Investigation of PAG2 mRNA Expression in Water Buffalo Peripheral Blood Mononuclear Cells and Polymorphonuclear Leukocytes from Maternal Blood at the Peri-Implantation Period.
PAG2 mRNA; peri-implantation; pregnancy diagnosis; water buffalo; Veterinary (all); General Veterinary; pregnancy-associated glycoprotein
Abstract :
[en] : The main objective of this study was to assess PAG2 mRNA expression in maternal blood cells at the peri-implantation period in water buffalo; moreover, we wanted to evaluate the earliest time in which PAG-2 could be detected in maternal blood. Thirty-two lactating buffaloes artificially inseminated (AI) were utilized. Blood was collected at Days 0, 14, 18, 28, 40 after AI (AI = day 0). Pregnancy was diagnosed by ultrasound at Days 28 and 40 post AI. Out of 32 buffaloes, 14 were pregnant (P group) and 18 were not pregnant (NP group). The plasma PAG-2 threshold of 1.0 ng/mL in the P group was reached at day 40 post AI. PAG2 mRNA expression differed between the P and NP groups, and was either evaluated in Peripheral Blood Mononuclear Cells (PBMC) or Polymorphonuclear Leukocytes (PMN), starting from day 14. However, both the estimated marginal means and multiple comparisons showed that PAG2 mRNA expression was higher in PMN than PBMC. In the present study, PAG-2 appeared in the blood (40 Days post AI), and an early expression of PAG2 mRNA at Day 14 post AI was also observed. Although further research is undoubtedly required, PAG2 mRNA in peripheral blood leukocytes could be using to better understand the role that PAGs play during pregnancy in buffalo.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Barbato, Olimpia ; Dipartimento di Medicina Veterinaria, Università degli studi di Perugia, 06100 Perugia, Italy. olimpia.barbato@unipg.it
Guelfi, Gabriella ; Dipartimento di Medicina Veterinaria, Università degli studi di Perugia, 06100 Perugia, Italy. gabriella.guelfi@unipg.it
Menchetti, Laura ; Dipartimento di Medicina Veterinaria, Università degli studi di Perugia, 06100 Perugia, Italy. laura.menchetti7@gmail.com
Brecchia, Gabriele; Dipartimento di Medicina Veterinaria, Università degli studi di Perugia, 06100 Perugia, Italy. gabriele.brecchia@unipg.it
de Sousa, Noelita Melo; Laboratoires d'Endocrinologie Animale et de Reproduction, Faculté de Médicine Vétérinaire, Université de Liège, B-4000 Liège, Belgium. noelitamelo@gmail.com
Canali, Claudio; Dipartimento di Medicina Veterinaria, Università degli studi di Perugia, 06100 Perugia, Italy. claudio.canali@unipg.it
Grandoni, Francesco; CREA Consiglio per la ricerca in agricoltura e l'analisi dell'economia agraria, Centro di ricerca Zootecnia e Acquacoltura, 00015 Monterotondo (Roma), Italy. francesco.grandoni@crea.gov.it
Scatà, Maria Carmela; CREA Consiglio per la ricerca in agricoltura e l'analisi dell'economia agraria, Centro di ricerca Zootecnia e Acquacoltura, 00015 Monterotondo (Roma), Italy. mariacarmela.scata@crea.gov.it
De Matteis, Giovanna; CREA Consiglio per la ricerca in agricoltura e l'analisi dell'economia agraria, Centro di ricerca Zootecnia e Acquacoltura, 00015 Monterotondo (Roma), Italy. giovanna.dematteis@crea.gov.it
Casano, Anna Beatrice; Dipartimento di Medicina Veterinaria, Università degli studi di Perugia, 06100 Perugia, Italy. noelitamelo@gmail.com
Beckers, Jean-François ; Université de Liège - ULiège > Département des sciences fonctionnelles (DSF) > Physiologie de la reproduction
Barile, Vittoria Lucia; CREA Consiglio per la ricerca in agricoltura e l'analisi dell'economia agraria, Centro di ricerca Zootecnia e Acquacoltura, 00015 Monterotondo (Roma), Italy. vittorialucia.barile@crea.gov.it
Language :
English
Title :
Investigation of PAG2 mRNA Expression in Water Buffalo Peripheral Blood Mononuclear Cells and Polymorphonuclear Leukocytes from Maternal Blood at the Peri-Implantation Period.
