Differential genome-wide gene expression profiling of bovine largest and second-largest follicles: Identification of genes associated with growth of dominant follicles

Reproductive Biology and Endocrinology

Volumn 8, Issue , 2010, Pages

  Hayashi, Ken Go ^a   Ushizawa, Koichi ^a   Hosoe, Misa ^a   Takahashi, Toru ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE; FOLLITROPIN RECEPTOR; GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 3; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; MONOCYTE CHEMOTACTIC PROTEIN 1; MUELLERIAN INHIBITING FACTOR; OSTEOPONTIN; PADGEM PROTEIN; PLACENTAL GROWTH FACTOR; SOMATOMEDIN BINDING PROTEIN 5; THROMBOSPONDIN 2; TISSUE INHIBITOR OF METALLOPROTEINASE 1;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COW; FEMALE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE LOCATION; GENETIC ASSOCIATION; GRANULOSA CELL; IN SITU HYBRIDIZATION; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY FOLLICLE ATRESIA; OVARY FOLLICLE DEVELOPMENT; POLYMERASE CHAIN REACTION; THECA CELL; UNINDEXED SEQUENCE; ANIMAL; CATTLE; CELL ENLARGEMENT; CELL SIZE; CLUSTER ANALYSIS; CYTOLOGY; DEVELOPMENTAL GENE; DNA MICROARRAY; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OVARY FOLLICLE; PHYSIOLOGY; VALIDATION STUDY;

BOVINAE;

ANIMALS; CATTLE; CELL ENLARGEMENT; CELL SIZE; CLUSTER ANALYSIS; FEMALE; GENE EXPRESSION PROFILING; GENES, DEVELOPMENTAL; GENOME; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OVARIAN FOLLICLE;

EID: 77949517518     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-8-11     Document Type: Article

References (69)

1. Sirois J, Fortune JE. Ovarian follicular dynamics during the estrous cycle in heifers monitored by real-time ultrasonography. Biol Reprod 1988, 39:308-317. 10.1095/biolreprod39.2.308, 3052602.
2. Ginther OJ, Knopf L, Kastelic JP. Temporal associations among ovarian events in cattle during oestrous cycles with two and three follicular waves. J Reprod Fertil 1989, 87:223-230.
3. Sunderland SJ, Crowe MA, Boland MP, Roche JF, Ireland JJ. Selection, dominance and atresia of follicles during the oestrous cycle of heifers. J Reprod Fertil 1994, 101:547-555.
4. Ginther OJ, Kot K, Kulick LJ, Wiltbank MC. Emergence and deviation of follicles during the development of follicular waves in cattle. Theriogenology 1997, 48:75-87. 10.1016/S0093-691X(97)00192-1, 16728109.
5. Ginther OJ, Wiltbank MC, Fricke PM, Gibbons JR, Kot K. Selection of the dominant follicle in cattle. Biol Reprod 1996, 55:1187-1194. 10.1095/biolreprod55.6.1187, 8949873.
6. Mihm M, Crowe MA, Knight PG, Austin EJ. Follicle wave growth in cattle. Reprod Domest Anim 2002, 37:191-200. 10.1046/j.1439-0531.2002.00371.x, 12173983.
7. Fortune JE, Rivera GM, Yang MY. Follicular development: the role of the follicular microenvironment in selection of the dominant follicle. Anim Reprod Sci 2004, 82-83:109-126. 10.1016/j.anireprosci.2004.04.031, 15271447.
8. Sisco B, Hagemann LJ, Shelling AN, Pfeffer PL. Isolation of genes differentially expressed in dominant and subordinate bovine follicles. Endocrinology 2003, 144:3904-3913. 10.1210/en.2003-0485, 12933664.
9. Evans AC, Ireland JL, Winn ME, Lonergan P, Smith GW, Coussens PM, Ireland JJ. Identification of genes involved in apoptosis and dominant follicle development during follicular waves in cattle. Biol Reprod 2004, 70:1475-1484. 10.1095/biolreprod.103.025114, 14736815.
10. Fayad T, Levesque V, Sirois J, Silversides DW, Lussier JG. Gene expression profiling of differentially expressed genes in granulosa cells of bovine dominant follicles using suppression subtractive hybridization. Biol Reprod 2004, 70:523-533. 10.1095/biolreprod.103.021709, 14568916.
