Transcriptomic changes in ruminal tissue induced by the periparturient transition in dairy cows

American Journal of Animal and Veterinary Sciences

Volumn 9, Issue 1, 2014, Pages 36-45

  Dionissopoulos, Louis ^a   AlZahal, Ousama ^a   Steele, Michael Alexander ^a   Matthews, James Clyde ^b   McBride, Brian William ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Biological Interactome; Fat Metabolism; Immune System; Microarray; Parturition; Transition Period

Indexed keywords

EID: 84896453614     PISSN: 15574555     EISSN: 15574563     Source Type: Journal    
DOI: 10.3844/ajavsp.2014.36.45     Document Type: Article

References (64)

1. Adrien, M.L., D.A. Mattiauda, V. Artegoitia, M. Carriquiry and G. Motta et al., 2012. Nutritional regulation of body condition score at the initiation of the transition period in primiparous and multiparous dairy cows under grazing conditions: Milk production, resumption of post-partum ovarian cyclicity and metabolic parameters. Animals, 6: 292-299.
2. AlZahal, O., B. Rustomo, N.E. Odongo, T.F. Duffield and B. W. McBride, 2007. Technical note: A system for continuous recording of ruminal pH in cattle. J. Anim. Sci., 85: 213-217. DOI: 10.2527/jas.2006-095
3. Aschenbach, J.R., G.B. Penner, F. Stumpff and G. Gabel, 2011. Ruminant nutrition symposium: Role of fermentation acid absorption in the regulation of ruminal pH. J. Anim. Sci., 89: 1092-1107. DOI: 10.2527/jas.2010-3301
4. Badeanlou, L., C. Furlan-Freguia, G. Yang, W. Ruf and F. Samad, 2011. Tissue factor-protease-activated receptor 2 signaling promotes diet-induced obesity and adipose inflammation. Nat. Med., 17: 1490-1497. DOI: 10.1038/nm.2461
5. Bost, F., M. Aouadi, L. Caron, P. Even and N. Belmonte et al., 2005. The extracellular signal-regulated kinase isoform ERK1 is specifically required for in vitro and in vivo adipogenesis. Diabetes, 54: 402-411. DOI: 10.2337/diabetes.54.2.402
6. Camby, I., M. Le Mercier, F. Lefranc and R. Kiss, 2006. Galectin-1: A small protein with major functions. Glycobiology, 16: 137R-157R. DOI: 10.1093/glycob/cwl025
7. Cao, H., L.C. Kabaroff, Q. You, A. Rodriguez, H. J. Boermans and N. A. Karrow, 2006. Characterization of ovine hepatic gene expression profiles in response to Escherichia coli lipopolysaccharide using a bovine cDNA microarray. BMC Vet. Res., 2: 34. DOI: 10.1186/1746-6148-2-34
8. Crowley, M.R., K.L. Head, D.J. Kwiatkowski, H.L. Asch and B.B. Asch, 2000. The mouse mammary gland requires the actin-binding protein gelsolin for proper ductal morphogenesis. Dev. Biol., 225: 407-423. DOI: 10.1006/dbio.2000.9844
9. Czech, B., I.D. Neumann, M. Muller, S.O. Reber and C. Hellerbrand, 2013. Effect of chronic psychosocial stress on nonalcoholic steatohepatitis in mice. Int. J. Clin. Exp. Pathol., 6: 1585-1593. PMID: 23923077
10. Dann, H.M., N.B. Litherland, J.P. Underwood, M. Bionaz and A. D'Angelo et al., 2006. Diets during far-off and close-up dry periods affect periparturient metabolism and lactation in multiparous cows. J. Dairy Sci., 89: 3563-3577. DOI: 10.3168/jds.S0022-0302(06)72396-7
11. Dionissopoulos, L., A.H. Laarman, O. AlZahal, S.L. Greenwood and M.A. Steele et al., 2013. Butyratemediated genomic changes involved in non-specific host defenses, matrix remodeling and the immune response in the rumen epithelium of cows afflicted with subacute ruminal acidosis. Am. J. Anim. Vet. Sci., 8: 8-27. DOI: 10.3844/ajavsp.2013.8.27
12. Dionissopoulos, L., C.E. Dewey, H. Namkung and C.F.M. de Lange, 2006. Interleukin-1ra increases growth performance and body protein accretion and decreases the cytokine response in a model of subclinical disease in growing pigs. Anim. Sci., 82: 509-515. DOI: 10.1079/ASC200654
