Home⇛NRCP Research Journal⇛vol. 24 no. 2 (2025)

Ticks’ Antioxidant Complex and its Implications in Acaricide Resistance

Job A. Corcuera | Emmanuel P. Hernandez | Ian Cary B. Prado | Tetsuya Tanaka | Remil L. Galay

Discipline: others in veterinary sciences

 

Abstract:

Ticks are parasitic arthropods that feed on the blood of humans and animals, making them notorious for the transmission of numerous diseases. To survive their potentially toxic blood-feeding lifestyle, ticks have developed a complex antioxidant response mechanism to counteract oxidative stress. While several antioxidants have been identified in ticks, only a few have been fully studied in terms of their functions. Chemical acaricides have traditionally been used and remain to be widely utilized in the control of ticks. However, the emergence of tick resistance to these acaricides has become a global concern, leading to economic losses, decreased animal productivity, and the spread of tick-borne diseases. This review article discusses the physiological functions of tick antioxidants and their role in detoxification, focusing on how they are involved in acaricide resistance.



References:

  1. Abbas, R. Z., Zaman, M. A., Colwell, D. D., Gilleard, J., & Iqbal, Z. (2014). Acaricide resistance in cattle ticks and approaches to its management: The state of play. Veterinary Parasitology, 203(1-2), 6-20. https://doi.org/10.1016/j.vetpar.2014.03.006
  2. Aboelhadid, S. M., Arafa, W. M., Mahrous, L. N., Fahmy, M. M., & Kamel, A. A. (2018). Molecular detection of Rhipicephalus (Boophilus) annulatus resistance against deltamethrin in middle Egypt. Veterinary parasitology, regional studies and reports, 13, 198-204.
  3. Adamson, S., Browning, R., Singh, P., Nobles, S., Villarreal, A. & Karim, S. (2014). Transcriptional activation of antioxidants may compensate for selenoprotein deficiencies in Amblyomma maculatum (Acari: Ixodidae) injected with selK- or selM-dsRNA. Insect Molecular Biology, 23(4), 497-510. https://doi.org/10.1111/imb.12098
  4. Almazán, C., Lagunes, R., Villar, M., Canales, M., Rosario-Cruz, R., Jongejan, F., & de la Fuente, J. (2009). Identification and characterization of Rhipicephalus (Boophilus) microplus candidate protective antigens for the control of cattle tick infestations. Parasitology Research, 106(2), 471-479. https://doi.org/10.1007/s00436-009-1689-1
  5. Anderson, J. M., Sonenshine, D. E., & Valenzuela, J. G. (2008). Exploring the mialome of ticks: An annotated catalogue of midgut transcripts from the hard tick, Dermacentor variabilis (Acari: Ixodidae). BMC Genomics, 9, 552. https://doi.org/10.1186/1471-2164-9-552
  6. Arafa, W. M., Aboelhadid, S. M., Moawad, A., Shokeir, K. M., & Ahmed, O. (2020a). Toxicity, repellency, and anti-cholinesterase activities of thymol-eucalyptus combinations against phenotypically resistant Rhipicephalus annulatus ticks. Experimental & Applied Acarology, 81(2), 265–277. https://doi.org/10.1007/s10493-020-00506-1
  7. Arafa, W. M., Klafke, G. M., Tidwell, J. P., de León, A. A. P., & Esteve-Gassent, M. (2020b). Detection of single nucleotide polymorphism in the para-sodium channel gene of Rhipicephalus annulatus populations from Egypt resistant to deltamethrin. Ticks and Tick-borne Diseases, 11(5), 101488.  https://doi.org/10.1016/j.ttbdis.2020.101488
  8. Arafa, W. M., Aboelhadid, S. M., Moawad, A., Shokeir, K. M., Ahmed, O., & Pérez de León, A. A. (2021). Control of Rhipicephalus annulatus resistant to deltamethrin by spraying infested cattle with a synergistic eucalyptus essential oil-thymol-deltamethrin combination. Veterinary Parasitology, 290, 109346. https://doi.org/10.1016/j.vetpar.2021.109346
  9. Baron, S., Barrera, R. A., Black, M., Bellgard, M. I., van Dalen, E. M. S., Fourie, J., & Maritz-Olivier, C. (2018). Differentially expressed genes in response to amitraz treatment suggest a proposed model of amitraz resistance in Rhipicephalus decoloratus tick. International Journal of Parasitology: Drugs and Drug Resistance, 8(3), 361-371. https://doi.org/10.1016/j.ijpddr.2018.06.005
  10. Bauer, H., Gromer, S., Urbani, A., Schnölzer, M., Schirmer, R. H., & Müller, H. M. (2003). Thioredoxin reductase from the malaria mosquito Anopheles gambiae. European Journal of Biochemistry, 270(18), 4272-4281. https://doi.org/10.1046/j.1432-1033.2003.03812.x
  11. Baxter, G. D., Green, P., Stuttgen, M., & Barker, S. C. (1999). Detecting resistance to organophosphates and carbamates in the cattle tick Boophilus microplus, with a propoxur-based biochemical test. Experimental and Applied Acarology, 23(10), 907-914. https://doi.org/10.1023/a:1006364816302
  12. Belova, O. A., Burenkova, L. A., & Karganova, G. G. (2012). Different tick-borne encephalitis virus (TBEV) prevalences in unfed versus partially engorged ixodid ticks—Evidence of virus replication and changes in tick behavior. Ticks and Tick-borne Diseases, 3(4), 240-246. https://doi.org/10.1016/j.ttbdis.2012.05.005
  13. Benelli, G. (2020). Pathogens manipulating tick behavior—Through a glass, darkly. Pathogens, 9(8), 664. https://doi.org/10.3390/pathogens9080664
  14. Betancur Hurtado, O. J., & Giraldo-Ríos, C. (2019). Economic and health impact of the ticks in production animals. In M. Abubakar & P. K. Perera (Eds.) Ticks and tick-borne pathogens. IntechOpen.
