Impact of the severity of negative energy balance on gene expression in the subcutaneous adipose tissue of periparturient primiparous Holstein dairy cows: Identification of potential novel metabolic signals for the reproductive system


Autoři: Namya Mellouk aff001;  Christelle Rame aff001;  Delphine Naquin aff004;  Yan Jaszczyszyn aff004;  Jean-Luc Touzé aff001;  Eric Briant aff005;  Daniel Guillaume aff001;  Theodoros Ntallaris aff006;  Patrice Humblot aff006;  Joëlle Dupont aff001
Působiště autorů: INRA UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France aff001;  CNRS UMR7247 Physiologie de la Reproduction et des Comportements, Nouzilly, France aff002;  Université François Rabelais de Tours F-37041 Tours, Nouzilly, France aff003;  Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Gif-sur-Yvette, France aff004;  INRA, UEPAO 1297, Nouzilly, France aff005;  Division of reproduction, Department of Clinical Sciences, SLU, Uppsala, Sweden aff006
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: 10.1371/journal.pone.0222954

Souhrn

The severity of negative energy balance (NEB) in high-producing dairy cows has a high incidence among health diseases. The cow’s energy status during early lactation critically affects metabolic and reproductive parameters. The first objective of this study was to investigate by RNA-seq analysis and RT-qPCR the gene expression profile in white adipose tissue and by gene ontology and upstream regulation tools the relationships with energy metabolism and reproduction in two groups of primiparous dairy cows with extreme NEB statuses (NEB < -9 Mcal/day vs. NEB > -9 Mcal/day) around parturition. The second objective was to determine the potential involvement of a new adipokine identified as a candidate for the regulation of ovarian function in our RNA-seq analysis by using bovine primary granulosa culture, thymidine incorporation to determine cell proliferation and ELISA assays to measure progesterone secretion. The RNA-seq analysis revealed that 514 genes were over-expressed and 695 were under-expressed in the adipose tissue of cows with severe NEB (SNEB) and cows with moderate NEB (MNEB) during the -4 and 16 wkpp period. In addition, 491 genes were over-expressed and 705 genes were under-expressed in the adipose tissue of SNEB cows compared to MNEB cows. Among these differently expressed genes (DEGs), 298 were related to metabolic functions and 264 to reproductive traits. A set of 19 DEGs were validated by RT-qPCR, including CCL21 (C-C motif chemokine ligand 21). Moreover, CCL21, a gene known to be secreted by adipose tissue, was chosen for further analysis in plasma and ovaries. The use of next-generation sequencing technologies allowed us to characterise the transcriptome of white adipose tissue from primiparous cows with different levels of NEB during lactation. This study highlighted the alteration of the expression of genes related to lipid metabolism, including CCL21, which is released in the bloodstream and associated with the in vitro regulation of ovarian functions.

Klíčová slova:

Adipose tissue – Biomarkers – Blood plasma – Gene expression – Lactation – Progesterone – Granulosa cells – Lipid metabolism


Zdroje

1. Ferguson JD. Nutrition and reproduction in dairy herds. Salt Lake City, Utah: Proceedings of Intermountain Nutrition Conference; 2001: 65–82.

2. Trevisi E, Amadori M, Cogrossi S, Razzuoli E, Bertoni G. Metabolic stress and inflammatory response in high-yielding, periparturient dairy cows. Res Vet Sci, 2012; 93:695–704. doi: 10.1016/j.rvsc.2011.11.008 22197526

3. Goff JP, Horst RL. Physiological changes at parturition and their relationship to metabolic disorders. 1997; J. Dairy Sci. 80:1260–1268.1. doi: 10.3168/jds.S0022-0302(97)76055-7 9241588

4. Sordillo LM, Raphael W. Significance of metabolic stress, lipid mobilization, and inflammation on transition cow disorders. Vet Clin North Am Food Anim Pract 2013; 29(2):267–278. doi: 10.1016/j.cvfa.2013.03.002 23809891

5. LeBlanc SJ, Leslie KE, Duffield TF. Metabolic predictors of displaced abomasum in dairy cattle. J Dairy Sci 2005; 88(1):159–170. doi: 10.3168/jds.S0022-0302(05)72674-6 15591379

6. Kuhla B, Metges CC, Hammon HM. Endogenous and dietary lipids influencing feed intake and energy metabolism of periparturient dairy cows. Domest Anim Endocrinol 2016; 56 Suppl:S2–S10.

