Tribbles expression in cumulus cells is related to oocyte maturation and fatty acid metabolism

Journal of Ovarian Research

Volumn 7, Issue 1, 2014, Pages

  Brisard, Daphné ^a,b,c,d   Chesnel, Franck ^e   Elis, Sébastien ^a,b,c,d   Desmarchais, Alice ^a,b,c,d   Sánchez Lazo, Laura ^a,b,c,d   Chasles, Manon ^a,b,c,d   Maillard, Virginie ^a,b,c,d   Uzbekova, Svetlana ^a,b,c,d  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d IFCE   (France)

^e CNRS   (France)

Author keywords

Cumulus cells; Fatty acid metabolism; Oocyte maturation; Tribbles

Indexed keywords

CARBOXYLASE; ETOMOXIR; MITOGEN ACTIVATED PROTEIN KINASE 3; SCAFFOLD PROTEIN; TRIBBLES PROTEIN; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; ENZYME INHIBITOR; EPOXIDE; FATTY ACID; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; TRB3 PROTEIN, MOUSE; TRIB1 PROTEIN, MOUSE; TRIBBLES 2 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATTLE; CELL PROLIFERATION; CONTROLLED STUDY; CUMULUS CELL; CYTOPLASM; FATTY ACID METABOLISM; FEMALE; GENE EXPRESSION; GERMINAL VESICLE; IMMUNOFLUORESCENCE; LIPID METABOLISM; MITOCHONDRION; MITOSIS; MOUSE; MURINAE; NONHUMAN; OOCYTE; OOCYTE MATURATION; OXIDATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BOVINE; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; METABOLISM; OOCYTE DEVELOPMENT; OVARY FOLLICLE; PHYSIOLOGY;

ANIMALS; CATTLE; CELL CYCLE PROTEINS; CELLS, CULTURED; CUMULUS CELLS; ENZYME INHIBITORS; EPOXY COMPOUNDS; FATTY ACIDS; FEMALE; GENE EXPRESSION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPID METABOLISM; MICE, INBRED C57BL; OOCYTES; OOGENESIS; OVARIAN FOLLICLE; PROTEIN-SERINE-THREONINE KINASES;

EID: 84899738646     PISSN: None     EISSN: 17572215     Source Type: Journal    
DOI: 10.1186/1757-2215-7-44     Document Type: Article

References (61)