13. Dionissopoulos, L., M.A. Steele, O. AlZahal, J.C. Plaizier and B.W. McBride, 2012. A characterization of inflammatory and structural markers within the rumen epithelium during grain-induced ruminal acidosis in lactating dairy cattle. Am. J. Anim. Vet. Sci., 7: 141-148. DOI: 10.3844/ajavsp.2012.141.148
14. Drackley, J. K., S.S. Donkin and C.K. Reynolds, 2006. Major advances in fundamental dairy cattle nutrition. J. Dairy Sci., 89: 1324-1336. DOI: 10.3168/jds.S0022-0302(06)72200-7
15. Drackley, J.K., 1999. Biology of dairy cows during the transition period: The final frontier? J. Dairy Sci., 82: 2259-2273. DOI: 10.3168/jds.S0022-0302(99)75474-3
16. Duffield, T., 1999. A fistful of rumen--a novel approach to rumen fistula surgery. Proceedings of the Annual Convention, (PAC' 99), American Association of Bovine Practitioners, pp: 179-179.
17. Eberle, D., B. Hegarty, P. Bossard, P. Ferre and F. Foufelle, 2004. SREBP transcription factors: Master regulators of lipid homeostasis. Biochimie, 86: 839-848. DOI: 10.1016/j.biochi.2004.09.018
18. Esposito, G., P.C. Irons, E.C. Webb and A. Chapwanya, 2013. Interactions between negative energy balance, metabolic diseases, uterine health and immune response in transition dairy cows. Anim. Reproduct. Sci. DOI: 10.1016/j.anireprosci.2013.11.007
19. Gabel, G. and J. Sehested, 1997. SCFA transport in the forestomach of ruminants. Comp. Biochem. Physiol. Physiol., 118: 367-374. DOI: 10.1016/S0300-9629(96)00321-0
20. Galindo, R.C., N. Ayllon, T. Carta, J. Vicente and K.M. Kocan et al., 2010. Characterization of pathogenspecific expression of host immune response genes in Anaplasma and Mycobacterium species infected ruminants. Comp. Immunol. Microbiol. Infect. Dis., 33: e133-142. DOI: 10.1016/j.cimid.2010.09.001
21. Grummer, R.R., 1995. Impact of changes in organic nutrient metabolism on feeding the transition dairy cow. J. Anim. Sci., 73: 2820-2833. PMID: 8582873
22. Guenard, F., L. Bouchard, A. Tchernof, Y. Deshaies and F.S. Hould et al., 2013. DUSP1 gene polymorphisms are associated with obesity-related metabolic complications among severely obese patients and impact on gene methylation and expression. Int. J. Genomics. DOI: 10.1155/2013/609748
23. Hutjens, F. and P. Aalseth, 2005. Caring for z. W.D. Hoard and Sons.
24. Ingvartsen, K.L., 2006. Feeding-and managementrelated diseases in the transition cow: Physiological adaptations around calving and strategies to reduce feeding-related diseases. Anim. Feed Sci. Technol., 126: 175-213. DOI: 10.1016/j.anifeedsci.2005.08.003
25. Ji, P., J.S. Osorio, J.K. Drackley and J.J. Loor, 2012. Overfeeding a moderate energy diet prepartum does not impair bovine subcutaneous adipose tissue insulin signal transduction and induces marked changes in peripartal gene network expression. J. Dairy Sci., 95: 4333-4351. DOI: 10.3168/jds.2011-5079
26. Kristensen, N.B., A. Danfaer and N. Agergaard, 1998. Absorption and metabolism of short-chain fatty acids in ruminants. Arch. Tierernahr., 51: 165-175. DOI: 10.1080/17450399809381916
27. Kuhla, B., G. Nurnberg, D. Albrecht, S. Gors, H.M. Hammon and C.C. Metges, 2011. Involvement of skeletal muscle protein, glycogen and fat metabolism in the adaptation on early lactation of dairy cows. J. Proteome Res., 10: 4252-4262. DOI: 10.1021/pr200425h
28. Laliotis, G.P., I. Bizelis and E. Rogdakis, 2010. Comparative approach of the de novo fatty acid synthesis (Lipogenesis) between ruminant and non ruminant mammalian species: From biochemical level to the main regulatory lipogenic genes. Curr. Genomics, 11: 168-183. DOI: 10.2174/138920210791110960
29. Leroy, J., T. Vanholder, A.T.M. Van Knegsel, I. Garcia-Ispierto and P.E.J. Bols, 2008. Nutrient prioritization in dairy cows early postpartum: Mismatch between metabolism and fertility? Reproduct. Domestic Anim., 43: 96-103. DOI: 10.1111/j.1439-0531.2008.01148.x
