Investigation of Genes Expression of the JAK/STAT Signalling Pathway and AMPs in the Presence of Borrelia Spirochetes in Ixodes Ricinus

Overview

Journal Sci Rep

Date 2025 Jan 22

PMID 39843584

Authors

Magdalena Szczotko

Sandra Antunes

Ana Domingos

Malgorzata Dmitryjuk

Affiliations

Soon will be listed here.

Abstract

Multicellular animals need to control the spread of invading pathogens. This is a particular challenge for blood-feeding vectors such as ticks, which ingest large amounts of blood potentially laden with harmful microorganisms. Ticks have a basic innate immune system and protect themselves from infection through innate immune responses involving pathways such as Janus kinase (JAK) or the signalling transducer activator of transcription (STAT). Direct antimicrobial defence occurs through the rapid synthesis of numerous antimicrobial agents including antimicrobial peptides (AMPs). The tick Ixodes ricinus is one of the main vectors of the Lyme disease pathogen, the spirochete Borrelia burgdorferi sensu lato. Data suggest that the JAK/STAT signalling pathway controls the expression of AMPs and regulates the infection of the pathogen in the tick body. The innate immune system during the off-host period keeps the level of spirochete infection in check. Spirochetes may influence the innate immune response in ticks. Therefore, the aim of this study was to analyse the expression of the genes related to the JAK/STAT pathway and selected AMPs in questing ticks in which B. burgorferi s.l. was detected. In the ticks infected with spirochetes, overexpression of genes related to the JAK/STAT signalling pathway was observed in the case of STAM and SOCS genes. AMPs genes such as def1, ric, lzs were overexpressed with different expression patterns. The results obtained suggest that AMPs may be involved in infection management in ticks.

References

Courtney J, Kostelnik L, Zeidner N, Massung R . Multiplex real-time PCR for detection of anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol. 2004; 42(7):3164-8. PMC: 446246. DOI: 10.1128/JCM.42.7.3164-3168.2004. View

Antunes S, Galindo R, Almazan C, Rudenko N, Golovchenko M, Grubhoffer L . Functional genomics studies of Rhipicephalus (Boophilus) annulatus ticks in response to infection with the cattle protozoan parasite, Babesia bigemina. Int J Parasitol. 2012; 42(2):187-95. DOI: 10.1016/j.ijpara.2011.12.003. View

Mansfield K, Cook C, Ellis R, Bell-Sakyi L, Johnson N, Alberdi P . Tick-borne pathogens induce differential expression of genes promoting cell survival and host resistance in Ixodes ricinus cells. Parasit Vectors. 2017; 10(1):81. PMC: 5312269. DOI: 10.1186/s13071-017-2011-1. View

Nakajima Y, Ishibashi J, Yukuhiro F, Asaoka A, Taylor D, Yamakawa M . Antibacterial activity and mechanism of action of tick defensin against Gram-positive bacteria. Biochim Biophys Acta. 2003; 1624(1-3):125-30. DOI: 10.1016/j.bbagen.2003.10.004. View

Michalski M, Kubiak K, Szczotko M, Chajecka M, Dmitryjuk M . Molecular Detection of Sensu Lato and in Ticks Collected from Dogs in Urban Areas of North-Eastern Poland. Pathogens. 2020; 9(6). PMC: 7350305. DOI: 10.3390/pathogens9060455. View

Sonenshine D, Ceraul S, Hynes W, Macaluso K, Azad A . Expression of defensin-like peptides in tick hemolymph and midgut in response to challenge with Borrelia burgdorferi, Escherichia coli and Bacillus subtilis. Exp Appl Acarol. 2003; 28(1-4):127-34. DOI: 10.1023/a:1025354326877. View

Brown S . The fertile field of Drosophila Jak/STAT signalling. Curr Biol. 2002; 12(16):R569-75. DOI: 10.1016/s0960-9822(02)01057-6. View

Mtierova Z, Derdakova M, Chvostac M, Didyk Y, Mangova B, Rusnakova Taragelova V . Local Population Structure and Seasonal Variability of Genotypes in Ticks, Slovakia. Int J Environ Res Public Health. 2020; 17(10). PMC: 7277216. DOI: 10.3390/ijerph17103607. View

Rudenko N, Golovchenko M, Edwards M, Grubhoffer L . Differential expression of Ixodes ricinus tick genes induced by blood feeding or Borrelia burgdorferi infection. J Med Entomol. 2005; 42(1):36-41. DOI: 10.1093/jmedent/42.1.36. View

10.

