Dynamics of digestive proteolytic system during blood feeding of the hard tick Ixodes ricinus

. 2010 Dec 14 ; 3 () : 119. [epub] 20101214

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid21156061

BACKGROUND: Ticks are vectors of a wide variety of pathogens causing severe diseases in humans and domestic animals. Intestinal digestion of the host blood is an essential process of tick physiology and also a limiting factor for pathogen transmission since the tick gut represents the primary site for pathogen infection and proliferation. Using the model tick Ixodes ricinus, the European Lyme disease vector, we have previously demonstrated by genetic and biochemical analyses that host blood is degraded in the tick gut by a network of acidic peptidases of the aspartic and cysteine classes. RESULTS: This study reveals the digestive machinery of the I. ricinus during the course of blood-feeding on the host. The dynamic profiling of concentrations, activities and mRNA expressions of the major digestive enzymes demonstrates that the de novo synthesis of peptidases triggers the dramatic increase of the hemoglobinolytic activity along the feeding period. Overall hemoglobinolysis, as well as the activity of digestive peptidases are negligible at the early stage of feeding, but increase dramatically towards the end of the slow feeding period, reaching maxima in fully fed ticks. This finding contradicts the established opinion that blood digestion is reduced at the end of engorgement. Furthermore, we show that the digestive proteolysis is localized intracellularly throughout the whole duration of feeding. CONCLUSIONS: Results suggest that the egressing proteolytic system in the early stage of feeding and digestion is a potential target for efficient impairment, most likely by blocking its components via antibodies present in the host blood. Therefore, digestive enzymes are promising candidates for development of novel 'anti-tick' vaccines capable of tick control and even transmission of tick-borne pathogens.

Zobrazit více v PubMed

Jongejan F, Uilenberg G. The global importance of ticks. Parasitology. 2004;129(Suppl):S3–14. PubMed

de la Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE. Overview: Ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci. 2008;13:6938–6946. doi: 10.2741/3200. PubMed DOI

Sonenshine DE. Biology of ticks. New York: Oxford University Press; 1991.

Francischetti IM, Sa-Nunes A, Mans BJ, Santos IM, Ribeiro JM. The role of saliva in tick feeding. Front Biosci. 2009;14:2051–2088. doi: 10.2741/3363. PubMed DOI PMC

Nuttall PA. Pathogen-tick-host interactions: Borrelia burgdorferi and TBE virus. Zentralbl Bakteriol. 1999;289:492–505. PubMed

Nene V. Tick genomics--coming of age. Front Biosci. 2009;14:2666–2673. doi: 10.2741/3404. PubMed DOI

Hovius JW, van Dam AP, Fikrig E. Tick-host-pathogen interactions in Lyme borreliosis. Trends Parasitol. 2007;23:434–438. doi: 10.1016/j.pt.2007.07.001. PubMed DOI

Sojka D, Franta Z, Horn M, Hajdusek O, Caffrey CR, Mares M, Kopacek P. Profiling of proteolytic enzymes in the gut of the tick Ixodes ricinus reveals an evolutionarily conserved network of aspartic and cysteine peptidases. Parasit Vectors. 2008;1:7. PubMed PMC

Caffrey CR, McKerrow JH, Salter JP, Sajid M. Blood 'n' guts: an update on schistosome digestive peptidases. Trends Parasitol. 2004;20:241–248. doi: 10.1016/j.pt.2004.03.004. PubMed DOI

Delcroix M, Sajid M, Caffrey CR, Lim KC, Dvorak J, Hsieh I, Bahgat M, Dissous C, McKerrow JH. A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. J Biol Chem. 2006;281:39316–39329. doi: 10.1074/jbc.M607128200. PubMed DOI

Williamson AL, Brindley PJ, Knox DP, Hotez PJ, Loukas A. Digestive proteases of blood-feeding nematodes. Trends Parasitol. 2003;19:417–423. doi: 10.1016/S1471-4922(03)00189-2. PubMed DOI

Horn M, Nussbaumerova M, Sanda M, Kovarova Z, Srba J, Franta Z, Sojka D, Bogyo M, Caffrey CR, Kopacek P, Mares M. Hemoglobin digestion in blood-feeding ticks: mapping a multipeptidase pathway by functional proteomics. Chem Biol. 2009;16:1053–1063. doi: 10.1016/j.chembiol.2009.09.009. PubMed DOI PMC

Coons LB, Rosell-Davis R, Tarnowski BI. In: Morphology, Physiology, and Behavioural Biology of Ticks. Sauer JR, Hair JA, editor. New York: Ellis Horwood Ltd., John Wiley & Sons; 1986. Blood meal digestion in ticks; pp. 248–279.

