Clinical Pathology, Immunopathology and Advanced Vaccine Technology in Bovine Theileriosis: A Review
Abstract
:1. Bovine Theileriosis
2. Clinical Pathology of Theileria-Infected Cattle
2.1. Complete Blood Cell Count and Coagulation Profile
2.2. Biochemical Profile and Urinalysis
3. Pathophysiological Mechanisms of Anaemia in Bovine Theileriosis
3.1. Anaemia in Oriental Theileriosis
3.2. Anaemia in East Coast Fever
4. Immune Response and Immunopathology in T. parva and T. annulata Infections
4.1. Innate and Adaptive Immune Responses in Theileria Species Infection
4.2. Immunopathogenesis in Cattle Tropical Theileriosis
4.3. Immunopathogenesis in East Coast Fever
5. Diagnosis of Bovine Theileriosis
6. Immunization against Bovine Theileriosis and Advanced Vaccine Technology
6.1. Theileria Vaccines under Evaluation
6.2. DNA Vaccines
7. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Ota, N.; Mizuno, D.; Kuboki, N.; Igarashi, I.; Nakamura, Y.; Yamashina, H.; Hanzaike, T.; Fujii, K.; Onoe, S.; Hata, H.; et al. Epidemiological survey of Theileria orientalis infection in grazing cattle in the eastern part of Hokkaido, Japan. J. Vet. Med. Sci. 2009, 71, 937–944. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Adjou Moumouni, P.F.; Aboge, G.O.; Terkawi, M.A.; Masatani, T.; Cao, S.; Kamyingkird, K.; Jirapattharasate, C.; Zhou, M.; Wang, G.; Liu, M.; et al. Molecular detection and characterization of Babesia bovis, Babesia bigemina, Theileria species and Anaplasma marginale isolated from cattle in Kenya. Parasites Vectors 2015, 8, 496. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kho, K.L.; Amarajothi, A.D.G.; Koh, F.X.; Panchadcharam, C.; Hassan Nizam, Q.N.; Tay, S.T. The first molecular survey of theileriosis in Malaysian cattle, sheep and goats. Vet. Parasitol. Reg. Stud. Rep. 2017, 10, 149–153. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hassan, M.A.; Liu, J.; Rashid, M.; Iqbal, N.; Guan, G.; Yin, H.; Luo, J. Molecular survey of piroplasm species from selected areas of China and Pakistan. Parasites Vectors 2018, 11, 1–7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mohamed, S.B.; Alagib, A.; AbdElkareim, T.B.; Hassan, M.M.; Johnson, W.C.; Hussein, H.E.; Taus, N.S.; Ueti, M.W. Molecular detection and characterization of Theileria spp. infecting cattle in Sennar State, Sudan. Parasitol. Res. 2018, 117, 1271–1276. [Google Scholar] [CrossRef] [Green Version]
- Rajendran, C.; Ray, D.D. Diagnosis of tropical bovine theileriosis by ELISA with recombinant merozoite surface protein of Theileria annulata (Tams1). J. Parasit. Dis. 2014, 38, 41–45. [Google Scholar] [CrossRef] [Green Version]
- Vollmer, D. Enhancing the Effectiveness of Sustainability Partnerships: Summary of a Workshop; The National Academies Press: Washington, DC, USA, 2009. [Google Scholar]
- Bishop, R.; Musoke, A.; Morzaria, S.; Gardner, M.; Nene, V. Theileria: Intracellular protozoan parasites of wild and domestic ruminants transmitted by ixodid ticks. Parasitology 2004, 129, S271–S283. [Google Scholar] [CrossRef]
- Cao, S.; Zhang, S.; Jia, L.; Xue, S.; Yu, L.; Kamyingkird, K.; Moumouni, P.F.; Moussa, A.A.; Zhou, M.; Zhang, Y.; et al. Molecular detection of Theileria species in sheep from northern China. J. Vet. Med. Sci. 2013, 75, 1227–1230. [Google Scholar] [CrossRef] [Green Version]
- Anupama, R.; Srinivasan, S.R.; Parthiban, M. Molecular studies on theileriosis and identification of Theileria orientalis in India using PCR. Indian Vet. J. 2015, 92, 9–11. [Google Scholar]
- Mohd Hasan, L.I.; Kho, K.L.; Koh, F.X.; Hassan Nizam, Q.N.; Tay, S.T. Molecular evidence of hemoplasmas in Malaysian cattle and ticks. Trop. Biomed. 2017, 34, 668–674. [Google Scholar]
- Ola-Fadunsin, S.D.; Maizatul, A.M.; Ibrahim, A.R.; Amlizawathy, A.; Chandrawathani, P.; Jesse, F.F.A.; Sani, R.A.; Sharma, R.S.K. Molecular Prevalence and Species Co-Infection of Bovine Haemoparasites in Peninsular Malaysia. Malaysian J. Vet. Res. 2017, 8, 13–22. [Google Scholar]
- Sivakumar, T.; Fujita, S.; Tuvshintulga, B.; Kothalawala, H.; Silva, S.S.P.; Yokoyama, N. Discovery of a new Theileria sp. closely related to Theileria annulata in cattle from Sri Lanka. Sci. Rep. 2019, 9, 1–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gou, H.; Guan, G.; Ma, M.; Liu, A.; Liu, Z.; Xu, Z.; Ren, Q.; Li, Y.; Yang, J.; Chen, Z.; et al. Phylogenetic analysis of ruminant Theileria spp. from China based on 28S ribosomal RNA gene. Korean J. Parasitol. 2013, 51, 511–517. [Google Scholar] [CrossRef]
- Sivakumar, T.; Hayashida, K.; Sugimoto, C.; Yokoyama, N. Evolution and genetic diversity of Theileria. Infect. Genet. Evol. 2014, 27, 250–263. [Google Scholar] [CrossRef] [Green Version]
- Gubbels, M.J.; Yin, H.; Bai, Q.; Liu, G.; Nijman, I.J.; Jongejan, F. The phylogenetic position of the Theileria buffeli group in relation to other Theileria species. Parasitol. Res. 2000, 88, S28–S32. [Google Scholar] [CrossRef] [PubMed]
- Liu, A.H.; Guan, G.Q.; Liu, J.L.; Liu, Z.J.; Leblanc, N.; Li, Y.Q.; Gao, J.L.; Ma, M.L.; Niu, Q.L.; Ren, Q.Y.; et al. Polymorphism Analysis of Chinese Theileria sergenti Using Allele-Specific Polymerase Chain Reaction of the Major Piroplasm Surface Protein Gene. J. Parasitol. 2011, 97, 116–121. [Google Scholar] [CrossRef] [PubMed]
- von Schubert, C.; Xue, G.; Schmuckli-Maurer, J.; Woods, K.L.; Nigg, E.A.; Dobbelaere, D.A.E. The transforming parasite Theileria Co-opts host cell mitotic and central spindles to persist in continuously dividing cells. PLoS Biol. 2010, 8. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shaw, M.K. Theileria development and host cell invasion. In World Class Parasites, Theileria; Dobbelaere, D., McKeever, D., Eds.; Kluwer Academic Publishers: Boston, MA, USA; London, UK, 2002; pp. 1–22. [Google Scholar]
- McKeever, D.J. Bovine immunity—A driver for diversity in Theileria parasites? Trends Parasitol. 2009, 25, 269–276. [Google Scholar] [CrossRef]
- Watts, J.G.; Playford, M.C.; Hickey, K.L. Theileria orientalis: A review. N. Z. Vet. J. 2016, 64, 3–9. [Google Scholar] [CrossRef]
