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Article ; Online: Advances in understanding canine pregnancy: Endocrine and morpho-functional regulation.

Kowalewski, Mariusz P

Reproduction in domestic animals = Zuchthygiene

2023 Volume 58 Suppl 2, Page(s) 163–175

Abstract: Canine pregnancy relies on luteal steroidogenesis for progesterone (P4) production. The canine placenta responds to P4, depending on the nuclear P4 receptor (PGR). This has sparked interest in investigating the interaction between ovarian luteal steroids ...

Abstract	Canine pregnancy relies on luteal steroidogenesis for progesterone (P4) production. The canine placenta responds to P4, depending on the nuclear P4 receptor (PGR). This has sparked interest in investigating the interaction between ovarian luteal steroids and the placenta in dogs. Canine placentation is characterized by restricted (shallow) trophoblast invasion, making the dog an interesting model for studying decidua-derived modulation of trophoblast invasion, compared with the more invasive (hemochorial) placentation. The PGR is expressed in maternally derived decidual cells and plays a crucial role in feto-maternal communication during pregnancy maintenance. Understanding PGR-mediated signalling has clinical implications for improving reproductive performance control in dogs. Altering the PGR signalling induces the release of PGF2α from the foetal trophoblast, hindering placental homeostasis, which can also be achieved with antigestagens like aglepristone. Consequently, luteolysis, both natural and antigestagen-induced, involves apoptosis, vascular lesion, and immune cell infiltration in the placenta, resulting in placentolysis and foetal membranes expulsion. Our laboratory developed the immortalized dog uterine stromal (DUS) cell line to study canine-specific decidualization. We study canine reproduction by observing physiological processes and investigating evidence-based mechanisms of decidualization and feto-maternal interaction. Our focus on morphology, function and molecular aspects enhances understanding and enables targeted and translational studies.
MeSH term(s)	Female ; Pregnancy ; Dogs ; Animals ; Placenta ; Ovary ; Apoptosis ; Corpus Luteum ; Dinoprost
Chemical Substances	Dinoprost (B7IN85G1HY)
Language	English
Publishing date	2023-09-19
Publishing country	Germany
Document type	Journal Article ; Review
ZDB-ID	1015187-4
ISSN	1439-0531 ; 0936-6768
ISSN (online)	1439-0531
ISSN	0936-6768
DOI	10.1111/rda.14443
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Article ; Online: Advances in understanding canine pregnancy: Endocrine and morpho‐functional regulation

Kowalewski, Mariusz P.

Reproduction in Domestic Animals. 2023 Sept., v. 58 Suppl S2 p.163-175

2023

Abstract	Canine pregnancy relies on luteal steroidogenesis for progesterone (P4) production. The canine placenta responds to P4, depending on the nuclear P4 receptor (PGR). This has sparked interest in investigating the interaction between ovarian luteal steroids and the placenta in dogs. Canine placentation is characterized by restricted (shallow) trophoblast invasion, making the dog an interesting model for studying decidua‐derived modulation of trophoblast invasion, compared with the more invasive (hemochorial) placentation. The PGR is expressed in maternally derived decidual cells and plays a crucial role in feto‐maternal communication during pregnancy maintenance. Understanding PGR‐mediated signalling has clinical implications for improving reproductive performance control in dogs. Altering the PGR signalling induces the release of PGF2α from the foetal trophoblast, hindering placental homeostasis, which can also be achieved with antigestagens like aglepristone. Consequently, luteolysis, both natural and antigestagen‐induced, involves apoptosis, vascular lesion, and immune cell infiltration in the placenta, resulting in placentolysis and foetal membranes expulsion. Our laboratory developed the immortalized dog uterine stromal (DUS) cell line to study canine‐specific decidualization. We study canine reproduction by observing physiological processes and investigating evidence‐based mechanisms of decidualization and feto‐maternal interaction. Our focus on morphology, function and molecular aspects enhances understanding and enables targeted and translational studies.
Keywords	apoptosis ; cell lines ; dogs ; homeostasis ; luteolysis ; models ; pregnancy ; progesterone ; reproductive performance ; steroidogenesis ; trophoblast
Language	English
Dates of publication	2023-09
Size	p. 163-175.
Publishing place	John Wiley & Sons, Ltd
Document type	Article ; Online
Note	REVIEW
ZDB-ID	1015187-4
ISSN	1439-0531 ; 0936-6768
ISSN (online)	1439-0531
ISSN	0936-6768
DOI	10.1111/rda.14443
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Article ; Online: Molecular Mechanisms of Lipopolysaccharide (LPS) Induced Inflammation in an Immortalized Ovine Luteal Endothelial Cell Line (OLENDO).

