High transcript level of fatty acid-binding protein 11 but not of very low-density lipoprotein receptor is correlated to ovarian follicle atresia in a teleost fish (Solea senegalensis)

Biology of Reproduction

Volumn 77, Issue 3, 2007, Pages 504-516

  Agulleiro, Maria J ^a   André, Michèle ^b   Morais, Sofia ^b   Cerdà, Joan ^c   Babin, Patrick J ^b,d  

^a IRTA   (Spain)

^b Unite mixte INRA IFREMER Universite Bordeaux 1 UMR Nuage   (France)

^c CSIC   (Spain)

^d UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Follicular development; Gametogenesis; Gene regulation; Oocyte development; Ovary

Indexed keywords

FATTY ACID BINDING PROTEIN; FATTY ACID BINDING PROTEIN 11; MESSENGER RNA; UNCLASSIFIED DRUG; VITELLOGENIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IN SITU HYBRIDIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; OVARY FOLLICLE ATRESIA; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SOMATIC CELL; SPLICEOSOME; TELEOST; UPREGULATION; ZEBRA FISH;

DANIO RERIO; SOLEA SENEGALENSIS; TELEOSTEI; TETRAPODA; VERTEBRATA;

EID: 34548287917     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.107.061598     Document Type: Article

References (89)

1. Saidapur SK. Follicular atresia in the ovaries of nonmammalian vertebrates. Int Rev Cytol 1978; 54:225-244.
2. Nagahama Y. The functional morphology of the teleost gonad. In: Hoar WS, Randall DJ, Donaldson EM (eds.), Fish Physiology, vol. IX, chapter 6. Reproduction, Part A: Endocrine Tissues and Hormones. Academic Press; 1983:223-275.
3. Nagahama Y. Endocrine regulation of gametogenesis in fish. Int J Dev Biol 1994; 38:217-229.
4. Guraya SS. The cell and molecular biology of fish oogenesis. In: Sauer HW (ed.), Monographs in Developmental Biology, vol. 18, chapter VIII. Karger, Basel; 1986:169-180.
5. Kling D. Total atresia of the ovaries of Tilapia leucosticta (Cichlidae) after intoxication with the insecticide Lebaycid. Experientia 1981; 37:73-74.
6. Van Den Belt K, Wester PW, Van Der Ven LTM, Verheyen R, Witters H. Effects of ethynylestradiol on the reproductive physiology in zebrafish (Danio rerio): time dependency and reversibility. Environ Toxicol Chem 2002; 21:767-775.
7. Kaipia A, Hsueh AJ. Regulation of ovarian follicle atresia. Annu Rev Physiol 1997; 59:349-363.
8. Morita Y, Perez GI, Maravei DV, Tilly KI, Tilly JL. Targeted expression of Bcl-2 in mouse oocytes inhibits ovarian follicle atresia and prevents spontaneous and chemotherapy-induced oocyte apoptosis in vitro. Mol Endocrinol 1999; 13:841-850.
9. Matova N, Cooley L. Comparative aspects of animal oogenesis. Dev Biol 2001; 231:291-320.
10. Hussein MR. Apoptosis in the ovary: molecular mechanisms. Hum Reprod Update 2005; 11:162-177.
11. Janz DM, Van Der Kraak G. Suppression of apoptosis by gonadotropin, 17beta-estradiol, and epidermal growth factor in rainbow trout preovulatory ovarian follicles. Gen Comp Endocrinol 1997; 105:186-193.
12. Wood AW, Van Der Kraak GJ. Apoptosis and ovarian function: novel perspectives from the teleosts. Biol Reprod 2001; 64:264-271.
13. Janz DM, McMaster ME, Munkittrick KR, Van der Kraak G. Elevated ovarian follicular apoptosis and heat shock protein-70 expression in white sucker exposed to bleached kraft pulp mill effluent. Toxicol Appl Pharmacol 1997; 147:391-398.
14. Uchida D, Yamashita M, Kitano T, Iguchi T. An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal. Comp Biochem Physiol A Mol Integr Physiol 2004; 137:11-20.
15. Wood AW, Van Der Kraak G. Yolk proteolysis in rainbow trout oocytes after serum-free culture: evidence for a novel biochemical mechanism of atresia in oviparous vertebrates. Mol Reprod Dev 2003; 65:219-227.
16. Andreu-Vieyra CV, Habibi HR. Factors controlling ovarian apoptosis. Can J Physiol Pharmacol 2000; 78:1003-1012.
17. Habibi HR, Andreu-Vieyra C, Mirhadi E. Functional significance of gonadal gonadotropin-releasing hormone. In: Goos HJTh, Rastogi RK, Vaudry H, Pierantoni R (eds.), Perspective in Comparative Endocrinology: Unity and Diversity. Bologna, Italy: Monduzzi Editore; 2001:959-968.
18. Wallace RA. Vitellogenesis and oocyte growth in non-mammalian vertebrates. In: Browder LW (ed.), Developmental Biology. New York: Plenum Press; 1985:127-177.
19. Mommsen PT, Walsh PJ. Vitellogenesis and oocyte assembly. In: Hoar WS, Randall DJ, Donaldson EM (eds.), Fish Physiology, vol. 11 A. New York: Academic Press; 1988:347-406.