- Hayashida, K.; Kajino, K.; Hattori, M.; Wallace, M.; Morrison, I.; Greene, M.I.; Sugimoto, C. MDM2 regulates a novel form of incomplete neoplastic transformation of Theileria parva infected lymphocytes. Exp. Mol. Pathol. 2013, 94, 228–238. [Google Scholar] [CrossRef] [Green Version]
- Tretina, K.; Gotia, H.T.; Mann, D.J.; Silva, J.C. Theileria-transformed bovine leukocytes have cancer hallmarks. Trends Parasitol. 2015, 31, 306–314. [Google Scholar] [CrossRef] [PubMed]
- Eamens, G.J.; Gonsalves, J.R.; Jenkins, C.; Collins, D.; Bailey, G. Theileria orientalis MPSP types in Australian cattle herds associated with outbreaks of clinical disease and their association with clinical pathology findings. Vet. Parasitol. 2013, 191, 209–217. [Google Scholar] [CrossRef]
- Khatoon, S.; Kolte, S.W.; Kurkure, N.V.; Chopde, N.A.; Jahan, A. Detection of tropical bovine theileriosis by polymerase chain reaction in cattle. J. Parasit. Dis. 2013, 39, 53–56. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lawrence, J.A.; Perry, B.D.; Williamson, S.M. Corridor disease. In Infectious Disease of Livestock; Coetzer, J.A.W., Tustin, R.C., Eds.; Oxford University Press: Cape Town, South Africa, 2004; pp. 468–471. [Google Scholar]
- Morrison, W.I.; Hemmink, J.D.; Toye, P.G. Theileria parva: A parasite of African buffalo, which has adapted to infect and undergo transmission in cattle. Int. J. Parasitol. 2020, 50, 403–412. [Google Scholar] [CrossRef] [PubMed]
- Latif, A.A.; Troskie, P.C.; Peba, S.B.; Maboko, B.B.; Pienaar, R.; Mans, B.J. Corridor disease (buffalo-associated Theileria parva) outbreak in cattle introduced onto a game ranch and investigations into their carrier-state. Vet. Parasitol. Reg. Stud. Reports 2019, 18, 100331. [Google Scholar] [CrossRef] [PubMed]
- Mbizeni, S.; Potgieter, F.T.; Troskie, C.; Mans, B.J.; Penzhorn, B.L.; Latif, A.A. Field and laboratory studies on Corridor disease (Theileria parva infection) in cattle population at the livestock/game interface of uPhongolo-Mkuze area, South Africa. Ticks Tick. Borne. Dis. 2013, 4, 227–234. [Google Scholar] [CrossRef]
- Mekata, H.; Minamino, T.; Mikurino, Y.; Yamamoto, M.; Yoshida, A.; Nonaka, N.; Horii, Y. Evaluation of the natural vertical transmission of Theileria orientalis. Vet. Parasitol. 2018, 263, 1–4. [Google Scholar] [CrossRef]
- Junlong, L.; Li, Y.; Liu, A.; Guan, G.; Xie, J.; Yin, H.; Luo, J. Development of a multiplex PCR assay for detection and discrimination of Theileria annulata and Theileria sergenti in cattle. Parasitol. Res. 2015, 114, 2715–2721. [Google Scholar] [CrossRef]
- Al-Deeb, M.A.; Muzaffar, S.B.; Abu-Zeid, Y.A.; Enan, M.R.; Karim, S. First Record of a Spotted Fever Group Rickettsia sp. and Theileria annulata in Hyalomma dromedarii (Acari: Ixodidae) Ticks in the United Arab Emirates. Fla. Entomol. 2015, 98, 135–139. [Google Scholar] [CrossRef]
- Gomes, J.; Salgueiro, P.; Inácio, J.; Amaro, A.; Pinto, J.; Tait, A.; Shiels, B.; Pereira da Fonseca, I.; Santos-Gomes, G.; Weir, W. Population diversity of Theileria annulata in Portugal. Infect. Genet. Evol. 2016, 42, 14–19. [Google Scholar] [CrossRef] [Green Version]
- El-Dakhly, K.M.; Arafa, W.; Ghanem, S.S.; Abdel-Fatah, O.R.; Wahba, A.A. Microscopic and Molecular Detection of Theileria annulata Infection of Cattle in Egypt. J. Adv. Parasitol. 2018, 5, 29–34. [Google Scholar] [CrossRef] [Green Version]
- Mohammed-Ahmed, G.M.; Hassan, S.M.; El Hussein, A.M.; Salih, D.A. Molecular, serological and parasitological survey of Theileria annulata in North Kordofan State, Sudan. Vet. Parasitol. Reg. Stud. Rep. 2018, 13, 24–29. [Google Scholar] [CrossRef] [PubMed]
- Mbassa, G.K.; Balemba, O.; Maselle, R.M.; Mwaga, N.V. Severe anaemia due to haematopoietic precursor cell destruction in field cases of East Coast Fever in Tanzania. Vet. Parasitol. 1994, 52, 243–256. [Google Scholar] [CrossRef]
- Mbassa, G.K.; Kipanyula, M.J.; Mellau, L.S.B.; Mwamakali, E.D.; Bulegeya, F.R.; Kauto-Mboni, K. Theileria parva infection in calves causes massive lymphocyte death in the thymus, spleen and lymph nodes without initial proliferation. Vet. Parasitol. 2006, 142, 260–270. [Google Scholar] [CrossRef]
- Kabi, F.; Masembe, C.; Muwanika, V.; Kirunda, H.; Negrini, R. Geographic distribution of non-clinical Theileria parva infection among indigenous cattle populations in contrasting agro-ecological zones of Uganda: Implications for control strategies. Parasite Vectors 2014, 7, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Liu, A.; Guan, G.; Liu, Z.; Liu, J.; Leblanc, N.; Li, Y.; Gao, J.; Ma, M.; Niu, Q.; Ren, Q.; et al. Detecting and differentiating Theileria sergenti and Theileria sinensis in cattle and yaks by PCR based on major piroplasm surface protein (MPSP). Exp. Parasitol. 2010, 126, 476–481. [Google Scholar] [CrossRef]
- Hammer, J.F.; Jenkins, C.; Bogema, D.; Emery, D. Mechanical transfer of Theileria orientalis: Possible roles of biting arthropods, colostrum and husbandry practices in disease transmission. Parasit. Vectors 2016, 9, 1DUMMMY. [Google Scholar] [CrossRef] [Green Version]
- Kim, S.; Yu, D.H.; Kang, S.W.; Chae, J.B.; Choi, K.S.; Kim, H.C.; Park, B.K.; Chae, J.S.; Park, J. Hematological changes associated with Theileria orientalis infection in Korean indigenous cattle. Korean J. Parasitol. 2017, 55, 481–489. [Google Scholar] [CrossRef] [Green Version]
- Lawrence, K.E.; Forsyth, S.F.; Vaatstra, B.L.; McFadden, A.M.J.; Pulford, D.J.; Govindaraju, K.; Pomroy, W.E. Clinical haematology and biochemistry profiles of cattle naturally infected with Theileria orientalis Ikeda type in New Zealand. N. Z. Vet. J. 2018, 66, 21–29. [Google Scholar] [CrossRef]
- Kakati, P.; Sarmah, P.C.; Ray, D.; Bhattacharjee, K.; Sharma, R.K.; Barkalita, L.M.; Sarma, D.K.; Baishya, B.C.; Borah, P.; Stanley, B. Emergence of oriental theileriosis in cattle and its transmission through Rhipicephalus (Boophilus) microplus in Assam, India. Vet. World 2015, 8, 1099–1104. [Google Scholar] [CrossRef]
