Serum Anti-Müllerian Hormone and Cytokine Profiling of Bubalus bubalis (Murrah buffalo) Calves for Puberty Prediction

S.H.  Sneha; Prahlad  Singh; Navdeep  Singh; Chanchal  Singh; Mrigank  Honparkhe

doi:10.6000/1927-520X.2024.13.07

Authors

S.H. Sneha Department of Veterinary Gynaecology and Obstetrics, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana – 141004, Punjab, India
Prahlad Singh Department of Teaching Veterinary Clinical Complex, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana – 141004, Punjab, India https://orcid.org/0000-0001-5298-7781
Navdeep Singh Department of Veterinary Gynaecology and Obstetrics, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana – 141004, Punjab, India https://orcid.org/0000-0002-7095-4438
Chanchal Singh Department of Veterinary Physiology and Biochemistry, College of Veterinary Science, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana – 141004, Punjab, India
Mrigank Honparkhe Department of Veterinary Gynaecology and Obstetrics, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana – 141004, Punjab, India

DOI:

https://doi.org/10.6000/1927-520X.2024.13.07

Keywords:

Cytokines, puberty, ELISA, buffalo, heifers, Karl Pearson correlation

Abstract

The present study incorporated ten buffalo calves aged 0 to 6 months, with an average weight of 35 kg, and ten buffalo heifers aged 12 months, with an average weight of 200 kg, to study the cytokine and AMH profile in relation to pubertal advancement. Venous blood samples (5ml) were collected from buffalo calves on the day of birth (day 0), day 15, day 30, day 60, day 90, day 120, day 150, and day 180. A single blood sample was collected from Buffalo heifers (1 year age). Cytokines: IFN-γ, IL-6, IL-1, IL-13, TNF-α, and TGF-β, and anti-Müllerian hormone: AMH were estimated using respective ELISA kits. At birth, cytokine levels in serum showed a varied pattern, with lower levels of IFN-γ, IL-6, and IL-13, whereas IL-1, TNF-α, and TGF-β were higher. Throughout the study, IFN-γ, IL-13, and TGF-β levels remained relatively stable, whereas IL-1, IL-6, and TNF-α increased notably by day 180. IL-1, TNF-α, and IL-6 levels were higher (P<0.01) from birth to 180 days as well as on day 365. AMH levels remained consistent from birth to 180 days, indicating a marked increase at Day 15 (33.49 ± 12.63 ng/L), followed by a decline to 4.60 ± 1.55 ng/Lat the end of the first year. Implications of the Karl Pearson correlation coefficient revealed a negative correlation between AMH levels and IFN-γ and TNF-α. AMH was positively correlated with IL 13 and TGF-β. Hence, it was concluded that IFN-γ and TNF-α are predictive markers for a reduction in AMH levels and hence, setting up puberty in buffalo heifers.

References

Vasantha, SKI, Kona SSR. Physiology of puberty in females: a review. Int J Vet Sci 2016; 1(2): 23-26.

Gupta SK, Singh P, Shinde KP, Lone SM, Kumar N, Kumar A. Strategies for attaining early puberty in cattle and buffalo: a review. Agric Rev 2016; 37: 160-167. https://doi.org/10.18805/ar.v37i2.10741 DOI: https://doi.org/10.18805/ar.v37i2.10741

Casazza K, Hanks LJ, Alvarez JA. Role of various cytokines and growth factors in pubertal development. In:Jürimäe J, Hills AP, Jürimäe T, (eds): Cytokines, Growth Mediators and Physical Activity in Children during Puberty. Med Sport Sci Basel, Karger 2010; 55: 14-31. https://doi.org/10. 1159/000321969 DOI: https://doi.org/10.1159/000321969

