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Transcriptome dynamics and molecular cross-talk between bovine oocyte and its companion cumulus cells.

Regassa A, Rings F, Hoelker M, Cinar U, Tholen E, Looft C, Schellander K, Tesfaye D - BMC Genomics (2011)

Bottom Line: Similarly, 566 transcripts are differentially expressed when CCs mature with (CCs+OO) or without (CCs-OO) their enclosed oocytes.Similarly, while transcripts over expressed in OO+CCs are involved in carbohydrate metabolism (ACO1, 2), molecular transport (GAPDH, GFPT1) and nucleic acid metabolism (CBS, NOS2), those over expressed in CCs+ OO are involved in cellular growth and proliferation (FOS, GADD45A), cell cycle (HAS2, VEGFA), cellular development (AMD1, AURKA, DPP4) and gene expression (FOSB, TGFB2).In conclusion, this study has generated large scale gene expression data from different oocyte and CCs samples that would provide insights into gene functions and interactions within and across different pathways that are involved in the maturation of bovine oocytes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, Germany.

ABSTRACT

Background: The bi-directional communication between the oocyte and its companion cumulus cells (CCs) is crucial for development and functions of both cell types. Transcripts that are exclusively expressed either in oocytes or CCs and molecular mechanisms affected due to removal of the communication axis between the two cell types is not investigated at a larger scale. The main objectives of this study were: 1. To identify transcripts exclusively expressed either in oocyte or CCs and 2. To identify those which are differentially expressed when the oocyte is cultured with or without its companion CCs and vice versa.

Results: We analyzed transcriptome profile of different oocyte and CC samples using Affymetrix GeneChip Bovine Genome array containing 23000 transcripts. Out of 13162 genes detected in germinal vesicle (GV) oocytes and their companion CCs, 1516 and 2727 are exclusively expressed in oocytes and CCs, respectively, while 8919 are expressed in both. Similarly, of 13602 genes detected in metaphase II (MII) oocytes and CCs, 1423 and 3100 are exclusively expressed in oocytes and CCs, respectively, while 9079 are expressed in both. A total of 265 transcripts are differentially expressed between oocytes cultured with (OO+CCs) and without (OO-CCs) CCs, of which 217 and 48 are over expressed in the former and the later groups, respectively. Similarly, 566 transcripts are differentially expressed when CCs mature with (CCs+OO) or without (CCs-OO) their enclosed oocytes. Of these, 320 and 246 are over expressed in CCs+OO and CCs-OO, respectively.While oocyte specific transcripts include those involved in transcription (IRF6, POU5F1, MYF5, MED18), translation (EIF2AK1, EIF4ENIF1) and CCs specific ones include those involved in carbohydrate metabolism (HYAL1, PFKL, PYGL, MPI), protein metabolic processes (IHH, APOA1, PLOD1), steroid biosynthetic process (APOA1, CYP11A1, HSD3B1, HSD3B7). Similarly, while transcripts over expressed in OO+CCs are involved in carbohydrate metabolism (ACO1, 2), molecular transport (GAPDH, GFPT1) and nucleic acid metabolism (CBS, NOS2), those over expressed in CCs+ OO are involved in cellular growth and proliferation (FOS, GADD45A), cell cycle (HAS2, VEGFA), cellular development (AMD1, AURKA, DPP4) and gene expression (FOSB, TGFB2).

Conclusion: In conclusion, this study has generated large scale gene expression data from different oocyte and CCs samples that would provide insights into gene functions and interactions within and across different pathways that are involved in the maturation of bovine oocytes. Moreover, the presence or absence of oocyte and CC factors during bovine oocyte maturation can have a profound effect on transcript abundance of each cell types, thereby showing the prevailing molecular cross-talk between oocytes and their corresponding CCs.

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Related in: MedlinePlus

Functional grouping of genes that are over expressed in the CCs + OO relative to CCs - OO samples showing the most significant functional groups, with P values, 0.05. The bars represent the P-value in logarithmic scale for each functional group.
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Figure 9: Functional grouping of genes that are over expressed in the CCs + OO relative to CCs - OO samples showing the most significant functional groups, with P values, 0.05. The bars represent the P-value in logarithmic scale for each functional group.

Mentions: We found that 36 and 375 of these genes over expressed in OO + CCs and CCs + OO, respectively, could be assigned to a specific functional group based on the information in the IPA Knowledge Base. Only 4 of the mapped genes over expressed in OO + CCs group, representing about 1.5% of the total, are classified under the functional group "Carbohydrate metabolism," which contains genes involved in energy conversion and modulation. Other functional groups, including molecular transport, nucleic acid metabolism, small molecule biochemistry and RNA post transcriptional modification are also observed. Similarly, 90 of the genes over expressed in CCs + OO, representing 34% of the total are classified under cellular growth and proliferation. A graphical representation of this functional classification of the genes over expressed in OO + CCs and CCs + OO are shown in Figures 8 and 9, in which 16 and 12 functional groups with higher P-values are noted. Some of these groups shared several common genes. In addition, 28 and 23 of the genes over expressed in OO + CCs and CCs + OO relative to OO - CCs and CCs - OO respectively, are assigned to 5 and 8 different canonical pathways (Additional files 14 and 15). Finally, these genes from the two groups were mapped on 5 top networks each network containing genes from the input data that shared known direct or indirect relationships. Examples of networks created from our data are shown in Figures 10 and 11, where the relationships between molecules that were over expressed in OO + CCs and CCs + OO are represented by the arrows that connect them. Figure 10 shows a complex network that plays an important role in gene expression, small molecule biochemistry and carbohydrate metabolism while Figure 11 shows a network that plays a role in cellular development.


Transcriptome dynamics and molecular cross-talk between bovine oocyte and its companion cumulus cells.