  15. Braz, G. R., Moreira, M. F., Masuda, H., & Oliveira, P. L. (2002). Rhodnius heme-binding protein (RHBP) is a heme source for embryonic development in the blood-sucking bug Rhodnius prolixus (Hemiptera, Reduviidae). Insect Biochemistry and Molecular Biology, 32(4), 361-367. https://doi.org/10.1016/s0965-1748(01)00163-1
  16. Brites-Neto, J., Duarte, K. M., & Martins, T. F. (2015). Tick-borne infections in human and animal populations worldwide. Veterinary World, 8(3), 301-315. https://doi.org/10.14202/vetworld.2015.301-315
  17. Budachetri, K., & Karim, S. (2015). An insight into the functional role of thioredoxin reductase, a selenoprotein, in maintaining normal native microbiota in the Gulf Coast tick (Amblyomma maculatum). Insect Molecular Biology, 24(6), 570-581. https://doi.org/10.1111/imb.12184
  18. Budachetri, K., Kumar, D., & Karim, S. (2017). Catalase is a determinant of the colonization and transovarial transmission of Rickettsia parkeri in the Gulf Coast tick Amblyomma maculatum. Insect Molecular Biology, 26(4), 414-419. https://doi.org/10.1111/imb.12304
  19. Byamukama, B., Vudriko, P., Tumwebaze, M. A., Tayebwa, D. S., Byaruhanga, J., Angwe, M. K., Li, J., Galon, E. M., Ringo, A., Liu, M., Li, Y., Ji, S., Rizk, M. A., Moumouni, P. F. A., Lee, S. H., Sevinc, F., & Xuan, X. (2021). Molecular detection of selected tick-borne pathogens infecting cattle at the wildlife-livestock interface of Queen Elizabeth National Park in Kasese District, Uganda. Ticks and Tick-borne Diseases, 12(5), 101772. https://doi.org/10.1016/j.ttbdis.2021.101772
  20. Carmona-Ribeiro, A. M., Prieto, T., & Nantes, I. L. (2015). Nanostructures for peroxidases. Frontiers in Molecular Biosciences, 2, 50. https://doi.org/10.3389/fmolb.2015.00050
  21. Castro-Janer, E., Klafke, G. M., Capurro, M. L., & Schumaker, T. T. S. (2015). Cross-resistance between fipronil and lindane in Rhipicephalus (Boophilus) microplus. Veterinary Parasitology, 210, 77-83. https://doi.org/10.1016/j.vetpar.2015.03.011
  22. Chaitanya, R., Shashank, K., & Sridevi, P. (2016). Oxidative stress in invertebrate systems. In R. Ahmad (Ed.), Free radicals and diseases (pp. 51–68). IntechOpen. https://doi.org/10.5772/64573
  23. Champion, C. J., & Xu, J. (2017). The impact of metagenomic interplay in the mosquito redox homeostasis. Free Radical Biology and Medicine, 105, 79-85. https://doi.org/10.1016/j.freeradbiomed.2016.11.031
  24. Cheng, C. C., Sofiyatun, E., Chen, W. J., & Wang, L. C. (2021). Life as a vector of dengue virus: The antioxidant strategy of mosquito cells to survive viral infection. Antioxidants, 10(3), 395. https://doi.org/10.3390/antiox10030395
  25. Citelli, M., Lara, F. A., da Silva Vaz, I. Jr, & Oliveira, P. L. (2007). Oxidative stress impairs heme detoxification in the midgut of the cattle tick, Rhipicephalus (Boophilus) microplus. Molecular and Biochemical Parasitology, 151, 81-88. https://doi.org/10.1016/j.molbiopara.2006.10.008
  26. Coles, T. B., & Dryden, M. W. (2014). Insecticide/acaricide resistance in fleas and ticks infesting dogs and cats. Parasites & Vectors, 7, 8. https://doi.org/10.1186/1756-3305-7-8
  27. Corley, S. W., Jonsson, N. N., Piper, E. K., Cutulle, C., Stear, M. J., & Seddon, J. M. (2013). Mutation in the Rm AOR gene is associated with amitraz resistance in the cattle tick Rhipicephalus microplus. Proceedings of the National Academy of Sciences of the United States of America, 110(41), 16772-16777. https://doi.org/10.1073/pnas.1309072110
  28. Cossío-Bayúgar, R., Barhoumi, R., Burghardt, R. C., Wagner, G. G., & Holman, P. J. (2002). Basal cellular alterations of esterase, glutathione, glutathione S-transferase, intracellular calcium, and membrane potentials in coumaphos-resistant Boophilus microplus (Acari: Ixodidae) cell lines. Pesticide Biochemistry and Physiology, 72, 1-9. https://doi.org/10.1006/pest.2001.2578
  29. Cossío-Bayúgar, R., Miranda, E., & Holman, P. J. (2005). Molecular cloning of a phospholipid-hydroperoxide glutathione peroxidase gene from the tick Boophilus microplus (Acari: Ixodidae). Insect Biochemistry and Molecular Biology, 35, 1378-1387. https://doi.org/10.1016/j.ibmb.2005.08.008
  30. Cossío-Bayúgar, R., Miranda-Miranda, E., Martínez-Ibañez, F., Narváez-Padilla, V., & Reynaud, E. (2020). Physiological evidence that three known mutations in the para-sodium channel gene confer cypermethrin knockdown resistance in Rhipicephalus microplus. Parasites & Vectors, 13, 370. https://doi.org/10.1186/s13071-020-04227-7