11. Ndiaye K, Fayad T, Silversides DW, Sirois J, Lussier JG. Identification of downregulated messenger RNAs in bovine granulosa cells of dominant follicles following stimulation with human chorionic gonadotropin. Biol Reprod 2005, 73:324-333. 10.1095/biolreprod.104.038026, 15829623.
12. Mihm M, Baker PJ, Ireland JL, Smith GW, Coussens PM, Evans AC, Ireland JJ. Molecular evidence that growth of dominant follicles involves a reduction in follicle-stimulating hormone dependence and an increase in luteinizing hormone dependence in cattle. Biol Reprod 2006, 74:1051-1059. 10.1095/biolreprod.105.045799, 16481595.
13. Zielak AE, Forde N, Park SD, Doohan F, Coussens PM, Smith GW, Ireland JJ, Lonergan P, Evans AC. Identification of novel genes associated with dominant follicle development in cattle. Reprod Fertil Dev 2007, 19:967-975. 10.1071/RD07102, 18076829.
14. Zielak AE, Canty MJ, Forde N, Coussens PM, Smith GW, Lonergan P, Ireland JJ, Evans AC. Differential expression of genes for transcription factors in theca and granulosa cells following selection of a dominant follicle in cattle. Mol Reprod Dev 2008, 75:904-914. 10.1002/mrd.20819, 17948250.
15. Baker PJ, Fleming LM, Mossa F, Lonergan P, Evans AC, Mihm M. Decreased mRNA expression of dominance maker genes in preovulatory compared to newly selected dominant follicles in cattle [abstract]. Biol Reprod 2008, 531.
16. Skinner MK, Schmidt M, Savenkova MI, Sadler-Riggleman I, Nilsson EE. Regulation of granulosa and theca cell transcriptomes during ovarian antral follicle development. Mol Reprod Dev 2008, 75:1457-1472. 10.1002/mrd.20883, 18288646.
17. Mihm M, Baker PJ, Fleming LM, Monteiro AM, O'Shaughnessy PJ. Differentiation of the bovine dominant follicle from the cohort upregulates mRNA expression for new tissue development genes. Reproduction 2008, 135:253-265. 10.1530/REP-06-0193, 18239053.
18. Liu Z, Youngquist RS, Garverick HA, Antoniou E. Molecular mechanisms regulating bovine ovarian follicular selection. Mol Reprod Dev 2009, 76:351-366. 10.1002/mrd.20967, 18932212.
19. TM4. , http://www.tm4.org/mev.html
20. MIAME. , http://www.mged.org/Workgroups/MIAME/miame.html
21. GEO. , http://www.ncbi.nlm.nih.gov/projects/geo/
22. Ushizawa K, Takahashi T, Hosoe M, Ishiwata H, Kaneyama K, Kizaki K, Hashizume K. Global gene expression analysis and regulation of the principal genes expressed in bovine placenta in relation to the transcription factor AP-2 family. Reprod Biol Endocrinol 2007, 5:17. 10.1186/1477-7827-5-17, 1867817, 17462098.
23. Takahashi T, Hamanaka S, Ikeda S, Kobayashi J, Hashizume K. A direct time-resolved fluorescent immunoassay (TR-FIA) for measuring plasma progesterone concentration in sika doe (Cervus nippon centralis). J Reprod Dev 2001, 47:119-123.
24. Takahashi T, Hamanaka S, Imai K, Hashizume K. A direct time-resolved fluoroimmunoassay (TR-FIA) for measuring plasma estradiol-17beta concentrations in cattle. J Vet Med Sci 2004, 66:225-229. 10.1292/jvms.66.225, 15107548.
25. Bao B, Garverick HA, Smith GW, Smith MF, Salfen BE, Youngquist RS. Changes in messenger ribonucleic acid encoding luteinizing hormone receptor, cytochrome P450-side chain cleavage, and aromatase are associated with recruitment and selection of bovine ovarian follicles. Biol Reprod 1997, 56:1158-1168. 10.1095/biolreprod56.5.1158, 9160714.
