Proteomics-based systems biology modeling of bovine germinal vesicle stage oocyte and cumulus cell interaction

PLoS ONE

Volumn 5, Issue 6, 2010, Pages

  Peddinti, Divyaswetha ^a,b   Memili, Erdogan ^b   Burgess, Shane C ^a,b,c  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

^b MISSISSIPPI STATE UNIVERSITY   (United States)

^c MISSISSIPPI STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A ACETYLTRANSFERASE; ADENOSINE TRIPHOSPHATASE; CELL PROTEIN; CLATHRIN; CYTOCHROME C OXIDASE; ENOLASE; ENOYL COENZYME A HYDRATASE; EXPORTIN 1; GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 1; GUANOSINE TRIPHOSPHATASE; HISTONE DEACETYLASE; HISTONE H3; HISTONE H4; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR 5A; KARYOPHERIN ALPHA; KARYOPHERIN BETA; LACTADHERIN; PEPTIDYLPROLYL ISOMERASE; PEROXIDASE; PEROXIREDOXIN 4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEASOME; PROTEOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RAB11 PROTEIN; RAG1 PROTEIN; RETINOID X RECEPTOR GAMMA; TUBULIN;

ANIMAL CELL; ARTICLE; BIOLOGICAL MODEL; CELL COMMUNICATION; CELL ENERGY; CELL FUNCTION; CELL GROWTH; CELL INTERACTION; CELL MATURATION; CELL TRANSPORT; CELL TYPE; CONTROLLED STUDY; COW; CUMULUS CELL; GERMINAL VESICLE; HYPOTHESIS; METABOLITE; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OOCYTE MATURATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEOMICS; SIGNAL TRANSDUCTION; ANIMAL; CATTLE; CELL NUCLEUS; CYTOLOGY; FEMALE; GENE REGULATORY NETWORK; METABOLISM; METHODOLOGY; SYSTEMS BIOLOGY;

BOVINAE;

ANIMALS; CATTLE; CELL COMMUNICATION; CELL NUCLEUS; CUMULUS CELLS; FEMALE; GENE REGULATORY NETWORKS; MODELS, BIOLOGICAL; OOCYTES; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY;

EID: 77955299202     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0011240     Document Type: Article

References (74)