  31. Crispell, G., Budachetri, K., & Karim, S. (2016). Rickettsia parkeri colonization in Amblyomma maculatum: The role of superoxide dismutases. Parasites & Vectors, 9, 291. https://doi.org/10.1186/s13071-016-1579-1
  32. DeJong, R. J., Miller, L. M., Molina-Cruz, A., Gupta, L., Kumar, S., & Barillas-Mury, C. (2007). Reactive oxygen species detoxification by catalase is a major determinant of fecundity in the mosquito Anopheles gambiae. Proceedings of the National Academy of Sciences, 104, 2121-2126. https://doi.org/10.1073/pnas.0608407104
  33. de la Fuente, J., Kocan, K. M., & Contreras, M. (2015). Prevention and control strategies for ticks and pathogen transmission. Revue Scientifique et Technique de l'OIE, 34, 249-264. https://doi.org/10.20506/rst.34.1.2357
  34. Descamps, S. (2013). Winter temperature affects the prevalence of ticks in an Arctic seabird. PLoS ONE, 8, Article e77464. https://doi.org/10.1371/journal.pone.0065374
  35. Devenport, M., Alvarenga, P. H., Shao, L., Fujioka, H., Bianconi, M. L., Oliveira, P. L., & Jacobs-Lorena, M. (2006). Identification of the Aedes aegypti peritrophic matrix protein AeIMUCI as a heme-binding protein. Biochemistry, 45, 9540–9549. https://doi.org/10.1021/bi0605991
  36. Dorrah, M., Bensaoud, C., Mohamed, A. A., Sojka, D., Bassal, T. T. M., & Kotsyfakis, M. (2021). Comparison of the hemolysis machinery in two evolutionarily distant blood-feeding arthropod vectors of human diseases. PLOS Neglected Tropical Diseases, 15, e0009693. https://doi.org/10.1371/journal.pntd.0009151
  37. Dupejova, J., Sterba, J., Vancova, M., & Grubhoffer, L. (2011). Hemelipoglycoprotein from the ornate sheep tick, Dermacentor marginatus: Structural and functional characterization. Parasites & Vectors, 4, 4. https://doi.org/10.1186/1756-3305-4-4
  38. Duscher, G. G., Galindo, R. C., Tichy, A., Hummel, K., Kocan, K. M., & de la Fuente, J. (2014). Glutathione S-transferase affects permethrin detoxification in the brown dog tick, Rhipicephalus sanguineus. Ticks and Tick-borne Diseases, 5, 225-233. https://doi.org/10.1016/j.ttbdis.2013.11.006
  39. Enayati, A. A., Asgarian, F., Sharif, M., Boujhmehrani, H., Amouei, A., Vahedi, N., Boudaghi, B., Piazak, N., & Hemingway, J. (2009). Propetamphos resistance in Rhipicephalus bursa (Acari, Ixodidae). Veterinary parasitology, 162(1-2), 135-141. https://doi.org/10.1016/j.vetpar.2009.02.005
  40. Estrada-Peña, A., & de la Fuente, J. (2014). The ecology of ticks and epidemiology of tick-borne viral diseases. Antiviral Research, 108, 104–128. https://doi.org/10.1016/j.antiviral.2014.05.016
  41. Fomenko, D. E., Koc, A., Agisheva, N., Jacobsen, M., Kaya, A., Malinouski, M., Rutherford, J. C., Siu, K. L., Winge, D. R., & Gladyshev, V. N. (2011). Thiol peroxidases mediate specific genome-wide regulation of gene expression in response to hydrogen peroxide. Proceedings of the National Academy of Sciences of the United States of America, 108(7), 2729-2734. https://doi.org/10.1073/pnas.1010721108
  42. Fraga, A., Moraes, J., da Silva, J. R., Costa, E. P., Menezes, J., da Silva Vaz, I. Jr., Logullo, C., da Fonseca, R. N., & Campos, E. (2013). Inorganic polyphosphates regulate hexokinase activity and reactive oxygen species generation in mitochondria of Rhipicephalus (Boophilus) microplus embryo. International Journal of Biological Sciences, 9, 842–852. https://doi.org/10.7150/ijbs.6628
  43. Freitas, D. R., Rosa, R. M., Moraes, J., Campos, E., Logullo, C., Da Silva Vaz, I. Jr., & Masuda, A. (2007). Relationship between glutathione S-transferase, catalase, oxygen consumption, lipid peroxidation, and oxidative stress in eggs and larvae of Boophilus microplus (Acarina: Ixodidae). Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology, 146(4), 688–694. https://doi.org/10.1016/j.cbpa.2006.04.032
  44. Galay, R. L., Aung, K. M., Umemiya-Shirafuji, R., Maeda, H., Matsuo, T., Kawaguchi, H., Miyoshi, N., Suzuki, H., Xuan, X., Mochizuki, M., Fujisaki, K., & Tanaka, T. (2013). Multiple ferritins are vital to successful blood feeding and reproduction of the hard tick Haemaphysalis longicornis. Journal of Experimental Biology, 216, 1905-1915. https://doi.org/10.1242/jeb.081240
  45. Galay, R. L., Umemiya-Shirafuji, R., Bacolod, E. T., Maeda, H., Kusakisako, K., Koyama, J., Tsuji, N., Mochizuki, M., Fujisaki, K., & Tanaka, T. (2014). Two kinds of ferritin protect ixodid ticks from iron overload and consequent oxidative stress. PLoS ONE, 9(3), e90661. https://doi.org/10.1371/journal.pone.0090661
  46. Galay R.L., Umemiya-Shirafuji R., Mochizuki M., Fujisaki K., Tanaka T. (2015). Iron metabolism in hard ticks (Acari: Ixodidae): the antidote to their toxic diet. Parasitology International, 64(2), 182-189. https://doi.org/10.1016/j.parint.2014.12.005