Agbede RI, Kemp DH. Digestion in the cattle-tick Boophilus microplus: light microscope study of the gut cells in nymphs and females. Int J Parasitol. 1985;15:147–157. doi: 10.1016/0020-7519(85)90080-3. PubMed DOI

Agyei AD, Runham NW. Studies on the morphological changes in the midguts of two ixodid tick species Boophilus microplus and Rhipicephalus appendiculatus during digestion of the blood meal. Int J Parasitol. 1995;25:55–62. doi: 10.1016/0020-7519(94)00114-4. PubMed DOI

Lara FA, Lins U, Paiva-Silva G, Almeida IC, Braga CM, Miguens FC, Oliveira PL, Dansa-Petretski M. A new intracellular pathway of haem detoxification in the midgut of the cattle tick Boophilus microplus: aggregation inside a specialized organelle, the hemosome. J Exp Biol. 2003;206:1707–1715. doi: 10.1242/jeb.00334. PubMed DOI

Sajid M, McKerrow JH, Hansell E, Mathieu MA, Lucas KD, Hsieh I, Greenbaum D, Bogyo M, Salter JP, Lim KC. et al.Functional expression and characterization of Schistosoma mansoni cathepsin B and its trans-activation by an endogenous asparaginyl endopeptidase. Mol Biochem Parasitol. 2003;131:65–75. doi: 10.1016/S0166-6851(03)00194-4. PubMed DOI

Coons LB, Alberti G. In: Microscopic Anatomy of Invertebrates. volume 8B, Chelicerate Arthropoda. Harrison FW, Foelix R, editor. New York: Wiley-Liss; 1999. The Acari-Ticks; pp. 267–514.

Balashov YS, Grigoryeva LA. Cytological changes in the midgut of tick females of the genus Ixodes during and after feeding. Dokl Biol Sci. 2003;393:527–530. doi: 10.1023/B:DOBS.0000010314.97335.2c. PubMed DOI

Tarnowski BI, Coons LB. Ultrastructure of the midgut and blood meal digestion in the adult tick Dermacentor variabilis. Exp Appl Acarol. 1989;6:263–289. doi: 10.1007/BF01193300. PubMed DOI

Sonenshine DE. Biology of ticks. New York: Oxford University Press; 1991.

Bogin E, Hadani A. Digestive Enzymes in "Hard Ticks" (Ixodoidea, Ixodidae) I. Proteolytic Enzyme in the Gut of Hyalomma excavatum Female Ticks. Z Parasitenk. 1973;41:139–146. doi: 10.1007/BF00328757. DOI

Grunclova L, Horn M, Vancova M, Sojka D, Franta Z, Mares M, Kopacek P. Two secreted cystatins of the soft tick Ornithodoros moubata: differential expression pattern and inhibitory specificity. Biol Chem. 2006;387:1635–1644. doi: 10.1515/BC.2006.204. PubMed DOI

Yamaji K, Tsuji N, Miyoshi T, Hatta T, Alim MA, Kushibiki S, Fujisaki K. Hlcyst-1 and Hlcyst-2 are potential inhibitors of HlCPL-A in the midgut of the ixodid tick haemaphysalis longicornis. J Vet Med Sci. 2010;72:599–604. doi: 10.1292/jvms.09-0561. PubMed DOI

Sojka D, Hajdusek O, Dvorak J, Sajid M, Franta Z, Schneider EL, Craik CS, Vancova M, Buresova V, Bogyo M. et al.IrAE: an asparaginyl endopeptidase (legumain) in the gut of the hard tick Ixodes ricinus. Int J Parasitol. 2007;37:713–724. doi: 10.1016/j.ijpara.2006.12.020. PubMed DOI PMC

Renard G, Lara FA, de Cardoso FC, Miguens FC, Dansa-Petretski M, Termignoni C, Masuda A. Expression and immunolocalization of a Boophilus microplus cathepsin L-like enzyme. Insect Mol Biol. 2002;11:325–328. doi: 10.1046/j.1365-2583.2002.00342.x. PubMed DOI

Tsuji N, Miyoshi T, Battsetseg B, Matsuo T, Xuan X, Fujisaki K. A cysteine protease is critical for Babesia spp. transmission in Haemaphysalis ticks. PLoS Pathog. 2008;4:e1000062. doi: 10.1371/journal.ppat.1000062. PubMed DOI PMC

Willadsen P. Anti-tick vaccines. Parasitology. 2004;129(Suppl):S367–387. doi: 10.1017/S0031182003004657. PubMed DOI

de la Fuente J, Kocan KM. Strategies for development of vaccines for control of ixodid tick species. Parasite Immunol. 2006;28:275–283. doi: 10.1111/j.1365-3024.2006.00828.x. PubMed DOI

Liu J, Istvan ES, Gluzman IY, Gross J, Goldberg DE. Plasmodium falciparum ensures its amino acid supply with multiple acquisition pathways and redundant proteolytic enzyme systems. Proc Natl Acad Sci USA. 2006;103:8840–8845. doi: 10.1073/pnas.0601876103. PubMed DOI PMC