26. Santiago CA, Voge JL, Aad PY, Allen DT, Stein DR, Malayer JR, Spicer LJ. Pregnancy-associated plasma protein-A and insulin-like growth factor binding protein mRNAs in granulosa cells of dominant and subordinate follicles of preovulatory cattle. Domest Anim Endocrinol 2005, 28:46-63. 10.1016/j.domaniend.2004.06.002, 15620806.
27. Ushizawa K, Kaneyama K, Takahashi T, Tokunaga T, Tsunoda Y, Hashizume K. Cloning and expression of a new member of prolactin-related protein in bovine placenta: bovine prolactin-related protein-VII. Biochem Biophys Res Commun 2005, 326:435-441. 10.1016/j.bbrc.2004.11.045, 15582596.
28. Ushizawa K, Takahashi T, Kaneyama K, Hosoe M, Hashizume K. Cloning of the bovine antiapoptotic regulator, BCL2-related protein A1, and its expression in trophoblastic binucleate cells of bovine placenta. Biol Reprod 2006, 74:344-351. 10.1095/biolreprod.105.042655, 16221993.
29. Bao B, Garverick HA. Expression of steroidogenic enzyme and gonadotropin receptor genes in bovine follicles during ovarian follicular waves: a review. J Anim Sci 1998, 76:1903-1921.
30. Canty MJ, Boland MP, Evans AC, Crowe MA. Alterations in follicular IGFBP mRNA expression and follicular fluid IGFBP concentrations during the first follicle wave in beef heifers. Anim Reprod Sci 2006, 93:199-217. 10.1016/j.anireprosci.2005.06.033, 16159699.
31. Silva JM, Price CA. Effect of follicle-stimulating hormone on steroid secretion and messenger ribonucleic acids encoding cytochromes P450 aromatase and cholesterol side-chain cleavage in bovine granulosa cells in vitro. Biol Reprod 2000, 62:186-191. 10.1095/biolreprod62.1.186, 10611084.
32. Silva JM, Price CA. Insulin and IGF-I are necessary for FSH-induced cytochrome P450 aromatase but not cytochrome P450 side-chain cleavage gene expression in oestrogenic bovine granulosa cells in vitro. J Endocrinol 2002, 174:499-507. 10.1677/joe.0.1740499, 12208671.
33. Voge JL, Aad PY, Santiago CA, Goad DW, Malayer JR, Allen D, Spicer LJ. Effect of insulin-like growth factors (IGF), FSH, and leptin on IGF-binding-protein mRNA expression in bovine granulosa and theca cells: quantitative detection by real-time PCR. Peptides 2004, 25:2195-2203. 10.1016/j.peptides.2004.07.008, 15572210.
34. Voge JL, Santiago CA, Aad PY, Goad DW, Malayer JR, Spicer LJ. Quantification of insulin-like growth factor binding protein mRNA using real-time PCR in bovine granulosa and theca cells: effect of estradiol, insulin, and gonadotropins. Domest Anim Endocrinol 2004, 26:241-258. 10.1016/j.domaniend.2003.11.002, 15036378.
35. Monniaux D, Clemente N, Touze JL, Belville C, Rico C, Bontoux M, Picard JY, Fabre S. Intrafollicular steroids and anti-mullerian hormone during normal and cystic ovarian follicular development in the cow. Biol Reprod 2008, 79:387-396. 10.1095/biolreprod.107.065847, 18448844.
36. Rico C, Fabre S, Medigue C, Clemente N, Clement F, Bontoux M, Touze JL, Dupont M, Briant E, Remy B, Beckers JF, Monniaux D. Anti-mullerian hormone is an endocrine marker of ovarian gonadotropin-responsive follicles and can help to predict superovulatory responses in the cow. Biol Reprod 2009, 80:50-59. 10.1095/biolreprod.108.072157, 18784351.
37. Takahashi M, Hayashi M, Manganaro TF, Donahoe PK. The ontogeny of mullerian inhibiting substance in granulosa cells of the bovine ovarian follicle. Biol Reprod 1986, 35:447-453. 10.1095/biolreprod35.2.447, 3533170.
38. Eder AM, Sasagawa T, Mao M, Aoki J, Mills GB. Constitutive and lysophosphatidic acid (LPA)-induced LPA production: role of phospholipase D and phospholipase A2. Clin Cancer Res 2000, 6:2482-2491.
