-CoA–binding Protein Involved in Endosomal Vesicle Transport in Caenorhabditis elegans. Mol Biol Cell. 2006;17: 4318–4329. doi: 10.1091/mbc.E06-01-0035 16870706

7. Elle IC, Simonsen KT, Olsen LCB, Birck PK, Ehmsen S, Tuck S, et al. Tissue- and paralogue-specific functions of acyl-CoA-binding proteins in lipid metabolism in Caenorhabditis elegans. Biochem J. 2011;437: 231–241. doi: 10.1042/BJ20102099 21539519

8. Oikari S, Ahtialansaari T, Heinonen M V., Mauriala T, Auriola S, Kiehne K, et al. Downregulation of PPARs and SREBP by acyl-CoA-binding protein overexpression in transgenic rats. Pflugers Arch Eur J Physiol. 2008;456: 369–377. doi: 10.1007/s00424-007-0416-y 18157544

9. Schroeder F, Petrescu AD, Huang H, Atshaves BP, McIntosh AL, Martin GG, et al. Role of fatty acid binding proteins and long chain fatty acids in modulating nuclear receptors and gene transcription. Lipids. 2008;43: 1–17. doi: 10.1007/s11745-007-3111-z 17882463

10. Takato H, Shimidzu M, Ashizawa Y, Takei H, Suzuki S. An acyl-CoA-binding protein from grape that is induced through ER stress confers morphological changes and disease resistance in Arabidopsis. J Plant Physiol. 2013;170: 591–600. doi: 10.1016/j.jplph.2012.11.011 23261264

11. Melloni E, Averna M, Salamino F, Sparatore B, Minafra R, Pontremoli S. Acyl-CoA-binding protein is a potent m-calpain activator. J Biol Chem. 2000;275: 82–86. doi: 10.1074/jbc.275.1.82 10617589

12. Neess D, Bek S, Bloksgaard M, Marcher AB, Færgeman NJ, Mandrup S. Delayed Hepatic Adaptation to Weaning in ACBP-/- Mice Is Caused by Disruption of the Epidermal Barrier. Cell Rep. 2013;5: 1403–1412. doi: 10.1016/j.celrep.2013.11.010 24316079

13. Landrock D, Atshaves BP, McIntosh AL, Landrock KK, Schroeder F, Kier AB. Acyl-CoA binding protein gene ablation induces pre-implantation embryonic lethality in mice. Lipids. 2010;45: 567–580. doi: 10.1007/s11745-010-3437-9 20559753

14. Ohnishi A, Hull JJ, Matsumoto S. Targeted disruption of genes in the Bombyx mori sex pheromone biosynthetic pathway. Proc Natl Acad Sci U S A. 2006;103: 4398–4403. doi: 10.1073/pnas.0511270103 16537410

15. Ryuda M, Tsuzuki S, Matsumoto H, Oda Y, Tanimura T, Hayakawa Y. Identification of a novel gene, Anorexia, regulating feeding activity via insulin signaling in Drosophila melanogaster. J Biol Chem. 2011;286: 38417–38426. doi: 10.1074/jbc.M111.267344 21917925

16. Rassi AJ, Rassi A, Marin-Neto JA. Chagas disease. Lancet. 2010;375: 1388–1402. doi: 10.1016/S0140-6736(10)60061-X 20399979

17. Gondim KC, Atella GC, Pontes EG, Majerowicz D. Lipid metabolism in insect disease vectors. Insect Biochem Mol Biol. 2018;101: 108–123. doi: 10.1016/j.ibmb.2018.08.005 30171905

18. Majerowicz D, Hannibal-Bach HK, Castro RSC, Bozaquel-Morais BL, Alves-Bezerra M, Grillo LAM, et al. The ACBP gene family in Rhodnius prolixus: Expression, characterization and function of RpACBP-1. Insect Biochem Mol Biol. Elsevier Ltd; 2016;72: 41–52. doi: 10.1016/j.ibmb.2016.03.002 27001070