30. Liu, Y.X., J. Wang, J. Guo, J. Wu, H. B. Lieberman and Y. Yin. 2008. DUSP1 is controlled by p53 during the cellular response to oxidative stress. Mol. Cancer Res., 6: 624-633. DOI: 10.1158/1541-7786.MCR-07-2019
31. Loor, J.J., 2010. Genomics of metabolic adaptations in the peripartal cow. Animal., 4: 1110-1139. DOI: 10.1017/S1751731110000960
32. Loor, J.J., H. M. Dann, N.A. Guretzky, R.E. Everts and R. Oliveira et al., 2006. Plane of nutrition prepartum alters hepatic gene expression and function in dairy cows as assessed by longitudinal transcript and metabolic profiling. Physiol. Genomics, 27: 29-41. DOI: 10.1152/physiolgenomics.00036.2006
33. Moyes, K.M., J.K. Drackley, D.E. Morin, S.L. Rodriguez-Zas and R.E. Everts et al., 2011. Predisposition of cows to mastitis in non-infected mammary glands: effects of dietary-induced negative energy balance during mid-lactation on immune-related genes. Funct. Integr. Genomics, 11: 151-156. DOI: 10.1007/s10142-010-0186-z
34. Mulligan, F.J. and M.L. Doherty, 2008. Production diseases of the transition cow. Vet. J., 176: 3-9. DOI: 10.1016/j.tvjl.2007.12.018
35. Mulligan, F.J., L. O'Grady, D.A. Rice and M.L. Doherty, 2006. A herd health approach to dairy cow nutrition and production diseases of the transition cow. Anim. Reprod. Sci., 96: 331-353. DOI: 10.1016/j.anireprosci.2006.08.011
36. NRC, 2001. Nutrient Requirements of Dairy Cattle. 1st Edn., National Academy Press, Washington, D.C.
37. Osorio, J.S., P. Ji, J. K. Drackley, D. Luchini and J. J. Loor, 2013. Supplemental smartamine m or metasmart during the transition period benefits postpartal cow performance and blood neutrophil function. J. Dairy Sci., 96: 6248-6263. DOI: 10.3168/jds.2012-5790
38. Overton, T.R. and M.R. Waldron, 2004. Nutritional management of transition dairy cows: Strategies to optimize metabolic health. J. Dairy Sci., 87: E105-E119. DOI: 10.3168/jds.S0022-0302(04)70066-1
39. Penner, G. B., M. A. Steele, J. R. Aschenbach and B.W. McBride, 2011. Ruminant nutrition symposium: Molecular adaptation of ruminal epithelia to highly fermentable diets. J. Anim. Sci., 89: 1108-1119. DOI: 10.2527/jas.2010-3378
40. Pfaffl, M.W., A. Tichopad, C. Prgomet and T.P. Neuvians, 2004. Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper--Excel-based tool using pairwise correlations. Biotechnol. Lett., 26: 509-515. DOI: 10.1023/B:BILE.0000019559.84305.47
41. Piantoni, P., P. Wang, J. K. Drackley, W.L. Hurley and J.J. Loor, 2010. Expression of metabolic, tissue remodeling, oxidative stress and inflammatory pathways in mammary tissue during involution in lactating dairy cows. Bioinform. Biol. Insights, 4: 85-97. PMID: 20981268
42. Plaizier, J.C., D.O. Krause, G.N. Gozho and B.W. McBride, 2008. Subacute ruminal acidosis in dairy cows: the physiological causes, incidence and consequences. Vet. J., 176: 21-31. DOI: 10.1016/j.tvjl.2007.12.016
43. Reiner, A., D. Yekutieli and Y. Benjamini, 2003. Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics, 19: 368-375. DOI: 10.1093/bioinformatics/btf877
44. Reinhardt, C., M. Bergentall, T. U. Greiner, F. Schaffner and G. Ostergren-Lunden et al., 2012. Tissue factor and PAR1 promote microbiota-induced intestinal vascular remodelling. Nature, 483: 627-631. DOI: 10.1038/nature10893
45. Sabbisetti, V., A. Di Napoli, A. Seeley, A. M. Amato and E. O'Regan et al., 2009. p63 promotes cell survival through fatty acid synthase. PLoS One, 4: e5877. DOI: 10.1371/journal.pone.0005877
46. Sanchez-Gurmaches, J., C.M. Hung, C.A. Sparks, Y. Tang, H. Li and D.A. Guertin, 2012. PTEN loss in the Myf5 lineage redistributes body fat and reveals subsets of white adipocytes that arise from Myf5 precursors. Cell Metab., 16: 348-362. DOI: 10.1016/j.cmet.2012.08.003
47. SAS, 2004. SAS/STAT User's Guide Release 9.1. 1st Edn., SAS Institute Inc., Cary, NC.