Gram, Aykut / Kowalewski, Mariusz P

Veterinary sciences

2022 Volume 9, Issue 3

Abstract: Escherichia coli (E. coli) is the most common Gram-negative bacterium causing infection of the uterus or mammary gland and is one of the major causes of infertility in livestock. In those animals affected by E. coli driven LPS-mediated infections, ... ...

Abstract	Escherichia coli (E. coli) is the most common Gram-negative bacterium causing infection of the uterus or mammary gland and is one of the major causes of infertility in livestock. In those animals affected by E. coli driven LPS-mediated infections, fertility problems occur in part due to disrupted follicular and luteal functionality. However, the molecular mechanisms by which LPS induces inflammation, and specifically, the role of LPS in the disruption of capillary morphogenesis and endothelial barrier function remain unclear. Here, we hypothesized that LPS may lead to alterations in luteal angiogenesis and vascular function by inducing inflammatory reactions in endothelial cells. Accordingly, OLENDO cells were treated with LPS followed by evaluation of the expression of selected representative proinflammatory cytokines: NF-kB, IL6, IL8, TNFα, and ICAM 1. While TNFα was not affected by treatment with LPS, transcripts of NF-kB, IL6, and IL8 were affected in a dosage-dependent manner. Additionally, the activity of TLR2 and TLR4 was blocked, resulting in suppression of the LPS-induced expression of ICAM 1, NF-kB, IL6, and IL8. Inhibition of the PKA or MAPK/ERK pathways suppressed the LPS-stimulated expression of NF-kB, IL6, and IL8, whereas blocking the PKC pathway had the opposite effect. Furthermore, LPS-induced phosphorylation of Erk1 and Erk2 was inhibited when the TLR4 or MAPK/ERK pathways were blocked. Finally, LPS seems to induce inflammatory processes in OLENDO cells via TLR2 and TLR4, utilizing different signaling pathways.
Language	English
Publishing date	2022-02-24
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2768971-2
ISSN	2306-7381 ; 2306-7381
ISSN (online)	2306-7381
ISSN	2306-7381
DOI	10.3390/vetsci9030099
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Article: Molecular Mechanisms of Lipopolysaccharide (LPS) Induced Inflammation in an Immortalized Ovine Luteal Endothelial Cell Line (OLENDO)

Gram, Aykut / Kowalewski, Mariusz P.

Veterinary sciences. 2022 Feb. 24, v. 9, no. 3

2022

Abstract	Escherichia coli (E. coli) is the most common Gram-negative bacterium causing infection of the uterus or mammary gland and is one of the major causes of infertility in livestock. In those animals affected by E. coli driven LPS-mediated infections, fertility problems occur in part due to disrupted follicular and luteal functionality. However, the molecular mechanisms by which LPS induces inflammation, and specifically, the role of LPS in the disruption of capillary morphogenesis and endothelial barrier function remain unclear. Here, we hypothesized that LPS may lead to alterations in luteal angiogenesis and vascular function by inducing inflammatory reactions in endothelial cells. Accordingly, OLENDO cells were treated with LPS followed by evaluation of the expression of selected representative proinflammatory cytokines: NF-kB, IL6, IL8, TNFα, and ICAM 1. While TNFα was not affected by treatment with LPS, transcripts of NF-kB, IL6, and IL8 were affected in a dosage-dependent manner. Additionally, the activity of TLR2 and TLR4 was blocked, resulting in suppression of the LPS-induced expression of ICAM 1, NF-kB, IL6, and IL8. Inhibition of the PKA or MAPK/ERK pathways suppressed the LPS-stimulated expression of NF-kB, IL6, and IL8, whereas blocking the PKC pathway had the opposite effect. Furthermore, LPS-induced phosphorylation of Erk1 and Erk2 was inhibited when the TLR4 or MAPK/ERK pathways were blocked. Finally, LPS seems to induce inflammatory processes in OLENDO cells via TLR2 and TLR4, utilizing different signaling pathways.
Keywords	Escherichia coli ; Gram-negative bacteria ; angiogenesis ; cell lines ; endothelial cells ; inflammation ; interleukin-6 ; interleukin-8 ; lipopolysaccharides ; mammary glands ; mitogen-activated protein kinase ; morphogenesis ; phosphorylation ; sheep ; transcription factor NF-kappa B ; uterus
Language	English
Dates of publication	2022-0224
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2768971-2
ISSN	2306-7381
ISSN	2306-7381
DOI	10.3390/vetsci9030099
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Endometrial extracellular matrix components do not change over the course of embryonic diapause and reactivation in the roe deer (Capreolus capreolus).

