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Article: Collagen Type III as a Possible Blood Biomarker of Fibrosis in Equine Endometrium

Alpoim-Moreira, Joana / Fernandes, Carina / Rebordão, Maria Rosa / Costa, Ana Luísa / Bliebernicht, Miguel / Nunes, Telmo / Szóstek-Mioduchowska, Anna / Skarzynski, Dariusz J. / Ferreira-Dias, Graça

Animals. 2022 July 21, v. 12, no. 14

2022

Abstract: Collagen pathological deposition in equine endometrium (endometrosis) is responsible for infertility. Kenney and Doig’s endometrial biopsy histopathological classification is the gold standard method for endometrosis evaluation, whereby blood biomarkers ... ...

Abstract	Collagen pathological deposition in equine endometrium (endometrosis) is responsible for infertility. Kenney and Doig’s endometrial biopsy histopathological classification is the gold standard method for endometrosis evaluation, whereby blood biomarkers identification would be less invasive and could provide additional information regarding endometrosis diagnosis and fertility prognosis. This study aimed to identify blood biomarkers for endometrosis diagnosis (42 mares were used in experiment 1), and fertility assessment (50 mares were used in experiment 2). Reproductive examination, endometrial biopsy histopathological classification (Kenney and Doig) and blood collection were performed. Endometrium and serum collagen type I (COL1) and type III (COL3), and hydroxyproline concentrations were measured (ELISA). Serum COL3 cut-off value of 60.9 ng/mL allowed healthy endometria (category I) differentiation from endometria with degenerative/fibrotic lesions (categories IIA, IIB or III) with 100% specificity and 75.9% sensitivity. This cut-off value enabled category I + IIA differentiation from IIB + III (76% specificity, 81% sensitivity), and category III differentiation from others (65% specificity, 92.3% sensitivity). COL1 and hydroxyproline were not valid as blood biomarkers. Serum COL3 cut-off value of 146 ng/mL differentiated fertile from infertile mares (82.4% specificity, 55.6% sensitivity), and was not correlated with mares’ age. Only COL3 may prove useful as a diagnostic aid in mares with endometrial fibrosis and as a fertility indicator.
Keywords	biomarkers ; biopsy ; blood sampling ; blood serum ; collagen ; endometrium ; fibrosis ; histopathology ; hydroxyproline ; prognosis
Language	English
Dates of publication	2022-0721
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2606558-7
ISSN	2076-2615
ISSN	2076-2615
DOI	10.3390/ani12141854
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Impact of inbreeding and genetic parameter estimates for seminal traits in Lusitano horses

Gonçalves, Ana Rita / Telo da Gama, Luis / Luis, Antunes / Guimarães, Helena / Bliebernicht, Miguel / Duarte, José Carlos / Cosinha, Cristina / Duarte Rego, Bruno / Ferro da Costa, Pedro / Guimarães, Tiago / Rocha, Antonio / Bettencourt, Elisa

Theriogenology. 2023 May 27,

2023

Abstract: The objectives of this study were to establish baseline information for seminal traits in Lusitano stallions, to assess the impact of inbreeding, interval between collections and age on semen quality during the breeding and non-breeding seasons, and to ... ...

Abstract	The objectives of this study were to establish baseline information for seminal traits in Lusitano stallions, to assess the impact of inbreeding, interval between collections and age on semen quality during the breeding and non-breeding seasons, and to estimate the corresponding genetic parameters. A total of 2129 ejaculates by 146 Lusitano stallions used for artificial insemination, obtained from four equine reproduction centers distributed throughout Portugal, over a period of 14 years (2008–2021), were included in the study. The seminal traits analyzed, and the corresponding means and standard deviations, were gel-free volume (56.95 ± 28.76 mL), concentration (186.48 ± 104.68 × 10⁶), motility (64.1 ± 16.9%), total number of spermatozoa (TNS) (9.271 ± 4.956 × 10⁹) and total number of motile spermatozoa per ejaculate (TNMS) (5.897 ± 3.587 × 10⁹). These results are in the normal range of values described for other breeds. In the stallions analyzed, the mean value for the inbreeding coefficient was 7.93 ± 5.29%, and for age it was 12.70 ± 6.83 years. A significant decline in sperm concentration, motility, TNS, and TNMS was observed as inbreeding increased. The season also influenced sperm concentration, motility, TNS and TNMS, with the highest values observed during the breeding season. When considering the impact of age on Lusitano seminal parameters, results showed a nonlinear relationship, with a positive effect until 18 years of age for volume, motility, TNS and TNMS and a negative effect after this age, with a slow decrease. However, age had a markedly negative effect on sperm concentration. The interval between semen collections only affected (P < 0.05) sperm motility, with a regression coefficient of +1.89 ± 2.17% per additional day. Genetic parameters were estimated with an Animal Model, and the estimated heritability (repeatability) was 0.27 (0.35) for volume, 0.02 (0.38) for sperm concentration, 0.24 (0.44) for motility, 0.29 (0.39) for TNS and 0.41 (0.41) for TNMS. These results suggest that it is possible to improve semen quality by selection and that the properties of semen produced by a stallion tend to remain consistent throughout its lifetime. Furthermore, the impact of inbreeding should be taken into consideration when selecting Lusitano stallions for fertility.
Keywords	Lusitano ; animal models ; artificial insemination ; heritability ; regression analysis ; semen quality ; sperm concentration ; sperm motility ; stallions ; Portugal ; Horse ; Inbreeding
Language	English
Dates of publication	2023-0527
Publishing place	Elsevier Inc.
Document type	Article ; Online
Note	Pre-press version
ZDB-ID	189232-0
ISSN	1879-3231 ; 0093-691X
ISSN (online)	1879-3231
ISSN	0093-691X
DOI	10.1016/j.theriogenology.2023.05.011
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Epigenetic regulation of collagen in the mare's placenta: putative relationship with maternal age