1. Tribbles, a cell-cycle brake that coordinates proliferation and morphogenesis during Drosophila gastrulation. Seher TC, Leptin M, Curr Biol 2000 10 11 623 629 10.1016/S0960-9822(00)00502-9 10837248
2. Developmental roles of tribbles protein family members. Dobens LL Jr, Bouyain S, Dev Dyn 2012 241 8 1239 1248 doi: 101002/dvdy23822 Epub 2012 Jun 27 2012 10.1002/dvdy.23822 22711497
3. Tribbles in disease: Signaling pathways important for cellular function and neoplastic transformation. Yokoyama T, Nakamura T, Cancer Sci 2011 102 6 1115 1122 10.1111/j.1349-7006.2011.01914.x 21338441
4. The functionally diverse roles of tribbles. Lohan F, Keeshan K, Biochem Soc Trans 2013 41 4 1096 1100 doi: 101042/BST20130105 2013 10.1042/BST20130105 23863185
5. Tribbles: 'puzzling' regulators of cell signalling. Kiss-Toth E, Biochem Soc Trans 2011 39 2 684 687 10.1042/BST0390684 21428962
6. Six new loci associated with blood low-density lipoprotein cholesterol, high-density lipoprotein cholesterol or triglycerides in humans. Kathiresan S, Melander O, Guiducci C, Surti A, Burtt NP, Rieder MJ, Cooper GM, Roos C, Voight BF, Havulinna AS, Wahlstrand B, Hedner T, Corella D, Tai ES, Ordovas JM, Berglund G, Vartiainen E, Jousilahti P, Hedblad B, Taskinen MR, Newton-Cheh C, Salomaa V, Peltonen L, Groop L, Altshuler DM, Orho-Melander M, Nat Genet 2008 40 2 189 197 10.1038/ng.75 18193044
7. Trib1 is a lipid- and myocardial infarction-associated gene that regulates hepatic lipogenesis and VLDL production in mice. Burkhardt R, Toh SA, Lagor WR, Birkeland A, Levin M, Li X, Robblee M, Fedorov VD, Yamamoto M, Satoh T, Akira S, Kathiresan S, Breslow JL, Rader DJ, J Clin Invest 2010 120 12 4410 4414 doi: 101172/JCI44213 Epub 2010 Nov 15 2013 10.1172/JCI44213 21084752
8. TRB3 is a PI 3-kinase dependent indicator for nutrient starvation. Schwarzer R, Dames S, Tondera D, Klippel A, Kaufmann J, Cell Signal 2006 18 6 899 909 10.1016/j.cellsig.2005.08.002 16129579
9. Tocopheryl-phosphate regulation of gene expression in preadipocytes and adipocytes. Lirangi M, Meydani M, Zingg JM, Azzi A, Biofactors 2012 38 6 450 457 10.1002/biof.1051 23047815
10. Enhanced TLR-mediated NF-IL6 dependent gene expression by Trib1 deficiency. Yamamoto M, Uematsu S, Okamoto T, Matsuura Y, Sato S, Kumar H, Satoh T, Saitoh T, Takeda K, Ishii KJ, Takeuchi O, Kawai T, Akira S, J Exp Med 2007 204 9 2233 2239 10.1084/jem.20070183 17724128
11. Oocyte-somatic cells interactions, lessons from evolution. Charlier C, Montfort J, Chabrol O, Brisard D, Nguyen T, Le Cam A, Richard-Parpaillon L, Moreews F, Pontarotti P, Uzbekova S, Chesnel F, Bobe J, BMC Genomics 2012 13 1 560 10.1186/1471-2164-13-560 23083410
12. Identification of downregulated messenger RNAs in bovine granulosa cells of dominant follicles following stimulation with human chorionic gonadotropin. Ndiaye K, Fayad T, Silversides DW, Sirois J, Lussier JG, Biol Reprod 2005 73 2 324 333 10.1095/biolreprod.104.038026 15829623
13. Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence. Assidi M, Dieleman SJ, Sirard M-A, Reproduction 2010 140 6 835 852 10.1530/REP-10-0248 20724459
14. Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Fan H-Y, Sun Q-Y, Biol Reprod 2004 70 3 535 547 14613897
15. The role of fatty acids in oocyte and early embryo development. McKeegan PJ, Sturmey RG, Reprod Fertil Dev 2012 24 1 59 67 10.1071/RD11907
16. Energy Metabolism Regulating Mammalian Oocyte Maturation, Meiosis. Songsasen N, Molecular Mechanisms and Cytogenetic Diversity, Andrew S, 2012 InTech, DOI: 10.5772/33752. Available from: http://www.intechopen.com/books/ meiosis-molecular-mechanisms-and-cytogenetic-diversity