  47. Ghosh, M., Sangwan, N., Sangwan, A. K., Kumar, R., & Gaur, R. S. (2017). Sexual alteration in antioxidant response and esterase profile in Hyalomma anatolicum anatolicum (Acari: Ixodidae) ticks. Journal of Parasitic Diseases, 41(1), 106–111. https://doi.org/10.1007/s12639-016-0758-5
  48. Ghosh, S., Kumar, R., Nagar, G., Kumar, S., Sharma, A. K., Srivastava, A., Kumar, S., Ajith Kumar, K. G., & Saravanan, B. C. (2015). Survey of acaricide resistance status of Rhipicephalus (Boophilus) microplus collected from selected places of Bihar, an eastern state of India. Ticks and Tick-borne Diseases, 6(5), 668–675. https://doi.org/10.1016/j.ttbdis.2015.05.013
  49. Graca-Souza, A. V., Maya-Monteiro, C., Paiva-Silva, G. O., Braz, G. R., Paes, M. C., Sorgine, M. H. F., Oliveira, M. F., & Oliveira, P. L. (2006). Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochemistry and Molecular Biology, 36, 322–335. https://doi.org/10.1016/j.ibmb.2006.01.009
  50. Gudderra, N. P., Neese, P. A., Sonenshine, D. E., Apperson, C. S., & Roe, R. M. (2001). Developmental profile, isolation, and biochemical characterization of a novel lipoglycoheme-carrier protein from the American dog tick, Dermacentor variabilis (Acari: Ixodidae) and observations on a similar protein in the soft tick, Ornithodoros parkeri (Acari: Argasidae). Insect Biochemistry and Molecular Biology, 31, 299–311. https://doi.org/10.1016/s0965-1748(00)00122-3
  51. Guglielmone, A. A., Robbins, R. G., Apanaskevich, D. A., Petney, T. N., Estrada-Peña, A., Horak, I. G., Shao, R., & Barker, S. C. (2010). The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: A list of valid species names. Zootaxa, 2528(1), 1–28.
  52. Hajdusek, O., Sima, R., Perner, J., Loosova, G., Harcubova, A., & Kopacek, P. (2016). Tick iron and heme metabolism—New target for an anti-tick intervention. Ticks and Tick-borne Diseases, 7(4), 565–572. https://doi.org/10.1016/j.ttbdis.2016.01.006
  53. Hajdusek, O., Sojka, D., Kopacek, P., Buresova, V., Franta, Z., Sauman, I., Winzerling, J., & Grubhoffer, L. (2009). Knockdown of proteins involved in iron metabolism limits tick reproduction and development. Proceedings of the National Academy of Sciences, 106(4), 1033–1038. https://doi.org/10.1073/pnas.0807961106
  54. He, H., Chen, A. C., Davey, R. B., Ivie, G. W., & George, J. E. (1999). Identification of a point mutation in the para-type sodium channel gene from a pyrethroid-resistant cattle tick. Biochemical and Biophysical Research Communications, 261, 558–561. https://doi.org/10.1006/bbrc.1999.1076
  55. Hernandez, E. P., Anisuzzaman, Alim, M. A., Kawada, H., Kwofie, K. D., Ladzekpo, D., Koike, Y., Inoue, T., Sasaki, S., Mikami, F., Matsubayashi, M., Tanaka, T., Tsuji, N., & Hatta, T. (2022). Ambivalent roles of oxidative stress in triangular relationships among arthropod vectors, pathogens and hosts. Antioxidants, 11, 1254. https://doi.org/10.3390/antiox11071254
  56. Hernandez, E. P., Kusakisako, K., Talactac, M. R., Galay, R. L., Hatta, T., Fujisaki, K., Tsuji, N., & Tanaka, T. (2018a). Characterization and expression analysis of a newly identified glutathione S-transferase of the hard tick Haemaphysalis longicornis during blood-feeding. Parasites & Vectors, 11, 91. https://doi.org/10.1186/s13071-018-2667-1
  57. Hernandez, E. P., Kusakisako, K., Talactac, M. R., Galay, R. L., Hatta, T., Matsuo, T., Fujisaki, K., Tsuji, N., & Tanaka, T. (2018b). Glutathione S-transferases play a role in the detoxification of flumethrin and chlorpyrifos in Haemaphysalis longicornis. Parasites & Vectors, 11, 460. https://doi.org/10.1186/s13071-018-3044-9
  58. Hernandez, E. P., Shimazaki, K., Niihara, K., Umemiya-Shirafuji, R., Fujisaki, K., & Tanaka, T. (2023). Localization of secreted ferritin (FER2) in the embryos of the tick Haemaphysalis longicornis. Parasites & Vectors, 16, 42. https://doi.org/10.1186/s13071-023-05669-5
  59. Hernandez, E. P., Talactac, M. R., Fujisaki, K., & Tanaka, T. (2019). The case for oxidative stress molecule involvement in the tick pathogen interactions – an omics approach. Developmental and Comparative Immunology, 100, 103409. https://doi.org/10.1016/j.dci.2019.103409
  60. Holmstrom, K. M., & Finkel, T. (2014). Cellular mechanisms and physiological consequences of redox-dependent signaling. Nature Reviews Molecular Cell Biology, 15, 411–421. https://doi.org/10.1038/nrm3801
  61. Hope, M., Menzies, M., & Kemp, D. (2010). Identification of a dieldrin resistance-associated mutation in Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Journal of Economic Entomology, 103, 1355–1359. https://doi.org/10.1603/ec09267
