Characteristics of genetic resistance to Maedi-Visna in sheep breeds raised in Russia
https://doi.org/10.32634/0869-8155-2026-409-08-84-94
Abstract
Relevance. Small Ruminant Lentiviruses (SRLVs), including the Visna-Maedi Virus (VMV) in sheep, induce chronic progressive inflammation primarily targeting the nervous system, lungs, mammary glands, and joints. These viruses exhibit significant genetic variability, leading to a lack of effective therapies or vaccines at an affordable cost. Foreign research has identified breed-specific variations in genetic resistance to these pathogens, but such comparative data remain largely unexplored for Russian sheep breeds. A reliable DNA marker of genetic resistance to VMV infection is the ovine transmembrane protein 154 (TMEM154) gene. This study aimed to evaluate the allelic diversity among different Russian sheep breeds through targeted SNP within the TMEM154 gene linked to genetic resistance.
Methods. The study utilized biological samples (tissues) of sheep maintained at the Ladozhsky PZ and from the biobank repository titled “Genetic Materials Bank of Domestic and Wild Animals.” To identify specific mutations correlated with resistance to VMV, fragments encompassing the target SNP (OAR17_5388531) within the TMEM154 gene were amplified via RT-PCR.
Results. Analysis of TMEM154 polymorphisms uncovered two distinct alleles (C and T) along with their corresponding genotypes: TT, CT, and CC. Genotype distributions associated with resistance to the Visna-Maedi virus across eighteen diverse Russian sheep breeds have been documented.
Keywords
About the Authors
O. S. YakovlevaRussian Federation
Olga Sergeevna Yakovleva, postgraduate student
60 Dubrovitsy, Podolsk Municipal District, Moscow Region, 142132
T. E. Deniskova
Russian Federation
Tatiana Evgenievna Deniskova, Candidate of Biological Sciences, Leading Researcher
60 Dubrovitsy, Podolsk Municipal District, Moscow Region, 142132
O. A. Koshkina
Russian Federation
Olga Andreevna Koshkina, Candidate of Biological Sciences, Senior Researcher
60 Dubrovitsy, Podolsk Municipal District, Moscow Region, 142132
A. V. Dotsev
Russian Federation
Arsen Vladimirovich Dotsev, Candidate of Biological Sciences, Leading Researcher
60 Dubrovitsy, Podolsk Municipal District, Moscow Region, 142132
A. D. Solovieva
Russian Federation
Anastasiya Dmitrievna Solovieva, leading specialist
60 Dubrovitsy, Podolsk Municipal District, Moscow Region, 142132
N. A. Zinovieva
Russian Federation
Natalia Anatolievna Zinovieva, Doctor of Biological Sciences, Professor, Academician of the Russian Academy of Sciences
60 Dubrovitsy, Podolsk Municipal District, Moscow Region, 142132
References
1. De Boer G.F. Zwoegerziekte virus, the causative agent for progressive interstitial pneumonia (maedi) and meningo-leucoencephalitis (visna) in sheep. Research in Veterinary Science. 1975; 18(1): 15–25. https://doi.org/10.1016/S0034-5288(18)33625-7