- Gebrekidan, H.; Gasser, R.B.; Baneth, G.; Yasur-Landau, D.; Nachum-Biala, Y.; Hailu, A.; Jabbar, A. Molecular characterization of Theileria orientalis from cattle in Ethiopia. Ticks Tick. Borne. Dis. 2016, 7, 742–747. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gebrekidan, H.; Nelson, L.; Smith, G.; Gasser, R.B.; Jabbar, A. An outbreak of oriental theileriosis in dairy cattle imported to Vietnam from Australia. Parasitology 2017, 144, 738–746. [Google Scholar] [CrossRef] [PubMed]
- Ola-Fadunsin, S.D.; Sharma, R.S.K.; Abdullah, D.A.; Gimba, F.I.; Jesse, F.F.A.; Sani, R.A. Molecular detection, prevalence and risk factors of Theileria orientalis infection among cattle in Peninsular Malaysia. Prev. Vet. Med. 2020, 180, 105027. [Google Scholar] [CrossRef] [PubMed]
- Minami, T.; Fujinaga, T.; Furuya, K.; Ishihara, T. Clinico-hematologic and serological comparison of Japanese and Russian strains of Theileria sergenti. Natl. Inst. Anim. Health Q. (Tokyo) 1980, 20, 44–52. [Google Scholar] [PubMed]
- Papadopoulos, B.; Perié, N.M.; Uilenberg, G. Piroplasms of domestic animals in the Macedonia region of Greece. 1. Serological cross-reactions. Vet. Parasitol. 1996, 63, 41–56. [Google Scholar] [CrossRef]
- Savini, G.; Onuma, M.; Scaramozzino, P.; Kakuda, T.; Semproni, G.; Langella, V. First report of Theileria sergenti and T. buffeli/orientalis in cattle in Italy. Ann. N. Y. Acad. Sci. 1998, 849, 404–407. [Google Scholar] [CrossRef]
- García-Sanmartín, J.; Nagore, D.; García-Pérez, A.L.; Juste, R.A.; Hurtado, A. Molecular diagnosis of Theileria and Babesia species infecting cattle in Northern Spain using reverse line blot macroarrays. BMC Vet. Res. 2006, 2, 16. [Google Scholar] [CrossRef] [Green Version]
- Gomes, J.; Soares, R.; Santos, M.; Santos-Gomes, G.; Botelho, A.; Amaro, A.; Inácio, J. Detection of Theileria and Babesia infections amongst asymptomatic cattle in Portugal. Ticks Tick. Borne. Dis. 2013, 4, 148–151. [Google Scholar] [CrossRef]
- Hornok, S.; Mester, A.; Takács, N.; Fernández De Mera, I.G.; De La Fuente, J.; Farkas, R. Re-emergence of bovine piroplasmosis in Hungary: Has the etiological role of Babesia divergens been taken over by B. major and Theileria buffeli? Parasites Vectors 2014, 7, 1–4. [Google Scholar] [CrossRef] [Green Version]
- De Vos, A.J.; Roos, J.A. The isolation of Theileria taurotragi in South Africa. Onderstepoort J. Vet. Res. 1981, 48, 149–153. [Google Scholar]
- Jongejan, F.; Musisi, F.L.; Moorhouse, P.D.S.; Snacken, M.; Uilenberg, G. Theileria taurotragi in Zambia. Vet. Q. 1986, 8, 261–263. [Google Scholar] [CrossRef] [PubMed]
- Katende, J.M.; Goddeeris, B.M.; Morzaria, S.P.; Nkonge, C.G.; Musoke, A.J. Identification of a Theileria mutans-specific antigen for use in an antibody and antigen detection ELISA. Parasite Immunol. 1990, 12, 419–433. [Google Scholar] [CrossRef] [PubMed]
- Gebrekidan, H.; Hailu, A.; Kassahun, A.; Rohoušová, I.; Maia, C.; Talmi-Frank, D.; Warburg, A.; Baneth, G. Theileria infection in domestic ruminants in northern Ethiopia. Vet. Parasitol. 2014, 200, 31–38. [Google Scholar] [CrossRef] [PubMed]
- Alonso, M.; Camus, E.; Rodriguez Diego, J.; Bertaudiere, L.C.; Tatareau, J.; Liabeuf, J.M. Current status of bovine haemoparasitic diseases in Martinique (French West Indies). Rev. d’Elevage Med. Vet. Des Pays Trop. 1992, 45, 9–14. [Google Scholar]
- Uilenberg, G.; Camus, E.; Barre, N. Existence of Theileria mutans andTheileria velifera (Sporozoa, Theileriidae) inGuadeloupe (French West Indies). Rev. d’Elevage M´edecine V´et´erinaire Des Pays Trop. 1983, 36, 261–264. [Google Scholar]
- Chaisi, M.E.; Collins, N.E.; Potgieter, F.T.; Oosthuizen, M.C. Sequence variation identified in the 18S rRNA gene of theileria mutans and theileria velifera from the african buffalo (syncerus caffer). Vet. Parasitol. 2013, 191, 132–137. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bai, Q.; Liu, G.; Yin, H.; Zhao, Q.; Liu, D.; Ren, J.; Li, X. Theileria sinensis sp nov: A new species of bovine Theileria—Molecular taxonomic studies. Xu Mu Shou Yi Xue Bao 2002, 33, 185–190. [Google Scholar]
- Bursakov, S.A.; Kovalchuk, S.N. Co-infection with tick-borne disease agents in cattle in Russia. Ticks Tick. Borne. Dis. 2019, 10. [Google Scholar] [CrossRef]
- Agina, O.A.; Mohd Rosly, S.; Nur Mahiza, I.; Mokrish, A.; Zamri-Saad, M.; Mazlina, M.; Azim- Salahuddin, M.; Afrah, A.K.; Lee, C.H.; Fairuz, H.R.; et al. First report of bovine anaemia associated Theileria sinensis infection and phylogenetic analyses of partial gene sequences of Theileria and Anaplasma species detected in naturally infected Malaysian cattle. Parasites Vectors 2020. Preprint. [Google Scholar] [CrossRef] [Green Version]
- Baek, B.K.; Soo, K.B.; Kim, J.H.; Hur, J.; Lee, B.O.; Jung, J.M.; Onuma, M.; Oluoch, A.O.; Kim, C.-H.; Kakoma, I. Verification by polymerase chain reaction of vertical transmission of Theileria sergenti in cows. Can. J. Vet. Res. 2003, 67, 278–282. [Google Scholar]
- Perera, P.K.; Gasser, R.B.; Firestone, S.M.; Anderson, G.A.; Malmo, J.; Davis, G.; Beggs, D.S.; Jabbar, A. Oriental theileriosis in dairy cows causes a significant milk production loss. Parasites Vectors 2014, 7, 73. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gebrekidan, H.; Perera, P.K.; Ghafar, A.; Abbas, T.; Gasser, R.B.; Jabbar, A. An appraisal of oriental theileriosis and the Theileria orientalis complex, with an emphasis on diagnosis and genetic characterisation. Parasitol. Res. 2020, 119, 11–22. [Google Scholar] [CrossRef] [PubMed]
- Izzo, M.M.; Poe, I.; Horadagoda, N.; De Vos, A.J.; House, J.K. Haemolytic anaemia in cattle in NSW associated with Theileria infections. Aust. Vet. J. 2010, 88, 45–51. [Google Scholar] [CrossRef] [PubMed]
- Jenkins, C.; Bogema, D.R. Factors associated with seroconversion to the major piroplasm surface protein of the bovine haemoparasite Theileria orientalis. Parasites Vectors 2016, 9, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Hayashida, K.; Umemiya-Shirafuji, R.; Sivakumar, T.; Yamagishi, J.; Suzuki, Y.; Sugimoto, C.; Yokoyama, N. Establishment of a mouse-tick infestation model for Theileria orientalis and analysis of its transcriptome. Int. J. Parasitol. 2018, 48, 915–924. [Google Scholar] [CrossRef]
- Sugimoto, C.; Fujisaki, K. Non-transforming Theileria parasites of ruminants. In Theileria (World Class Parasites); Dobbelaere, D., McKeever, D., Eds.; Kluwer Academic Publishers: Boston, MA, USA; London, UK, 2002; Volume 3, pp. 93–106. [Google Scholar]