Monniaux D, Drouilhet L, Rico C, Estienne A, Jarrier P, Touzé JL, Sapa J, Phocas F, Dupont J, Dalbiès-Tran R, Fabre S. Regulation of anti-Müllerian hormone production in domestic animals. ReprodFertil Dev 2012; 25(1): 1-16. https://doi.org/10.18805/ar.v37i2.10741 DOI: https://doi.org/10.1071/RD12270

Lee HJ, Kim JY, Park JE, Yoon YD, Tsang BK, Kim JM. Induction of Fas-Mediated Apoptosis by Interferon-γ is Dependent on Granulosa Cell Differentiation and Follicular Maturation in the Rat Ovary. Dev Reprod 2016; 20(4): 315-329. https://doi.org/10.12717/DR.2016.20.4.315 DOI: https://doi.org/10.12717/DR.2016.20.4.315

Tabibzadeh S. Cytokines and the hypothalamic-pituitary-ovarian-endometrial axis. Human Reproduction 1994; 9(5): 947-67. https://doi.org/10.1093/oxfordjournals.humrep.a138621 DOI: https://doi.org/10.1093/oxfordjournals.humrep.a138621

Ghodsi M, Hojati V, Attaranzade A, Saifi B. A Cross-sectional study on the follicular fluid concentration of some interleukins and clinical factors in polycystic ovary syndrome patients. Int J Women's Health Reprod Sci 2021; 9: 124-9. https://doi.org/10.1093/oxfordjournals.humrep.a138621 DOI: https://doi.org/10.15296/ijwhr.2021.22

Ripley D, Shoup B, Majewski A, Chegini N. Differential expression of interleukins IL-13 and IL-15 in normal ovarian tissue and ovarian carcinomas. Gynecologic Oncology 2004; 92(3): 761-8. https://doi.org/10.1016/j.ygyno.2003.12.011 DOI: https://doi.org/10.1016/j.ygyno.2003.12.011

Saragüeta PE, Lanuza GM, Baranao JL. Autocrine role of transforming growth factor β1 on rat granulosa cell proliferation. Biology of Reproduction 2002; 66(6): 1862-8. https://doi.org/10.1095/biolreprod66.6.1862 DOI: https://doi.org/10.1095/biolreprod66.6.1862

Terranova PF, Rice VM. Cytokine involvement in ovarian processes. American Journal of Reproductive Immunology 1997; 37(1): 50-63. https://doi.org/10.1111/j.1600-0897.1997.tb00192.x DOI: https://doi.org/10.1111/j.1600-0897.1997.tb00192.x

Durlinger AL, Kramer P, Karels B, de Jong FH, Uilenbroek JT, Grootegoed JA, Themmen AP. Control of primordial follicle recruitment by anti-Müllerian hormone in the mouse ovary. Endocrinology 1999; 140(12): 5789-96. https://doi.org/10.1210/endo.140.12.7204 DOI: https://doi.org/10.1210/en.140.12.5789

Yang Z, Kong B, Mosser DM, Zhang X. TLRs, macrophages, and NK cells: our understandings of their functions in uterus and ovary. International Immunopharmacology 2011; 11(10): 1442-50. https://doi.org/10.1016/j.intimp.2011.04.024 DOI: https://doi.org/10.1016/j.intimp.2011.04.024

Hisaeda K, Hagiwara K, Eguchi J, Yamanaka H, Kirisawa R, Iwai H. Interferon-γ and tumor necrosis factor-α levels in sera and whey of cattle with naturally occurring coliform mastitis. Journal of Veterinary Medical Science 2001; 63(9): 1009-11. https://doi.org/10.1292/jvms.63.1009 DOI: https://doi.org/10.1292/jvms.63.1009

Kanakoudi-Tsakalidou F, Drossou-Agakidou V, Noutsia C, Tzimouli V, Taparkou A, Mavridis P, Kremenopoulos G. Intracellular and plasma cytokine profile in neonates born to non-atopic parents: the impact of breastfeeding. European Journal of Pediatrics 2004; 163: 395-401. https://doi.org/10.1007/s00431-004-1463-4 DOI: https://doi.org/10.1007/s00431-004-1463-4