Publication date :
14 January 2019
Journal title :
Veterinary Sciences
eISSN :
2306-7381
Publisher :
MDPI Multidisciplinary Digital Publishing Institute, Switzerland
Funding: This study was supported by Scientific and Technological Research Program founded by Fondazione Cassa di Risparmio of Perugia and Sterling SPA.
Zoli, A.P.; Beckers, J.F.; Wouters-Ballman, P.; Closset, J.; Falmagne, P.; Ectors, F. Purification and characterization of a bovine pregnancy-associated glycoprotein. Boil. Reprod. 1991, 45, 1-10
Beckers, J.F.; Roberts, R.M.; Zoli, A.P.; Ectors, F.; Derivaux, J. Molécules de la familles des proteases aspartique dans la placenta des Runinats: Hormones ou proteins? Bull. Acad. Méd. Belg. 1994, 143, 355-367
Xie, S.; Low, B.G.; Nagel, R.J.; Beckers, J.F.; Roberts, R.M. A novel glycoprotein of the aspartic proteinase gene family expressed in bovine placental trophectoderm. Boil. Reprod. 1994, 51, 1145-1153
Szafranska, B.; Xie, S.; Green, J.; Roberts, R.M. Porcine Pregnancy-Associated Glycoproteins: New members of the aspartic Proteinase gene family expressed in the trophectoderm. Boil. Reprod. 1995, 53, 21-28
Xie, S.; Green, J.; Bao, B.; Beckers, J.F.; Valdez, K.E.; Hakami, L.; Roberts, R.M. Multiple pregnancy-associated glycoproteins are secreted by day 100 ovine placental tissue. Boil. Reprod. 1997, 57, 1384-1393
Garbayo, J.M.; Remy, B.; Alabart, J.L.; Folch, J.;Wattiez, R.; Falmagne, P.; Beckers, J.F. Isolation and partial characterization of a pregnancy-associated glycoprotein family from the goat placenta. Boil. Reprod. 1998, 58, 109-115
Garbayo, J.M.; Green, J.; Manikkam, M.; Beckers, J.F.; Kiesling, D.; Ealy, A.D.; Roberts, R.M. Caprine Pregnancy-associated glycoproteins (PAG): Their cloning, expression and evolutionary relationship to other PAG. Mol. Reprod. Dev. 2000, 57, 311-322
El Amiri, B.; Remy, B.; De Sousa, N.M.; Beckers, J.F. Isolation and characterization of eight pregnancy-associated glycoproteins present at high levels in the ovine placenta between day 60 and day 100 of gestation. Reprod. Nutr. Dev. 2004, 44, 169-181
Brandt, G.A.; Parks, T.E.; Killian, G.; Ealy, A.D.; Green, J.A. A cloning and expression analysis of pregnancy-associated glycoproteins expressed in trophoblast of the white-tail deer placenta. Mol. Reprod. Dev. 2007, 74, 1355-1362
Barbato, O.; Sousa, N.; Klisch, K.; Clerget, E.; Debenedetti, A.; Barile, V.; Malfatti, A.; Beckers, J. Isolation of new pregnancy-associated glycoproteins from water buffalo (bubalus bubalis) placenta by Vicia villosa affinity cromatography. Res. Vet. Sci. 2008, 85, 457-466
Kiewisz, K.; Sousa, N.M.; Beckers, J.F.; Panasiewics, G.; Gizejewski, Z.; Szafranska, B. Identification of multiple pregnancy-associated glycoproteins (PAGs) purified from European bison (Eb; Bison bison) placenta. Anim. Reprod. Sci. 2009, 112, 229-250
Telugu, B.P.;Walker, A.M.; Green, J.A. Characterization of the bovine pregnancy-associated glycoprotein gene family-Analysis of gene sequences, regulatory regions within the promoter and expression of selected genes. BMC Genom. 2009, 10, 185
Nguyen, V.H.; Barbato, O.; Bui, X.N.; Beckers, J.F.; Melo de Sousa, N. Assessment of pregnancy-associated glycoprotein (PAG) concentrations in swamp buffalo samples from fetal and maternal origins using interspecies antisera. Anim. Sci. J. 2012, 83, 683-689
Barbato, O.; Melo de Sousa, N.; Barile, V.L.; Canali, C.; Beckers, J.F. Purification of pregnancy-associated glycoproteins from late-pregnancy Bubalus bubalis placentas and development of a radioimmunoassay for pregnancy diagnosis in water buffalo females. BMC Vet. Res. 2013, 9, 89