  62. Janadaree Bandara, K. M. U., & Parakrama Karunaratne, S. H. P. (2017). Mechanisms of acaricide resistance in the cattle tick Rhipicephalus (Boophilus) microplus in Sri Lanka. Pesticide Biochemistry and Physiology, 139, 68–72. https://doi.org/10.1016/j.pestbp.2017.05.002
  63. Junquera, P., Hosking, B., Gameiro, M., & Macdonald, A. (2019). Benzoylphenyl ureas as veterinary antiparasitics. An overview and outlook with emphasis on efficacy, usage and resistance. Parasite, 26, 26. https://doi.org/10.1051/parasite/2019026
  64. Jyoti, Singh, N. K., Singh, H., Singh, N. K., & Rath, S. S. (2016). Multiple mutations in the acetylcholinesterase 3 gene associated with organophosphate resistance in Rhipicephalus (Boophilus) microplus ticks from Punjab, India. Veterinary Parasitology, 216, 108–117. https://doi.org/10.1016/j.vetpar.2015.12.004
  65. Kostaropoulos, I., Papadopoulos, A. I., Metaxakis, A., Boukouvala, E., & Papadopoulou-Mourkidou, E. (2001). Glutathione S-transferase in the defence against pyrethroids in insects. Insect Biochemistry and Molecular Biology, 31, 313–319. https://doi.org/10.1016/s0965-1748(00)00123-5
  66. Kumar, D., Budachetri, K., Meyers, V. C., & Karim, S. (2016). Assessment of tick antioxidant responses to exogenous oxidative stressors and insight into the role of catalase in the reproductive fitness of the Gulf Coast tick, Amblyomma maculatum. Insect Biochemistry and Molecular Biology, 25(4), 283–294. https://doi.org/10.1111/imb.12218
  67. Kumar, D., Embers, M., Mather, T. N., & Karim, S. (2019). Is selenoprotein K required for Borrelia burgdorferi infection within the tick vector Ixodes scapularis?. Parasites & Vectors, 12, 289. https://doi.org/10.1186/s13071-019-3548-y
  68. Kumar, R., Klafke, G. M., & Miller, R. J. (2020a). Voltage-gated sodium channel gene mutations and pyrethroid resistance in Rhipicephalus microplus. Ticks and Tick-borne Diseases, 11, 101404. https://doi.org/10.1016/j.ttbdis.2020.101404
  69. Kumar, R., Sharma, A. K., & Ghosh, S. (2020b). Menace of acaricide resistance in cattle tick, Rhipicephalus microplus in India: Status and possible mitigation strategies. Veterinary Parasitology, 278, 108993. https://doi.org/10.1016/j.vetpar.2019.108993
  70. Kusakisako, K., Galay, R. L., Umemiya-Shirafuji, R., Hernandez, E. P., Maeda, H., Talactac, M. R., Tsuji, N., Mochizuki, M., Fujisaki, K., & Tanaka, T. (2016). 2-Cys peroxiredoxin is required in successful blood-feeding, reproduction, and antioxidant response in the hard tick Haemaphysalis longicornis. Parasites & Vectors, 9, 457. https://doi.org/10.1186/s13071-016-1748-2
  71. Lara, F. A., Lins, U., Paiva-Silva, G., Almeida, I. C., Braga, C. M., Miguens, F. C., Oliveira, P. L., & Dansa-Petretski, M. (2003). A new intracellular pathway of haem detoxification in the midgut of the cattle tick Boophilus microplus: Aggregation inside a specialized organelle, the hemosome. Journal of Experimental Biology, 206, 1707–1715. https://doi.org/10.1242/jeb.00334
  72. Le Gall, V. L., Klafke, G. M., & Torres, T. T. (2018). Detoxification mechanisms involved in ivermectin resistance in the cattle tick, Rhipicephalus (Boophilus) microplus. International Journal of Scientific Reports, 8, 12401. https://doi.org/10.1038/s41598-018-30907-7
  73. Li, A. Y., Davey, R. B., Miller, R. J., & George, J. E. (2003). Resistance to Coumaphos and Diazinon in Boophilus microplus (Acari: Ixodidae) and evidence for the involvement of an oxidative detoxification mechanism. Journal of Medical Entomology, 40, 482–490. https://doi.org/10.1603/0022-2585-40.4.482
  74. Li, R., Jia, Z., & Trush, M. A. (2016). Defining ROS in biology and medicine. The Reactive Oxygen Species (Apex), 1, 9–21. https://doi.org/10.20455/ros.2016.803
  75. Lima, V. L., Dias, F., Nunes, R. D., Pereira, L. O., Santos, T. S., Chiarini, L. B., Ramos, T. D., Silva-Mendes, B. J., Perales, J., Valente, R. H., & Oliveira, P. L. (2012). The antioxidant role of xanthurenic acid in the Aedes aegypti midgut during digestion of a blood meal. PLoS One, 7, e38349. https://doi.org/10.1371/journal.pone.0038349
  76. Maya-Monteiro, C. M., Daffre, S., Logullo, C., Lara, F. A., Alves, E. W., Capurro, M. L., Zingali, R., Almeida, I. C., & Oliveira, P. L. (2000). HeLp, a heme lipoprotein from the hemolymph of the cattle tick, Boophilus microplus. Journal of Biological Chemistry, 275, 36584–36589. https://doi.org/10.1074/jbc.M007344200