1. Eppig JJ (1991) Intercommunication between mammalian oocytes and companion somatic cells. Bioessays 13: 569-574.
2. Gilchrist RB, Ritter LJ, Armstrong DT (2004) Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci 82-83: 431-446.
3. Grazul-Bilska AT, Reynolds LP, Redmer DA (1997) Gap junctions in the ovaries. Biol Reprod 57: 947-957.
4. Tanghe S, Van Soom A, Nauwynck H, Coryn M, de Kruif A (2002) Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 61: 414-424.
5. Assidi M, Dufort I, Ali A, Hamel M, Algriany O, et al. (2008) Identification of Potential Markers of Oocyte Competence Expressed in Bovine Cumulus Cells Matured with Follicle-Stimulating Hormone and/or Phorbol Myristate Acetate In Vitro. Biol Reprod.
6. Vozzi C, Formenton A, Chanson A, Senn A, Sahli R, et al. (2001) Involvement of connexin 43 in meiotic maturation of bovine oocytes. Reproduction 122: 619-628.
7. Fatehi AN, Zeinstra EC, Kooij RV, Colenbrander B, Bevers MM (2002) Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate. Theriogenology 57: 1347-1355.
8. Mori T, Amano T, Shimizu H (2000) Roles of gap junctional communication of cumulus cells in cytoplasmic maturation of porcine oocytes cultured in vitro. Biol Reprod 62: 913-919.
9. Wongsrikeao P, Kaneshige Y, Ooki R, Taniguchi M, Agung B, et al. (2005) Effect of the removal of cumulus cells on the nuclear maturation, fertilization and development of porcine oocytes. Reprod Domest Anim 40: 166-170.
10. de Matos DG, Furnus CC, Moses DF (1997) Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol Reprod 57: 1420-1425.
11. Matzuk MM, Burns KH, Viveiros MM, Eppig JJ (2002) Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296: 2178-2180.
12. Su YQ, Sugiura K, Wigglesworth K, O'Brien MJ, Affourtit JP, et al. (2008) Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 135: 111-121.
13. Sugiura K, Su YQ, Diaz FJ, Pangas SA, Sharma S, et al. (2007) Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 134: 2593-2603.
14. Biggers JD, Whittingham DG, Donahue RP (1967) The pattern of energy metabolism in the mouse oocyte and zygote. Proc Natl Acad Sci U S A 58: 560-567.
15. Buccione R, Schroeder AC, Eppig JJ (1990) Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol Reprod 43: 543-547.
16. Kim H, Schuetz AW (1991) Regulation of nuclear membrane assembly and maintenance during in vitro maturation of mouse oocytes: role of pyruvate and protein synthesis. Cell Tissue Res 265: 105-112.
17. Sugiura K, Pendola FL, Eppig JJ (2005) Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev Biol 279: 20-30.
18. Eppig JJ, Wigglesworth K, Chesnel F (1993) Secretion of cumulus expansion enabling factor by mouse oocytes: relationship to oocyte growth and competence to resume meiosis. Dev Biol 158: 400-409.
19. Memili E, Peddinti D, Shack LA, Nanduri B, McCarthy F, et al. (2007) Bovine germinal vesicle oocyte and cumulus cell proteomics. Reproduction 133: 1107-1120.
20. Sutton ML, Cetica PD, Beconi MT, Kind KL, Gilchrist RB, et al. (2003) Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction 126: 27-34.
21. Amano T, Mori T, Matsumoto K, Iritani A, Watanabe T (2005) Role of cumulus cells during maturation of porcine oocytes in the rise in intracellular Ca2+ induced by inositol 1,4,5-trisphosphate. Theriogenology 64: 261-274.
22. Zhang L, Jiang S, Wozniak PJ, Yang X, Godke RA (1995) Cumulus cell function during bovine oocyte maturation, fertilization, and embryo development in vitro. Mol Reprod Dev 40: 338-344.
23. Richter JD (1991) Translational control during early development. Bioessays 13: 179-183.
24. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
25. Buza TJ, McCarthy FM, Wang N, Bridges SM, Burgess SC (2008) Gene Ontology annotation quality analysis in model eukaryotes. Nucleic Acids Res 36: e12.
26. Martens L, Hermjakob H, Jones P, Adamski M, Taylor C, et al. (2005) PRIDE: the proteomics identifications database. Proteomics 5: 3537-3545.
27. McCarthy FM, Cooksey AM, Wang N, Bridges SM, Pharr GT, et al. (2006) Modeling a whole organ using proteomics: the avian bursa of Fabricius. Proteomics 6: 2759-2771.