Beriot, M.; Tchimbou, A.F.; Barbato, O.; Beckers, J.F.; Sousa, N.M. Identification of pregnancy-associated glycoproteins and alpha-fetoprotein in in fallow deer (Dama dama) placenta. Acta Vet. Scand. 2014, 56, 4
Hughes, A.L.; Green, J.A.; Piontkivska, H.; Robetrs, R.M. Adaptive diversification within a large family of recently duplicated, placentally expressed genes. Proc. Natl. Acad. Sci. USA 2000, 97, 3119-3323
Hughes, A.L.; Green, J.A.; Piontkivska, H.; Robetrs, R.M. Aspartic Proteinase Phylogenetic and the Origin of Pregnancy-Associated Glycoproteins. Mol. Biol. Evol. 2013, 20, 1940-1945
Wooding, F.B.; Roberts, R.M.; Green, J.A. Light and electron microscope immunocytochemical studies of the distribution of pregnancy-associated glycoproteins (PAGs) throughout pregnancy in the cow: Possible functional implications. Placenta 2005, 26, 807-827
Garbayo, J.M.; Serrano, B.; Lopez-Gatius, F. Identification of novel pregnancy-associated glycoproteins (PAG) expressed by the perimplantion conceptus of domestic ruminants. Anim. Reprod. Sci. 2008, 103, 120-134
Wallace, R.M.; Pohler, K.J.; Smith, M.F.; Green, J.A. Placental PAGs: Gene origins, expression patterns, and use as markers of pregnancy. Reproduction 2015, 149, R115-R126
Sousa, N.M.; Remy, B.; El Amiri, B.; De Figueiredo, J.R.; Banga-Mboko, H.; Goncalves, P.B.D.; Beckers, J.F. Characterization of pregnancy-associated glycoproteins extracted from zebu (Bos indicus) placentas removed at different gestational period. Reprod. Nutr. Dev. 2002, 42, 227-241
Touzard, E.; Reinaud, P.; Dubois, O.; Guyader-Joly, C.; Humblot, P. Specific expression patterns and cell distribution of ancient and modern PAG in bovine placenta during pregnancy. Reproduction 2013, 146, 347-362
Zoli, A.P.; Guibault, L.A.; Delahaut, P.; Benitez Ortiz, W.; Beckers, J.F. Radioimmunoassay of a bovine pregnancy-associated glycoprotein in serum: Its application for pregnancy diagnosis. Boil. Reprod. 1992, 46, 83-92
Szenci, O.; Beckers, J.F.; Sulon, J.; Sasser, G.; Taverne, M.A.M.; Varga, J.; Borzsony, L.; Hanzen, C.; Schekk, G. Comparison of ultrasonography, bovine pregnancy specific B and bovine pregnancy-associated glycoprotein 1 test for pregnancy detection in dairy cows. Theriogenology 1998, 50, 77-88
Barbato, O.; Sousa, N.M.; Debenedetti, A.; Canali, C.; Todini, L.; Beckers, J.F. Validation of a new pregnancy-associated glycoprotein radioimmunoassay method for the detection of early pregnancy in ewes. Theriogenology 2009, 72, 993-1000
El Amiri, B.; Sousa, N.M.; Alvarez Oxiley, A.; Hadarbach, D.; Beckers, J.F. Pregnancy-associated glycoprotein (PAG) concentration in plasma and milk samples for early pregnancy diagnosis in Lacaune dairy sheep. Res. Vet. Sci. 2015, 99, 30-36
Barbato, O.; Chiardia, E.; Barile, V.L.; Pierri, F.; Sousa, M.N.; Terracina, L.; Canali, C.; Avellini, L. Investigation into omocysteine, vitamin E and malondialdeyde as indicators of successful artificial insemination in synchronized buffalo cows (Bubalus bubalis). Res. Vet. Sci. 2016, 104, 100-105
Barbato, O.; Menchetti, L.; Sousa, N.M.; Malfatti, A.; Brecchia, G.; Canali, C.; Beckers, J.F.; Barile, V.L. Pregnancy-associated glycoproteins (PAGs) concentrations in water buffaloes (Bubalus bubalis) during gestation and the postpartum period. Theriogenology 2017, 97, 73-77