  77. Miller, A. F. (2012). Superoxide dismutases: Ancient enzymes and new insights. FEBS Letters, 586, 585–595. https://doi.org/10.1016/j.febslet.2011.10.048
  78. Miller, R. J., Davey, R. B., & George, J. E. (1999). Characterization of pyrethroid resistance and susceptibility to coumaphos in Mexican Boophilus microplus (Acari: Ixodidae). Journal of Medical Entomology, 36, 533–538. https://doi.org/10.1093/jmedent/36.5.533
  79. Morgan, J. A., Corley, S. W., Jackson, L. A., Lew-Tabor, A. E., Moolhuijzen, P. M., & Jonsson, N. N. (2009). Identification of a mutation in the para-sodium channel gene of the cattle tick Rhipicephalus (Boophilus) microplus associated with resistance to synthetic pyrethroid acaricides. International Journal for Parasitology, 39, 775–779. https://doi.org/10.1016/j.ijpara.2008.12.006
  80. Mounsey, K. E., Pasay, C. J., Arlian, L. G., Morgan, M. S., Holt, D. C., Currie, B. J., Walton, S. F., & McCarthy, J. S. (2010). Increased transcription of glutathione S-transferases in acaricide-exposed scabies mites. Parasites & Vectors, 3, 43. https://doi.org/10.1186/1756-3305-3-43
  81. Mugabi, K. N., Mugisha, A., & Ocaido, M. (2010). Socio-economic factors influencing the use of acaricides on livestock: A case study of the pastoralist communities of Nakasongola District, Central Uganda. Tropical Animal Health and Production, 42(1), 131–136. https://doi.org/10.1007/s11250-009-9396-6
  82. Nagar, G., Upadhaya, D., Sharma, A. K., Kumar, R., Fular, A., & Ghosh, S. (2021). Association between overexpression of cytochrome P450 genes and deltamethrin resistance in Rhipicephalus microplus. Ticks and Tick-borne Diseases, 12, 101610. https://doi.org/10.1016/j.ttbdis.2020.101610
  83. Nandi, A., Jyoti, Singh, H., & Singh, N. K. (2015). Esterase and glutathione S-transferase levels associated with synthetic pyrethroid resistance in Hyalomma anatolicum and Rhipicephalus microplus ticks from Punjab, India. Experimental and Applied Acarology, 66, 141–157. https://doi.org/10.1007/s10493-015-9884-5
  84. Nandi, A., Yan, L. J., Jana, C. K., & Das, N. (2019). Role of Catalase in Oxidative Stress- and Age-Associated Degenerative Diseases. Oxidative medicine and cellular longevity, 2019, 9613090. https://doi.org/10.1155/2019/9613090
  85. Narasimhan, S., Sukumaran, B., Bozdogan, U., Thomas, V., Liang, X., DePonte, K., Marcantonio, N., Koski, R. A., Anderson, J. F., Kantor, F., & Fikrig, E. (2007). A tick antioxidant facilitates the Lyme disease agent's successful migration from the mammalian host to the arthropod vector. Cell Host & Microbe, 2, 7–18. https://doi.org/10.1016/j.chom.2007.06.001
  86. Narasimhan, S., & Fikrig, E. (2015). Tick microbiome: The force within. Trends in Parasitology, 31, 315–323. https://doi.org/10.1016/j.pt.2015.03.010
  87. Nishinaka, Y., Masutani, H., Nakamura, H., & Yodoi, J. (2001). Regulatory roles of thioredoxin in oxidative stress-induced cellular responses. Redox Report, 6, 289–295. https://doi.org/10.1179/135100001101536427
  88. Nolan, J., Roulston, W. J., & Wharton, H. (1977). Resistance to synthetic pyrethroids in a DDT-resistant strain of Boophilus microplus. Pest Management Science, 8, 484–486. https://doi.org/10.1002/ps.2780080508
  89. Oliveira, J. H., Gonçalves, R. L., Lara, F. A., Dias, F. A., Gandara, A. C., Menna-Barreto, R. F., Edwards, M. C., Laurindo, F. R., Silva-Neto, M. A., Sorgine, M. H., & Oliveira, P. L. (2011). Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathogens, 7, e1001320. https://doi.org/10.1371/journal.ppat.1001320
  90. Oliveira, J. H. M., Talyuli, O. A. C., Goncalves, R. L. S., Paiva-Silva, G. O., Sorgine, M. H. F., Alvarenga, P. H., & Oliveira, P. L. (2017). Catalase protects Aedes aegypti from oxidative stress and increases midgut infection prevalence of Dengue but not Zika. PLOS Neglected Tropical Diseases, 11, e0005525. https://doi.org/10.1371/journal.pntd.0005525
  91. Oliveira, P. L., Kawooya, J. K., Ribeiro, J. M., Meyer, T., Poorman, R., Alves, E. W., Walker, F. A., Machado, E. A., Nussenzveig, R. H., & Padovan, G. J. (1995). A heme-binding protein from hemolymph and oocytes of the blood-sucking insect, Rhodnius prolixus: Isolation and characterization. Journal of Biological Chemistry, 270, 10897–10901. https://doi.org/10.1074/jbc.270.18.10897
  92. Oliver, S. V., & Brooke, B. D. (2016). The role of oxidative stress in the longevity and insecticide resistance phenotype of the major malaria vectors Anopheles arabiensis and Anopheles funestus. PLoS ONE, 11, e0151049. https://doi.org/10.1371/journal.pone.0151049