28. Lubec G, Afjehi-Sadat L, Yang JW, John JP (2005) Searching for hypothetical proteins: theory and practice based upon original data and literature. Prog Neurobiol 77: 90-127.
29. McCarthy FM, Bridges SM, Wang N, Magee GB, Williams WP, et al. (2007) AgBase: a unified resource for functional analysis in agriculture. Nucleic Acids Res 35: D599-603.
30. Bhojwani M, Rudolph E, Kanitz W, Zuehlke H, Schneider F, et al. (2006) Molecular analysis of maturation processes by protein and phosphoprotein profiling during in vitro maturation of bovine oocytes: a proteomic approach. Cloning Stem Cells 8: 259-274.
31. Coonrod SA, Wright PW, Herr JC (2002) Oolemmal proteomics. J Reprod Immunol 53: 55-65.
32. Ellederova Z, Halada P, Man P, Kubelka M, Motlik J, et al. (2004) Protein patterns of pig oocytes during in vitro maturation. Biol Reprod 71: 1533-1539.
33. Hamamah S, Matha V, Berthenet C, Anahory T, Loup V, et al. (2006) Comparative protein expression profiling in human cumulus cells in relation to oocyte fertilization and ovarian stimulation protocol. Reprod Biomed Online 13: 807-814.
34. Ma M, Guo X, Wang F, Zhao C, Liu Z, et al. (2008) Protein expression profile of the mouse metaphase-II oocyte. J Proteome Res 7: 4821-4830.
35. Meng Y, Liu XH, Ma X, Shen Y, Fan L, et al. (2007) The protein profile of mouse mature cumulus-oocyte complex. Biochim Biophys Acta 1774: 1477-1490.
36. Chen G, Gharib TG, Huang CC, Taylor JM, Misek DE, et al. (2002) Discordant protein and mRNA expression in lung adenocarcinomas. Mol Cell Proteomics 1: 304-313.
37. Cox B, Kislinger T, Emili A (2005) Integrating gene and protein expression data: pattern analysis and profile mining. Methods 35: 303-314.
38. Gygi SP, Rochon Y, Franza BR, Aebersold R (1999) Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 19: 1720-1730.
39. Nie L, Wu G, Culley DE, Scholten JC, Zhang W (2007) Integrative analysis of transcriptomic and proteomic data: challenges, solutions and applications. Crit Rev Biotechnol 27: 63-75.
40. Elias JE, Gygi SP (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207-214.
41. Dalbies-Tran R, Papillier P, Pennetier S, Uzbekova S, Monget P (2005) Bovine mater-like NALP9 is an oocyte marker gene. Mol Reprod Dev 71: 414-421.
42. Fair T, Carter F, Park S, Evans AC, Lonergan P (2007) Global gene expression analysis during bovine oocyte in vitro maturation. Theriogenology 68 Suppl 1: S91-97.
43. Pennetier S, Perreau C, Uzbekova S, Thelie A, Delaleu B, et al. (2006) MATER protein expression and intracellular localization throughout folliculogenesis and preimplantation embryo development in the bovine. BMC Dev Biol 6: 26.
44. Pfeffer PL, Sisco B, Donnison M, Somers J, Smith C (2007) Isolation of genes associated with developmental competency of bovine oocytes. Theriogenology 68 Suppl 1: S84-90.
45. Racedo SE, Wrenzycki C, Lepikhov K, Salamone D, Walter J, et al. (2009) Epigenetic modifications and related mRNA expression during bovine oocyte in vitro maturation. Reprod Fertil Dev 21: 738-748.
46. Thelie A, Papillier P, Pennetier S, Perreau C, Traverso JM, et al. (2007) Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev Biol 7: 125.
47. Memili E, First NL (1999) Control of gene expression at the onset of bovine embryonic development. Biol Reprod 61: 1198-1207.
48. Donahue RP, Stern S (1968) Follicular cell support of oocyte maturation: production of pyruvate in vitro. J Reprod Fertil 17: 395-398.
49. Leese HJ, Barton AM (1985) Production of pyruvate by isolated mouse cumulus cells. J Exp Zool 234: 231-236.
50. Weber J, Senior AE (2003) ATP synthesis driven by proton transport in F1F0- ATP synthase. FEBS Lett 545: 61-70.
51. Sugiura K, Eppig JJ (2005) Society for Reproductive Biology Founders' Lecture 2005. Control of metabolic cooperativity between oocytes and their companion granulosa cells by mouse oocytes. Reprod Fertil Dev 17: 667-674.
52. Bettegowda A, Patel OV, Lee KB, Park KE, Salem M, et al. (2008) Identification of Novel Bovine Cumulus Cell Molecular Markers Predictive of Oocyte Competence: Functional and Diagnostic Implications. Biol Reprod.