Barbato, O.; Menchetti, L.; Sousa, N.M.; Malfatti, A.; Brecchia, G.; Canali, C.; Beckers, J.F.; Barile, V.L. Correlation of two radioimmunoassay systems for measuring plasma pregnancy-associated glycoproteins concentrations during early pregnancy and postpartum periods in water buffalo. Reprod. Domest. Anim. 2018, 53, 1483-1490
Garcia-Ispierto, B.; Almeria, S.; Serrano-Perez, B.; Sousa, N.M.; Beckers, J.F.; López-Gatius, F. Plasma Concentrations of Pregnancy-Associated Glycoproteins measured using anti-bovine PAG-2 antibodies on day 120 of gestation predict abortion in dairy cows naturally infected with Neospora caninum. Reprod. Domest. Anim. 2013, 48, 613-618
Garcia-Ispierto, B.; Serrano-Pérez, S.; Martínez-Bello, D.; Tchimbou, A.F.; Sousa, N.M.; Beckers, J.F.; López-Gatius, F. Effects of crossbreeding on endocrine patterns determined in beef/dairy cows naturally infected with Neospora caninum. Theriogenology 2015, 83, 491-496
Garcia-Ispierto, B.; Ressello-Visa, M.A.; Serrano-Pérez, B.; Mur-Nuvales, R.; Sousa, N.M.; Beckers, J.F.; López-Gatius, F. Plasma concentration of pregnancy-associated glycoproteins I and II and progesterone on day 28 post AI as marker of twin pregnancy in dairy cattle. Livest. Sci. 2016, 192, 44-47
Mur-Novales, R.; López-Gatius, F.; Serrano-Pérez, B.; Garcia-Ispierto, B.; Darwich, L.; Cabezon, O.; Sousa, N.M.; Beckers, J.F.; Almeria, S. Experimental Neospora Caninum infection in pregnant dairy heifers raises voncentrations of pregnancy-associated glycoproteins 1 and 2 in in foetal fluids. Reprod. Domest. Anim. 2016, 51, 282-286
Almeria, S.; Serrano-Pérez, B.; López-Gatius, F. Immune response in bovine neosporis: Protection or contribution to the pathogenesis of abortion. Microb. Pathog. 2017, 109, 177-182
Barbato, O.; Guelfi, G.; Barile, V.L.; Menchetti, L.; Tortiello, C.; Canali, C.; Brecchia, G.; Traina, G.; Beckers, J.F.; Sousa, N.M. Using real-time PCR to identify pregnancy-associated glycoprotein 2 (PAG-2) in water buffalo (Bubalus bubalis) blood in early pregnany. Theriogenology 2017, 97, 73-77
Sharma, R.K.; Singh, J.K.; Khanna, S.; Phulia, S.K.; Sarkar, S.K.; Singh, I. Fetal age determination in Murrah buffaloes from days 22 through 60 with ultrasonography. Indian J. Anim. Sci. 2012, 82, 374-376
Serrano-Pérez, B.; Hansen, P.J.; Mur-Novales, R.; Garcia-Ispierto, B.; Sousa, N.M.; Beckers, J.F.; Almeria, S.; López-Gatius, F. Crosstalk between uterine serpin (SERPINA14) and pregnancy-associated glycoproteins at the fetal-maternal interface in pregnant dairy heifer experimentally infected with Neospora caninum. Theriogenology 2016, 86, 824-830
Beckers, J.F.; Dewulf, M.; Verstegen, J.; Wouters-Ballman, P.; Ectors, F. Isolation of a bovine chorionic gonadotrophin (bCG). Theriogenology 1988, 29, 218
Vaitukaitis, J.; Robbins, J.B.; Nieschlag, E.; Ross, G.T. A method for producing specific antisera with small doses of immonogen. J. Clin. Endocrinol. Metab. 1971, 33, 988-991
Thorell, J.I.; Johansson, B.G. Enzymatic iodination of polypeptides with 125I to high specific activity. Biochim. Biophys. Acta 1971, 251, 363-369
Diverio, S.; Guelfi, G.; Barbato, O.; Di Mari, W.; Egidi, G.; Santoro, M.M. Non-invasive assessment of animal exercise stress: Real-time PCR of GLUT4, COX2, SOD1 and HSP70 in avalanche military dog saliva. Animal 2015, 5, 774-792
Greiner, M.; Pfeiffer, D.; Smith, R.D. Principles and practical application of the receiver-operating characteristic analysis for diagnostic tests. Prev. Vet. Med. 2000, 45, 23-41
Yankey, S.J.; Hicks, B.A.; Carnahan, K.G.; Assiri, A.M.; Sinor, S.J.; Kodali, K.; Stellflug, J.N.; Ott, T.L. Expression of the antiviral protein Mx in peripheral blood mononuclear cells of pregnant and bred, non-pregnant ewes. J. Endocrinol. 2001, 170, R7-R11