2. Thormar H. Maedi-Visna Virus and its Relationship to Human Immunodeficiency Virus. AIDS Reviews. 2005; 7(4): 233–245.
3. Sait A., Ince O.B. Investigation of the Epidemiology of Small Ruminant Lentivirus Infections southeast part of the Marmara region of Turkey. Journal of the Hellenic Veterinary Medical Society. 2023; 73(4): 5053–5060. https://doi.org/10.12681/jhvms.29095
4. Goujgoulova G., Koev K. Clinical and pathological investigation of Maedivisna outbreak in a farm from Bulgaria. Open Veterinary Journal. 2025; 15(11): 5772–5780. https://doi.org/10.5455/OVJ.2025.v15.i11.32
5. Heaton M.P. et al. Genetic Testing for TMEM154 Mutations Associated with Lentivirus Susceptibility in Sheep. PlOS One. 2013; 8(2): e55490. https://doi.org/10.1371/journal.pone.0055490
6. Kalogianni A.I., Bossis I., Ekateriniadou L.V., Gelasakis A.I. Etiology, Epizootiology and Control of Maedi-Visna in Dairy Sheep: A Review. Animals. 2020; 10(4): 616. https://doi.org/10.3390/ani10040616
7. Vincenz F., Samoilenko M., Abril C.E., Zanolari P., Bertoni G., Thomann B. A Look Under the Carpet of a Successful Eradication Campaign Against Small Ruminant Lentiviruses. Pathogens. 2025; 14(7): 719. https://doi.org/10.3390/pathogens14070719
8. Blacklaws B.A., Harkiss G.D. Small Ruminant Lentiviruses and Human Immunodeficiency Virus: Cousins that Take a Long View. Current HIV Research. 2010; 8(1): 26–52. https://doi.org/10.2174/157016210790416406
9. Peluso R., Haase A., Stowring L., Edwards M., Ventura P. A Trojan Horse mechanism for the spread of visna virus in monocytes. Virology. 1985; 147(1): 231–236. https://doi.org/10.1016/0042-6822(85)90246-6
10. Haase A.T. Pathogenesis of lentivirus infections. Nature. 1986; 322(6075): 130–136. https://doi.org/10.1038/322130a0
11. Narayan O., Clements J.E. Biology and Pathogenesis of Lentiviruses. Journal of General Virology. 1989; 70(7): 1617–1639. https://doi.org/10.1099/0022-1317-70-7-1617
12. Sigurdsson B., Grímsson H., Pálsson P. Maedi, a Chronic, Progressive Infection of Sheep’s Lungs. The Journal of Infectious Diseases. 1952; 90(3): 233–241. https://doi.org/10.1093/infdis/90.3.233
13. Koçkaya E.S. et al. Newly developed peptide-ELISA successfully detected anti-IgG antibodies against Maedi-Visna virus in sheep. Veterinary Immunology and Immunopathology. 2024; 274: 110806. https://doi.org/10.1016/j.vetimm.2024.110806
14. Keen J.E., Hungerford L.L., Littledike E.T., Wittum T.E., Kwang J. Effect of ewe ovine lentivirus infection on ewe and lamb productivity. Preventive Veterinary Medicine. 1997; 30(2): 155–169. https://doi.org/10.1016/S0167-5877(96)01101-4
15. Heaton M.P., Leymaster K.A., Clawson M.L. Association of TMEM154 missense mutations with lentiviral infection and virus subtypes in sheep. Proceedings of the 10th World Congress of Genetics Applied to Livestock Production. 2014.
16. Clements J.E., Zink M.C. Molecular biology and pathogenesis of animal lentivirus infections. Clinical Microbiology Reviews. 1996; 9(1): 100–117. https://doi.org/10.1128/cmr.9.1.100
17. Jacob-Ferreira J., Coelho A.C., Grau Vila A., Lacasta D., Quintas H. Small Ruminant Lentivirus Infection in Sheep and Goats in North Portugal: Seroprevalence and Risk Factors. Pathogens. 2023; 12(6): 829. https://doi.org/10.3390/pathogens12060829
18. Caroline L., Minardi C.J.C., Jean-Francois M. SRLVs: A Genetic Continuum of Lentiviral Species in Sheep and Goats with Cumulative Evidence of Cross Species Transmission. Current HIV Research. 2010; 8(1): 94–100. https://doi.org/10.2174/157016210790416415
19. Kalogianni A.I., Bossis I., Ekateriniadou L.V., Gelasakis A.I. Etiology, Epizootiology and Control of Maedi-Visna in Dairy Sheep: A Review. Animals. 2020; 10(4): 616. https://doi.org/10.3390/ani10040616
20. AlSaad K.M., Lafta A.J., Lafta M.H., Ahmed J.A. Clinical and diagnostic study of ovine chronic progressive pneumonia (Maedi-Visna) in sheep of Basrah, Iraq. Iraqi Journal of Veterinary Sciences, 2025; 39(1): 15–23. https://doi.org/10.33899/ijvs.2024.152796.3833