Regassa A, Rings F, Hoelker M, Cinar U, Tholen E, Looft C, Schellander K, Tesfaye D - BMC Genomics (2011)

Functional grouping of genes that are over expressed in the CCs + OO relative to CCs - OO samples showing the most significant functional groups, with P values, 0.05. The bars represent the P-value in logarithmic scale for each functional group.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3045333&req=5

Figure 9: Functional grouping of genes that are over expressed in the CCs + OO relative to CCs - OO samples showing the most significant functional groups, with P values, 0.05. The bars represent the P-value in logarithmic scale for each functional group.
Mentions: We found that 36 and 375 of these genes over expressed in OO + CCs and CCs + OO, respectively, could be assigned to a specific functional group based on the information in the IPA Knowledge Base. Only 4 of the mapped genes over expressed in OO + CCs group, representing about 1.5% of the total, are classified under the functional group "Carbohydrate metabolism," which contains genes involved in energy conversion and modulation. Other functional groups, including molecular transport, nucleic acid metabolism, small molecule biochemistry and RNA post transcriptional modification are also observed. Similarly, 90 of the genes over expressed in CCs + OO, representing 34% of the total are classified under cellular growth and proliferation. A graphical representation of this functional classification of the genes over expressed in OO + CCs and CCs + OO are shown in Figures 8 and 9, in which 16 and 12 functional groups with higher P-values are noted. Some of these groups shared several common genes. In addition, 28 and 23 of the genes over expressed in OO + CCs and CCs + OO relative to OO - CCs and CCs - OO respectively, are assigned to 5 and 8 different canonical pathways (Additional files 14 and 15). Finally, these genes from the two groups were mapped on 5 top networks each network containing genes from the input data that shared known direct or indirect relationships. Examples of networks created from our data are shown in Figures 10 and 11, where the relationships between molecules that were over expressed in OO + CCs and CCs + OO are represented by the arrows that connect them. Figure 10 shows a complex network that plays an important role in gene expression, small molecule biochemistry and carbohydrate metabolism while Figure 11 shows a network that plays a role in cellular development.

Bottom Line: Similarly, 566 transcripts are differentially expressed when CCs mature with (CCs+OO) or without (CCs-OO) their enclosed oocytes.Similarly, while transcripts over expressed in OO+CCs are involved in carbohydrate metabolism (ACO1, 2), molecular transport (GAPDH, GFPT1) and nucleic acid metabolism (CBS, NOS2), those over expressed in CCs+ OO are involved in cellular growth and proliferation (FOS, GADD45A), cell cycle (HAS2, VEGFA), cellular development (AMD1, AURKA, DPP4) and gene expression (FOSB, TGFB2).In conclusion, this study has generated large scale gene expression data from different oocyte and CCs samples that would provide insights into gene functions and interactions within and across different pathways that are involved in the maturation of bovine oocytes.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Animal Science, Animal Breeding and Husbandry Group, University of Bonn, Germany.

ABSTRACT

Background: The bi-directional communication between the oocyte and its companion cumulus cells (CCs) is crucial for development and functions of both cell types. Transcripts that are exclusively expressed either in oocytes or CCs and molecular mechanisms affected due to removal of the communication axis between the two cell types is not investigated at a larger scale. The main objectives of this study were: 1. To identify transcripts exclusively expressed either in oocyte or CCs and 2. To identify those which are differentially expressed when the oocyte is cultured with or without its companion CCs and vice versa.

Results: We analyzed transcriptome profile of different oocyte and CC samples using Affymetrix GeneChip Bovine Genome array containing 23000 transcripts. Out of 13162 genes detected in germinal vesicle (GV) oocytes and their companion CCs, 1516 and 2727 are exclusively expressed in oocytes and CCs, respectively, while 8919 are expressed in both. Similarly, of 13602 genes detected in metaphase II (MII) oocytes and CCs, 1423 and 3100 are exclusively expressed in oocytes and CCs, respectively, while 9079 are expressed in both. A total of 265 transcripts are differentially expressed between oocytes cultured with (OO+CCs) and without (OO-CCs) CCs, of which 217 and 48 are over expressed in the former and the later groups, respectively. Similarly, 566 transcripts are differentially expressed when CCs mature with (CCs+OO) or without (CCs-OO) their enclosed oocytes. Of these, 320 and 246 are over expressed in CCs+OO and CCs-OO, respectively.While oocyte specific transcripts include those involved in transcription (IRF6, POU5F1, MYF5, MED18), translation (EIF2AK1, EIF4ENIF1) and CCs specific ones include those involved in carbohydrate metabolism (HYAL1, PFKL, PYGL, MPI), protein metabolic processes (IHH, APOA1, PLOD1), steroid biosynthetic process (APOA1, CYP11A1, HSD3B1, HSD3B7). Similarly, while transcripts over expressed in OO+CCs are involved in carbohydrate metabolism (ACO1, 2), molecular transport (GAPDH, GFPT1) and nucleic acid metabolism (CBS, NOS2), those over expressed in CCs+ OO are involved in cellular growth and proliferation (FOS, GADD45A), cell cycle (HAS2, VEGFA), cellular development (AMD1, AURKA, DPP4) and gene expression (FOSB, TGFB2).

Conclusion: In conclusion, this study has generated large scale gene expression data from different oocyte and CCs samples that would provide insights into gene functions and interactions within and across different pathways that are involved in the maturation of bovine oocytes. Moreover, the presence or absence of oocyte and CC factors during bovine oocyte maturation can have a profound effect on transcript abundance of each cell types, thereby showing the prevailing molecular cross-talk between oocytes and their corresponding CCs.

Show MeSH
Related in: MedlinePlus