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Supplementation with long-acting injectable progesterone 3 days after TAI impaired luteal function in buffaloes

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Abstract

Three experiments were conducted to evaluate the effects of long-acting injectable progesterone (iP4) in buffalo cows. In Experiment 1, ovariectomized buffaloes received 300 mg (iP300) or 600 mg (iP600) of iP4, and serum P4 concentrations were evaluated. In experiment 2, three groups were compared: control or administration of 300 mg of iP4 3 (iP4-D3) or 6 days (iP4-D6) after timed artificial insemination (TAI). On day 16, reproductive tract was recovered for conceptus, endometrium, and corpus luteum (CL) analysis. In experiment 3, pregnancy per AI (P/TAI) and proportion of pregnancy losses were evaluated after administration of 300 mg of iP4 3 (iP4-D3) or 6 days (iP4-D6) after TAI in lactating buffaloes. In experiment 1, serum P4 concentrations remained over 1 ng/mL for ~ 3 days in both groups. The 300 mg dose was used in subsequent experiments. In experiment 2, CL weight and endometrial glands density were decreased, and conceptus length was increased in iP4-D3 compared to control and to iP4-D6 (P < 0.05). Transcript abundance of Prostaglandin F Receptor (FP) and ISG15 in CL and of ISG15 and MX1 in endometrium was greater in iP4-D3 when compared to control and to iP4-D6 (P < 0.05). In experiment 3, there was no difference among experimental groups for P/TAI at D30 and pregnancy losses (P > 0.1); however, iP4-D3 presented a lower P/TAI at day 60 (41.7%) when compared to control (56.8%) and iP4-D6 (57.7%; P = 0.07). In conclusion, administration iP4 at 3 days after TAI affects CL development and consequently decreases final pregnancy outcome in buffaloes.

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Abbreviations

BCS:

Body condition score

CL:

Corpus Luteum

DCL:

Diameter of the CL

ESR1 :

Estrogen Receptor 1

FP :

Prostaglandin F Receptor

im:

Intramuscularly

INFt:

Interferon tau

iP300:

300 Mg of iP4

iP4:

Long-acting injectable progesterone

iP4-D3:

300 Mg of iP4 three days after timed-artificial insemination

iP4-D6:

300 Mg of iP4 six days after timed artificial insemination.

iP600:

600 Mg of iP4

ISG15 :

Interferon, Alpha-Inducible Protein Clone IFI-15 K

LLC:

Large luteal cells

MX1 :

Myxovirus Resistance 1 Interferon-Inducible

P/TAI:

Pregnancy per Artificial Insemination

P4:

Progesterone

PGF:

Prostaglandin f2 alpha

PGR :

Progesterone Receptor

PTGES :

Prostaglandin E Synthase

SLC:

Small luteal cells

TAI:

Timed artificial Insemination

References

  • Ashworth CJ, Sales DI, Wilmut I. Evidence of an association between the survival of embryos and the periovulatory plasma progesterone concentration in the ewe. J Reprod Fertil. 1989; 87(1): 23-32.

    Article  CAS  PubMed  Google Scholar 

  • Araújo, Estela R., Mariana Sponchiado, Guilherme Pugliesi, Veerle Van Hoeck, Fernando S. Mesquita, Claudia MB Membrive, and Mario Binelli. "Spatio-specific regulation of endocrine-responsive gene transcription by periovulatory endocrine profiles in the bovine reproductive tract." Reproduction, Fertility and Development 28, no. 10 (2016): 1533-1544.

  • Barnes FL. The effects of the early uterine environment on the subsequent development of embryo and fetus. Theriogenology. 2000; 53(2): 649-658.

    Article  CAS  PubMed  Google Scholar 

  • Batista EOS, Cardoso BO, Oliveira ML, Cuadros FDC, Mello BP, Sponchiado M, Monteiro BM, Pugliesi G, Binelli M. Supplemental progesterone induces temporal changes in luteal development and endometrial transcription in beef cattle. Domest Anim Endocrinol. 2019; 68: 126-134.

    Article  CAS  PubMed  Google Scholar 

  • Berisha B, Thaqi G, Rodler D, Schams D, Sinowatz F, Pfaffl MW. Regulatory changes of local produced prostaglandins in corpus luteum after experimentally induced luteolysis in the cow. Anat Histol Embryol. 2022; 51(2): 289-299.