Vasconcelos, Manuel A. / Wong, Yat / Alpoim-Moreira, Joana / Rebordão, Maria R. / Fradinho, Maria J. / Costa, Ana L. / Bliebernicht, Miguel / Castro, Fidel O. / Silva, Elisabete / Ferreira-Dias, Graça M.

Journal of Equine Veterinary Science. 2023 June, v. 125 p.104790-

2023

Abstract: Placental plasticity influences fetal development, pregnancy success, and foal growth. Older fertile mares deliver heavier foals and placentas, with increased collagen deposition. In humans, epigenetics regulates placental development and function. ... ...

Abstract	Placental plasticity influences fetal development, pregnancy success, and foal growth. Older fertile mares deliver heavier foals and placentas, with increased collagen deposition. In humans, epigenetics regulates placental development and function. Epigenetics, through DNA methylation, also modulates endometrial fibrosis. As such, we hypothesized that as mares get older, collagen deposition in the placenta might be epigenetically modulated. This study assessed if transcription of collagen genes in the equine placenta was epigenetically modulated through DNA methyltransferases (DNMTs), and affected by aging. Immediately after foaling, samples from different chorioallantoic areas (gravid horn, non-gravid horn, and body) were collected from young (n=10; 4-6 years) and older mares (n=10; 12-18 years). Gene transcription of collagen type 1 (COL1A1), collagen type 3 (COL3A1), and DNA methyltransferases (DNMT1, DNMT3A and DNMT3B) was determined (qRT-PCR). Unpaired T-test and Mann-Whitney test were used with statistical significance set a p <0.05. In older mares, COL1A1 mRNA levels were higher in the gravid than in the non-gravid horn (p<0.05), and also upregulated in comparison to young mares’ placentas (p<0.05). In young mares, these transcripts were increased in the placenta body in comparison to the gravid (p<0.05) and non-gravid horns (p<0.01). In older mares, COL3A1 transcriptionwas higher in gravid and non-gravid horns, with respect to the same placenta regions in young mares (p<0.05). In older mares, DNMT1 mRNA expression in the body was lower than in younger mares (p<0.05). For all placentas, DNMT1 transcripts in the non-gravid horn were lowest, compared to the gravid horn (p<0.01) and body (p<0.001). In young mares, DNMT1 mRNA expression in the body was also higher than in the gravid horn (p<0.05). With mares aging, there was a downregulation of DNMT3A transcripts in gravid and non-gravid placenta horns, compared to young mares’ placentas (p< 0.05). In older mares, its levels were lowest in the gravid horn, compared to the non-gravid horn (p<0.05) and body (p<0.01). Similarly, in older mares’ placentas, DNMT3B transcripts were downregulated in the gravid horn (p<0.05) and placenta body (p<0.001), compared to young mares. DNMT3B mRNA levels were lowest in the non-gravid horn, both in young mares, in comparison to placenta body (p<0.01) and in older mares, with respect to the gravid horn and body (p<0.01). Considering mares aging, hypomethylation indicated by decreased DNMTs transcripts, in parallel with upregulation of collagen gene expression in gravid and non-gravid horns, may suggest epigenetic involvement on placental plasticity. However, further research is needed to unravel the intricacies of epigenetic modulation of collagen in equine placentas.
Keywords	DNA methylation ; DNA methyltransferase ; collagen ; endometrium ; epigenetics ; fetal development ; fibrosis ; foals ; gene expression ; mares ; placenta ; plasticity ; pregnancy ; t-test ; transcription (genetics) ; veterinary medicine
Language	English
Dates of publication	2023-06
Publishing place	Elsevier Inc.
Document type	Article ; Online
ZDB-ID	2102631-2
ISSN	1542-7412 ; 0737-0806
ISSN (online)	1542-7412
ISSN	0737-0806
DOI	10.1016/j.jevs.2023.104790
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Article ; Online: Impact of inbreeding and genetic parameter estimates for seminal traits in Lusitano horses.