- Shimizu, S.; Yoshiura, N.; Mizomoto, T.; Kondou, Y. Theileria sergenti infection in dairy cattle. J. Vet. Med. Sci. 1992, 54, 375–377. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Çöl, R.; Uslu, U. Haematological and coagulation profiles during severe tropical theileriosis in cattle. Turkish J. Vet. Anim. Sci. 2006, 30, 577–582. [Google Scholar]
- Somu, Y.; Mani, S.; Muthusamy, R.; Mani, S.; Thangamani, A.; Konappan, J.; Muthusamy, V.; Subbaih, K.K.; Palanisamy, S. Haemato- Biochemical and Electrolyte Alterations in Naturally Occurring Theileria Associated Bovine Anaemia (Taba). J. Anim. Health Prod. 2017, 5, 64–67. [Google Scholar] [CrossRef]
- Razavi, S.M.; Nazifi, S.; Emadi, M.; Rakhshandehroo, E. The correlations among serum tumor necrosis factor-α (TNF-α), interferon-γ (IFN-γ) and sialic acids with peripheral lymphocytes in bovine tropical theileriosis. Vet. Res. Commun. 2010, 34, 579–587. [Google Scholar] [CrossRef]
- Tolouei Kaleibar, M.; Ashrafi Helan, J.; Fathi, E. Occurrence of congenital cerebral theileriosis in a newborn twin Holstein calves in Iran: Case report. Vet. Res. Forum Int. Q. J. 2014, 5, 237–241. [Google Scholar]
- Osman, S.A.; AL-Gaabary, M. Clinical, haematological and therapeutic studies on tropical theileriosis in water buffaloes (Bulbalus bulbalis) in Egypt. Vet. Parasitol. 2007, 146, 334–337. [Google Scholar] [CrossRef] [PubMed]
- El-Deeb, W.M.; Younis, E.E. Clinical and biochemical studies on Theileria annulata in Egyptian buffaloes (Bubalus bubalis) with particular orientation to oxidative stress and ketosis relationship. Vet. Parasitol. 2009, 164, 301–305. [Google Scholar] [CrossRef] [PubMed]
- Stockham, S.L.; Kjemtrup, A.M.; Conrad, P.A.; Schmidt, D.A.; Scott, M.A.; Robinson, T.W.; Tyler, J.W.; Johnson, G.C.; Carson, C.A.; Cuddihee, P. Theileriosis in a Missouri Beef Herd Caused by Theileria buffeli: Case Report, Herd Investigation, Ultrastructure, Phylogenetic Analysis, and Experimental Transmission. Vet. Pathol. 2000, 37, 11–21. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, S.; Yu, D.H.; Chae, J.B.; Choi, K.S.; Kim, H.C.; Park, B.K.; Chae, J.S.; Park, J. Pathogenic genotype of major piroplasm surface protein associated with anemia in Theileria orientalis infection in cattle. Acta Vet. Scand. 2017, 1–5. [Google Scholar] [CrossRef] [Green Version]
- Haron, A.; Jesse, F.; Ahmed, S.; Abba, Y.; Mohammed, K.; Tijjani, A.; Adamu, L.; Sadiq, M. Detection of Theileria spp and Hematological Profiles of Infected Cattle from Selected Farms in Selangor, Malaysia. Alexandria J. Vet. Sci. 2015, 44, 9. [Google Scholar] [CrossRef]
- Omer, O.H.; El-Malik, K.H.; Mahmoud, O.M.; Haroun, E.M.; Hawas, A.; Sweeney, D.; Magzoub, M. Haematological profiles of pure bred cattle naturally infected with Theileria annulata in Saudi Arabia. Vet. Parasitol. 2002, 107, 161–168. [Google Scholar] [CrossRef]
- Ghanem, M.M.; Abdelhamid, O.M.; Bakir, N.M. Clinico-biochemical, serological and molecular study on tropical theileriosis in Egyptian water buffaloes. Alexandria J. Vet. Sci. 2013, 39, 1–11. [Google Scholar]
- El-Deeb, W.M.; Iacob, O.C. Serum acute phase proteins in control and Theileria annulata infected water buffaloes (Bubalus bubalis). Vet. Parasitol. 2012, 190, 12–18. [Google Scholar] [CrossRef]
- Tindih, H.S.; Marcotty, T.; Naessens, J.; Goddeeris, B.M.; Geysen, D. Demonstration of differences in virulence between two Theileria parva isolates. Vet. Parasitol. 2010, 168, 223–230. [Google Scholar] [CrossRef]
- Nazifi, S.; Razavi, S.M.; Mansourian, M.; Nikahval, B.; Moghaddam, M. Studies on correlations among parasitaemia and some hemolytic indices in two tropical diseases (theileriosis and anaplasmosis) in Fars province of Iran. Trop. Anim. Health Prod. 2008, 40, 47–53. [Google Scholar] [CrossRef]
- Kunugiyama, I.; Yagi, Y.; Ito, N. Decrease in erythrocyte survival in Theileria sergenti-infected calves determined by non-radioactive chromium labelling method. Jpn. Soc. Vet. Sci. 1991, 53, 391–394. [Google Scholar]
- Shiono, H.; Yagi, Y.; Thongnoon, P.; Kurabayashi, N.; Chikayama, Y.; Miyazaki, S.; Nakamura, I. Acquired methemoglobinemia in anemic cattle infected with Theileria sergenti. Vet. Parasitol. 2001, 102, 45–51. [Google Scholar] [CrossRef]
- Jalali, S.M.; Ghorbanpour, M.; Jalali, M.R.; Rasooli, A.; Safaie, P.; Norvej, F.; Delavari, I. Occurrence and potential causative factors of immune-mediated hemolytic anemia in cattle and river buffaloes. Vet. Res. Forum 2018, 9, 7–12. [Google Scholar] [PubMed]
- Hagiwara, K.; Tsuji, M.; Ishihara, C.; Tajima, M.; Kurosawa, T.; Takahashi, K. Serum from Theileria sergenti-infected cattle accelerates the clearance of bovine erythrocytes in SCID mice. Parasitol. Res. 1995, 81, 470–474. [Google Scholar] [CrossRef] [PubMed]
- Seitzer, U.; Ahmed, J. Tropical theileriosis: Cytotoxic T lymphocyte response to vaccination. Vaccine 2008, 265, G24–G28. [Google Scholar] [CrossRef]
- Fearson, D.; Locksley, R. The instructive role of innate immunity in the acquired immune response. Science 1996, 272, 50–54. [Google Scholar] [CrossRef]
- Preston, P.; Hall, R.; Glass, E.; Campbell, J.; Darghouth, M.; Ahmed, J.; Shiels, B.; Spooner, R.; Brown, D.; Jongejan, F. Innate and adaptive immune responses co-operate to protect cattle against Theileria annulata. Parasitol. Today 1999, 15, 268–274. [Google Scholar] [CrossRef]
- Ahmed, J.S.; Mehlhorn, H. Review: The cellular basis of the immunity to and immunopathogenesis of tropical theileriosis. Parasitol. Res. 1999, 85, 539–549. [Google Scholar] [CrossRef]
- Forsyth, L.M.; Jackson, L.A.; Wilkie, G.; Sanderson, A.; Brown, C.G.; Preston, P.M. Bovine cells infected with Theileria annulata express DC11b, the C3bi complement receptor. Vet. Res. Commun. 1997, 21, 249–263. [Google Scholar] [CrossRef]
- Preston, P.M.; Brown, C.G.D.; Bell-Sakyi, L.; Richardson, W.; Sanderson, A. Tropical theileriosis in Bos taurus and Bos taurus cross Bos indicus calves: Response to infection with graded doses of sporozoites of Theileria annulata. Res. Vet. Sci. 1992, 53, 230–243. [Google Scholar] [CrossRef]