21. Liebler-Tenorio E.M., Moog U., Barth S.A., König P. Indurative mastitis in a herd of Dorper sheep caused by an infection with Maedi Visna virus. Tierärztliche Praxis Großtiere/Nutztiere, 2023; 51(3): 175–183 (in German). https://doi.org/10.1055/a-2107-7834
22. Kalogianni A.I., Bossis I., Ekateriniadou L.V., Gelasakis A.I. Etiology, Epizootiology and Control of Maedi-Visna in Dairy Sheep: A Review. Animals. 2020; 10(4): 616. https://doi.org/10.3390/ani10040616
23. Blacklaws B.A. et al. Transmission of small ruminant lentiviruses. Veterinary Microbiology. 2004; 101(3): 199–208. https://doi.org/10.1016/j.vetmic.2004.04.006
24. Peterhans E. et al. Routes of transmission and consequences of small ruminant lentiviruses (SRLVs) infection and eradication schemes. Veterinary Research. 2004; 35(3): 257–274. https://doi.org/10.1051/vetres:2004014
25. Illius A.W., Savill N.J. Maternal transmission of Small Ruminant Lentivirus has no epidemiological importance. Preventive Veterinary Medicine. 2024; 230: 106297. https://doi.org/10.1016/j.prevetmed.2024.106297
26. Blacklaws B.A. Small ruminant lentiviruses: Immunopathogenesis of visnamaedi and caprine arthritis and encephalitis virus. Comparative Immunology, Microbiology and Infectious Diseases. 2012; 35(3): 259–269. https://doi.org/10.1016/j.cimid.2011.12.003
27. Christodoulopoulos G. Maedi–Visna: Clinical review and short reference on the disease status in Mediterranean countries. Small Ruminant Research. 2006; 62(1–2): 47–53. https://doi.org/10.1016/j.smallrumres.2005.07.046
28. Ramírez H., Reina R., Amorena B., Andrés D.D., Martínez H.A. Small Ruminant Lentiviruses: Genetic Variability, Tropism and Diagnosis. Viruses. 2013; 5(4): 1175–1207. https://doi.org/10.3390/v5041175
29. Patel J.R., Heldens J.G.M., Bakonyi T., Rusvai M. Important mammalian veterinary viral immunodiseases and their control. Vaccine. 2012; 30(10): 1767– 1781. https://doi.org/10.1016/j.vaccine.2012.01.014
30. Gezer T., Akyüz E., Gökçe G. Investigation of Seroprevalence of Maedi-Visna Infection in Some Sheep Flocks in Kars Province, Turkey. Dicle Üniversitesi Veteriner Fakültesi Dergisi. 2021; 14(1): 48–51. https://doi.org/10.47027/duvetfd.881430
31. Shah C. et al. Phylogenetic analysis and reclassification of caprine and ovine lentiviruses based on 104 new isolates: evidence for regular sheep-to-goat transmission and worldwide propagation through livestock trade. Virology. 2004; 319(1): 12–26. https://doi.org/10.1016/j.virol.2003.09.047
32. Gjerset B., Storset A.K., Rimstad E. Genetic diversity of small-ruminant lentiviruses: characterization of Norwegian isolates of Caprine arthritis encephalitis virus. Journal of General Virology. 2006; 87(3): 573–580. https://doi.org/10.1099/vir.0.81201-0
33. Grego E., Lacerenza D., Reina Arias R., Profiti M., Rosati S. Serological characterization of the new genotype E of small ruminant lentivirus in roccaverano goat flocks. Veterinary Research Communications. 2009; 33(S1): 137–140. https://doi.org/10.1007/s11259-009-9266-8
34. Herrmann-Hoesing L.M., White S.N., Mousel M.R., Lewis G.S., Knowles D.P. Ovine progressive pneumonia provirus levels associate with breed and OvarDRB1. Immunogenetics. 2008; 60(12): 749–758. https://doi.org/10.1007/s00251-008-0328-9
35. Larruskain A. et al. MHC class II DRB1 gene polymorphism in the pathogenesis of Maedi–Visna and pulmonary adenocarcinoma viral diseases in sheep. Immunogenetics. 2010; 62(2): 75–83. https://doi.org/10.1007/s00251-009-0419-2
36. Yaman Y. et al. A novel 2 bp deletion variant in Ovine-DRB1 gene is associated with increased Visna/maedi susceptibility in Turkish sheep. Scientific Reports. 2021; 11: 14435. https://doi.org/10.1038/s41598-021-93864-8
37. White S.N., Mousel M.R., Reynolds J.O., Lewis G.S., Herrmann-Hoesing L.M. Common promoter deletion is associated with 3.9-fold differential transcription of ovine CCR5 and reduced proviral level of ovine progressive pneumonia virus. Animal Genetics. 2009; 40(5): 583–589. https://doi.org/10.1111/j.1365-2052.2009.01882.x