Gifford, C.A.; Racicot, K.; Clark, D.S.; Austin, K.J.; Hansen, T.R.; Lucy, M.C.; Davies, C.J.; Ott, T.L. Regulation of interferon-stimulated genes in peripheral blood leukocytes in pregnant and bred, non pregnant dairy cows. J. Dairy Sci. 2007, 90, 274-280
Pugliesi, G.; Miagawa, B.T.; Paiva, Y.N.; Franca, M.R.; Silva, L.A.; Binelli, M. Conceptus-induced changes in the Gene Expression of Blood Immune Cells and the ultrasound-accessed luteal function in beef-cattle: How early can we detect pregnancy? Boil. Reprod. 2014, 91, 95
Chethan, S.G.; Singh, S.K.; Nongsiej, J.; Rakesh, H.B.; Singh, R.P.; Kumar, N.; Agarwal, S.K. IFN-τ acts in a dose-dependent manner on prostaglandin production by buffalo endometrial stromal cells cultured in vitro. Reprod. Domest. Anim. 2014, 49, 403-408
Spencer, T.E.; Burghardt, R.C.; Johnson, G.A.; Bazer, F.W. Conceptus signals for establishment and maintenance of pregnancy. Anim. Reprod. Sci. 2004, 82-83, 537-550
Parent, J.; Chapdelaine, P.; Sirois, J.; Fortier, M.A. Expression of microsomal prostaglandin E synthase in bovine endometrium: Coexpression with cyclooxygenase type 2 and regulation by interferon-τ. Endocrinology 2002, 143, 2936-2943
Spencer, T.E.; Bazer, F.W. Biology of progesterone action during pregnancy recognition and maintenance of pregnancy. Front. Biosci. 2002, 7, 1879-1898
Mamo, S.; Mehta, J.P.; McGettigan, P.; Fair, T.; Spencer, T.E.; Bazer, F.W.; Lonergan, P. RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation. Biol. Reprod. 2011, 85, 1143-1151
Thompson, I.M.; Cerri, R.L.; Kim, I.H.; Ealy, A.D.; Hansen, P.J.; Staples, C.R.; Thatcher, W.W. Effects of lactation and pregnancy on metabolic and hormonal responses and expression of selected conceptus and endometrial genes of Holstein dairy cattle. J. Dairy Sci. 2012, 95, 5645-5656
Hue, I.; Degrelle, S.A.; Turenne, N. Conceptus elongation in cattle: Genes, models and questions. Anim. Reprod. Sci. 2012, 134, 19-28
Del Vecchio, R.P.; Sutherland, W.D.; Sasse, R.G. Effect of pregnancy-specific protein B on luteal cell progesterone, prostaglandin, and oxytocin production during two stages of the bovine estrous cycle. J. Anim. Sci. 1995, 73, 2662-2668
Del Vecchio, R.P.; Sutherland,W.D.; Sasser, R.G. Bovine luteal cell production in vitro of prostaglandin E2, oxytocin and progesterone in response to pregnancy-specific protein B and prostaglandin F2ff. J. Reprod. Fertil. 1996, 107, 131-136
Weems, S.Y.; Lammoglia, M.A.; Vera-Avila, H.R.; Randel, R.D.; King, C.; Sasser, R.G.; Weems, C.W. Effect of luteinizing hormone (LH), PGE2, 8-EPI-PGE1, 8-EPI-PGE2, trichosanthin, and pregnancy specific protein B (PSPB) on secretion of progesterone in vitro by corpora lutea (CL) from non pregnant and pregnant cows. Prostaglandins 1998, 55, 27-42
Austin, K.J.; King, L.P.; Vierk, J.E.; Spencer, R.C.; Hauren, T.R. Pregnancy-specific-protein B induces release on an alpha chemokine in bovine endometrium. Endocrinology 1999, 140, 542-545
Hoeben, D.; Burvenicha, C.; Massart-Leena, A.; Lenjou, M.; Nij, G. In vitro effect of ketone bodies, glucocorticosteroids and bovine pregnancy-associated glycoprotein on cultures of bone marrow progenitor cells of cows and calves. Vet. Immunol. Immunopathol. 1999, 68, 229-240
Sandra, O.; Constanta, C.; Carvalho, A.V.; Eozénoua, C.; Valoura, D.; Mauffréa, V.; Huea, I.; Charpignya, G. Maternal organism and embryo biosensoring: Insights from ruminants. J. Reprod. Immunol. 2015, 108, 105-113