- Preston, M.; Brown, C.; Entrican, G.; Richardson, W.; Boid, R. Synthesis of tumour necrosis factor-alpha and interferons by mononuclear cells from Theileria annulata-infected cattle. Parasite Immunol. 1993, 15, 525–534. [Google Scholar] [CrossRef] [PubMed]
- Visser, A.E.; Abraham, A.; Saky, L.J.B.; Preston, P.M. Nitric oxide inhibits establishment of macroschizont-infected cell lines and is produced by macrophages of calves undergoing bovine tropical theileriosis or East Coast fever. Parasite Immunol. 1995, 17, 91–102. [Google Scholar] [CrossRef] [PubMed]
- Campbell, J.D.M.; Spooner, R.L. Macrophages behaving badly: Infected cells and subversion of immune responses to Theileria annulata. Parasitol. Today 1999, 15, 10–16. [Google Scholar] [CrossRef]
- Brown, D.J.; Campbell, J.D.M.; Russell, G.C.; Hopkins, J.; Glass, E.J. T cell activation by Theileria annulata-infected macrophages correlates with cytokine production. Clin. Exp. Immunol. 1995, 102, 507–514. [Google Scholar] [CrossRef]
- Baldwin, C.L.; Black, S.J.; Brown, W.C.; Conrad, P.A.; Goddeeris, B.M.; Kinuthia, S.W.; Lalor, P.A.; MacHugh, N.D.; Morrison, W.I.; Morzaria, S.P. Bovine T cells, B cells, and null cells are transformed by the protozoan parasite Theileria parva. Infect. Immun. 1988, 56, 462–467. [Google Scholar] [CrossRef] [Green Version]
- Spooner, R.L.; Innes, E.A.; Glass, E.J.; Brown, C.G. Theileria annulata and T. parva infect and transform different bovine mononuclear cells. Immunology 1989, 66, 288. [Google Scholar]
- Adamson, R.E.; Hall, F.R. A role for matrix metalloproteinases in the pathology and attenuation of Theileria annulata infections. Parasitol. Today 1997, 13, 390–393. [Google Scholar] [CrossRef]
- Forsyth, L.; Minns, F.C.; Kirvar, E.; Adamson, R.E.; Hall, F.R.; McOrist, S.; Brown, C.G.D.; Preston, P.M. Tissue Damage in Cattle Infected withTheileria annulataAccompanied by Metastasis of Cytokine-producing, Schizont-infected Mononuclear Phagocytes. J. Comp. Pathol. 1999, 120, 39–57. [Google Scholar] [CrossRef]
- Heussler, V.T.; Küenzi, P.; Rottenberg, S. Inhibition of apoptosis by intracellular protozoan parasites. Int. J. Parasitol. 2001, 31, 1166–1176. [Google Scholar] [CrossRef]
- 104. Dobbelaere, D.; Heussler, V. Transformation of leukocytes by Theileria parva and T. annulata. Annu. Rev. Microbiol. 1999, 53, 1–42. [Google Scholar] [CrossRef]
- Cock-Rada, A.M.; Medjkane, S.; Janski, N.; Yousfi, N.; Perichon, M.; Chaussepied, M.; Chluba, J.; Langsley, G.; Weitzman, J.B. SMYD3 promotes cancer invasion by epigenetic upregulation of the metalloproteinase MMP-9. Cancer Res. 2012, 72, 810–820. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kinnaird, J.H.; Weir, W.; Durrani, Z.; Pillai, S.S.; Baird, M.; Shiels, B.R. A Bovine Lymphosarcoma Cell Line Infected with Theileria annulata Exhibits an Irreversible Reconfiguration of Host Cell Gene Expression. PLoS ONE 2013, 8, e66833. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Haller, D.; MacKiewicz, M.; Gerber, S.; Beyer, D.; Kullmann, B.; Schneider, I.; Ahmed, J.S.; Seitzer, U. Cytoplasmic sequestration of p53 promotes survival in leukocytes transformed by Theileria. Oncogene 2010, 29, 3079–3086. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vogelstein, B.; Lane, D.; Levine, A.J. Surfing the p53 network. Nature 2000, 408, 307–310. [Google Scholar] [CrossRef]
- Vogelstein, B.; Kinzler, K.W. Cancer genes and the pathways they control. Nat. Med. 2004, 10, 789–799. [Google Scholar] [CrossRef]
- Momand, J.; Zambetti, G.P.; Olson, D.C.; George, D.; Levine, A.J. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 1992, 69, 1237–1245. [Google Scholar] [CrossRef]
- Toledo, F.; Wahl, G.M. Regulating the p53 pathway: In vitro hypotheses, in vivo veritas. Nat. Rev. Cancer 2006, 909–923. [Google Scholar] [CrossRef]
- Bartel, F.; Taubert, H.; Harris, L.C. Alternative and aberrant splicing of MDM2 mRNA in human cancer. Cancer Cell 2002, 2, 9–15. [Google Scholar] [CrossRef] [Green Version]
- Kumar, S.K.; Hager, E.; Pettit, C.; Gurulingappa, H.; Davidson, N.E.; Khan, S.R. Design, synthesis, and evaluation of novel boronic-chalcone derivatives as antitumor agents. J. Med. Chem. 2003, 46, 2813–2815. [Google Scholar] [CrossRef]
- Siddik, Z.H. Cisplatin: Mode of cytotoxic action and molecular basis of resistance. Oncogene 2003, 22, 7265–7279. [Google Scholar] [CrossRef] [Green Version]
- Fry, L.M.; Schneider, D.A.; Frevert, C.W.; Nelson, D.D.; Morrison, W.I.; Knowles, D.P. East coast fever caused by Theileria parva is characterized by macrophage activation associated with vasculitis and respiratory failure. PLoS ONE 2016, 11, e0156004. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.; Wang, F.; Wang, L.; Huang, L.; Wang, J.; Zhang, B.; Zhang, Y. CD163+ tumor-associated macrophage is a prognostic biomarker and is associated with therapeutic effect on malignant pleural effusion of lung cancer patients. Oncotarget 2015, 6, 10592–10603. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McKeever, D.J.; Nyanjui, J.K.; Ballingall, K.T. In vitro infection with Theileria parva is associated with IL10 expression in all bovine lymphocyte lineages. Parasite Immunol. 1997, 19, 319–324. [Google Scholar] [CrossRef] [PubMed]
- Tomioka, H.; Tatano, Y.; Maw, W.W.; Sano, C.; Kanehiro, Y.; Shimizu, T. Characteristics of suppressor macrophages induced by mycobacterial and protozoal infections in relation to alternatively activated M2 macrophages. Clin. Dev. Immunol. 2012, 2012, 635451. [Google Scholar] [CrossRef]
- Khan, I.A.; Matsuura, T.; Kasper, L.H. IL-10 mediates immunosuppression following primary infection with Toxoplasma gondii in mice. Parasite Immunol. 1995, 17, 185–195. [Google Scholar] [CrossRef]
- Flynn, J.N.; Sileghem, M. The role of the macrophage in induction of immunosuppression in Trypanosoma congolense-infected cattle. Immunology 1991, 74, 310–316. [Google Scholar]
- Sternberg, J.M. Elevated serum nitrate in Trypanosoma brucei “rhodesiense” infections: Evidence for inducible nitric oxide synthesis in trypanosomiasis. Trans. R. Soc. Trop. Med. Hyg. 1996, 90, 395. [Google Scholar] [CrossRef]