  93. O'Reilly, A. O., Williamson, M. S., González-Cabrera, J., Turberg, A., Field, L. M., Wallace, B. A., & Davies, T. G. (2014). Predictive 3D modelling of the interactions of pyrethroids with the voltage-gated sodium channels of ticks and mites. Pest Management Science, 70, 369–377. https://doi.org/10.1002/ps.3561
  94. Otali, D., Novak, R. J., Wan, W., Bu, S., Moellering, D. R., & De Luca, M. (2014). Increased production of mitochondrial reactive oxygen species and reduced adult lifespan in an insecticide-resistant strain of Anopheles gambiae. Bulletin of Entomological Research, 104, 323–333. https://doi.org/10.1017/S0007485314000091
  95. Paiva-Silva, G. O., Cruz-Oliveira, C., Nakayasu, E. S., Maya-Monteiro, C. M., Dunkov, B. C., Masuda, H., Almeida, I. C., & Oliveira, P. L. (2006). A heme-degradation pathway in a blood-sucking insect. Proceedings of the National Academy of Sciences, 103, 8030–8035. https://doi.org/10.1073/pnas.0602224103
  96. Pereira, L. O., Oliveira, P. L., Almeida, I. C., & Paiva-Silva, G. O. (2007). Biglutaminyl-biliverdin IX alpha as a heme degradation product in the dengue fever insect-vector Aedes aegypti. Biochemistry, 46, 6822–6829. https://doi.org/10.1021/bi700011d
  97. Perner, J., Sobotka, R., Sima, R., Konvickova, J., Sojka, D., Oliveira, P. L., Hajdusek, O., & Kopacek, P. (2016). Acquisition of exogenous haem is essential for tick reproduction. eLife, 5, e12318. https://doi.org/10.7554/eLife.12318
  98. Pfäffle, M., Littwin, N., Muders, S. V., & Petney, T. N. (2013). The ecology of tick-borne diseases. International Journal for Parasitology, 43, 1059–1077. https://doi.org/10.1016/j.ijpara.2013.06.009
  99. Pisoschi, A. M., & Pop, A. (2015). The role of antioxidants in the chemistry of oxidative stress: A review. European Journal of Medicinal Chemistry, 97, 55–74. https://doi.org/10.1016/j.ejmech.2015.04.040
  100. Rhee, S. G., Woo, H. A., Kil, I. S., & Bae, S. H. (2012). Peroxiredoxin functions as a peroxidase and a regulator and sensor of local peroxides. Journal of Biological Chemistry, 287, 4403–4410. https://doi.org/10.1074/jbc.R111.283432
  101. Rochlin, I. & Toledo, A. (2020). Emerging tick-borne pathogens of public health importance: a mini-review. Journal of Medical Microbiology, 69(6), 781–791. https://doi.org/10.1099/jmm.0.001206
  102. Rodriguez-Vivas, R. I., Jonsson, N. N., & Bhushan, C. (2018). Strategies for the control of Rhipicephalus microplus ticks in a world of conventional acaricide and macrocyclic lactone resistance. Parasitology Research, 117, 3–29. https://doi.org/10.1007/s00436-017-5677-6
  103. Sabadin, G. A., Parizi, L. F., Kiio, I., Xavier, M. A., da Silva Matos, R., Camargo-Mathias, M. I., Githaka, N. W., Nene, V., & da Silva Vaz, I. Jr. (2017). Effect of recombinant glutathione S-transferase as vaccine antigen against Rhipicephalus appendiculatus and Rhipicephalus sanguineus infestation. Vaccine, 35, 6649–6656. https://doi.org/10.1016/j.vaccine.2017.10.026
  104. Sabadin, G. A., Xavier, M. A., & Vaz Jr, I. S. (2019). Control of redox homeostasis in tick blood feeding. Acta Scientiae Veterinariae, 47, Article 89. https://doi.org/10.22456/1679-9216.94819
  105. Sabadin, G. A., Salomon, T. B., Leite, M. S., Benfato, M. S., Oliveira, P. L., & da Silva Vaz, I., Jr (2021). An insight into the functional role of antioxidant and detoxification enzymes in adult Rhipicephalus microplus female ticks. Parasitology International, 81, 102274. https://doi.org/10.1016/j.parint.2020.102274
  106. Saldivar, L., Guerrero, F. D., Miller, R. J., Bendele, K. G., Gondro, C., & Brayton, K. A. (2008). Microarray analysis of acaricide-inducible gene expression in the southern cattle tick, Rhipicephalus (Boophilus) microplus. Insect Molecular Biology, 17, 597–606. https://doi.org/10.1111/j.1365-2583.2008.00831.x
  107. Sangster, N. C. (2001). Managing parasiticide resistance. Veterinary Parasitology, 98, 89–109. https://doi.org/10.1016/s0304-4017(01)00425-3
  108. Saramago, L., Gomes, H., Aguilera, E., Cerecetto, H., González, M., Cabrera, M., Alzugaray, M. F., da Silva Vaz Junior, I., Nunes da Fonseca, R., Aguirre-López, B., Cabrera, N., Pérez-Montfort, R., Merlino, A., Moraes, J., & Álvarez, G. (2018). Novel and selective Rhipicephalus microplus triosephosphate isomerase inhibitors with acaricidal activity. Veterinary Sciences, 5, 74. https://doi.org/10.3390/vetsci5030074
  109. Sarıkaya, E., & Doğan, S. (2020). Glutathione peroxidase in health and diseases. In M. D. Bagatini (Ed.), Glutathione system and oxidative stress in health and disease (pp. 49). London: IntechOpen. https://doi.org/10.5772/intechopen.91009