Kevil CG, Walsh L, Laroux FS, Kalogeris T, Grisham MB, Alexander JS. An improved, rapid Northern protocol. Biochem Biophys Res Commun. 1997;238:277–279. doi: 10.1006/bbrc.1997.7284. PubMed DOI

Nijhof AM, Balk JA, Postigo M, Jongejan F. Selection of reference genes for quantitative RT-PCR studies in Rhipicephalus (Boophilus) microplus and Rhipicephalus appendiculatus ticks and determination of the expression profile of Bm86. BMC Mol Biol. 2009;10:112. doi: 10.1186/1471-2199-10-112. PubMed DOI PMC

Kopacek P, Weise C, Gotz P. The prophenoloxidase from the wax moth Galleria mellonella: purification and characterization of the proenzyme. Insect Biochem Mol Biol. 1995;25:1081–1091. doi: 10.1016/0965-1748(95)00040-2. PubMed DOI

Barrett AJ, Kirschke H. Cathepsin B, Cathepsin H, and cathepsin L. Methods Enzymol. 1981;80 Pt C:535–561. full_text. PubMed

Knight CG, Barrett AJ. Interaction of human cathepsin D with the inhibitor pepstatin. Biochem J. 1976;155:117–125. PubMed PMC

Kopacek P, Zdychova J, Yoshiga T, Weise C, Rudenko N, Law JH. Molecular cloning, expression and isolation of ferritins from two tick species--Ornithodoros moubata and Ixodes ricinus. Insect Biochem Mol Biol. 2003;33:103–113. doi: 10.1016/S0965-1748(02)00181-9. PubMed DOI

Russo C, Callegaro L, Lanza E, Ferrone S. Purification of IgG monoclonal antibody by caprylic acid precipitation. J Immunol Methods. 1983;65:269–271. doi: 10.1016/0022-1759(83)90324-1. PubMed DOI

Masa M, Maresova L, Vondrasek J, Horn M, Jezek J, Mares M. Cathepsin D propeptide: mechanism and regulation of its interaction with the catalytic core. Biochemistry. 2006;45:15474–15482. doi: 10.1021/bi0614986. PubMed DOI

Murata M, Miyashita S, Yokoo C, Tamai M, Hanada K, Hatayama K, Towatari T, Nikawa T, Katunuma N. Novel epoxysuccinyl peptides. Selective inhibitors of cathepsin B, in vitro. FEBS Lett. 1991;280:307–310. doi: 10.1016/0014-5793(91)80318-W. PubMed DOI

Kam CM, Gotz MG, Koot G, McGuire M, Thiele D, Hudig D, Powers JC. Design and evaluation of inhibitors for dipeptidyl peptidase I (Cathepsin C) Arch Biochem Biophys. 2004;427:123–134. doi: 10.1016/j.abb.2004.04.011. PubMed DOI

Ekici OD, Gotz MG, James KE, Li ZZ, Rukamp BJ, Asgian JL, Caffrey CR, Hansell E, Dvorak J, McKerrow JH. et al.Aza-peptide Michael acceptors: a new class of inhibitors specific for caspases and other clan CD cysteine proteases. J Med Chem. 2004;47:1889–1892. doi: 10.1021/jm049938j. PubMed DOI

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Insight Into the Dynamics of the Ixodes ricinus Nymphal Midgut Proteome

. 2023 Nov ; 22 (11) : 100663. [epub] 20231012

Blood-feeding adaptations and virome assessment of the poultry red mite Dermanyssus gallinae guided by RNA-seq

. 2023 May 13 ; 6 (1) : 517. [epub] 20230513

Haem-responsive gene transporter enables mobilization of host haem in ticks

. 2021 Sep ; 11 (9) : 210048. [epub] 20210901

Ixodes ricinus Salivary Serpin Iripin-8 Inhibits the Intrinsic Pathway of Coagulation and Complement

. 2021 Aug 31 ; 22 (17) : . [epub] 20210831

Mialostatin, a Novel Midgut Cystatin from Ixodes ricinus Ticks: Crystal Structure and Regulation of Host Blood Digestion

. 2021 May 20 ; 22 (10) : . [epub] 20210520

RNA-seq analyses of the midgut from blood- and serum-fed Ixodes ricinus ticks

. 2016 Nov 08 ; 6 () : 36695. [epub] 20161108

Sialomes and Mialomes: A Systems-Biology View of Tick Tissues and Tick-Host Interactions

. 2016 Mar ; 32 (3) : 242-254. [epub] 20151028

Characterization of gut-associated cathepsin D hemoglobinase from tick Ixodes ricinus (IrCD1)

. 2012 Jun 15 ; 287 (25) : 21152-63. [epub] 20120426

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...