19. Alves-Bezerra M, Majerowicz D, Grillo LA, Tremonte H, Almeida CB, Braz GR, et al. Serotonin regulates an acyl-CoA-binding protein (ACBP) gene expression in the midgut of Rhodnius prolixus. Insect Biochem Mol Biol. 2010;40: 119–125. doi: 10.1016/j.ibmb.2010.01.002 20079838

20. Majerowicz D, Alves-Bezerra M, Logullo R, Fonseca-De-Souza AL, Meyer-Fernandes JR, Braz GRC, et al. Looking for reference genes for real-time quantitative PCR experiments in Rhodnius prolixus (Hemiptera: Reduviidae). Insect Mol Biol. 2011;20: 713–722. doi: 10.1111/j.1365-2583.2011.01101.x 21929722

21. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009;55: 611–622. doi: 10.1373/clinchem.2008.112797 19246619

22. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt Method. Methods. 2001;25: 402–408. doi: 10.1006/meth.2001.1262 11846609

23. Mandrup S, Højrup P, Kristiansen K, Knudsen J. Gene synthesis, expression in Escherichia coli, purification and characterization of the recombinant bovine acyl-CoA-binding protein. Biochem J. 1991;276 (Pt 3: 817–23. doi: 10.1042/bj2760817 2064616

24. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193: 265–275. 14907713

25. Monzani PS, Pereira HM, Melo FA, Meirelles F V., Oliva G, Cascardo JCM. A new topology of ACBP from Moniliophthora perniciosa. Biochim Biophys Acta—Proteins Proteomics. 2010;1804: 115–123. doi: 10.1016/j.bbapap.2009.09.020 19782157

26. Færgeman NJ, Sigurskjold BW, Kragelund BB, Andersen K V., Knudsen J. Thermodynamics of ligand binding to acyl-coenzyme A binding protein studied by titration calorimetry. Biochemistry. 1996;35: 14118–14126. doi: 10.1021/bi960545z 8916897

27. Blight EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37: 911–917. doi: 10.1139/o59-099 13671378

28. Majerowicz D, Cezimbra MP, Alves-Bezerra M, Entringer PF, Atella GC, Sola-Penna M, et al. Rhodnius prolixus lipophorin: lipid composition and effect of high temperature on physiological role. Arch Insect Biochem Physiol. 2013;82: 129–140. doi: 10.1002/arch.21080 23361613

29. Kolmer M, Roos C, Tirronen M, Myöhänen S, Alho H. Tissue-specific expression of the diazepam-binding inhibitor in Drosophila melanogaster: cloning, structure, and localization of the gene. Mol Cell Biol. 1994;14: 6983–6995. doi: 10.1128/mcb.14.10.6983 7935415

30. Matsumoto S, Yoshiga T, Yokoyama N, Iwanaga M, Koshiba S, Kigawa T, et al. Characterization of acyl-CoA-binding protein (ACBP) in the pheromone gland of the silkworm, Bombyx mori. Insect Biochem Mol Biol. 2001;31: 603–609. doi: 10.1016/s0965-1748(00)00165-x 11267899

31. Snyder MJ, Van Antwerpen R. Cellular distribution, levels, and function of the diazepam-binding inhibitor/acyl-CoA-binding protein in last instar Manduca sexta midgut. Cell Tissue Res. 1997;288: 177–184. doi: 10.1007/s004410050804 9042784

32. Wang JL, Wang JX, Zhao XF. Molecular cloning and expression profiles of the acyl-CoA-binding protein gene from the cotton bollworm Helicoverpa armigera. Arch Insect Biochem Physiol. 2008;68: 79–88. doi: 10.1002/arch.20250 18481302