Rüegg, Anna B / Kowalewski, Mariusz P / Ulbrich, Susanne E

Reproduction in domestic animals = Zuchthygiene

2023 Volume 58, Issue 5, Page(s) 594–604

Abstract: The modification of the endometrial extracellular matrix (ECM) is a crucial step for embryo implantation in many mammalian species. The embryo of the European roe deer (Capreolus capreolus) displays a 4-5 months long temporary reduction of developmental ... ...

Abstract	The modification of the endometrial extracellular matrix (ECM) is a crucial step for embryo implantation in many mammalian species. The embryo of the European roe deer (Capreolus capreolus) displays a 4-5 months long temporary reduction of developmental pace termed embryonic diapause. A reduction of epithelial cell height during diapause has previously been described. Co-occurring ECM modifications may contribute to the changes of the intra-uterine milieu during reactivation at which the embryo regains developmental velocity. We assessed the localization of five ECM proteins (collagen I and IV, fibronectin, laminin, and extracellular matrix protein 1) using immunohistochemistry in animals with early, late, and post-diapause (elongating) embryos. While our results confirmed the reduction of epithelial height during diapause, we only detected marginal differences in localization and staining intensities of the selected ECM proteins. Major ECM remodelling events in the roe deer endometrium are thus likely to occur only at implantation.
MeSH term(s)	Female ; Animals ; Deer/physiology ; Endometrium/metabolism ; Embryo Implantation/physiology ; Extracellular Matrix ; Diapause
Language	English
Publishing date	2023-01-25
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.14320
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Article: The involvement of hypoxia-inducible factor 1α (HIF1α)-stabilising factors in steroidogenic acute regulatory (STAR) protein-dependent steroidogenesis in murine KK1 granulosa cells in vitro.

Gysin, Tina / Kowalewski, Mariusz P

Reproduction, fertility, and development

2021 Volume 33, Issue 18, Page(s) 865–880

Abstract: As a component of hypoxia-inducible factor1 (HIF1)-complexes, HIF1α regulates the expression of steroidogenic acute regulatory (STAR) protein in granulosa cells. However, severe hypoxia or exaggeratedly expressed HIF1α have detrimental effects. HIF1α is ... ...

Abstract	As a component of hypoxia-inducible factor1 (HIF1)-complexes, HIF1α regulates the expression of steroidogenic acute regulatory (STAR) protein in granulosa cells. However, severe hypoxia or exaggeratedly expressed HIF1α have detrimental effects. HIF1α is regulated by factor inhibiting HIF (FIH), prolyl hydroxylases (PHD1, 2, 3) and von Hippel-Lindau (VHL) suppressor protein. In this study, the expression of FIH, PHD1, 2, 3 and VHL was investigated in murine ovaries and immortalised KK1 granulosa cells. We found FIH, VHL and PHD2 transcripts predominantly in growing tertiary follicles. Functional aspects were assessed in KK1 cells exposed to decreasing O2 (20%, 10%, 1%), by determining HIF1α, FIH, VHL, PHD1-3 and STAR expression. The main findings indicated gradually increasing PHD2 under lowered O2. Functional blocking of PHDs revealed biphasic effects on STAR expression; concomitantly with increasing HIF1α, STAR expression, which was initially induced, decreased significantly when HIF1α was strongly stabilised. Finally, PHD2 in particular might act as a specific regulator of HIF1α and, thereby, of STAR availability in granulosa cells.
MeSH term(s)	Animals ; Cell Line ; Female ; Granulosa Cells/metabolism ; Hypoxia/metabolism ; Hypoxia-Inducible Factor 1, alpha Subunit/metabolism ; Mice ; Mixed Function Oxygenases/metabolism ; Ovary/metabolism ; Phosphoproteins/metabolism ; Signal Transduction/physiology ; Von Hippel-Lindau Tumor Suppressor Protein/metabolism
Chemical Substances	HIF1A protein, human ; Hypoxia-Inducible Factor 1, alpha Subunit ; Phosphoproteins ; steroidogenic acute regulatory protein ; Mixed Function Oxygenases (EC 1.-) ; factor inhibiting hypoxia-inducible factor 1, mouse (EC 1.-) ; Von Hippel-Lindau Tumor Suppressor Protein (EC 2.3.2.27) ; VHL protein, mouse (EC 6.3.2.-)
Language	English
Publishing date	2021-12-06
Publishing country	Australia
Document type	Journal Article
ZDB-ID	1019913-5
ISSN	1448-5990 ; 1031-3613
ISSN (online)	1448-5990
ISSN	1031-3613
DOI	10.1071/RD21170
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Zs.A 2756: Show issues

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Article ; Online: Applying a novel kinomics approach to study decidualization and the effects of antigestagens using a canine model†.