Medlock J, Hansford K, Bormane A, Derdakova M, Estrada-Pena A, George J . Driving forces for changes in geographical distribution of Ixodes ricinus ticks in Europe. Parasit Vectors. 2013; 6:1. PMC: 3549795. DOI: 10.1186/1756-3305-6-1. View

11.

Aaronson D, Horvath C . A road map for those who don't know JAK-STAT. Science. 2002; 296(5573):1653-5. DOI: 10.1126/science.1071545. View

12.

Silva F, Rezende C, Rossi D, Esteves E, Dyszy F, Schreier S . Structure and mode of action of microplusin, a copper II-chelating antimicrobial peptide from the cattle tick Rhipicephalus (Boophilus) microplus. J Biol Chem. 2009; 284(50):34735-46. PMC: 2787336. DOI: 10.1074/jbc.M109.016410. View

13.

Takeshita T, Arita T, Higuchi M, Asao H, Endo K, Kuroda H . STAM, signal transducing adaptor molecule, is associated with Janus kinases and involved in signaling for cell growth and c-myc induction. Immunity. 1997; 6(4):449-57. DOI: 10.1016/s1074-7613(00)80288-5. View

14.

Aguilar-Diaz H, Quiroz-Castaneda R, Salazar-Morales K, Cossio-Bayugar R, Miranda-Miranda E . Tick Immunobiology and Extracellular Traps: An Integrative Vision to Control of Vectors. Pathogens. 2021; 10(11). PMC: 8621429. DOI: 10.3390/pathogens10111511. View

15.

Perner J, Kropackova S, Kopacek P, Ribeiro J . Sialome diversity of ticks revealed by RNAseq of single tick salivary glands. PLoS Negl Trop Dis. 2018; 12(4):e0006410. PMC: 5919021. DOI: 10.1371/journal.pntd.0006410. View

15.

Meng H, Xu S, Yu Z, Li N, Wang R, Gao X . Abundance and seasonal activity of Haemaphysalis concinna (Acari: Ixodidae) at the border between China and Russia in Northern Inner Mongolia, China. Parasit Vectors. 2016; 9:1. PMC: 4700674. DOI: 10.1186/s13071-015-1291-6. View

16.

Cicculli V, Capai L, Quilichini Y, Masse S, Fernandez-Alvarez A, Minodier L . Molecular investigation of tick-borne pathogens in ixodid ticks infesting domestic animals (cattle and sheep) and small rodents (black rats) of Corsica, France. Ticks Tick Borne Dis. 2019; 10(3):606-613. DOI: 10.1016/j.ttbdis.2019.02.007. View

17.

Kubiak K, Szymanska H, Dmitryjuk M, Dzika E . Abundance of Ticks (Acari: Ixodidae) and the Diversity of Species in Northeastern Poland. Int J Environ Res Public Health. 2022; 19(12). PMC: 9223791. DOI: 10.3390/ijerph19127378. View

18.

Tonk M, Cabezas-Cruz A, Valdes J, Rego R, Grubhoffer L, Estrada-Pena A . Ixodes ricinus defensins attack distantly-related pathogens. Dev Comp Immunol. 2015; 53(2):358-65. DOI: 10.1016/j.dci.2015.08.001. View

18.

Juhn J, Naeem-Ullah U, Guedes B, Majid A, Coleman J, Paolucci Pimenta P . Spatial mapping of gene expression in the salivary glands of the dengue vector mosquito, Aedes aegypti. Parasit Vectors. 2011; 4:1. PMC: 3043528. DOI: 10.1186/1756-3305-4-1. View