    Article  PubMed  Google Scholar 

  • Binelli M, Thatcher WW, Mattos R, Baruselli PS. Antiluteolytic strategies to improve fertility in cattle. Theriogenology. 2001; 56(9): 1451-63.

    Article  CAS  PubMed  Google Scholar 

  • Bishop CV, Stormshak F. Non-genomic actions of progesterone and estrogens in regulating reproductive events in domestic animals. Vet J. 2008; 176(3): 270-280.

    Article  CAS  PubMed  Google Scholar 

  • Burke CR. Mihm M, Macmillan KL, Roche JF. Some effects of prematurely elevated concentrations of progesterone on luteal and follicular characteristics during the oestrous cycle in heifers. Anim Reprod Sci. 1994; 35(1-2): 27-39.

    Article  CAS  Google Scholar 

  • Carter F, Forde N, Duffy P, Wade M, Fair T, Crowe MA, Evans ACO, Kenny DA, Roche JF, Lonergan P. Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers. Reprod Fertil Dev. 2008; 20(3): 368-375.

    Article  CAS  PubMed  Google Scholar 

  • Carvalho NAT, Soares JG, Souza DC, Vannucci FS, Amaral R, Maio JRG, Sales JNS, Sá Filho MF, Baruselli PS. Different circulating progesterone concentrations during synchronization of ovulation protocol did not affect ovarian follicular and pregnancy responses in seasonal anestrous buffalo cows. Theriogenology. 2014; 81(3): 490-5.

    Article  CAS  PubMed  Google Scholar 

  • Carvalho NAT, Soares JG, Souza DC, Maio JRG, Sales JNS, Martins Júnior B, Macari RC, D'Occhio MJ, Baruselli PS. Ovulation synchronization with estradiol benzoate or GnRH in a timed artificial insemination protocol in buffalo cows and heifers during the non-breeding season. Theriogenology. 2017; 87: 333-338.

    Article  CAS  PubMed  Google Scholar 

  • Casano AB, Menchetti L, Trabalza-Marinucci M, Riva F, De Matteis G, Brecchia G, Inglesi A, Rossi E, Signorelli F, Barile VL, Barbato O. Gene expression of pregnancy-associated glycoproteins-1 (PAG-1), interferon-tau (IFNt) and interferon stimulated genes (ISGs) as diagnostic and prognostic markers of maternal-fetal cellular interaction in buffalo cows. Theriogenology. 2023, 209: 89-97.

    Article  CAS  PubMed  Google Scholar 

  • Dadarwal D, Mapletoft RJ, Adams GP, Pfeifer LFM, Creelman C, Singh J. Effect of progesterone concentration and duration of proestrus on fertility in beef cattle after fixed-time artificial insemination. Theriogenology. 2013; 79(5): 859-866.

    Article  CAS  PubMed  Google Scholar 

  • Dalmaso de Melo G, Mello BP, Ferreira CA, Souto Godoy Filho CA, Rocha CC, Silva AG, Reese ST, Madureira EH, Pohler KG, Pugliesi G. Applied use of interferon-tau stimulated genes expression in polymorphonuclear cells to detect pregnancy compared to other early predictors in beef cattle. Theriogenology. 2020, 152: 94-105.

    Article  CAS  PubMed  Google Scholar 

  • Dash S, Chakravarty AK, Singh A, Upadhyay A, Singh M, Yousuf S. Effect of heat stress on reproductive performances of dairy cattle and buffaloes: A review. Vet World, 2016; 9(3): 235-44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Carvalho NA, Soares JG, Baruselli PS. Strategies to overcome seasonal anestrus in water buffalo. Theriogenology. 2016; 86(1): 200-6.

    Article  PubMed  Google Scholar 

  • De Rensis F, Lopez-Gatius F. Protocols for synchronizing estrus and ovulation in buffalo (Bubalus bubalis): A review. Theriogenology. 2007; 67(2): 209-216.

    Article  PubMed  Google Scholar 

  • Di Francesco S, Neglia G, Vecchio D, Rossi P, Russo M, Zicarelli L, D'Occhio MJ, Campanile G. Influence of season on corpus luteum structure and function and AI outcome in the Italian Mediterranean buffalo (Bubalus bubalis). Theriogenology. 2012; 78(8): 1839-1845.

    Article  PubMed  Google Scholar 

  • Diskin MG, Morris DG. Embryonic and early foetal losses in cattle and other ruminants. Reprod Domest Anim. 2008; 43: 260-267.

    Article  PubMed  Google Scholar 

  • Drost M. Bubaline versus bovine reproduction. Theriogenology. 2007; 68(3): 447-449.