Gonçalves, Ana Rita / Telo da Gama, Luis / Antunes, Luis / Guimarães, Helena / Bliebernicht, Miguel / Duarte, José Carlos / Cosinha, Cristina / Duarte Rego, Bruno / Ferro da Costa, Pedro / Guimarães, Tiago / Rocha, António / Bettencourt, Elisa

Theriogenology

2023 Volume 208, Page(s) 43–51

Abstract	The objectives of this study were to establish baseline information for seminal traits in Lusitano stallions, to assess the impact of inbreeding, interval between collections and age on semen quality during the breeding and non-breeding seasons, and to estimate the corresponding genetic parameters. A total of 2129 ejaculates by 146 Lusitano stallions used for artificial insemination, obtained from four equine reproduction centers distributed throughout Portugal, over a period of 14 years (2008-2021), were included in the study. The seminal traits analyzed, and the corresponding means and standard deviations, were gel-free volume (56.95 ± 28.76 mL), concentration (186.48 ± 104.68 × 10
MeSH term(s)	Male ; Animals ; Horses/genetics ; Inbreeding ; Semen Analysis/veterinary ; Semen ; Sperm Motility/genetics ; Sperm Count/veterinary
Language	English
Publishing date	2023-05-27
Publishing country	United States
Document type	Journal Article
ZDB-ID	189232-0
ISSN	1879-3231 ; 0093-691X
ISSN (online)	1879-3231
ISSN	0093-691X
DOI	10.1016/j.theriogenology.2023.05.011
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Je nach Verfügbarkeit (siehe Angabe bei Bestand)
bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular
Jg. 1995 - 2021: Lesesall (2.OG)
ab Jg. 2022: Lesesaal (EG)

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Article: Metallopeptidades 2 and 9 genes epigenetically modulate equine endometrial fibrosis.

Alpoim-Moreira, Joana / Fernandes, Carina / Pimenta, Jorge / Bliebernicht, Miguel / Rebordão, Maria Rosa / Castelo-Branco, Pedro / Szóstek-Mioduchowska, Anna / Skarzynski, Dariusz J / Ferreira-Dias, Graça

Frontiers in veterinary science

2022 Volume 9, Page(s) 970003

Abstract: Endometrium type I (COL1) and III (COL3) collagen accumulation, periglandular fibrosis and mare infertility characterize endometrosis. Metalloproteinase-2 (MMP-2), MMP-9 and tissue inhibitors of metalloproteinases (TIMP-1 and TIMP-2) are involved in ... ...

Abstract	Endometrium type I (COL1) and III (COL3) collagen accumulation, periglandular fibrosis and mare infertility characterize endometrosis. Metalloproteinase-2 (MMP-2), MMP-9 and tissue inhibitors of metalloproteinases (TIMP-1 and TIMP-2) are involved in collagen turnover. Since epigenetic changes may control fibroproliferative diseases, we hypothesized that epigenetic mechanisms could modulate equine endometrosis. Epigenetic changes can be reversed and therefore extremely promising for therapeutic use. Methylation pattern analysis of a particular gene zone is used to detect epigenetic changes. DNA methylation commonly mediates gene repression. Thus, this study aimed to evaluate if the transcription of some genes involved in equine endometrosis was altered with endometrial fibrosis, and if the observed changes were epigenetically modulated, through DNA methylation analysis. Endometrial biopsies collected from cyclic mares were histologically classified (Kenney and Doig category I,
Language	English
Publishing date	2022-08-12
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2834243-4
ISSN	2297-1769
ISSN	2297-1769
DOI	10.3389/fvets.2022.970003
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Article: Collagen Type III as a Possible Blood Biomarker of Fibrosis in Equine Endometrium.