7. Han van der Kolk JH, Gross JJ, Gerber V, Bruckmaier RM. Disturbed bovine mitochondrial lipid metabolism: a review. Vet Q 2017; 37(1):262–273. doi: 10.1080/01652176.2017.1354561 28712316

8. Gillund P, Reksen O, Grohn YT, Karlberg K. Body condition related to ketosis and reproductive performance in Norwegian dairy cows. J Dairy Sci 2001; 84(6):1390–1396. doi: 10.3168/jds.S0022-0302(01)70170-1 11417697

9. Abdelli A, Raboisson D, Kaidi R, Ibrahim B, Kalem A, Iguer-Ouada M. Elevated non-esterified fatty acid and beta-hydroxybutyrate in transition dairy cows and their association with reproductive performance and disorders: A meta-analysis. Theriogenology 2017; 93:99–104. doi: 10.1016/j.theriogenology.2017.01.030 28257874

10. Moore SG, Pryce JE, Hayes BJ, Chamberlain AJ, Kemper KE, Berry DP, et al. Differentially Expressed Genes in Endometrium and Corpus Luteum of Holstein Cows Selected for High and Low Fertility Are Enriched for Sequence Variants Associated with Fertility. Biol Reprod 2016; 94(1):19. doi: 10.1095/biolreprod.115.132951 26607721

11. Wathes DC, Clempson AM, Pollott GE. Associations between lipid metabolism and fertility in the dairy cow. Reprod Fertil Dev 2012; 25(1):48–61. doi: 10.1071/RD12272 23244828

12. Mohamed-Ali V, Pinkney JH, Coppack SW. Adipose tissue as an endocrine and paracrine organ. Int J Obes Relat Metab Disord 1998; 22(12):1145–1158. 9877249

13. McNamara JP. Regulation of bovine adipose tissue metabolism during lactation. 5. Relationships of lipid synthesis and lipolysis with energy intake and utilization. J Dairy Sci 1989; 72(2):407–418. doi: 10.3168/jds.S0022-0302(89)79122-0 2703565

14. Sumner-Thomson JM, Vierck JL, McNamara JP. Differential expression of genes in adipose tissue of first-lactation dairy cattle. J Dairy Sci 2011; 94(1):361–369. doi: 10.3168/jds.2010-3447 21183046

15. Sumner JM, McNamara JP. Expression of lipolytic genes in the adipose tissue of pregnant and lactating Holstein dairy cattle. J Dairy Sci 2007; 90(11):5237–5246. doi: 10.3168/jds.2007-0307 17954764

16. Alharthi A, Zhou Z, Lopreiato V, Trevisi E, Loor JJ. Body condition score prior to parturition is associated with plasma and adipose tissue biomarkers of lipid metabolism and inflammation in Holstein cows. J Anim Sci Biotechnol 2018; 9:12. doi: 10.1186/s40104-017-0221-1 29387386

17. Rocco SM, McNamara JP. Regulation of bovine adipose tissue metabolism during lactation. 7. Metabolism and gene expression as a function of genetic merit and dietary energy intake. J Dairy Sci 2013; 96: 3108–19. doi: 10.3168/jds.2012-6097 23477813

18. Ji P1, Osorio JS, Drackley JK, Loor JJ. 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. 2012;95:4333–51. doi: 10.3168/jds.2011-5079 22818447

19. Selim S, Salin S, Taponen J, Vanhatalo A, Kokkonen T, Elo KT. Prepartal dietary energy alters transcriptional adaptations of the liver and subcutaneous adipose tissue of dairy cows during the transition period. Physiol Genomics 2014; 46(9):328–337. doi: 10.1152/physiolgenomics.00115.2013 24569674

20. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009; 10(1):57–63. doi: 10.1038/nrg2484 19015660

21. Wærp HKL, Waters SM, McCabe MS, Cormican P, Salte R. RNA-seq analysis of bovine adipose tissue in heifers fed diets differing in energy and protein content. PLoS One. 2018; 13(9):e0201284. doi: 10.1371/journal.pone.0201284 30235219