    Article  CAS  PubMed  Google Scholar 

  • Ferreira de Souza ED. Efeito da progesterona injetável de longa ação na função luteínica e na taxa de concepção de vacas Holandesas de alta produção submetidas à IATF. 2015: University of Sao Paulo.

  • Forde N, Carter F, Fair T, Crowe MA, Evans ACO, Spencer TE, Bazer FW, McBride R, Boland MP, O'Gaora P, Lonergan P, Roche JF. Progesterone-Regulated Changes in Endometrial Gene Expression Contribute to Advanced Conceptus Development in Cattle. Biol Reprod. 2009; 81(4): 784-794.

    Article  CAS  PubMed  Google Scholar 

  • Forde N, Beltman ME, Duffy GB, Duffy P, Mehta JP, O'Gaora P, Roche JF, Lonergan P, Crowe MA. Changes in the Endometrial Transcriptome During the Bovine Estrous Cycle: Effect of Low Circulating Progesterone and Consequences for Conceptus Elongation. Biol Reprod. 2011; 84(2): 266-278.

    Article  CAS  PubMed  Google Scholar 

  • Forde N, Duffy GB, McGettigan PA, Browne JA, Mehta JP, Kelly AK, Mansouri-Attia N, Sandra O, Loftus BJ, Crowe MA, Fair T, Roche JF, Lonergan P, Evans ACO. Evidence for an early endometrial response to pregnancy in cattle: both dependent upon and independent of interferon tau. Physiol Genomics. 2012, 44(16): 799-810.

    Article  CAS  PubMed  Google Scholar 

  • Forde n, Mehta JP, McGettigan PA, Mamo S, Bazer FW, Spencer TE, Lonergan P. Alterations in expression of endometrial genes coding for proteins secreted into the uterine lumen during conceptus elongation in cattle. BMC Genom; 2013. 14: 321.

    Article  CAS  Google Scholar 

  • Garbarino EJ, Hernandez JA, Shearer JK, Risco CA, Thatcher WW. Effect of lameness on ovarian activity in postpartum Holstein cows. J Dairy Sci. 2004; 87(12): 4123-4131.

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Ispierto I, López-Gatius F. Progesterone supplementation in the early luteal phase after artificial insemination improves conception rates in high-producing dairy cows. Theriogenology. 2017; 90: 20-24.

    Article  CAS  PubMed  Google Scholar 

  • Ginther OJ. Effect of progesterone on length of estrous cycle in cattle. Am J Vet Res. 1970; 31(3): 493-6.

    CAS  PubMed  Google Scholar 

  • Gonella-Diaza, Angela María, Sónia Cristina da Silva Andrade, Mariana Sponchiado, Guilherme Pugliesi, Fernando Silveira Mesquita, Veerle Van Hoeck, Ricardo de Francisco Strefezzi, Gustavo R. Gasparin, Luiz L. Coutinho, and Mario Binelli. "Size of the ovulatory follicle dictates spatial differences in the oviductal transcriptome in cattle." PLoS One 10, no. 12 (2015): e0145321.

  • Gonella-Diaza AM, Ojeda-Rojas OA, Grajales-Lombana H, Abuabara Y, Hernández A. Serum concentration of sex-steroids, endometrial expression of their receptors, and endometrial morphology during the estrous cycle in Bos taurus Criollo and crossbred cows. J Appl Anim Res. 2018; 46(1): 1403-1411.

    Article  CAS  Google Scholar 

  • Haq UI, HanY, Ali T, Wang Y, Gao H, Lin L, Wu Y, Wu S, Zeng S. Expression of interferon-stimulated gene ISG15 and ubiquitination enzymes is upregulated in peripheral blood monocyte during early pregnancy in dairy cattle. Reprod Biol, 2016. 16(4): p. 255-260.

    Article  PubMed  Google Scholar 

  • Kunii H, Koyama K, Ito T, Suzuki T, Balboula AZ, Shirozu T, Bai H, Nagano M, Kawahara M, Takahashi M. Pregnancy-induced expression of interferon-stimulated genes in the cervical and vaginal mucosal membranes. J Dairy Sci. 2018. 101(9): 8396-8400.

    Article  CAS  PubMed  Google Scholar 

  • Mann GE, Lamming GE. Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction. 2001; 121(1): 175-180.