Alpoim-Moreira, Joana / Fernandes, Carina / Rebordão, Maria Rosa / Costa, Ana Luísa / Bliebernicht, Miguel / Nunes, Telmo / Szóstek-Mioduchowska, Anna / Skarzynski, Dariusz J / Ferreira-Dias, Graça

Animals : an open access journal from MDPI

2022 Volume 12, Issue 14

Abstract: Collagen pathological deposition in equine endometrium (endometrosis) is responsible for infertility. Kenney and Doig's endometrial biopsy histopathological classification is the gold standard method for endometrosis evaluation, whereby blood biomarkers ... ...

Abstract	Collagen pathological deposition in equine endometrium (endometrosis) is responsible for infertility. Kenney and Doig's endometrial biopsy histopathological classification is the gold standard method for endometrosis evaluation, whereby blood biomarkers identification would be less invasive and could provide additional information regarding endometrosis diagnosis and fertility prognosis. This study aimed to identify blood biomarkers for endometrosis diagnosis (42 mares were used in experiment 1), and fertility assessment (50 mares were used in experiment 2). Reproductive examination, endometrial biopsy histopathological classification (Kenney and Doig) and blood collection were performed. Endometrium and serum collagen type I (COL1) and type III (COL3), and hydroxyproline concentrations were measured (ELISA). Serum COL3 cut-off value of 60.9 ng/mL allowed healthy endometria (category I) differentiation from endometria with degenerative/fibrotic lesions (categories IIA, IIB or III) with 100% specificity and 75.9% sensitivity. This cut-off value enabled category I + IIA differentiation from IIB + III (76% specificity, 81% sensitivity), and category III differentiation from others (65% specificity, 92.3% sensitivity). COL1 and hydroxyproline were not valid as blood biomarkers. Serum COL3 cut-off value of 146 ng/mL differentiated fertile from infertile mares (82.4% specificity, 55.6% sensitivity), and was not correlated with mares' age. Only COL3 may prove useful as a diagnostic aid in mares with endometrial fibrosis and as a fertility indicator.
Language	English
Publishing date	2022-07-21
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2606558-7
ISSN	2076-2615
ISSN	2076-2615
DOI	10.3390/ani12141854
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Article: Collagen and Microvascularization in Placentas From Young and Older Mares.

Neto da Silva, Ana Catarina / Costa, Ana Luísa / Teixeira, Ana / Alpoim-Moreira, Joana / Fernandes, Carina / Fradinho, Maria João / Rebordão, Maria Rosa / Silva, Elisabete / Ferreira da Silva, José / Bliebernicht, Miguel / Alexandre-Pires, Graça / Ferreira-Dias, Graça

Frontiers in veterinary science

2022 Volume 8, Page(s) 772658

Abstract: In older mares, increasing collagen fibers (fibrosis) in the endometrium and oviduct predisposes to sub-fertility and infertility. In this study, (i) gene transcription of collagen (qPCR: ...

Abstract	In older mares, increasing collagen fibers (fibrosis) in the endometrium and oviduct predisposes to sub-fertility and infertility. In this study, (i) gene transcription of collagen (qPCR:
Language	English
Publishing date	2022-01-04
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2834243-4
ISSN	2297-1769
ISSN	2297-1769
DOI	10.3389/fvets.2021.772658
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Collagens and DNA methyltransferases in mare endometrosis.

Alpoim-Moreira, Joana / Fernandes, Carina / Rebordão, Maria Rosa / Amaral, Ana / Pinto-Bravo, Pedro / Bliebernicht, Miguel / Skarzynski, Dariusz J / Ferreira-Dias, Graça

Reproduction in domestic animals = Zuchthygiene

2019 Volume 54 Suppl 3, Page(s) 46–52

Abstract: Inflammation and fibroproliferative diseases may be modulated by epigenetic changes. Therefore, we suggest that epigenetic mechanisms could be involved in equine endometrosis pathogenesis. DNA methylation is one of the methods to evaluate epigenetics, ... ...