- Dutra, M.S.; Béla, S.R.; Peixoto-Rangel, A.L.; Fakiola, M.; Cruz, A.G.; Gazzinelli, A.; Quites, H.F.; Bahia-Oliveira, L.M.G.; Peixe, R.G.; Campos, W.R.; et al. Association of a NOD2 gene polymorphism and T-helper 17 cells with presumed ocular toxoplasmosis. J. Infect. Dis. 2013, 207, 152–163. [Google Scholar] [CrossRef] [Green Version]
- Del Cacho, E.; Gallego, M.; Lillehoj, H.S.; Quílez, J.; Lillehoj, E.P.; Ramo, A.; Sánchez-Acedo, C. IL-17A regulates Eimeria tenella schizont maturation and migration in avian coccidiosis. Vet. Res. 2014, 45, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Bacellar, O.; Faria, D.; Nascimento, M.; Cardoso, T.M.; Gollob, K.J.; Dutra, W.O.; Scott, P.; Carvalho, E.M. Interleukin 17 production among patients with American cutaneous leishmaniasis. J. Infect. Dis. 2009, 200, 75–78. [Google Scholar] [CrossRef] [Green Version]
- Rainard, P.; Cunha, P.; Bougarn, S.; Fromageau, A.; Rossignol, C.; Gilbert, F.B.; Berthon, P. T helper 17-associated cytokines are produced during antigen-specific inflammation in the mammary gland. PLoS ONE 2013, 8, e63471. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mai, J.; Nanayakkara, G.; Lopez-Pastrana, J.; Li, X.; Li, Y.-F.; Wang, X.; Song, A.; Virtue, A.; Shao, Y.; Shan, H.; et al. Interleukin-17A Promotes Aortic Endothelial Cell Activation via Transcriptionally and Post-translationally Activating p38 Mitogen-activated Protein Kinase (MAPK) Pathway. J. Biol. Chem. 2016, 291, 4939–4954. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xing, X.; Yang, J.; Yang, X.; Wei, Y.; Zhu, L.; Gao, D.; Li, M. IL-17A induces endothelial inflammation in systemic sclerosis via the ERK signaling pathway. PLoS ONE 2013, 8, e85032. [Google Scholar] [CrossRef] [PubMed]
- Weyand, C.M.; Goronzy, J.J. Immune mechanisms in medium and large-vessel vasculitis. Nat. Rev. Rheumatol. 2013, 9, 731–740. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Henter, J.-I.; Horne, A.; Aricó, M.; Egeler, R.M.; Filipovich, A.H.; Imashuku, S.; Ladisch, S.; McClain, K.; Webb, D.; Winiarski, J.; et al. HLH-2004: Diagnostic and therapeutic guidelines for hemophagocytic lymphohistiocytosis. Pediatr. Blood Cancer 2007, 48, 124–131. [Google Scholar] [CrossRef]
- Brisse, E.; Wouters, C.H.; Matthys, P. Hemophagocytic lymphohistiocytosis (HLH): A heterogeneous spectrum of cytokine-driven immune disorders. Cytokine Growth Factor Rev. 2015, 26, 263–280. [Google Scholar] [CrossRef]
- Naessens, J. Bovine trypanotolerance: A natural ability to prevent severe anaemia and haemophagocytic syndrome? Int. J. Parasitol. 2006, 36, 521–528. [Google Scholar] [CrossRef]
- Shayan, P.; Rahbari, S. Simultaneous differentiation between Theileria spp. and Babesia spp. on stained blood smear using PCR. Parasitol. Res. 2005, 97, 281–286. [Google Scholar] [CrossRef]
- Li, Y.; Chen, Z.; Liu, Z.; Liu, J.; Yang, J.; Li, Q.; Li, Y.; Cen, S.; Guan, G.; Ren, Q.; et al. Molecular identification of Theileria parasites of northwestern Chinese Cervidae. Parasites Vectors 2014, 7, 1–7. [Google Scholar] [CrossRef] [Green Version]
- Maharana, B.R.; Tewari, A.K.; Saravanan, B.C.; Sudhakar, N.R. Important hemoprotozoan diseases of livestock: Challenges in current diagnostics and therapeutics: An update. Vet. World 2016, 9, 487–495. [Google Scholar] [CrossRef]
- Mohamed, A.M.; Abdel-Rady, A.; Ahmed, L.S.; El-Hosary, A. Evaluation of indirect TaSP enzyme-linked immunosorbent assay for diagnosis of tropical theileriosis in cattle (Bos indicus) and water buffaloes (Bubalus bubalis) in Egypt. Vet. Parasitol. 2012, 186, 486–489. [Google Scholar] [CrossRef] [PubMed]
- Magona, J.W.; Walubengo, J.; Olaho-Mukani, W.; Jonsson, N.N.; Welburn, S.C.; Eisler, M.C. Clinical features associated with seroconversion to Anaplasma marginale, Babesia bigemina and Theileria parva infections in African cattle under natural tick challenge. Vet. Parasitol. 2008, 155, 273–280. [Google Scholar] [CrossRef]
- Billiouw, M.; Brandt, J.; Vercruysse, J.; Speybroeck, N.; Marcotty, T.; Mulumba, M.; Berkvens, D. Evaluation of the indirect fluorescent antibody test as a diagnostic tool for East Coast fever in eastern Zambia. Vet. Parasitol. 2005, 127, 189–198. [Google Scholar] [CrossRef] [PubMed]
- Park, J.; Han, Y.J.; Han, D.G.; Chae, J.B.; Chae, J.S.; Yu, D.H.; Lee, Y.S.; Park, B.K.; Kim, H.C.; Choi, K.S. Genetic characterization of Theileria orientalis from cattle in the Republic of Korea. Parasitol. Res. 2017, 116, 449–454. [Google Scholar] [CrossRef] [PubMed]
- Bogema, D.R.; Deutscher, A.T.; Fell, S.; Collins, D.; Eamens, G.J.; Jenkinsa, C. Development and validation of a quantitative PCR assay using multiplexed hydrolysis probes for detection and quantification of Theileria orientalis isolates and differentiation of clinically relevant subtypes. J. Clin. Microbiol. 2015, 53, 941–950. [Google Scholar] [CrossRef] [Green Version]
- Altangerel, K.; Sivakumar, T.; Inpankaew, T.; Jittapalapong, S.; Terkawi, M.A.; Ueno, A.; Xuan, X.; Igarashi, I.; Yokoyama, N. Molecular Prevalence of different genotypes of Theileria orientalis detected from cattle and water buffaloes buffaloes in Thailand. J. Parasitol. 2011, 97, 1075–1079. [Google Scholar] [CrossRef]
- Chaouch, M.; Mhadhbi, M.; Limam, S.; Darghouth, M.A.; Benabderrazak, S. Development and evaluation of a loop-mediated isothermal amplification assay for rapid detection of Theileria annulata targeting the cytochrome B gene. Iran. J. Parasitol. 2018, 13, 225–234. [Google Scholar]
- Ros-García, A.; García-Pérez, A.L.; Verdera, J.; Juste, R.A.; Hurtado, A. Monitoring piroplasms infection in three cattle farms in Minorca (Balearic Islands, Spain) with previous history of clinical piroplamosis. Vet. Parasitol. 2012, 190, 318–325. [Google Scholar] [CrossRef]
- Saravanan, B.C.; Sankar, M.; Bansal, G.C.; Sreekumar, C.; Tewari, A.K.; Rao, J.R.; Ray, D. Random amplified polymorphic DNA profiles in two Indian strains of Theileria annulata. J. Vet. Parasitol. 2010, 24, 39–43. [Google Scholar]