    Article  CAS  PubMed  Google Scholar 

  • Martins T, Pugliesi G, Sponchiado M, Cardoso BO, da Silva KR, Celeghini ECC, Binelli M. Supplementation with long-acting progesterone in early diestrus in beef cattle: II. Relationships between follicle growth dynamics and luteolysis. Domest Anim Endocrinol. 2019a; 68: 1-10.

    Article  CAS  PubMed  Google Scholar 

  • Martins T, Pugliesi G, Sponchiado M, Cardoso BO, Gomes NS, Mello BP, Celeghini ECC, Binelli M. Supplementation with long-acting progesterone in early diestrus in beef cattle: I. effect of artificial insemination on onset of luteolysis. Domest Anim Endocrinol. 2019b; 67: 63-70.

    Article  CAS  PubMed  Google Scholar 

  • Mezera MA, Li w, Wiltbank MC. Pregnancy-induced changes in the transcriptome of the bovine corpus luteum during and after embryonic interferon-tau secretion. Biol Reprod. 2021, 105(1): 148-163.

    Article  PubMed  Google Scholar 

  • Monteiro Jr PLJ, Nascimento AB, Pontes GCS, Fernandes GO, Melo LF, Wiltbank MC, Sartori R. Progesterone supplementation after ovulation: effects on corpus luteum function and on fertility of dairy cows subjected to AI or ET. Theriogenology. 2015; 84(7): 1215-24.

    Article  CAS  PubMed  Google Scholar 

  • Mullen MP, Elia G, Hilliard M, Parr MH, Diskin MG, Evans ACO, Crowe MA. Proteomic characterization of histotroph during the preimplantation phase of the estrous cycle in cattle. J Proteome Res. 2012; 11(5): 3004-18.

    Article  CAS  PubMed  Google Scholar 

  • O'Hara L, Forde N, Carter F, Rizos D, Maillo V, Ealy AD, Kelly AK, Rodriguez P, Isaka N, Evans ACO, Lonergan P. Paradoxical effect of supplementary progesterone between Day 3 and Day 7 on corpus luteum function and conceptus development in cattle. Reprod Fertil Dev. 2014; 26(2): 328-36.

    Article  CAS  PubMed  Google Scholar 

  • O'Hara L, Forde N, Duffy P, Randi F, Kelly AK, Valenza A, Rodriguez P, Lonergan P. Effect of combined exogenous progesterone with luteotrophic support via equine chorionic gonadotrophin (eCG) on corpus luteum development, circulating progesterone concentrations and embryo development in cattle. Reprod Fertil Dev. 2016; 28(3): 269-77.

    Article  CAS  PubMed  Google Scholar 

  • Ojeda OA, Londoño R, Gutierrez C, Gonella-Diaza AM. Follicular dynamics, corpus luteum growth and regression in multiparous buffalo cows and buffalo heifers. Rev MVZ Córdoba. 2014; 19(2): 4130-4140.

    Article  Google Scholar 

  • Oliveira, Milena Lopes, Fabio Luiz D’Alexandri, Guilherme Pugliesi, Veerle Van Hoeck, Fernando Silveira Mesquita, Claudia MB Membrive, Joao Alberto Negrao, Craig E. Wheelock, and Mario Binelli. "Peri-ovulatory endocrine regulation of the prostanoid pathways in the bovine uterus at early dioestrus." Reproduction, Fertility and Development 29, no. 3 (2017): 544-556.

  • Parr MH, Crowe MA, Lonergan P, Evans ACO, Rizos D, Diskin MG. Effect of exogenous progesterone supplementation in the early luteal phase post-insemination on pregnancy per artificial insemination in Holstein-Friesian cows. Anim Reprod Sci. 2014; 150(1-2): 7-14.

    Article  CAS  PubMed  Google Scholar 

  • Parr MH, Scully S, Lonergan P, Evans ACO, Crowe MA, Diskin MG. Establishment of critical timing of progesterone supplementation on corpus luteum and embryo development in beef heifers. Anim Reprod Sci. 2017; 180: 1-9.

    Article  CAS  PubMed  Google Scholar 

  • Perera B. Reproductive cycles of buffalo. Anim Reprod Sci. 2011. 124(3-4): 194-199.

    Article  CAS  PubMed  Google Scholar 

  • Pugliesi G, Oliveria ML, Scolari SC, Lopes E, Pinaffi FV, Miagawa BT, Paiva YN, Maio JRG, Nogueira GP, Binelli M. Corpus Luteum Development and Function after Supplementation of Long-Acting Progesterone During the Early Luteal Phase in Beef Cattle. Reprod Domest Anim. 2014; 49(1): 85-91.