  110. Sheehan, D., Meade, G., Foley, V. M., & Dowd, C. A. (2001). Structure, function and evolution of glutathione transferases: Implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochemical Journal, 360, 1–16. https://doi.org/10.1042/0264-6021:3600001
  111. Shyma, K. P., Kumar, S., Sharma, A. K., Ray, D. D., & Ghosh, S. (2012). Acaricide resistance status in Indian isolates of Hyalomma anatolicum.  Experimental & applied acarology, 58(4), 471–481. https://doi.org/10.1007/s10493-012-9592-3
  112. Sojka, D., Franta, Z., Horn, M., Caffrey, C. R., Mareš, M., & Kopáček, P. (2013). New insights into the machinery of blood digestion by ticks. Trends in Parasitology, 29, 276–285. https://doi.org/10.1016/j.pt.2013.04.002
  113. Sojka, D., Pytelková, J., Perner, J., Horn, M., Konvičková, J., Schrenková, J., Mareš, M., & Kopáček, P. (2016). Multienzyme degradation of host serum albumin in ticks. Ticks and Tick-borne Diseases, 7(4), 604–613. https://doi.org/10.1016/j.ttbdis.2015.12.014
  114. Stone, N. E., Olafson, P. U., Davey, R. B., Buckmeier, G., Bodine, D., Sidak-Loftis, L. C., Giles, J. R., Duhaime, R., Miller, R. J., Mosqueda, J., Scoles, G. A., Wagner, D. M., & Busch, J. D. (2014). Multiple mutations in the para-sodium channel gene are associated with pyrethroid resistance in Rhipicephalus microplus from the United States and Mexico. Parasites and Vectors, 7, 456. https://doi.org/10.1186/s13071-014-0456-z
  115. Takata, M., Misato, S., Ozoe, F., & Ozoe, Y. (2020). A point mutation in the β-adrenergic-like octopamine receptor: Possible association with amitraz resistance. Pest Management Science, 76, 3720–3728. https://doi.org/10.1002/ps.5921
  116. Talalay, P. (2000). Chemoprotection against cancer by induction of phase 2 enzymes. Biofactors, 12(1–4), 5–11. https://doi.org/10.1002/biof.5520120102
  117. Tavares, C. P., Sabadin, G. A., Sousa, I. C., Gomes, M. N., Soares, A. M. S., Monteiro, C. M. O., Vaz, I. S. Jr., & Costa-Junior, L. M. (2022). Effects of carvacrol and thymol on the antioxidant and detoxifying enzymes of Rhipicephalus microplus (Acari: Ixodidae). Ticks and Tick-borne Diseases, 13(3), Article 101929. https://doi.org/10.1016/j.ttbdis.2022.101929
  118. Taylor, D.J., (2006). Innate immunity in ticks: a review. Journal of the Acarological Society of Japan, 15, 109–127. [A1] 
  119. Temeyer, K. B., Davey, R. B., & Chen, A. C. (2004). Identification of a third Boophilus microplus (Acari: Ixodidae) cDNA presumptively encoding an acetylcholinesterase. Journal of Medical Entomology, 41, 259–268. https://doi.org/10.1603/0022-2585-41.3.259
  120. Temeyer, K. B., Pruett, J. H., Olafson, P. U., & Chen, A. C. (2007). R86Q, a mutation in BmAChE3 yielding a Rhipicephalus microplus organophosphate-insensitive acetylcholinesterase. Journal of Medical Entomology, 44, 1013–1018. https://doi.org/10.1603/0022-2585(2007)44[1013:ramiby]2.0.co;2
  121. Thorpe, G. W., Fong, C. S., Alic, N., Higgins, V. J., & Dawes, I. W. (2004). Cells have distinct mechanisms to maintain protection against different reactive oxygen species: Oxidative stress-response genes. Proceedings of the National Academy of Sciences of the United States of America, 101, 6564–6569. https://doi.org/10.1073/pnas.0305888101
  122. Untalan, P. M., Guerrero, F. D., Haines, L. R., & Pearson, T. W. (2005). Proteome analysis of abundantly expressed proteins from unfed larvae of the cattle tick, Boophilus microplus. Insect Biochemistry and Molecular Biology, 35, 141–151. https://doi.org/10.1016/j.ibmb.2004.10.009
  123. Whitehead, G. B. (1961). Investigation of the mechanism of resistance to sodium arsenite in the blue tick, Boophilus decoloratus Koch. Journal of Insect Physiology, 7, 177–185. https://doi.org/10.1016/0022-1910(61)90070-1
  124. Whiten, S. R., Eggleston, H., & Adelman, Z. N. (2018). Ironing out the details: Exploring the role of iron and heme in blood-sucking arthropods. Frontiers in Physiology, 8, 1134. https://doi.org/10.3389/fphys.2017.01134
  125. Yu, Z., Wang, R., Zhang, T., Wang, T., Nwanade, C. F., Pei, T., Bai, R., Wang, Z., & Liu, J. (2023). The genome-wide characterization and associated cold-tolerance function of the superoxide dismutase in the cold response of the tick Haemaphysalis longicornis. Pesticide Biochemistry and Physiology, 195, Article 105573. https://doi.org/10.1016/j.pestbp.2023.105573
  126. Zoidis, E., Seremelis, I., Kontopoulos, N., & Danezis, G. P. (2018). Selenium-dependent antioxidant enzymes: Actions and properties of selenoproteins. Antioxidants, 7, 66. https://doi.org/10.3390/antiox7050066

Tools


Copyright © 2025  KITE Digital Educational Solutions |  Exclusively distributed by CE-Logic