22. Maillard V, Uzbekova S, Guignot F, Perreau C, Rame C, Coyral-Castel S, et al. Effect of adiponectin on bovine granulosa cell steroidogenesis, oocyte maturation and embryo development. Reprod Biol Endocrinol 2010; 8:23. doi: 10.1186/1477-7827-8-23 20219117

23. Maillard V, Froment P, Rame C, Uzbekova S, Elis S, Dupont J. Expression and effect of resistin on bovine and rat granulosa cell steroidogenesis and proliferation. Reproduction 2011; 141(4):467–479. doi: 10.1530/REP-10-0419 21239528

24. Reverchon M, Bertoldo MJ, Rame C, Froment P, Dupont J. CHEMERIN (RARRES2) decreases in vitro granulosa cell steroidogenesis and blocks oocyte meiotic progression in bovine species. Biol Reprod 2014; 90(5):102. doi: 10.1095/biolreprod.113.117044 24671882

25. Reverchon M, Rame C, Bunel A, Chen W, Froment P, Dupont J. VISFATIN (NAMPT) Improves In Vitro IGF1-Induced Steroidogenesis and IGF1 Receptor Signaling Through SIRT1 in Bovine Granulosa Cells. Biol Reprod 2016; 94(3):54. doi: 10.1095/biolreprod.115.134650 26792944

26. Reverchon M, Rame C, Cognie J, Briant E, Elis S, Guillaume D, et al. Resistin in dairy cows: plasma concentrations during early lactation, expression and potential role in adipose tissue. PLoS One 2014; 9(3):e93198. doi: 10.1371/journal.pone.0093198 24675707

27. Singh SP, Haussler S, Gross JJ, Schwarz FJ, Bruckmaier RM, Sauerwein H. Short communication: circulating and milk adiponectin change differently during energy deficiency at different stages of lactation in dairy cows. J Dairy Sci 2014; 97(3):1535–1542. doi: 10.3168/jds.2013-7598 24472130

28. Mellouk N, Ramé C, Diot M, Briant E, Touzé JL, Guillaume D, et al. Possible involvement of the RARRES2/CMKLR1-system in metabolic and reproductive parameters in Holstein dairy cows. Reprod Biol Endocrinol 2019; 17(1):25. doi: 10.1186/s12958-019-0467-x 30777067

29. De Koster J, Urh C, Hostens M, Van den Broeck W, Sauerwein H, Opsomer G. Relationship between serum adiponectin concentration, body condition score, and peripheral tissue insulin response of dairy cows during the dry period. Domest Anim Endocrinol 2017; 59:100–104. doi: 10.1016/j.domaniend.2016.12.004 28063290

30. Mellouk N, Rame C, Touze JL, Briant E, Ma L, Guillaume D, et al. Involvement of plasma adipokines in metabolic and reproductive parameters in Holstein dairy cows fed with diets with differing energy levels. J Dairy Sci 2017; 100(10):8518–8533. doi: 10.3168/jds.2017-12657 28803009

31. Rémond B. Changes in rumen contents over the 1st months of lactation in dairy cows. Reprod Nutr Dev 1988; 28:109–111.

32. Salazar-Ortiz J, Camous S, Briant C, Lardic L, Chesneau D, Guillaume D. Effects of nutritional cues on the duration of the winter anovulatory phase and on associated hormone levels in adult female Welsh pony horses (Equus caballus). Reprod Biol Endocrinol 2011; 9:130. doi: 10.1186/1477-7827-9-130 21958120

33. Sirois J, Fortune JE. Ovarian follicular dynamics during the estrous cycle in heifers monitored by real-time ultrasonography. Biol Reprod 1988; 2:308–17.

34. Gaidatzis D, Burger L, Florescu M, Stadler MB. Analysis of intronic and exonic reads in RNA-seq data characterizes transcriptional and post-transcriptional regulation. Nat Biotechnol 2015; 33(7):722–729. doi: 10.1038/nbt.3269 26098447

35. Krämer A1, Green J, Pollard J Jr, Tugendreich S. Causal analysis approaches in Ingenuity Pathway Analysis. Bioinformatics. 2014; 30:523–30. doi: 10.1093/bioinformatics/btt703 24336805

36. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002; 3(7):RESEARCH0034.