17. Role of fatty acids in energy provision during oocyte maturation and early embryo development. Sturmey RG, Reis A, Leese HJ, McEvoy TG, Reprod Domest Anim 2009 44 Suppl 3 50 58 doi: 101111/j1439-0531200901402x 2009 19660080
18. Oleic acid prevents detrimental effects of saturated fatty acids on bovine oocyte developmental competence. Aardema H, Vos PLAM, Lolicato F, Roelen BAJ, Knijn HM, Vaandrager AB, Helms JB, Gadella BM, Biol Reprod 2011 85 1 62 69 10.1095/biolreprod.110.088815 21311036
19. Absence of cumulus cells during in vitro maturation affects lipid metabolism in bovine oocytes. Auclair S, Uzbekov R, Elis S, Sanchez L, Kireev I, Lardic L, Dalbies-Tran R, Uzbekova S, Am J Physiol Endocrinol Metab 2013 304 6 599 E613 10.1152/ajpendo.00469.2012 23321473
20. Lipid and fatty acid analysis of fresh and frozen-thawed immature and in vitro matured bovine oocytes. Kim JY, Kinoshita M, Ohnishi M, Fukui Y, Reproduction 2001 122 1 131 138 10.1530/rep.0.1220131 11425337
21. The mitochondrial carnitine palmitoyltransferase system. From concept to molecular analysis. McGarry JD, Brown NF, Eur J Biochem 1997 244 1 1 14 10.1111/j.1432-1033.1997.00001.x 9063439
22. Minireview: malonyl CoA, AMP-activated protein kinase, and adiposity. Ruderman NB, Saha AK, Kraegen EW, Endocrinology 2003 144 12 5166 5171 10.1210/en.2003-0849 14500570
23. TRB3 links the E3 ubiquitin ligase COP1 to lipid metabolism. Qi L, Heredia JE, Altarejos JY, Screaton R, Goebel N, Niessen S, Macleod IX, Liew CW, Kulkarni RN, Bain J, Newgard C, Nelson M, Evans RM, Yates J, Montminy M, Science 2006 312 5781 1763 1766 10.1126/science.1123374 16794074
24. Fatty acid oxidation and meiotic resumption in mouse oocytes. Downs SM, Mosey JL, Klinger J, Mol Reprod Dev 2009 76 9 844 853 10.1002/mrd.21047 19455666
25. Promoting lipid utilization with l-carnitine to improve oocyte quality. Dunning KR, Robker RL, Anim Reprod Sci 2012 134 1-2 69 75 22917873
26. A requirement for fatty acid oxidation in the hormone-induced meiotic maturation of mouse oocytes. Valsangkar D, Downs SM, Biol Reprod 2013 89 2 43 10.1095/biolreprod.113.109058 23863407
27. Increased beta-oxidation and improved oocyte developmental competence in response to l-carnitine during ovarian in vitro follicle development in mice. Dunning KR, Akison LK, Russell DL, Norman RJ, Robker RL, Biol Reprod 2011 85 3 548 555 10.1095/biolreprod.110.090415 21613630
28. Beta-oxidation is essential for mouse oocyte developmental competence and early embryo development. Dunning KR, Cashman K, Russell DL, Thompson JG, Norman RJ, Robker RL, Biol Reprod 2010 83 6 909 918 10.1095/biolreprod.110. 084145 20686180
29. Comparative importance of fatty acid beta-oxidation to nuclear maturation, gene expression, and glucose metabolism in mouse, bovine, and porcine cumulus oocyte complexes. Paczkowski M, Silva E, Schoolcraft WB, Krisher RL, Biol Reprod 2013 88 5 111 10.1095/biolreprod.113.108548 23536372
30. TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Du K, Herzig S, Kulkarni RN, Montminy M, Science 2003 300 5625 1574 1577 10.1126/science.1079817 12791994
31. Human tribbles, a protein family controlling mitogen-activated protein kinase cascades. Kiss-Toth E, Bagstaff SM, Sung HY, Jozsa V, Dempsey C, Caunt JC, Oxley KM, Wyllie DH, Polgar T, Harte M, O'Neill L, Qwarnstrom EE, Dower SK, J Biol Chem 2004 279 41 42703 42708 10.1074/jbc.M407732200 15299019
32. TRB3 interacts with SMAD3 promoting tumor cell migration and invasion. Hua F, Mu R, Liu J, Xue J, Wang Z, Lin H, Yang H, Chen X, Hu Z, J Cell Sci 2011 124 19 3235 3246 10.1242/jcs.082875 21896644