- Sudan, V.; Shanker, D.; Jaiswal, A.; Singh, A.; Pandey, V. Standardization and validation of simple PCR, duplex PCR and RAPD in comparison to blood smear examination for diagnosing bovine tropical theileriosis. Biologicals 2017, 46, 88–91. [Google Scholar] [CrossRef]
- Abanda, B.; Paguem, A.; Achukwi, M.D.; Renz, A.; Eisenbarth, A. Development of a Low-Density DNA Microarray for Detecting Tick-Borne Bacterial and Piroplasmid Pathogens in African Cattle. Trop. Med. Infect. Dis. 2019, 4, 64. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- McAllister, M.M. Successful vaccines for naturally occurring protozoal diseases of animals should guide human vaccine research. A review of protozoal vaccines and their designs. Parasitology 2014, 141, 624–640. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bastos, R.G.; Franceschi, V.; Tebaldi, G.; Connelley, T.; Ivan Morrison, W.; Knowles, D.P.; Donofrio, G.; Fry, L.M.; Morrison, W.I.; Knowles, D.P.; et al. Molecular and Antigenic Properties of Mammalian Cell-Expressed Theileria parva Antigen Tp9. Front. Immunol. 2019, 10, 897. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Norling, M.; Bishop, R.P.; Pelle, R.; Qi, W.; Henson, S.; Drábek, E.F.; Tretina, K.; Odongo, D.; Mwaura, S.; Njoroge, T.; et al. The genomes of three stocks comprising the most widely utilized live sporozoite Theileria parva vaccine exhibit very different degrees and patterns of sequence divergence. BMC Genom. 2015, 16, 729. [Google Scholar] [CrossRef] [Green Version]
- Ellis, S.A.; Hammond, J.A. The functional significance of cattle major histocompatibility complex class I genetic diversity. Annu. Rev. Anim. Biosci. 2014, 2, 285–306. [Google Scholar] [CrossRef]
- Hemmink, J.D.; Sitt, T.; Pelle, R.; de Klerk-Lorist, L.-M.; Shiels, B.; Toye, P.G.; Morrison, W.I.; Weir, W. Ancient diversity and geographical sub-structuring in African buffalo Theileria parva populations revealed through metagenetic analysis of antigen-encoding loci. Int. J. Parasitol. 2018, 48, 287–296. [Google Scholar] [CrossRef]
- Morrison, W.I.; Connelley, T.; Hemmink, J.D.; MacHugh, N.D. Understanding the basis of parasite strain-restricted immunity to Theileria parva. Annu. Rev. Anim. Biosci. 2015, 3, 397–418. [Google Scholar] [CrossRef]
- Graham, S.P.; Pellé, R.; Honda, Y.; Mwangi, D.M.; Tonukari, N.J.; Yamage, M.; Glew, E.J.; de Villiers, E.P.; Shah, T.; Bishop, R.; et al. Theileria parva candidate vaccine antigens recognized by immune bovine cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA 2006, 103, 3286–3291. [Google Scholar] [CrossRef] [Green Version]
- Hemmink, J.D.; Weir, W.; MacHugh, N.D.; Graham, S.P.; Patel, E.; Paxton, E.; Shiels, B.; Toye, P.G.; Morrison, W.I.; Pelle, R. Limited genetic and antigenic diversity within parasite isolates used in a live vaccine against Theileria parva. Int. J. Parasitol. 2016, 46, 495–506. [Google Scholar] [CrossRef] [Green Version]
- Dobbelaere, D.A.E.; Shapiro, S.Z.; Webster, P. Identification of a surface antigen on Theileria parva sporozoites by monoclonal antibody. Proc. Natl. Acad. Sci. USA 1985, 82, 1771–1775. [Google Scholar] [CrossRef] [Green Version]
- Williamson, S.; Walker, A.; Fletcher, J. Theileria Escherichia. Immunology 1989, 86, 4639–4643. [Google Scholar]
- MacHugh, N.D.; Connelley, T.; Graham, S.P.; Pelle, R.; Formisano, P.; Taracha, E.L.; Ellis, S.A.; McKeever, D.J.; Burrells, A.; Morrison, W.I. CD8+ T-cell responses to Theileria parva are preferentially directed to a single dominant antigen: Implications for parasite strain-specific immunity. Eur. J. Immunol. 2009, 39, 2459–2469. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Toye, P.; Gobright, E.; Nyanjui, J.; Nene, V.; Bishop, R. Structure and sequence variation of the genes encoding the polymorphic, immunodominant molecule (PIM), an antigen of Theileria parva recognized by inhibitory monoclonal antibodies. Mol. Biochem. Parasitol. 1995, 73, 165–177. [Google Scholar] [CrossRef]
- Pelle, R.; Graham, S.P.; Njahira, M.N.; Osaso, J.; Saya, R.M.; Odongo, D.O.; Toye, P.G.; Spooner, P.R.; Musoke, A.J.; Mwangi, D.M.; et al. Two Theileria parva CD8 T cell antigen genes are more variable in buffalo than cattle parasites, but differ in pattern of sequence diversity. PLoS ONE 2011, 6, e19015. [Google Scholar] [CrossRef] [Green Version]
- Bakheit, M.; Scholzen, T.; Ahmed, J.S.; Seitzer, U. Identification of potential antigenic proteins of Theileria lestoquardi. Ann. N. Y. Acad. Sci. 2006, 1081, 463–464. [Google Scholar] [CrossRef]
- Schnittger, L.; Katzer, F.; Biermann, R.; Shayan, P.; Boguslawski, K.; McKellar, S.; Beyer, D.; Shiels, B.R.; Ahmed, J.S. Characterization of a polymorphic Theileria annulata surface protein (TaSP) closely related to PIM of Theileria parva: Implications for use in diagnostic tests and subunit vaccines. Mol. Biochem. Parasitol. 2002, 120, 247–256. [Google Scholar] [CrossRef]
- Nene, V.; Morrison, W.I. Approaches to vaccination against Theileria parva and Theileria annulata. Parasite Immunol. 2016, 38, 724–734. [Google Scholar] [CrossRef] [Green Version]
- Hall, R.; R.boulter, N.; dunca Brown, C.G.; Wilkie, G.; Kirvar, E.; Nene, V.; J.musoke, A.; J.glass, E.; Morzaria, S.P. Reciprocal cross-protection induced by sporozoite antigens SPAG-1 from Theileria annulata and p67 from Theileria parva. Parasite Immunol. 2000, 22, 223–230. [Google Scholar] [CrossRef]
- Knight, P.; Musoke, A.J.; Gachanja, J.N.; Nene, V.; Katzer, F.; Boulter, N.; Hall, R.; Brown, C.G.D.; Williamson, S.; Kirvar, E.; et al. Conservation of neutralizing determinants between the sporozoite surface antigens of Theileria annulata and Theileria parva. Exp. Parasitol. 1996, 82, 229–241. [Google Scholar] [CrossRef]
- De Vos Bert, A.J. Theileria: Assess. Potential to Develop a Vaccine for Theileria Orientalis Infection; Meat & Livestock Limited: North Sydney, Australia, 2011; Volume 364, ISBN 9781741917840. [Google Scholar]
- Yam, J.; Bogema, D.R.; Jenkins, C. Oriental Theileriosis. In Ticks and Tick-Borne Pathogens; Abubakar, M., Perera, P., Eds.; IntechOpen: Rijeka, Croatia, 2019; pp. 1–13. ISBN 978-1-78985-766-5. [Google Scholar]