De Geyter, Isabelle / Kowalewski, Mariusz P / Tavares Pereira, Miguel

Biology of reproduction

2023 Volume 110, Issue 3, Page(s) 583–598

Abstract: Maternal decidual cells are crucial for the maintenance of canine pregnancy as they are the only cells expressing the nuclear progesterone (P4) receptor (PGR) in the placenta. Interfering with P4/PGR signaling adversely affects decidual cells and ... ...

Abstract	Maternal decidual cells are crucial for the maintenance of canine pregnancy as they are the only cells expressing the nuclear progesterone (P4) receptor (PGR) in the placenta. Interfering with P4/PGR signaling adversely affects decidual cells and terminates pregnancy. Although immortalized dog uterine stromal (DUS) cells can be decidualized in vitro using cAMP, the involvement of cAMP-dependent kinases in canine decidualization had not been investigated. Therefore, the present project investigated changes in the kinome of DUS cells following in vitro decidualization, using the serine/threonine kinase (STK) PamChip assay (PamGene). Decidualization led to a predicted activation of 85 STKs in DUS cells, including protein kinase (PK) A, PKC, extracellular signal-regulated kinase (ERK)1/2 and other mitogen-activated protein kinases (MAPKs), calcium/calmodulin-dependent protein kinases (CAMKs), and Akt1/2. In addition, blocking PGR with type 2 antigestagens (aglepristone or mifepristone) decreased the activity of virtually all kinases modulated by decidualization. The underlying transcriptional effects were inferred from comparison with available transcriptomic data on antigestagen-mediated effects in DUS cells. In targeted studies, interfering with PKA or MAPK kinase (MEK)1/2 resulted in downregulation of important decidualization markers (e.g., insulin-like growth factor 1 (IGF1), prostaglandin E2 synthase (PTGES), prolactin receptor (PRLR), PGR, and prostaglandin-endoperoxide synthase 2 (PTGS2/COX2)). Conversely, blocking of PKC decreased the mRNA availability of IGF1, PGR, and PTGS2, but not of PTGES and PRLR. Moreover, suppressing PKA decreased the phosphorylation of the transcription factors cJUN and CREB, whereas blocking of PKC affected only cJUN. This first kinomics analysis to target decidualization showed an increased activity of a wide range of STKs, which could be hindered by disrupting P4/PGR signaling. Decidualization appears to be regulated in a kinase-dependent manner, with PKA and PKC evoking different effects.
MeSH term(s)	Pregnancy ; Female ; Dogs ; Animals ; Decidua/metabolism ; Cyclooxygenase 2/metabolism ; Uterus ; Progesterone/pharmacology ; Placenta ; Protein Serine-Threonine Kinases/metabolism ; Stromal Cells/metabolism
Chemical Substances	Cyclooxygenase 2 (EC 1.14.99.1) ; Progesterone (4G7DS2Q64Y) ; Protein Serine-Threonine Kinases (EC 2.7.11.1)
Language	English
Publishing date	2023-11-22
Publishing country	United States
Document type	Journal Article
ZDB-ID	1118-6
ISSN	1529-7268 ; 0006-3363
ISSN (online)	1529-7268
ISSN	0006-3363
DOI	10.1093/biolre/ioad170
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Article ; Online: Erratum to 'Factors affecting the fate of the canine corpus luteum: Potential contributors to pregnancy and non-pregnancy' Theriogenology; Volume 150, 1 July 2020, Pages 339-346.

Papa, Paula C / Kowalewski, Mariusz P

Theriogenology

2020 Volume 158, Page(s) 207–208

Language	English
Publishing date	2020-09-21
Publishing country	United States
Document type	Published Erratum
ZDB-ID	189232-0
ISSN	1879-3231 ; 0093-691X
ISSN (online)	1879-3231
ISSN	0093-691X
DOI	10.1016/j.theriogenology.2020.07.037
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Zs.A 3929: Show issues

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Article ; Online: Factors affecting the fate of the canine corpus luteum: Potential contributors to pregnancy and non-pregnancy.