38. Molaee V., Eltanany M., Lühken G. First survey on association of TMEM154 and CCR5 variants with serological maedi-visna status of sheep in German flocks. Veterinary Research. 2018; 49: 36. https://doi.org/10.1186/s13567-018-0533-y
39. White S.N. et al. Genome-Wide Association Identifies Multiple Genomic Regions Associated with Susceptibility to and Control of Ovine Lentivirus. PLOS One. 2012; 7(10): e47829. https://doi.org/10.1371/journal.pone.0047829
40. White S.N., Knowles D.P. Expanding Possibilities for Intervention against Small Ruminant Lentiviruses through Genetic Marker-Assisted Selective Breeding. Viruses. 2013; 5(6): 1466–1499. https://doi.org/10.3390/v5061466
41. Sarafidou T. et al. Toll Like Receptor 9 (TLR9) Polymorphism G520R in Sheep Is Associated with Seropositivity for Small Ruminant Lentivirus. PLOS One. 2013; 8(5): e63901. https://doi.org/10.1371/journal.pone.0063901
42. White S.N. et al. Association analysis of variant near ZNF389 with ewe cumulative production in three sheep breeds. Animal Genetics. 2014; 45(4): 613–614. https://doi.org/10.1111/age.12161
43. Riggio S. et al. A high-density genome-wide approach reveals novel genetic markers linked to small ruminant lentivirus susceptibility in sheep. Frontiers in Genetics. 2024; 15: 1376883. https://doi.org/10.3389/fgene.2024.1376883
44. Larruskain A., Bernales I., Luján L., de Andrés D., Amorena B., Jugo B.M. Expression analysis of 13 ovine immune response candidate genes in Visna/ Maedi disease progression. Comparative Immunology, Microbiology and Infectious Diseases. 2013; 36(4): 405–413. https://doi.org/10.1016/j.cimid.2013.02.003
45. Orkara S. et al. Epidemiological landscape and genetic prospects for marker-assisted selection in Kazakh sheep. Frontiers in Veterinary Science. 2025; 12: 1647959. https://doi.org/10.3389/fvets.2025.1647959
46. Sebastiani C. et al. Effect of deletion of the CCR5 gene promoter on resistance to Lentivirus infection in small ruminants (SRLV)-preliminary results. XIX National Congress Italian Society of Veterinary Laboratory Diagnostics. Proceedings. 2019; 399–400 (in Italian).
47. Arcangeli C. et al. First Survey of SNPs in TMEM154, TLR9, MYD88 and CCR5 Genes in Sheep Reared in Italy and Their Association with Resistance to SRLVs Infection. Viruses. 2021; 13(7): 1290. https://doi.org/10.3390/v13071290
48. Yaman Y. Evaluation of Two SNP Markers in DPPA2 and SYTL3 Genes for Association with Host Response against Visna/Maedi Infection in Turkish Sheep. Lalahan Hayvancılık Araştırma Enstitüsü Dergisi. 2020; 60(2): 68–73. https://doi.org/10.46897/livestockstudies.846425
49. Massa A.T. et al. A DNA Regulatory Element Haplotype at Zinc Finger Genes Is Associated with Host Resilience to Small Ruminant Lentivirus in Two Sheep Populations. Animals. 2021; 11(7): 1907. https://doi.org/10.3390/ani11071907
50. Sayed A.E., Hafez A., Ateya A., Darwish A., Tahoun A. Single nucleotide polymorphisms, gene expression and evaluation of immunological, antioxidant, and pathological parameters associated with bacterial pneumonia in Barki sheep. Irish Veterinary Journal. 2025; 78: 11. https://doi.org/10.1186/s13620-025-00296-1
51. Liu X. et al. Ovine Toll-like Receptor 9 (TLR9) Gene Variation and Its Association with Flystrike Susceptibility. Animals. 2021; 11(12): 3549. https://doi.org/10.3390/ani11123549
52. Tumino S. et al. Alternative Molecular Tools for the Fight against Infectious Diseases of Small Ruminants: Native Sicilian Sheep Breeds and Maedi-Visna Genetic Susceptibility. Animals. 2022; 12(13): 1630. https://doi.org/10.3390/ani12131630
53. Thorne J.W. et al. Evolution of the sheep industry and genetic research in the United States: opportunities for convergence in the twenty-first century. Animal Genetics. 2021; 52(4): 395–408. https://doi.org/10.1111/age.13067
54. Rodrigues C.S. et al. Lentivirus Susceptibility in Brazilian and US Sheep with TMEM154 Mutations. Genes. 2023; 14(1): 70. https://doi.org/10.3390/genes14010070