- Chae, J.S.; Allsopp, B.A.; Waghela, S.D.; Park, J.H.; Kakuda, T.; Sugimoto, C.; Allsopp, M.T.E.P.; Wagner, G.G.; Holman, P.J. A study of the systematics of Theileria spp. based upon small-subunit ribosomal RNA gene sequences. Parasitol. Res. 1999, 85, 877–883. [Google Scholar] [CrossRef]
- Bogema, D.R.; Micallef, M.L.; Liu, M.; Padula, M.P.; Djordjevic, S.P.; Darling, A.E.; Jenkins, C. Analysis of Theileria orientalis draft genome sequences reveals potential species-level divergence of the Ikeda, Chitose and Buffeli genotypes. BMC Genom. 2018, 19, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Hu, K.; He, X.; Yu, F.; Yuan, X.; Hu, W.; Liu, C.; Zhao, F.; Dou, J. Immunization with DNA vaccine expressing herpes simplex virus type 1 gD and IL-21 protects against mouse herpes keratitis. Immunol. Investig. 2011, 40, 265–278. [Google Scholar] [CrossRef] [PubMed]
- Dong, L.L.; Tang, R.; Zhai, Y.J.; Malla, T.; Hu, K. DNA vaccine expressing herpes simplex virus 1 glycoprotein C and D protects mice against herpes simplex keratitis. Int. J. Ophthalmol. 2017, 10, 1633–1639. [Google Scholar] [CrossRef] [PubMed]
- Villarreal, D.O.; Talbott, K.T.; Choo, D.K.; Shedlock, D.J.; Weiner, D.B. Synthetic DNA vaccine strategies against persistent viral infections. Expert Rev. Vaccines 2013, 12, 537–554. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Su, B.; Wang, J.; Wang, X.; Jin, H.; Zhao, G.; Ding, Z.; Kang, Y.; Wang, B. The effects of IL-6 and TNF-α as molecular adjuvants on immune responses to FMDV and maturation of dendritic cells by DNA vaccination. Vaccine 2008, 26, 5111–5122. [Google Scholar] [CrossRef] [PubMed]
- Nour El-Din, A.N.M.; Shkreta, L.; Talbot, B.G.; Diarra, M.S.; Lacasse, P. DNA immunization of dairy cows with the clumping factor a of Staphylococcus aureus. Vaccine 2006, 24, 1997–2006. [Google Scholar] [CrossRef]
- Mwangi, W.; Brown, W.C.; Lewin, H.A.; Howard, C.J.; Hope, J.C.; Baszler, T.V.; Caplazi, P.; Abbott, J.; Palmer, G.H. DNA-encoded fetal liver tyrosine kinase 3 ligand and granulocyte macrophage-colony-stimulating factor increase dendritic cell recruitment to the inoculation site and enhance antigen-specific CD4+ T cell responses induced by DNA vaccination of outbred anim. J. Immunol. 2002, 169, 3837–3846. [Google Scholar] [CrossRef]
- Mwangi, D.M.; Honda, Y.; Graham, S.P.; Pelle, R.; Taracha, E.L.N.; Gachanja, J.; Nyanjui, J.K.; Bray, J.; Palmer, G.H.; Brown, W.C.; et al. Treatment of cattle with DNA-encoded Flt3L and GM-CSF prior to immunization with Theileria parva candidate vaccine antigens induces CD4 and CD8 T cell IFN-γ responses but not CTL responses. Vet. Immunol. Immunopathol. 2011, 140, 244–251. [Google Scholar] [CrossRef]
- Oliveira, S.C.; Rosinha, G.M.; De-Brito, C.F.; Fonseca, C.T.; Afonso, R.R.; Costa, M.C.; Goes, A.M.; Rech, E.L.; Azevedo, V. Immunological properties of gene vaccines delivered by different routes. Braz. J. Med. Biol. Res. 1999, 32, 207–214. [Google Scholar] [CrossRef] [Green Version]
- Fry, L.M.; Bastos, R.G.; Stone, B.C.; Williams, L.B.; Knowles, D.P.; Murphy, S.C. Gene gun DNA immunization of cattle induces humoral and CD4 T-cell-mediated immune responses against the Theileria parva polymorphic immunodominant molecule. Vaccine 2019, 37, 1546–1553. [Google Scholar] [CrossRef]
- Yager, E.J.; Stagnar, C.; Gopalakrishnan, R.; Fuller, J.T.; Fuller, D.H. Optimizing particle-mediated epidermal delivery of an influenza DNA vaccine in ferrets. Methods Mol. Biol. 2013, 940, 223–237. [Google Scholar] [CrossRef] [PubMed]
- Pertmer, T.M.; Eisenbraun, M.D.; McCabe, D.; Prayaga, S.K.; Fuller, D.H.; Haynes, J.R. Gene gun-based nucleic acid immunization: Elicitation of humoral and cytotoxic T lymphocyte responses following epidermal delivery of nanogram quantities of DNA. Vaccine 1995, 13, 1427–1430. [Google Scholar] [CrossRef]
Theileria Species (Disease Names) | Ixodid Vectors | Geographic Distribution | References |
---|---|---|---|
Theileria annulata (tropical theileriosis/mediterranean theileriosis) | Hyalomma species | Asia (India, China), Africa (Egypt, Sudan), Middle East, Europe (Portugal) | [10,31,32,33,34,35] |
Theileria parva (East Coast fever), buffalo-derived T. parva (Corridor Disease) | Rhipicephalus appendiculatus, R. duttoni, R. appendiculatus, R. zambesiensis | Africa (Kenya, Tanzania, Uganda, Mozambique) | [2,26,36,37,38] |
Theileria orientalis (orientalis/sergenti/buffeli) (Oriental theileriosis) | Haemaphysalis longicornis; Rhipicephalus microplus | Oceania region (Australia, New Zealand), Europe (Russia, Greece, Italy, Spain, Portugal, Hungary), Asia (Vietnam, China, Korea, Malaysia, India), Africa (Ethiopia) | [24,39,40,41,42,43,44,45,46,47,48,49,50,51,52] |
Theileria taurotragi (Benign African theileriosis) | Rhipicephalus appendiculatus, R. zambeziensis, R. pulchellus | Africa (Kenya, South Africa, Zambia) | [2,53,54] |
Theileria mutans (Benign theileriosis) | Amblyomma species | Africa (Kenya, Ethiopia, South Africa), Central America (Caribbean Islands) | [2,55,56,57,58,59] |
Theileria velifera (Benign theileriosis) | Amblyomma variegatum | Africa (Kenya, Ethiopia, South Africa), Central America (Caribbean Islands) | [2,56,58,59] |
Theileria sinensis (Benign theileriosis) | Haemaphysalis qinghaiensis; H. bispinosa; Rhipicephalus microplus; | Asia (China, Malaysia), Europe (Russia) | [3,60,61,62] |
Theileria sp. Yokoyama | Not known | Asia (Sri Lanka) | [13] |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Agina, O.A.; Shaari, M.R.; Isa, N.M.M.; Ajat, M.; Zamri-Saad, M.; Hamzah, H. Clinical Pathology, Immunopathology and Advanced Vaccine Technology in Bovine Theileriosis: A Review. Pathogens 2020, 9, 697. https://doi.org/10.3390/pathogens9090697
Agina OA, Shaari MR, Isa NMM, Ajat M, Zamri-Saad M, Hamzah H. Clinical Pathology, Immunopathology and Advanced Vaccine Technology in Bovine Theileriosis: A Review. Pathogens. 2020; 9(9):697. https://doi.org/10.3390/pathogens9090697
Chicago/Turabian StyleAgina, Onyinyechukwu Ada, Mohd Rosly Shaari, Nur Mahiza Md Isa, Mokrish Ajat, Mohd Zamri-Saad, and Hazilawati Hamzah. 2020. "Clinical Pathology, Immunopathology and Advanced Vaccine Technology in Bovine Theileriosis: A Review" Pathogens 9, no. 9: 697. https://doi.org/10.3390/pathogens9090697