Abstract	Inflammation and fibroproliferative diseases may be modulated by epigenetic changes. Therefore, we suggest that epigenetic mechanisms could be involved in equine endometrosis pathogenesis. DNA methylation is one of the methods to evaluate epigenetics, through the transcription of methyltransferases (DNMT1, DNMT3A, DNMT3B). The correlation between DNMTs and collagen (COL) transcripts was assessed for the different Kenney and Doig's (Current Therapy in Theriogenology. Philadelphia: WB Saunders; 1986) endometrium categories. Endometrial biopsies were randomly collected from cyclic mares. Histological classification (category I, n = 13; II A, n = 17; II B, n = 12; and III, n = 7) and evaluation of COL1A2, COL3A1 and DNMTs transcripts by qPCR, were performed. Data were analysed by one-way analysis of variance (ANOVA), Kruskal-Wallis test and Pearson correlation. As mares aged, there was an increase in endometrium fibrosis (p < .01), and in DNMT1 mRNA (p < .001). Considering DNMT3B transcripts for each category, there was an increase with fibrosis (p < .05). No changes were observed for DNMT1 and DNMT3A transcripts. However, DNMT3A mRNA levels were the highest in all categories (p < .01). In category I endometrium, a positive correlation was observed for transcripts of all DNMTs in both COLs (p < .01). In category IIA, this correlation was also maintained for all DNMTs transcripts in COL1A2 (p < .05), but only for DNMT3B in COL3A1 (p < .05). In category IIB, there was a positive correlation between DNMT3B and COL3A1 (p < .05). In category III, a positive correlation was only observed between DNMT3B and COL3A1 (p < .05). Our results suggest that there is a disturbance in COLs and DNMTs correlation during fibrosis.
MeSH term(s)	Aging/physiology ; Animals ; Collagen/genetics ; Collagen/metabolism ; DNA (Cytosine-5-)-Methyltransferases/genetics ; DNA Methylation ; Endometritis/genetics ; Endometritis/metabolism ; Endometritis/veterinary ; Endometrium/pathology ; Female ; Fibrosis/physiopathology ; Horse Diseases/genetics ; Horse Diseases/metabolism ; Horses ; RNA, Messenger
Chemical Substances	RNA, Messenger ; Collagen (9007-34-5) ; DNA (Cytosine-5-)-Methyltransferases (EC 2.1.1.37)
Language	English
Publishing date	2019-09-11
Publishing country	Germany
Document type	Journal Article
ZDB-ID	1015187-4
ISSN	1439-0531 ; 0936-6768
ISSN (online)	1439-0531
ISSN	0936-6768
DOI	10.1111/rda.13515
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Article: Collagens and DNA methyltransferases in mare endometrosis

Alpoim‐Moreira, Joana / Fernandes, Carina / Rebordão, Maria Rosa / Amaral, Ana / Pinto‐Bravo, Pedro / Bliebernicht, Miguel / Skarzynski, Dariusz J / Ferreira‐Dias, Graça

Reproduction in domestic animals. 2019 Sept., v. 54 Suppl S3

2019

Abstract	Inflammation and fibroproliferative diseases may be modulated by epigenetic changes. Therefore, we suggest that epigenetic mechanisms could be involved in equine endometrosis pathogenesis. DNA methylation is one of the methods to evaluate epigenetics, through the transcription of methyltransferases (DNMT1, DNMT3A, DNMT3B). The correlation between DNMTs and collagen (COL) transcripts was assessed for the different Kenney and Doig's (Current Therapy in Theriogenology. Philadelphia: WB Saunders; 1986) endometrium categories. Endometrial biopsies were randomly collected from cyclic mares. Histological classification (category I, n = 13; II A, n = 17; II B, n = 12; and III, n = 7) and evaluation of COL1A2, COL3A1 and DNMTs transcripts by qPCR, were performed. Data were analysed by one‐way analysis of variance (ANOVA), Kruskal–Wallis test and Pearson correlation. As mares aged, there was an increase in endometrium fibrosis (p < .01), and in DNMT1 mRNA (p < .001). Considering DNMT3B transcripts for each category, there was an increase with fibrosis (p < .05). No changes were observed for DNMT1 and DNMT3A transcripts. However, DNMT3A mRNA levels were the highest in all categories (p < .01). In category I endometrium, a positive correlation was observed for transcripts of all DNMTs in both COLs (p < .01). In category IIA, this correlation was also maintained for all DNMTs transcripts in COL1A2 (p < .05), but only for DNMT3B in COL3A1 (p < .05). In category IIB, there was a positive correlation between DNMT3B and COL3A1 (p < .05). In category III, a positive correlation was only observed between DNMT3B and COL3A1 (p < .05). Our results suggest that there is a disturbance in COLs and DNMTs correlation during fibrosis.
Keywords	DNA ; DNA methylation ; analysis of variance ; animal reproduction ; biopsy ; collagen ; endometrium ; epigenetics ; fibrosis ; histology ; inflammation ; mares ; messenger RNA ; methyltransferases ; pathogenesis ; quantitative polymerase chain reaction ; transcription (genetics)
Language	English
Dates of publication	2019-09
Size	p. 46-52.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	1015187-4
ISSN	1439-0531 ; 0936-6768
ISSN (online)	1439-0531
ISSN	0936-6768
DOI	10.1111/rda.13515
Database	NAL-Catalogue (AGRICOLA)

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