Papa, Paula C / Kowalewski, Mariusz P

Theriogenology

2020 Volume 150, Page(s) 339–346

Abstract: The fate of the canine corpus luteum (CL) differs from that of other domestic species: beyond the extended luteal regression observed in both pregnant and non-pregnant cycles, active luteolysis is observed only in pregnant dogs. Luteal regression in the ... ...

Abstract	The fate of the canine corpus luteum (CL) differs from that of other domestic species: beyond the extended luteal regression observed in both pregnant and non-pregnant cycles, active luteolysis is observed only in pregnant dogs. Luteal regression in the absence of pregnancy lacks a luteolytic trigger. The CL lifespan during pregnancy is around 60 days, as long as that of the cyclic CL. Although they are already available in the first half of diestrus, LH and especially prolactin (PRL) play a decisive luteotropic role from approximately day 25 post-ovulation onwards. Nevertheless, many locally-produced factors are orchestrated to ensure a fully functional CL, which in the bitch produces progesterone (P4), 17b-estradiol, and other local regulators. Recently, insulin has been described as another luteotropic factor in this species, able to increase glucose uptake in luteal cells and contribute to steroid biosynthesis. The locally-produced PGE2 is also a potent luteotropic factor in the first half of diestrus, promoting STAR expression, as are also proliferating, vasoactive- and immunomodulatory factors. These, in turn, all contribute to the formation and maintenance of the canine CL. Meanwhile PGF2a, produced by the utero-placental compartment, participates actively in triggering pre-partum luteolysis. Cytokines play different roles, either contributing as luteotropic or as acute inflammation molecules. So far, the one clinically most efficient mechanism of interrupting a pregnancy in the dog is to block P4 receptors, using an antigestagen (e.g., aglepristone) in the second half of diestrus. To enhance the chances of pregnancy, however, several luteotropic factors could be used.
MeSH term(s)	Animals ; Corpus Luteum/physiology ; Cytokines/genetics ; Cytokines/metabolism ; Dogs/physiology ; Estradiol/metabolism ; Female ; Gene Expression Regulation/physiology ; Luteinizing Hormone/metabolism ; Pregnancy ; Pregnancy, Animal/physiology ; Progesterone/metabolism ; Prolactin/metabolism ; Steroids/metabolism
Chemical Substances	Cytokines ; Steroids ; Progesterone (4G7DS2Q64Y) ; Estradiol (4TI98Z838E) ; Prolactin (9002-62-4) ; Luteinizing Hormone (9002-67-9)
Language	English
Publishing date	2020-02-19
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.2020.01.081
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Article ; Online: Endometrial extracellular matrix components do not change over the course of embryonic diapause and reactivation in the roe deer (Capreolus capreolus)

Rüegg, Anna B. / Kowalewski, Mariusz P. / Ulbrich, Susanne E.

Reproduction in Domestic Animals. 2023 May, v. 58, no. 5 p.594-604

2023

Abstract: The modification of the endometrial extracellular matrix (ECM) is a crucial step for embryo implantation in many mammalian species. The embryo of the European roe deer (Capreolus capreolus) displays a 4–5 months long temporary reduction of developmental ... ...

Abstract	The modification of the endometrial extracellular matrix (ECM) is a crucial step for embryo implantation in many mammalian species. The embryo of the European roe deer (Capreolus capreolus) displays a 4–5 months long temporary reduction of developmental pace termed embryonic diapause. A reduction of epithelial cell height during diapause has previously been described. Co‐occurring ECM modifications may contribute to the changes of the intra‐uterine milieu during reactivation at which the embryo regains developmental velocity. We assessed the localization of five ECM proteins (collagen I and IV, fibronectin, laminin, and extracellular matrix protein 1) using immunohistochemistry in animals with early, late, and post‐diapause (elongating) embryos. While our results confirmed the reduction of epithelial height during diapause, we only detected marginal differences in localization and staining intensities of the selected ECM proteins. Major ECM remodelling events in the roe deer endometrium are thus likely to occur only at implantation.
Keywords	Capreolus capreolus ; collagen ; diapause ; embryo implantation ; endometrium ; epithelial cells ; epithelium ; extracellular matrix ; fibronectins ; immunohistochemistry ; laminin ; mammals ; reproduction
Language	English
Dates of publication	2023-05
Size	p. 594-604.
Publishing place	John Wiley & Sons, Ltd
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	1015187-4
ISSN	1439-0531 ; 0936-6768
ISSN (online)	1439-0531
ISSN	0936-6768
DOI	10.1111/rda.14320
Database	NAL-Catalogue (AGRICOLA)

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