55. Freking B.A., Murphy T.W., Chitko-McKown C.G., Workman A.M., Heaton M.P. Impact of Four Ovine TMEM154 Haplotypes on Ewes during Multiyear Lentivirus Exposure. International Journal of Molecular Sciences. 2022; 23(23): 14966. https://doi.org/10.3390/ijms232314966
56. Letko A., Bützberger C., Hirter N., Paris J.M., Abril C., Drögemüller C. Genetic evaluation of small ruminant lentivirus susceptibility in Valais blacknose sheep. Animal Genetics. 2021; 52(5): 781–782. https://doi.org/10.1111/age.13108
57. Riggio S., Di Gerlando R., Mastrangelo S., Rizzuto I., Tolone M., Sardina M.T. Maedi Visna virus infection and TMEM154 genotypes in Valle del Belìce sheep breed. Italian Journal of Animal Science. 2023; 22(1): 754–759. https://doi.org/10.1080/1828051X.2023.2243095
58. Frölich C., Ganter M., Adeniyi O.O., Lühken G. Genetic diversity in German Pomeranian Coarsewool sheep and the possibility of breeding for maedi-visna resistance. Archives Animal Breeding. 2025; 68(3): 517–530. https://doi.org/10.5194/aab-68-517-2025
59. Ramírez H. et al. Accurate Diagnosis of Small Ruminant Lentivirus Infection Is Needed for Selection of Resistant Sheep through TMEM154 E35K Genotyping. Pathogens. 2021; 10(1): 83. https://doi.org/10.3390/pathogens10010083
60. Cancedda M.G. et al. The role of CD163-positive macrophages in the pathogenesis of atypical proliferative lesions caused by ORF virus in sheep. Animal - science proceedings. 2023; 14(1): 231. https://doi.org/10.1016/j.anscip.2023.01.310
61. Jones S. et al. Clearance of Maedi-visna infection in a longitudinal study of naturally infected rams is associated with homozygosity for the TMEM154 resistance allele. Journal of Medical Microbiology. 2022; 71(2): 001506. https://doi.org/10.1099/jmm.0.001506
62. Heaton M.P. et al. Reduced Lentivirus Susceptibility in Sheep with TMEM154 Mutations. PLOS Genetics. 2012; 8(1): e1002467. https://doi.org/10.1371/journal.pgen.1002467
63. Yaman Y. et al. Association of TMEM154 variants with visna/maedi virus infection in Turkish sheep. Small Ruminant Research. 2019; 177: 61–67. https://doi.org/10.1016/j.smallrumres.2019.06.006
64. Dickey A.M., Smith T.P.L., Clawson M.L., Heaton M.P., Workman A.M. Classification of small ruminant lentivirus subtype A2, subgroups 1 and 2 based on whole genome comparisons and complex recombination patterns. F1000Research. 2021; 9: 1449. https://doi.org/10.12688/f1000research.27898.2
65. Materniak-Kornas M. et al. First Report of SNPs Detection in TMEM154 Gene in Sheep from Poland and Their Association with SRLV Infection Status. Pathogens. 2025; 14(1): 16. https://doi.org/10.3390/pathogens14010016
66. Belliveau N. et al. Galvanin (TMEM154) is an electric-field sensor for directed cell migration. Cell. 2026; 189(13): 4107–4121.e22. https://doi.org/10.1016/j.cell.2026.04.026
67. Deniskova T.E., Solovieva A.D., Koshkina O.A., Yakovleva O.S., Dotsev A.V., Zinovieva N.A. Development and validation of a test system for identifying resistant haplotypes to Maedi-Visna virus in sheep. Animal Husbandry and Fodder Production. 2025; 108(4): 151–161 (in Russian). https://doi.org/10.33284/2658-3135-108-4-151
68. Yurchenko A.A. et al. High-density genotyping reveals signatures of selection related to acclimation and economically important traits in 15 local sheep breeds from Russia. BMC Genomics. 2019; 20(S3): 294. https://doi.org/10.1186/s12864-019-5537-0
69. Peakall R., Smouse P.E. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics. 2012; 28(19): 2537–2539. https://doi.org/10.1093/bioinformatics/bts460
Review
For citations:
Yakovleva O.S., Deniskova T.E., Koshkina O.A., Dotsev A.V., Solovieva A.D., Zinovieva N.A. Characteristics of genetic resistance to Maedi-Visna in sheep breeds raised in Russia. Agrarian science. 2026;1(8):84-94. (In Russ.) https://doi.org/10.32634/0869-8155-2026-409-08-84-94
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