39. Budnik LT, Mukhopadhyay AK. Lysophosphatidic acid and its role in reproduction. Biol Reprod 2002, 66:859-865. 10.1095/biolreprod66.4.859, 11906902.
40. Diouf MN, Sayasith K, Lefebvre R, Silversides DW, Sirois J, Lussier JG. Expression of phospholipase A2 group IVA (PLA2G4A) is upregulated by human chorionic gonadotropin in bovine granulosa cells of ovulatory follicles. Biol Reprod 2006, 74:1096-1103. 10.1095/biolreprod.105.048579, 16510840.
41. Nakamura MT, Nara TY. Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Annu Rev Nutr 2004, 24:345-376. 10.1146/annurev.nutr.24.121803.063211, 15189125.
42. Moreau C, Froment P, Tosca L, Moreau V, Dupont J. Expression and regulation of the SCD2 desaturase in the rat ovary. Biol Reprod 2006, 74:75-87. 10.1095/biolreprod.105.044545, 16207839.
43. Abel S, Smuts CM, de Villiers C, Gelderblom WC. Changes in essential fatty acid patterns associated with normal liver regeneration and the progression of hepatocyte nodules in rat hepatocarcinogenesis. Carcinogenesis 2001, 22:795-804. 10.1093/carcin/22.5.795, 11323400.
44. McEvoy TG, Coull GD, Broadbent PJ, Hutchinson JS, Speake BK. Fatty acid composition of lipids in immature cattle, pig and sheep oocytes with intact zona pellucida. J Reprod Fertil 2000, 118:163-170. 10.1530/reprod/118.1.163, 10793638.
45. Kiss-Toth E, Bagstaff SM, Sung HY, Jozsa V, Dempsey C, Caunt JC, Oxley KM, Wyllie DH, Polgar T, Harte M, O'neill LA, Qwarnstrom EE, Dower SK. Human tribbles, a protein family controlling mitogen-activated protein kinase cascades. J Biol Chem 2004, 279:42703-42708. 10.1074/jbc.M407732200, 15299019.
46. Ryan KE, Casey SM, Canty MJ, Crowe MA, Martin F, Evans AC. Akt and Erk signal transduction pathways are early markers of differentiation in dominant and subordinate ovarian follicles in cattle. Reproduction 2007, 133:617-626. 10.1530/REP-06-0130, 17379656.
47. Rohm F, Spanel-Borowski K, Eichler W, Aust G. Correlation between expression of selectins and migration of eosinophils into the bovine ovary during the periovulatory period. Cell Tissue Res 2002, 309:313-322. 10.1007/s00441-002-0602-3, 12172791.
48. Vestweber D, Blanks JE. Mechanisms that regulate the function of the selectins and their ligands. Physiol Rev 1999, 79:181-213.
49. Mazzali M, Kipari T, Ophascharoensuk V, Wesson JA, Johnson R, Hughes J. Osteopontin--a molecule for all seasons. Qjm 2002, 95:3-13. 10.1093/qjmed/95.1.3, 11834767.
50. Suzuki T, Sasano H, Takaya R, Fukaya T, Yajima A, Date F, Nagura H. Leukocytes in normal-cycling human ovaries: immunohistochemical distribution and characterization. Hum Reprod 1998, 13:2186-2191. 10.1093/humrep/13.8.2186, 9756294.
51. Ny T, Wahlberg P, Brandstrom IJ. Matrix remodeling in the ovary: regulation and functional role of the plasminogen activator and matrix metalloproteinase systems. Mol Cell Endocrinol 2002, 187:29-38. 10.1016/S0303-7207(01)00711-0, 11988309.
52. Blasi F, Carmeliet P. uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol 2002, 3:932-943. 10.1038/nrm977, 12461559.
53. Cao M, Buratini J, Lussier JG, Carriere PD, Price CA. Expression of protease nexin-1 and plasminogen activators during follicular growth and the periovulatory period in cattle. Reproduction 2006, 131:125-137. 10.1530/rep.1.00849, 16388016.
54. Goldberg GI, Strongin A, Collier IE, Genrich LT, Marmer BL. Interaction of 92-kDa type IV collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitial collagenase, and activation of the proenzyme with stromelysin. J Biol Chem 1992, 267:4583-4591.