El-Bahr SM, EL-Deeb WM. Acute Phase Proteins, Lipid Profile and Pro-inflammatory Cytokines in Healthy and Bronchopneumonic Water Buffalo Calves. American Journal of Biochemistry and Biotechnology 2013; 9(1): 34-40. https://doi.org/10.3844/ajbbsp.2013.34.40 DOI: https://doi.org/10.3844/ajbbsp.2013.34.40

Kabu M, Elitok B, Kucukkurt I. Detection of serum amyloid-A concentration in the calf clinically diagnosed with pneumonia, enteritis and pneumo-enteritis. Ciência Rural 2016; 46: 293-9. https://doi.org/10.1590/0103-8478cr20150571 DOI: https://doi.org/10.1590/0103-8478cr20150571

Kabu M, Sayin Z. Concentrations of serum amyloid A, haptoglobin, tumour necrosis factor, and interleukin-1 and-6 in Anatolian buffaloes naturally infected with dermatophytosis. Veterinárnímedicína 2016; 61(3): 133-5. https://doi.org/10.17221/8770-VETMED DOI: https://doi.org/10.17221/8770-VETMED

Poole RK, Ault-Seay TB, Payton RR, Myer PR, Lear AS, Pohler KG. Evaluation of reproductive tract cytokines in post-partum beef cows relating to reproductive microbiota and fertility outcomes. Frontiers in Animal Science 2021; 24(2): 20. https://doi.org/10.3389/fanim.2021.704714 DOI: https://doi.org/10.3389/fanim.2021.704714

Ho LJ, Luo SF, Lai JH. Biological effects of interleukin-6: Clinical applications in autoimmune diseases and cancers. Biochemical Pharmacology 2015; 97(1): 16-26. https://doi.org/10.1016/j.bcp.2015.06.009 DOI: https://doi.org/10.1016/j.bcp.2015.06.009

Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S. The pro-and anti-inflammatory properties of the cytokine interleukin-6. Biochimica et BiophysicaActa (BBA)-Molecular Cell Research 2011; 13(5): 878-88. https://doi.org/10.1016/j.bbamcr.2011.01.034

Wooldridge LK, Ealy AD. Interleukin-6 increases inner cell mass numbers in bovine embryos. BMC Developmental Biology 2019; 1-1. https://doi.org/10.1186/s12861-019-0182-z DOI: https://doi.org/10.1186/s12861-019-0182-z

Wooldridge LK, Johnson SE, Cockrum RR, Ealy AD. Interleukin-6 requires JAK to stimulate inner cell mass expansion in bovine embryos. Reproduction 2019; 158(4): 303-12. https://doi.org/10.1530/REP-19-0286 DOI: https://doi.org/10.1530/REP-19-0286

Tríbulo P, Siqueira LG, Oliveira LJ, Scheffler T, Hansen PJ. Identification of potential embryokines in the bovine reproductive tract. Journal of Dairy Science 2018; 101(1): 690-704. https://doi.org/10.3168/jds.2017-13221 DOI: https://doi.org/10.3168/jds.2017-13221

Molina EC. Serum interferon-gamma and interleukins-6 and-8 during infection with Fasciolagigantica in cattle and buffaloes. Journal of Veterinary Science 6(2): 135-9. https://doi.org/10.4142/jvs.2005.6.2.135 DOI: https://doi.org/10.4142/jvs.2005.6.2.135

Borish L, Rosenbaum R, Albury L, Clark S. Activation of neutrophils by recombinant interleukin 6. Cellular Immunology 1989; 121(2): 280-9. https://doi.org/10.1016/0008-8749(89)90026-9 DOI: https://doi.org/10.1016/0008-8749(89)90026-9

ueiredo CA, Alcântara-Neves NM, Veiga R, Amorim LD, Dattoli V, Mendonça LR, Junqueira S, Genser B, Santos M, de Carvalho LC, Cooper PJ. Spontaneous cytokine production in children according to biological characteristics and environmental exposures. Environmental Health Perspectives 2009; 117(5): 845-9. https://doi.org/10.1289/ehp.0800366 DOI: https://doi.org/10.1289/ehp.0800366

