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Genome-wide DNA methylation pattern in a mouse model reveals two novel genes associated with Staphylococcus aureus mastitis

  • Wang, Di (Key Laboratory of Agricultural Animal Genetics and Breeding, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University) ;
  • Wei, Yiyuan (Key Laboratory of Agricultural Animal Genetics and Breeding, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University) ;
  • Shi, Liangyu (Key Laboratory of Agricultural Animal Genetics and Breeding, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University) ;
  • Khan, Muhammad Zahoor (Key Laboratory of Agricultural Animal Genetics and Breeding, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University) ;
  • Fan, Lijun (Key Laboratory of Agricultural Animal Genetics and Breeding, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University) ;
  • Wang, Yachun (Key Laboratory of Agricultural Animal Genetics and Breeding, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University) ;
  • Yu, Ying (Key Laboratory of Agricultural Animal Genetics and Breeding, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University)
  • Received : 2018.11.15
  • Accepted : 2019.03.07
  • Published : 2020.02.01

Abstract

Objective: Staphylococcus aureus (S. aureus) is one of the major microorganisms responsible for subclinical mastitis in dairy cattle. The present study was designed with the aim to explore the DNA methylation patterns using the Fluorescence-labeled methylation-sensitive amplified polymorphism (F-MSAP) techniques in a S. aureus-infected mouse model. Methods: A total of 12 out-bred Institute of Cancer Research female mice ranging from 12 to 13 weeks-old were selected to construct a mastitis model. F-MSAP analysis was carried out to detect fluctuations of DNA methylation between control group and S. aureus mastitis group. Results: Visible changes were observed in white cell counts in milk, percentage of granulocytes, percentage of lymphocytes, CD4+/CD8+ ratio (CD4+/CD8+), and histopathology of mice pre- and post-challenge with S. aureus. These findings showed the suitability of the S. aureus-infected mouse model. A total of 369 fragments was amplified from udder tissue samples from the two groups (S. aureus-infected mastitis group and control group) using eight pairs of selective primers. Results indicated that the methylation level of mastitis mouse group was higher than that in the control group. In addition, NCK-associated protein 5 (Nckap5) and transposon MTD were identified to be differentially methylated through secondary polymerase chain reaction and sequencing in the mastitis group. These observations might play an important role in the development of S. aureus mastitis. Conclusion: Collectively, our study suggests that the methylation modification in Nckap5 and transposon MTD might be considered as epigenetic markers in resistance to S. aureus-infected mastitis and provided a new insight into S. aureus mastitis research in dairy industry and public health.

Acknowledgement

Supported by : Beijing Natural Science Foundation, National Natural Science Foundation of China