33. Alves-Bezerra M, Klett EL, De Paula IF, Ramos IB, Coleman RA, Gondim KC. Long-chain acyl-CoA synthetase 2 knockdown leads to decreased fatty acid oxidation in fat body and reduced reproductive capacity in the insect Rhodnius prolixus. Biochim Biophys Acta. 2016;1861: 650–662. doi: 10.1016/j.bbalip.2016.04.007 27091636

34. Alves-Bezerra M, Gondim KC. Triacylglycerol biosynthesis occurs via the glycerol-3-phosphate pathway in the insect Rhodnius prolixus. Biochim Biophys Acta—Mol Cell Biol Lipids. 2012;1821: 1462–1471. doi: 10.1016/j.bbalip.2012.08.002 22902317

35. Oliveira PL, Gondim KC, Guedes D, Masuda H. Uptake of yolk proteins in Rhodnius prolixus. J Insect Physiol. 1986;32: 859–866.

36. Petrescu AD, Huang H, Hostetler HA, Schroeder F, Kier AB. Structural and functional characterization of a new recombinant histidine-tagged acyl coenzyme A binding protein (ACBP) from mouse. Protein Expr Purif. 2008;58: 184–193. doi: 10.1016/j.pep.2007.11.010 18178100

37. Augoff K, Kolondra A, Chorzalska A, Lach A, Grabowski K, Sikorski AF. Expression, purification and functional characterization of recombinant human acyl-CoA-binding protein (ACBP) from erythroid cells. Acta Biochim Pol. 2010;57: 533–540. 21079819

38. Meng W, Su YCF, Saunders RMK, Chye ML. The rice acyl-CoA-binding protein gene family: Phylogeny, expression and functional analysis. New Phytol. 2011;189: 1170–1184. doi: 10.1111/j.1469-8137.2010.03546.x 21128943

39. Abo-Hashema KAH, Cake MH, Lukas MA, Knudsen J. The interaction of acyl-CoA with acyl-CoA binding protein and carnitine palmitoyltransferase I. Int J Biochem Cell Biol. 2001;33: 807–815. doi: 10.1016/s1357-2725(01)00049-8 11404184

40. Rasmussen JT, Faergeman NJ, Kristiansen K, Knudsen J. Acyl-CoA-binding protein (ACBP) can mediate intermembrane acyl-CoA transport and donate acyl-CoA for beta-oxidation and glycerolipid synthesis. Biochem J. 1994;299: 165–170. doi: 10.1042/bj2990165 8166635

41. Rosendal J, Ertbjerg P, Knudsen J. Characterization of ligand binding to acyl-CoA-binding protein. Biochem J. 1993;290: 321–326. doi: 10.1042/bj2900321 7680855

42. Grillo LA, Majerowicz D, Gondim KC. Lipid metabolism in Rhodnius prolixus (Hemiptera: Reduviidae): Role of a midgut triacylglycerol-lipase. Insect Biochem Mol Biol. 2007;37: 579–588. doi: 10.1016/j.ibmb.2007.03.002 17517335

43. Murphy DJ. The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog Lipid Res. 2001;40: 325–438. doi: 10.1016/s0163-7827(01)00013-3 11470496

44. Pontes EG, Leite P, Majerowicz D, Atella GC, Gondim KC. Dynamics of lipid accumulation by the fat body of Rhodnius prolixus: the involvement of lipophorin binding sites. J Insect Physiol. 2008;54: 790–797. doi: 10.1016/j.jinsphys.2008.02.003 18395740

45. Gondim KC, Oliveira PL, Masuda H. Lipophorin and oogenesis in Rhodnius prolixus: transfer of phospholipids. J Insect Physiol. 1989;35: 19–27.

46. Santos R, Rosas-Oliveira R, Saraiva FB, Majerowicz D, Gondim KC. Lipid accumulation and utilization by oocytes and eggs of Rhodnius prolixus. Arch Insect Biochem Physiol. 2011;77: 1–16. doi: 10.1002/arch.20414 21308762

Expression of acyl-CoA-binding protein 5 from Rhodnius prolixus and its inhibition by RNA interference

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