53. Giancotti FG, Ruoslahti E (1999) Integrin signaling. Science 285: 1028-1032.
54. Monniaux D, Huet-Calderwood C, Le Bellego F, Fabre S, Monget P, et al. (2006) Integrins in the ovary. Semin Reprod Med 24: 251-261.
55. Veselska RRJ (2001) Cortical actin cytoskeleton in human oocytes: a comparison with mouse oocytes. Scripta medica 74: 265-274.
56. Seger R, Krebs EG (1995) The MAPK signaling cascade. Faseb J 9: 726-735.
57. Su YQ, Wigglesworth K, Pendola FL, O'Brien MJ, Eppig JJ (2002) Mitogenactivated protein kinase activity in cumulus cells is essential for gonadotropininduced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinology 143: 2221-2232.
58. Snow AJ, Puri P, Acker-Palmer A, Bouwmeester T, Vijayaraghavan S, et al. (2008) Phosphorylation-dependent interaction of tyrosine 3-monooxygenase/ tryptophan 5-monooxygenase activation protein (YWHA) with PADI6 following oocyte maturation in mice. Biol Reprod 79: 337-347.
59. Leyens G, Verhaeghe B, Landtmeters M, Marchandise J, Knoops B, et al. (2004) Peroxiredoxin 6 is upregulated in bovine oocytes and cumulus cells during in vitro maturation: role of intercellular communication. Biol Reprod 71: 1646-1651.
60. Sagirkaya H, Misirlioglu M, Kaya A, First NL, Parrish JJ, et al. (2006) Developmental and molecular correlates of bovine preimplantation embryos. Reproduction 131: 895-904.
61. Peddinti D, Nanduri B, Kaya A, Feugang JM, Burgess SC, et al. (2008) Comprehensive proteomic analysis of bovine spermatozoa of varying fertility rates and identification of biomarkers associated with fertility. BMC Syst Biol 2: 19.
62. Pruitt KD, Tatusova T, Maglott DR (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35: D61-65.
63. Elias JE, Gibbons FD, King OD, Roth FP, Gygi SP (2004) Intensity-based protein identification by machine learning from a library of tandem mass spectra. Nat Biotechnol 22: 214-219.
64. Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2: 43-50.
65. Park GW, Kwon KH, Kim JY, Lee JH, Yun SH, et al. (2006) Human plasma proteome analysis by reversed sequence database search and molecular weight correlation based on a bacterial proteome analysis. Proteomics 6: 1121-1132.
66. Qian WJ, Liu T, Monroe ME, Strittmatter EF, Jacobs JM, et al. (2005) Probability-based evaluation of peptide and protein identifications from tandem mass spectrometry and SEQUEST analysis: the human proteome. J Proteome Res 4: 53-62.
67. Nesvizhskii AI, Keller A, Kolker E, Aebersold R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646-4658.
68. MacCoss MJ, Wu CC, Yates JR, 3rd (2002) Probability-based validation of protein identifications using a modified SEQUEST algorithm. Anal Chem 74: 5593-5599.
69. Orchard S, Jones AR, Stephan C, Binz PA (2007) The HUPO pre-congress Proteomics Standards Initiative workshop. HUPO 5th annual World Congress. Long Beach, CA, USA 28 October-1 November 2006. Proteomics 7: 1006-1008.
70. Nanduri B, Lawrence ML, Vanguri S, Pechan T, Burgess SC (2005) Proteomic analysis using an unfinished bacterial genome: the effects of subminimum inhibitory concentrations of antibiotics on Mannheimia haemolytica virulence factor expression. Proteomics 5: 4852-4863.
71. Bridges SM, Bryce GB, Wang N, Williams WP, Burgess SC, et al. (2007) ProtQuant: a tool for the label -free quantification of mudPIT proteomics data. BMC Bioinformatics 8.
72. McCarthy FM, Wang N, Magee GB, Nanduri B, Lawrence ML, et al. (2006) AgBase: a functional genomics resource for agriculture. BMC Genomics 7: 229.
73. Gerling IC, Singh S, Lenchik NI, Marshall DR, Wu J (2006) New data analysis and mining approaches identify unique proteome and transcriptome markers of susceptibility to autoimmune diabetes. Mol Cell Proteomics 5: 293-305.
74. Huang Y, Yan J, Lubet R, Kensler TW, Sutter TR (2006) Identification of novel transcriptional networks in response to treatment with the anticarcinogen 3H- 1,2-dithiole-3-thione. Physiol Genomics 24: 144-153.