33. Several signaling pathways are involved in the control of cattle oocyte maturation. Vigneron C, Perreau C, Dupont J, Uzbekova S, Prigent C, Mermillod P, Mol Reprod Dev 2004 69 4 466 474 10.1002/mrd.20173 15457547
34. Kinetics of gene expression and signaling in bovine cumulus cells throughout IVM in different mediums in relation to oocyte developmental competence, cumulus apoptosis and progesterone secretion. Salhab M, Tosca L, Cabau C, Papillier P, Perreau C, Dupont J, Mermillod P, Uzbekova S, Theriogenology 2011 75 1 90 104 10.1016/j.theriogenology.2010.07.014 20961603
35. In vitro maturation of oocytes alters gene expression and signaling pathways in bovine cumulus cells. Salhab M, Dhorne-Pollet S, Auclair S, Guyader-Joly C, Brisard D, Dalbies-Tran R, Dupont J, Ponsart C, Mermillod P, Uzbekova S, Mol Reprod Dev 2013 80 2 166 182 10.1002/mrd.22148 23280668
36. Regulation of expression and signalling modulator function of mammalian tribbles is cell-type specific. Sung HY, Francis SE, Crossman DC, Kiss-Toth E, Immunol Lett 2006 104 1â"2 171 177 16364454
37. Tribbles: novel regulators of cell function; evolutionary aspects. Hegedus Z, Czibula A, Kiss-Toth E, Cell Mol Life Sci 2006 63 14 1632 1641 10.1007/s00018-006-6007-9 16715410
38. Tribbles-1 as a novel biomarker of chronic antibody-mediated rejection. Ashton-Chess J, Giral M, Mengel M, Renaudin K, Foucher Y, Gwinner W, Braud C, Dugast E, Quillard T, Thebault P, Chiffoleau E, Braudeau C, Charreau B, Soulillou JP, Brouard S, J Am Soc Nephrol 2008 19 6 1116 1127 10.1681/ASN.2007101056 18369086
39. The Tribbles-1 protein in humans: roles and functions in health and disease. Dugast E, Kiss-Toth E, Soulillou JP, Brouard S, Ashton-Chess J, Curr Mol Med 2013 13 1 80 85 10.2174/156652413804486197 22834837
40. Tribbles homolog 2 inactivates C/EBPÎ ± and causes acute myelogenous leukemia. Keeshan K, He Y, Wouters BJ, Shestova O, Xu L, Sai H, Rodriguez CG, Maillard I, Tobias JW, Valk P, Carroll M, Aster JC, Delwel R, Pear WS, Cancer Cell 2006 10 5 401 411 10.1016/j.ccr.2006.09.012 17097562
41. Identification of tribbles-1 as a novel binding partner of Foxp3 in regulatory T cells. Dugast E, Kiss-Toth E, Docherty L, Danger R, Chesneau M, Pichard V, Judor JP, Pettre S, Conchon S, Soulillou JP, Brouard S, Ashton-Chess J, J Biol Chem 2013 288 14 10051 10060 10.1074/jbc.M112.448654 23417677
42. Overexpression of TRIB2 in human lung cancers contributes to tumorigenesis through downregulation of C/EBPalpha. Grandinetti KB, Stevens TA, Ha S, Salamone RJ, Walker JR, Zhang J, Agarwalla S, Tenen DG, Peters EC, Reddy VA, Oncogene 2011 30 30 3328 3335 10.1038/onc.2011.57 21399661
43. Genomic response of hypoxic Muller cells involves the very low density lipoprotein receptor as part of an angiogenic network. Loewen N, Chen J, Dudley VJ, Sarthy VP, Mathura JR Jr, Exp Eye Res 2009 88 5 928 937 10.1016/j.exer.2008. 11.037 19233325
44. Glycogen synthase kinase 3B in bovine oocytes and granulosa cells: possible involvement in meiosis during in vitro maturation. Uzbekova S, Salhab M, Perreau C, Mermillod P, Dupont J, Reproduction 2009 138 2 235 246 10.1530/REP-09-0136 19470708
45. Tribbles: a family of kinase-like proteins with potent signalling regulatory function. Hegedus Z, Czibula A, Kiss-Toth E, Cell Signal 2007 19 2 238 250 10.1016/j.cellsig.2006.06.010 16963228
46. Oocyte developmental failure in response to elevated non-esterified fatty acid concentrations: mechanistic insights. Van Hoeck V, Leroy JL, Arias-Alvarez M, Rizos D, Gutierrez-Adan A, Schnorbusch K, Bols PE, Leese HJ, Sturmey RG, Reproduction 2012 145 1 33 44