48. Seo, H.Y., M.K. Kim, Y.A. Jung, B.K. Jang and E.K. Yoo et al., 2013. Clusterin decreases hepatic SREBP-1c expression and lipid accumulation. Endocrinology, 154: 1722-1730. DOI: 10.1210/en.2012-2009
49. Shimba, S., T. Wada, S. Hara and M. Tezuka, 2004. EPAS1 promotes adipose differentiation in 3T3-L1 cells. J. Biol. Chem., 279: 40946-40953. DOI: 10.1074/jbc.M400840200
50. Sordillo, L.M. and W. Raphael, 2013. Significance of metabolic stress, lipid mobilization and inflammation on transition cow disorders. Vet. Clin. North Am. Food Anim. Pract., 29: 267-278. DOI: 10.1016/j.cvfa.2013.03.002
51. Springer, H.R. and I.S.U.B. Sciences, 2008. Effect of pre-calving diet energy content on immunologic and metabolic parameters in the transition cow. MSc Thesis, Science Iowa State University.
52. Steele, M.A., J. Croom, M. Kahler, O. AlZahal, S.E. Hook, K. Plaizier and B.W. McBride, 2011a. Bovine rumen epithelium undergoes rapid structural adaptations during grain-induced subacute ruminal acidosis. Am. J. Physiol. Regul. Integr. Comp. Physiol., 300: R1515-1523. DOI: 10.1152/ajpregu.00120.2010
53. Steele, M.A., G. Vandervoort, O. AlZahal, S.E. Hook and J.C. Matthews et al., 2011b. Rumen epithelial adaptation to high-grain diets involves the coordinated regulation of genes involved in cholesterol homeostasis. Physiol. Genom., 43: 308-316. DOI: 10.1152/physiolgenomics.00117.2010
54. Steele, M.A., O. Alzahal, M.E. Walpole and B.W. McBride, 2012a. Short communication: Graininduced subacute ruminal acidosis is associated with the differential expression of insulin-like growth factor-binding proteins in rumen papillae of lactating dairy cattle. J. Dairy Sci., 95: 6072-6076. DOI: 10.3168/jds.2011-4864
55. Steele, M.A., L. Dionissopoulos, O. AlZahal, J. Doelman and B.W. McBride, 2012b. Rumen epithelial adaptation to ruminal acidosis in lactating cattle involves the coordinated expression of insulin-like growth factor-binding proteins and a cholesterolgenic enzyme. J. Dairy Sci., 95: 318-327. DOI: 10.3168/jds.2011-4864
56. Tanabe, M. and M. Kanehisa, 2012. Using the KEGG Database Resource. In: Current Protocols in Bioinformatics.
57. Vernon, R.G., 2005. Lipid metabolism during lactation: A review of adipose tissue-liver interactions and the development of fatty liver. J. Dairy Res., 72: 460-469. DOI: 10.1017/S0022029905001299
58. Weber, C., C. Hametner, A. Tuchscherer, B. Losand and E. Kanitz et al., 2013. Hepatic gene expression involved in glucose and lipid metabolism in transition cows: Effects of fat mobilization during early lactation in relation to milk performance and metabolic changes. J. Dairy Sci., 96: 5670-5681. DOI: 10.3168/jds.2012-6277
59. Wrana, J.L., 2009. The secret life of Smad4. Cell, 136: 13-14. DOI: 10.1016/j.cell.2008.12.028
60. Xue, Y., S.F. Liao, K.W. Son, S.L. Greenwood and B.W. McBride et al., 2010. Metabolic acidosis in sheep alters expression of renal and skeletal muscle amino acid enzymes and transporters. J. Anim. Sci., 88: 707-717. DOI: 10.2527/jas.2009-2101
61. Yang, C.S., D.S. Lee, C.H. Song, S.J. An and S. Li et al., 2007. Roles of peroxiredoxin II in the regulation of proinflammatory responses to LPS and protection against endotoxin-induced lethal shock. J. Exp. Med., 204: 583-594. DOI: 10.1084/jem.20061849041807c
62. Yang, R. and L.A. Barouch, 2007. Leptin signaling and obesity: Cardiovascular consequences. Circ. Res., 101: 545-559. DOI: 10.1161/CIRCRESAHA.107.156596
63. Zhou, T., 2013. Computational reconstruction of metabolic networks from KEGG. Methods Mol. Biol., 930: 235-249. DOI: 10.1007/978-1-62703-059-5_10
64. Zmuda, E.J., L. Qi, M.X. Zhu, R.G. Mirmira, M.R. Montminy and T. Hai, 2010. The roles of ATF3, an adaptive-response gene, in high-fat-dietinduced diabetes and pancreatic beta-cell dysfunction. Mol. Endocrinol., 24: 1423-1433. DOI: 10.1210/me.2009-0463