Wynn TA. IL-13 effector functions. Annual Review of Immunology 2003; 21(1): 425-56. https://doi.org/10.1146/annurev.immunol.21.120601.141142 DOI: https://doi.org/10.1146/annurev.immunol.21.120601.141142

Rota A, Ballarin C, Vigier B, Cozzi B, Rey R. Age-dependent changes in plasma anti-Müllerian hormone concentrations in the bovine male, female, and freemartin from birth to puberty: relationship between testosterone production and influence on sex differentiation. General and Comparative Endocrinology 2002; 129(1): 39-44. https://doi.org/10.1016/S0016-6480(02)00514-2 DOI: https://doi.org/10.1016/S0016-6480(02)00514-2

Batista EO, Guerreiro BM, Freitas BG, Silva JC, Vieira LM, Ferreira RM, Rezende RG, Basso AC, Lopes RN, Rennó FP, Souza AH. Plasma anti-Müllerian hormone as a predictive endocrine marker to select Bostaurus (Holstein) and Bos indicus (Nelore) calves for in vitro embryo production. Domestic Animal Endocrinology 2016; 54: 1-9. https://doi.org/10.1016/j.domaniend.2015.08.001 DOI: https://doi.org/10.1016/j.domaniend.2015.08.001

Ireland JL, Scheetz D, Jimenez-Krassel F, Themmen AP, Ward F, Lonergan P, Smith GW, Perez GI, Evans AC, Ireland JJ. Antral follicle count reliably predicts the number of morphologically healthy oocytes and follicles in the ovaries of young adult cattle. Biology of Reproduction 2008; 79(6): 1219-25. https://doi.org/10.1095/biolreprod.108.071670 DOI: https://doi.org/10.1095/biolreprod.108.071670

Knight PG, Glister C. TGF-β superfamily members, and ovarian follicle development. Reproduction 2006; 132(2): 191-206. https://doi.org/10.1530/rep.1.01074 DOI: https://doi.org/10.1530/rep.1.01074

Mehtala S, Interleukin 13 and its receptors in follicular ovarian cancer. Oncotarget 2018; 9(63): 32261-73.

Ha LX, Wu YY, Yin T, Yuan YY, Du YD. Effect of TNF-alpha on endometrial glucose transporter-4 expression in patients with polycystic ovary syndrome through nuclear factor-kappa B signalling pathway activation. Journal of Physiology & Pharmacology 2021; 72(6).

Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Annual Review of Immunology 2009; 27: 519-50. https://doi.org/10.1146/annurev.immunol.021908.132612 DOI: https://doi.org/10.1146/annurev.immunol.021908.132612

Wagner EF, Nebreda AR. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat Rev Cancer 2009; 9(8): 537-549. https://doi.org/10.1038/nrc2694 DOI: https://doi.org/10.1038/nrc2694

Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S. The pro-and anti-inflammatory properties of the cytokine interleukin-6. Biochimica et BiophysicaActa (BBA)-Molecular Cell Research 2011; 1813(5): 878-88.

Tatone C. Evidence that transforming growth factor beta is an autocrine inhibitor of mouse oocyte maturation. BiolReprod 1996; 54(4): 915-920. https://doi.org/10.1016/j.bbamcr.2011.01.034 DOI: https://doi.org/10.1016/j.bbamcr.2011.01.034

Letterio JJ, Roberts AB. Regulation of immune responses by TGF-β. Annual Review of Immunology 1998; 16(1): 137-61. https://doi.org/10.1146/annurev.immunol.16.1.137 DOI: https://doi.org/10.1146/annurev.immunol.16.1.137