47. The tribbles gene family and lipoprotein metabolism. Angyal A, Kiss-Toth E, Curr Opin Lipidol 2012 23 2 122 126 10.1097/MOL.0b013e3283508c3b 22274752
48. Polygenic determinants of severe hypertriglyceridemia. Wang J, Ban MR, Zou GY, Cao H, Lin T, Kennedy BA, Anand S, Yusuf S, Huff MW, Pollex RL, Hegele RA, Hum Mol Genet 2008 17 18 2894 2899 doi: 101093/hmg/ddn188 Epub 2008 Jul 1 2008 10.1093/hmg/ddn188 18596051
49. 3 transcriptional activity. Takahashi Y, Ohoka N, Hayashi H, Sato R, J Lipid Res 2008 49 4 880 892 10.1194/jlr.M700545-JLR200 18187772
50. Regulation of fatty acid oxidation in mouse cumulus-oocyte complexes during maturation and modulation by PPAR agonists. Dunning KR, Anastasi MR, Zhang VJ, Russell DL, Robker RL, PLoS One 2014 9 2 87327 10.1371/journal.pone. 0087327 24505284
51. Effects of long-chain fatty acids on cytosolic triacylglycerol accumulation and lipid droplet formation in primary cultured bovine mammary epithelial cells. Yonezawa T, Yonekura S, Kobayashi Y, Hagino A, Katoh K, Obara Y, J Dairy Sci 2004 87 8 2527 2534 10.3168/jds.S0022-0302(04)73377-9 15328276
52. Selective transport of long-chain fatty acids by FAT/CD36 in skeletal muscle of broilers. Guo J, Shu G, Zhou L, Zhu X, Liao W, Wang S, Yang J, Zhou G, Xi Q, Gao P, Zhang Y, Zhang S, Yuan L, Jiang Q, Animal 2013 7 3 422 429 doi: 101017/S1751731112001619 Epub 2012 Aug 16 2013 10.1017/S1751731112001619 23031491
53. CD36 genetics and the metabolic complications of obesity. Love-Gregory L, Abumrad NA, Curr Opin Clin Nutr Metab Care 2011 14 6 527 534 10.1097/MCO.0b013e32834bbac9 21912245
54. Induced expression of pattern recognition receptors in cumulus oocyte complexes: novel evidence for innate immune-like functions during ovulation. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robanya I, Richards JS, Mol Endocrinol 2006 20 12 3228 3239 10.1210/me.2006-0194 16931571
55. Tribbles-2 is a novel regulator of inflammatory activation of monocytes. Eder K, Guan H, Sung HY, Ward J, Angyal A, Janas M, Sarmay G, Duda E, Turner M, Dower SK, Francis SE, Crossman DC, Kiss-Toth E, Int Immunol 2008 20 12 1543 1550 10.1093/intimm/dxn116 18952906
56. Inhibition of fatty acid oxidation by etomoxir impairs NADPH production and increases reactive oxygen species resulting in ATP depletion and cell death in human glioblastoma cells. Pike LS, Smift AL, Croteau NJ, Ferrick DA, Wu M, Bioenerg 2011 1807 6 726 734
57. Nutrient sensing, metabolism, and cell growth control. Yuan H-X, Xiong Y, Guan K-L, Mol Cell 2013 49 3 379 387 10.1016/j.molcel.2013.01.019 23395268
58. A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes. Downs SM, Hudson ER, Hardie DG, Dev Biol 2002 245 1 200 212 10.1006/dbio.2002.0613 11969266
59. Possible role of 5'AMP-activated protein kinase in the metformin-mediated arrest of bovine oocytes at the germinal vesicle stage during in vitro maturation. Tosca L, Uzbekova S, Chabrolle C, Dupont J, Biol Reprod 2007 77 3 452 465 10.1095/biolreprod.107.060848 17567959
60. Adenosine 5'-monophosphate kinase-activated protein kinase (PRKA) activators delay meiotic resumption in porcine oocytes. Mayes MA, Laforest MF, Guillemette C, Gilchrist RB, Richard FJ, Biol Reprod 2007 76 4 589 597 10.1095/biolreprod.106.057828 17167165
61. Timing of nuclear progression and protein synthesis necessary for meiotic maturation of bovine oocytes. Sirard MA, Florman HM, Leibfried-Rutledge ML, Barnes FL, Sims ML, First NL, Biol Reprod 1989 40 6 1257 1263 10.1095/biolreprod40.6.1257 2775818