References

  1. Bradley AJ. Bovine mastitis: an evolving disease. Vet J 2002; 164:116-28. https://doi.org/10.1053/tvjl.2002.0724 https://doi.org/10.1053/tvjl.2002.0724
  2. Viguier C, Arora S, Gilmartin N, Welbeck K, O'Kennedy R. Mastitis detection: current trends and future perspectives. Trends Biotechnol 2009;27:486-93. https://doi.org/10.1016/j.tibtech.2009.05.004 https://doi.org/10.1016/j.tibtech.2009.05.004
  3. Hagnestam-Nielsen C, Emanuelson U, Berglund B, Strandberg E. Relationship between somatic cell count and milk yield in different stages of lactation. J Dairy Sci 2009;92:3124-33. https://doi.org/10.3168/jds.2008-1719 https://doi.org/10.3168/jds.2008-1719
  4. Sordillo LM, Streicher KL. Mammary gland immunity and mastitis susceptibility. J Mammary Gland Biol Neoplasia 2002; 7:135-46. https://doi.org/10.1023/A:1020347818725
  5. Donovan DV, Kerr DE, Wall RJ. Engineering disease resistant cattle. Transgenic Res 2005;14:563-7. https://doi.org/10.1007/s11248-005-0670-8 https://doi.org/10.1007/s11248-005-0670-8
  6. Sharma N, Singh NK, Bhadwal MS. Relationship of somatic cell count and mastitis: an overview. Asian-Australas J Anim Sci 2011;24:429-38. https://doi.org/10.5713/ajas.2011.10233 https://doi.org/10.5713/ajas.2011.10233
  7. Sears PM, McCarthy KK. Management and treatment of staphylococcal mastitis. Vet Clin North Am Food Anim Pract 2003;19:171-85. https://doi.org/10.1016/S0749-0720(02)00079-8 https://doi.org/10.1016/S0749-0720(02)00079-8
  8. Zilberman D, Henikoff S. Genome-wide analysis of DNA methylation patterns. Development 2007;134:3959-65. https://doi.org/10.1242/dev.001131 https://doi.org/10.1242/dev.001131
  9. Whayne TF. Epigenetics in the development, modification, and prevention of cardiovascular disease. Mol Biol Rep 2015; 42:765-76. https://doi.org/10.1007/s11033-014-3727-z https://doi.org/10.1007/s11033-014-3727-z
  10. Ogorevc J, Kunej T, Razpet A, Dovc P. Database of cattle candidate genes and genetic markers for milk production and mastitis. Anim Genet 2009;40:832-51. https://doi.org/10.1111/j.1365-2052.2009.01921.x https://doi.org/10.1111/j.1365-2052.2009.01921.x
  11. Wang XS, Zhang Y, He YH, et al. Aberrant promoter methylation of the CD4 gene in peripheral blood cells of mastitic dairy cows. Genet Mol Res 2013;12:6228-39. https://doi.org/10.4238/2013.December.4.10 https://doi.org/10.4238/2013.December.4.10
  12. Chang G, Petzl W, Vanselow J, Gunther J, Shen X, Seyfert HM. Epigenetic mechanisms contribute to enhanced expression of immune response genes in the liver of cows after experimentally induced Escherichia coli mastitis. Vet J 2015;203: 339-41. https://doi.org/10.1016/j.tvjl.2014.12.023 https://doi.org/10.1016/j.tvjl.2014.12.023
  13. Song MY, He YH, Zhou HK, Zhang Y, Yu Y. Combined analysis of DNA methylome and transcriptome reveal novel candidate genes with susceptibility to bovine Staphylococcus aureus subclinical mastitis. Sci Rep 2016;6:29390. https://doi.org/10.1038/srep29390 https://doi.org/10.1038/srep29390
  14. Breyne K, Honaker RW, Hobbs Z, et al. Efficacy and safety of a bovine-associated Staphylococcus aureus phage cocktail in a murine model of mastitis. Front Microbiol 2017;8:2348. https://doi.org/10.3389/fmicb.2017.02348 https://doi.org/10.3389/fmicb.2017.02348
  15. Guevara MA, de Maria N, Saez-Laguna E, Velez MD, Cervera MT, Cabezas JA. Analysis of DNA cytosine methylation patterns using methylation-sensitive amplification polymorphism (MSAP). In: Kovalchuk I, editor. Plant Epigenetics. Methods in Molecular Biology. Boston, MA, USA: Humana Press; 2017. vol 1456. pp. 99-112. https://doi.org/10.1007/978-1-4899-7708-3_9
  16. Xu Q, Sun D, Zhang Y. F-MSAP: A practical system to detect methylation in chicken genome. Chin Sci Bull 2005;50:2039-44. https://doi.org/10.1007/BF03322798 https://doi.org/10.1360/982005-834
  17. National Mastitis Council. Laboratory handbook on bovine mastitis. Nat Mastitis Council; 1999.
  18. Gao J, Ferreri M, Liu XQ, Chen LB, Su JL, Han B. Development of multiplex polymerase chain reaction assay for rapid detection of Staphylococcus aureus and selected antibiotic resistance genes in bovine mastitic milk samples. J Vet Diagn Invest 2011;23:894-901. https://doi.org/10.1177/1040638711416964 https://doi.org/10.1177/1040638711416964
  19. Brakstad OG, Aasbakk K, Maeland JA. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J Clin Microbiol 1992;30:1654-60. https://doi.org/10.1128/JCM.30.7.1654-1660.1992
  20. Lettau M, Qian J, Linkermann A, Latreille M, Larose L, Kabelitz D, et al. The adaptor protein Nck interacts with Fas ligand: Guiding the death factor to the cytotoxic immunological synapse. Proc Natl Acad Sci USA 2006;103:5911-6. https://doi.org/10.1073/pnas.0508562103 https://doi.org/10.1073/pnas.0508562103
  21. Brouillette E, Malouin F. The pathogenesis and control of Staphylococcus aureus-induced mastitis: study models in the mouse. Microbes Infect 2005;7:560-8. https://doi.org/10.1016/j.micinf.2004.11.008 https://doi.org/10.1016/j.micinf.2004.11.008
  22. Fan LJ, Zhang MZ, Wei YY, et al. Establishment of mice models of staphylococcus aureus of dairy cows mastitis. Laboratory Anim Sci 2011;28:1-6.
  23. Vos P, Hogers R, Bleeker M, et al. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 1995;23:4407-14. https://doi.org/10.1093/nar/23.21.4407 https://doi.org/10.1093/nar/23.21.4407
  24. Huang J, Sun M. A modified AFLP with fluorescence-labelled primers and automated DNA sequencer detection for efficient fingerprinting analysis in plants. Biotechnol Tech 1999;13: 277-8. https://doi.org/10.1023/A:1008970618252 https://doi.org/10.1023/A:1008970618252
  25. Luciano M, Huffman JE, Arias-Vasquez A, et al. Genome-wide association uncovers shared genetic effects among personality traits and mood states. Am J Med Genet B Neuropsychiatr Genet 2016;159B:684-95. https://doi.org/10.1002/ajmg.b.32072
  26. Chen C, Bartenhagen C, Gombert M, et al. Next-generation-sequencing-based risk stratification and identification of new genes involved in structural and sequence variations in near haploid lymphoblastic leukemia. Genes Chromosomes Cancer 2013;52:564-79. https://doi.org/10.1002/gcc.22054 https://doi.org/10.1002/gcc.22054
  27. Yu Y, Zhang H, Tian F, et al. Quantitative evaluation of DNA methylation patterns for ALVE and TVB genes in a neoplastic disease susceptible and resistant chicken model. PloS One 2008;3:e1731. https://doi.org/10.1371/journal.pone.0001731 https://doi.org/10.1371/journal.pone.0001731
  28. Eymery A, Liu Z, Ozonov EA, Stadler MB, Peters AH. The methyltransferase Setdb1 is essential for meiosis and mitosis in mouse oocytes and early embryos. Development 2016;143: 2767-79. https://doi.org/10.1242/dev.132746 https://doi.org/10.1242/dev.132746
  29. Sekhon RS, Peterson T, Chopra S. Epigenetic modifications of distinct sequences of the p1 regulatory gene specify tissue-specific expression patterns in maize. Genetics 2007;175:1059-70. https://doi.org/10.1534/genetics.106.066134 https://doi.org/10.1534/genetics.106.066134
  30. Ong-Abdullah M, Ordway JM, Jiang N, et al. Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 2015;525:533-7. https://doi.org/10.1038/nature15365 https://doi.org/10.1038/nature15365