37. Canepa S LA, Bluteau A, Fagu C, Flon C, Monniaux D. Validation d'une methode immunoenzymatique pour le dosage de la progesterone dans le plasma des ovins et des bovins. Les Cahiers Techniques de L'INRA 2008; 64:19–30.

38. Mann S, Nydam DV, Abuelo A, Leal Yepes FA, Overton TR, Wakshlag JJ. Insulin signaling, inflammation, and lipolysis in subcutaneous adipose tissue of transition dairy cows either overfed energy during the prepartum period or fed a controlled-energy diet. J Dairy Sci 2016; 99(8):6737–6752. doi: 10.3168/jds.2016-10969 27209137

39. Salin S, Vanhatalo A, Elo K, Taponen J, Boston RC, Kokkonen T. Effects of dietary energy allowance and decline in dry matter intake during the dry period on responses to glucose and insulin in transition dairy cows. J Dairy Sci 2017; 100(7):5266–5280. doi: 10.3168/jds.2016-11871 28501410

40. Shirley JE, Emery RS, Convey EM, Oxender WD. Enzymic changes in bovine adipose and mammary tissue, serum and mammary tissue hormonal changes with initiation of lactation. J Dairy Sci 1973; 56(5):569–574. doi: 10.3168/jds.S0022-0302(73)85220-8 4704188

41. Khan MJ, Hosseini A, Burrell S, Rocco SM, McNamara JP, Loor JJ. Change in subcutaneous adipose tissue metabolism and gene network expression during the transition period in dairy cows, including differences due to sire genetic merit. J Dairy Sci 2013; 96(4):2171–2182. doi: 10.3168/jds.2012-5794 23415532

42. McNamara JP. Lipid metabolism in adipose tissue during lactation: a model of a metabolic control system. J Nutr 1994; 124(8 Suppl):1383S–1391S. doi: 10.1093/jn/124.suppl_8.1383S 8064388

43. McNamara JP, Hillers JK. Adaptations in lipid metabolism of bovine adipose tissue in lactogenesis and lactation. J Lipid Res 1986; 27(2):150–157. 3958617

44. Janovick N, Loor J, Ji P, Bionaz M, Everts R, Lewin H, et al. Overfeeding energy prepartum dramatically affects peripartal expression of mRNA transcripts in subcutaneous adipose tissue compared with controlling energy intake prepartum. J Dairy Sci 2009; 92(Suppl 1):709.

45. Huang W, Guo Y, Du W, Zhang X, Li A, Miao X. Global transcriptome analysis identifies differentially expressed genes related to lipid metabolism in Wagyu and Holstein cattle. Sci Rep 2017; 7(1):5278. doi: 10.1038/s41598-017-05702-5 28706200

46. Waerp HKL, Waters SM, McCabe MS, Cormican P, Salte R. RNA-seq analysis of bovine adipose tissue in heifers fed diets differing in energy and protein content. PLoS One 2018; 13(9):e0201284. doi: 10.1371/journal.pone.0201284 30235219

47. Ji P, Drackley JK, Khan MJ, Loor JJ. Inflammation- and lipid metabolism-related gene network expression in visceral and subcutaneous adipose depots of Holstein cows. J Dairy Sci 2014; 97(6):3441–3448. doi: 10.3168/jds.2013-7296 24704230

48. Saremi B, Winand S, Friedrichs P, Kinoshita A, Rehage J, Danicke S, et al. Longitudinal profiling of the tissue-specific expression of genes related with insulin sensitivity in dairy cows during lactation focusing on different fat depots. PLoS One 2014; 9(1):e86211. doi: 10.1371/journal.pone.0086211 24465964

49. Butler WR, Smith RD. Interrelationships between energy balance and postpartum reproductive function in dairy cattle. J Dairy Sci 1989; 72(3):767–783. doi: 10.3168/jds.S0022-0302(89)79169-4 2654227

50. Lucy MC, Beck J, Staples CR, Head HH, De La Sota RL, Thatcher WW. Follicular dynamics, plasma metabolites, hormones and insulin-like growth factor I (IGF-I) in lactating cows with positive or negative energy balance during the preovulatory period. Reprod Nutr Dev 1992; 32(4):331–341. 1418395