55. Khandoker MA, Imai K, Takahashi T, Hashizume K. Role of gelatinase on follicular atresia in the bovine ovary. Biol Reprod 2001, 65:726-732. 10.1095/biolreprod65.3.726, 11514334.
56. Zhan Q. Gadd45a a p53- and BRCA1-regulated stress protein, in cellular response to DNA damage. Mutat Res 2005, 569:133-143.
57. Yu BP. Cellular defenses against damage from reactive oxygen species. Physiol Rev 1994, 74:139-162.
58. Tilly JL, Tilly KI. Inhibitors of oxidative stress mimic the ability of follicle-stimulating hormone to suppress apoptosis in cultured rat ovarian follicles. Endocrinology 1995, 136:242-252. 10.1210/en.136.1.242, 7828537.
59. Bonnet A, Frappart PO, Dehais P, Tosser-Klopp G, Hatey F. Identification of differential gene expression in in vitro FSH treated pig granulosa cells using suppression subtractive hybridization. Reprod Biol Endocrinol 2006, 4:35. 10.1186/1477-7827-4-35, 1533831, 16827936.
60. Valdez KE, Cuneo SP, Turzillo AM. Regulation of apoptosis in the atresia of dominant bovine follicles of the first follicular wave following ovulation. Reproduction 2005, 130:71-81. 10.1530/rep.1.00430, 15985633.
61. Zeleznik AJ, Schuler HM, Reichert LE. Gonadotropin-binding sites in the rhesus monkey ovary: role of the vasculature in the selective distribution of human chorionic gonadotropin to the preovulatory follicle. Endocrinology 1981, 109:356-362. 10.1210/endo-109-2-356, 6265188.
62. Acosta TJ, Hayashi KG, Matsui M, Miyamoto A. Changes in follicular vascularity during the first follicular wave in lactating cows. J Reprod Dev 2005, 51:273-280. 10.1262/jrd.16092, 15699584.
63. Jiang JY, Macchiarelli G, Tsang BK, Sato E. Capillary angiogenesis and degeneration in bovine ovarian antral follicles. Reproduction 2003, 125:211-223. 10.1530/rep.0.1250211, 12578535.
64. Maglione D, Guerriero V, Viglietto G, Delli-Bovi P, Persico MG. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci USA 1991, 88:9267-9271. 10.1073/pnas.88.20.9267, 52695, 1924389.
65. Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, Wu Y, Bono F, Devy L, Beck H, Scholz D, Acker T, DiPalma T, Dewerchin M, Noel A, Stalmans I, Barra A, Blacher S, Vandendriessche T, Ponten A, Eriksson U, Plate KH, Foidart JM, Schaper W, Charnock-Jones DS, Hicklin DJ, Herbert JM, Collen D, Persico MG. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 2001, 7:575-583. 10.1038/87904, 11329059.
66. Streit M, Riccardi L, Velasco P, Brown LF, Hawighorst T, Bornstein P, Detmar M. Thrombospondin-2: a potent endogenous inhibitor of tumor growth and angiogenesis. Proc Natl Acad Sci USA 1999, 96:14888-14893. 10.1073/pnas.96.26.14888, 24743, 10611308.
67. Greenaway J, Gentry PA, Feige JJ, LaMarre J, Petrik JJ. Thrombospondin and vascular endothelial growth factor are cyclically expressed in an inverse pattern during bovine ovarian follicle development. Biol Reprod 2005, 72:1071-1078. 10.1095/biolreprod.104.031120, 15616224.
68. Thomas FH, Wilson H, Silvestri A, Fraser HM. Thrombospondin-1 expression is increased during follicular atresia in the primate ovary. Endocrinology 2008, 149:185-192. 10.1210/en.2007-0835, 17884943.
69. Grado-Ahuir JA, Aad PY, Ranzenigo G, Caloni F, Cremonesi F, Spicer LJ. Microarray analysis of insulin-like growth factor-I-induced changes in messenger ribonucleic acid expression in cultured porcine granulosa cells: possible role of insulin-like growth factor-I in angiogenesis. J Anim Sci 2009, 87:1921-1933. 10.2527/jas.2008-1222, 19251926.