    Article  CAS  PubMed  Google Scholar 

  • Russo M, Vecchio D, Neglia G, Pacelli C, Prandi A, Gasparrini B, Zicarelli L, D'Occhio MJ, Campanile G. Corpus luteum function and pregnancy outcome in buffaloes during the transition period from breeding to non-breeding season. Reprod Domest Anim. 2010; 45(6):988-91.

    Article  CAS  PubMed  Google Scholar 

  • Satheshkumar S, Palanisamy A, Rangasamy S, Kathiresan D, Kumanan K. Comparative analysis of follicular and luteal dynamics in oestrous cycles of buffaloes and crossbred cattle. Buffalo Bull. 2011; 30(2): 148-156.

    Google Scholar 

  • Sponchiado, Mariana, Nathalia Souza Gomes, Patricia Kubo Fontes, Thiago Martins, Maite Del Collado, Athos de Assumpcao Pastore, Guilherme Pugliesi, Marcelo Fábio Gouveia Nogueira, and Mario Binelli. "Pre-hatching embryo-dependent and-independent programming of endometrial function in cattle." PloS one 12, no. 4 (2017): e0175954.

  • Tsai, SJ, Wiltbank MC. Prostaglandin F2alpha regulates distinct physiological changes in early and mid-cycle bovine corpora lutea. Biol Reprod. 1998; 58(2): 346-52.

    Article  CAS  PubMed  Google Scholar 

  • Tsai SJ, Kot K, Ginther OJ, Wiltbank MC. Temporal gene expression in bovine corpora lutea after treatment with PGF2alpha based on serial biopsies in vivo. Reproduction. 2001; 121(6): 905-13.

    Article  CAS  PubMed  Google Scholar 

  • Vecchio D, Neglia G, Gasparrini B, Russo M, Pacelli C, Prandi A, D'Occhio MJ, Campanile G. Corpus luteum development and function and relationship to pregnancy during the breeding season in the Mediterranean buffalo. Theriogenology. 2012; 77(9): 1811-1815.

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Robinson R, Shi Z, Mann G. Efficacy of progesterone supplementation during early pregnancy in cows: A meta-analysis. Theriogenology. 2016, 85(8): 1390-1398.e1.

    Article  CAS  PubMed  Google Scholar 

  • Yoshino H, Toji N, Sasaki K, Koshi K, Yamagishi N, Takahashi T, Ishiguro-Oonuma T, Matsuda H, Yamanouchi T, Hashiyada Y, Imai K, Izaike Y, Kizaki K, Hashizume K. A predictive threshold value for the diagnosis of early pregnancy in cows using interferon-stimulated genes in granulocytes. Theriogenology. 2018. 107: 188-193.

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) PDJ program (AMGD award number 150844/2017–4) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP). The funders had no role in study design, data collection and analysis, decision to publish, or manuscript preparation.

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Nelcio Antonio Tonizza de Carvalho, Pietro Sampaio Baruselli, Mario Binelli, Paula de Carvalho Papa, and Ed Hoffman Madureira designed the study protocol and reviewed the manuscript. Diego Cavalcante de Souza, Angela Maria Gonella-Diaza, Nelcio Antonio Tonizza de Carvalho, Júlia Gleyci Soares de Carvalho, Flavia Morag Elliff, Lais Mendes Vieira, Antenor Pereira Bonfim Neto, and Sarvpreet Singh Ghuman conducted the study and performed the laboratory analysis. Diego Cavalcante de Souza and Angela Maria Gonella-Diaza analyzed and interpreted the data and wrote the first version of the manuscript. Guilherme Pugliesi, Mario Binelli, and Nelcio Antonio Tonizza de Carvalho reviewed and improved the manuscript. All authors read and approved the final manuscript.

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Correspondence to Angela Maria Gonella-Diaza.

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All animal procedures were approved by the Ethics and Animal Handling Committee of the School of Veterinary Medicine and Animal Science of the University of São Paulo (USP) in São Paulo, Brazil (CEUA/FMVZ; protocol number 5326030214).

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Cavalcante de Souza, D., Gonella-Diaza, A.M., de Carvalho, N.A.T. et al. Supplementation with long-acting injectable progesterone 3 days after TAI impaired luteal function in buffaloes. Trop Anim Health Prod 56, 76 (2024). https://doi.org/10.1007/s11250-024-03913-3

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