51. Jorritsma R, Wensing T, Kruip TA, Vos PL, Noordhuizen JP. Metabolic changes in early lactation and impaired reproductive performance in dairy cows. Vet Res 2003; 34(1):11–26. doi: 10.1051/vetres:2002054 12588681

52. von Leesen R, Tetens J, Stamer E, Junge W, Thaller G, Krattenmacher N. Effect of genetic merit for energy balance on luteal activity and subsequent reproductive performance in primiparous Holstein-Friesian cows. J Dairy Sci 2014; 97(2):1128–1138. doi: 10.3168/jds.2013-7185 24359817

53. Townson DH, Tsang PC, Butler WR, Frajblat M, Griel LC Jr., Johnson CJ, et al. Relationship of fertility to ovarian follicular waves before breeding in dairy cows. J Anim Sci 2002; 80(4):1053–1058. doi: 10.2527/2002.8041053x 12008660

54. Girard A, Dufort I, Sirard MA. The effect of energy balance on the transcriptome of bovine granulosa cells at 60 days postpartum. Theriogenology 2015; 84(8):1350–1361 e1356. doi: 10.1016/j.theriogenology.2015.07.015 26316219

55. Golini VE, Stradaioli G, Sirard MA. Transcriptome analysis of bovine granulosa cells of preovulatory follicles harvested 30, 60, 90, and 120 days postpartum. Theriogenology 2014; 82(4):580–591 e585. doi: 10.1016/j.theriogenology.2014.05.019 24985356

56. Arango Duque G, Descoteaux A. Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol. 2014; 491. doi: 10.3389/fimmu.2014.00491 25339958 eCollection 2014.

57. Jabbour HN, Sales KJ, Catalano RD, Norman JE. Inflammatory pathways in female reproductive health and disease. Reproduction. 2009; 138(6):903–19. doi: 10.1530/REP-09-0247 19793840

58. Rutanen EM. Cytokines in reproduction. Ann Med 1993; 25(4):343–347. 8217099

59. Sheldon IM, Cronin JG, Healey GD, Gabler C, Heuwieser W, Streyl D, et al. Innate immunity and inflammation of the bovine female reproductive tract in health and disease. Reproduction 2014; 148(3):R41–51. doi: 10.1530/REP-14-0163 24890752

60. Tribulo P, Siqueira LGB, Oliveira LJ, Scheffler T, Hansen PJ. Identification of potential embryokines in the bovine reproductive tract. J Dairy Sci 2018; 101(1):690–704. doi: 10.3168/jds.2017-13221 29128220

61. Spicer LJ, Alpizar E. Effects of cytokines on FSH-induced estradiol production by bovine granulosa cells in vitro: dependence on size of follicle. Domest Anim Endocrinol 1994; 11(1):25–34. 8124930


Článek vyšel v časopise

PLOS One


2019 Číslo 9

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Krvácení v důsledku portální hypertenze při jaterní cirhóze – od pohledu záchranné služby až po závěrečný hepato-gastroenterologický pohled
nový kurz
Autoři: PhDr. Petr Jaššo, MBA, MUDr. Hynek Fiala, Ph.D., prof. MUDr. Radan Brůha, CSc., MUDr. Tomáš Fejfar, Ph.D., MUDr. David Astapenko, Ph.D., prof. MUDr. Vladimír Černý, Ph.D.

Rozšíření možností lokální terapie atopické dermatitidy v ordinaci praktického lékaře či alergologa
Autoři: MUDr. Nina Benáková, Ph.D.

Léčba bolesti v ordinaci praktického lékaře
Autoři: MUDr. PhDr. Zdeňka Nováková, Ph.D.

Revmatoidní artritida: včas a k cíli
Autoři: MUDr. Heřman Mann

Jistoty a nástrahy antikoagulační léčby aneb kardiolog - neurolog - farmakolog - nefrolog - právník diskutují
Autoři: doc. MUDr. Štěpán Havránek, Ph.D., prof. MUDr. Roman Herzig, Ph.D., doc. MUDr. Karel Urbánek, Ph.D., prim. MUDr. Jan Vachek, MUDr. et Mgr. Jolana Těšínová, Ph.D.

Všechny kurzy
Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.