20. Tyler CR, Sumpter JP. Oocyte growth and development in teleosts. Rev Fish Biol Fish 1996; 6:289-318.
21. Wiegand MD. Composition, accumulation and utilization of yolk lipids in teleost fish. Rev Fish Biol Fish 1996; 6:259-286.
22. Jeon H, Blacklow SC. Structure and physiologic function of the low-density lipoprotein receptor. Annu Rev Biochem 2005; 74:535-562.
23. Schneider WJ, Nimpf J, Brandes C, Drexler M. Low-density lipoprotein receptor family: genetics, function, and evolution. Curr Atheroscler Rep 1999; 1:115-122.
24. Schneider WJ, Nimpf J. LDL receptor relatives at the crossroad of endocytosis and signaling. Cell Mol Life Sci 2003; 60:892-903.
25. Zimmerman AW, Veerkamp JH. New insights into the structure and function of fatty acid-binding proteins. Cell Mol Life Sci 2002; 59:1096-1116.
26. Haunerland NH, Spener F. Fatty acid-binding proteins-insights from genetic manipulations. Prog Lipid Res 2004; 43:328-349.
27. Watanabe M, Ono T, Kondo H. Immunohistochemical studies on the localisation and ontogeny of heart fatty acid binding protein in the rat. J Anat 1991; 174:81-95.
28. Iseki I, Amano O, Fujii H, Kanda T, Ono T. Inmunohistochemical localization of two types of fatty acid-binding protein in rat during postnatal development and in immature rat ovaries treated with gonadotropins. Anat Rec 1995; 241:235-243.
29. Nourani MR, Owada Y, Kitanaka N, Abdelwahab SA, Iwasa H, Sakagami H, Spener F, Kondo H. Localization of epidermal-type fatty acid binding protein in macrophages in advanced atretic follicles of adult mice. J Mol Hist 2005; 36:391-400.
30. Nourani MR, Owada Y, Kitanaka N, Sakagami H, Hoshi H, Iwasa H, Spener F, Kondo H. Occurence of inmunoreactivity for adipocyte-type fatty acid binding protein in degenerating granulosa cells in atretic antral follicles of mouse ovary. J Mol Hist 2005; 36:491-497.
31. Leo CP, Pisarska MD, Hsueh AJ. DNA array analysis of changes in preovulatory gene expression in the rat ovary. Biol Reprod 2001; 65:269-276.
32. Perazzolo LM, Coward K, Davail B, Normand E, Tyler CR, Pakdel F, Schneider WJ, Le Menn F. Expression and localization of messenger ribonucleic acid for the vitellogenin receptor in ovarian follicles throughout oogenesis in the rainbow trout, Oncorhynchus mykiss. Biol Reprod 1999; 60:1057-1068.
33. Liu RZ, Denovan-Wright EM, Wright JM. Structure, linkage mapping and expression of the heart-type fatty acid-binding protein gene (fabp3) from zebrafish (Danio rerio). Eur J Biochem 2003; 270:3223-3234.
34. Babin PJ. Apolipoproteins and the association of egg yolk proteins with plasma high density lipoproteins after ovulation and follicular atresia in the rainbow trout (Salmo gairdneri). J Biol Chem 1987; 282:4290-4296.
35. Blazer VS. Histopathological assessment of gonadal tissue in wild fishes. Fish Physiol Biochem 2002; 26:85-101.
36. Agulleiro MJ, Anguis V, Cañavate JP, Martínez- Rodríguez G, Mylonas CC, Cerdà J. Induction of spawning of captive-reared Senegal sole (Solea senegalensis) using different administration methods for gonadotropin-releasing hormone agonist. Aquaculture 2006; 257:511-524.
37. García-López A, Couto E, Canario AVM, Sarasquete C, Martínez-Rodríguez G. Ovarian development and plasma sex steroid levels in cultured female Senegalese sole Solea senegalensis. Comp Biochem Physiol A Mol Integr Physiol 2007; 146:342-354.
38. Davail B, Pakdel F, Bujo H, Perazzolo LM, Waclawek M, Schneider WJ, Le Menn F. Evolution of oogenesis: the receptor for vitellogenin from the rainbow trout. J Lipid Res 1998; 39:1929-1937.
39. André M, Ando S, Ballagny C, Durliat M, Poupard G, Briançon C, Babin PJ. Intestinal fatty acid binding protein gene expression reveals the cephalocaudal pattering during zebrafish gut morphogenesis. Int J Dev Biol 2000; 44:249-252.
40. Marza E, Barthe C, Andre M, Villeneuve L, Helou C, Babin PJ. Developmental expression and nutritional regulation of a zebrafish gene homologous to mammalian microsomal triglyceride transfer protein large subunit. Dev Dyn 2005; 232:506-518.
41. Avarre JC, Lubzens E, Babin PJ. Apolipocrustacein, formerly vitellogenin, is the major egg yolk precursor protein in decapod crustaceans and is homologous to insect apolipophorin II/I and vertebrate apolipoprotein B. BMC Evol Biol 2007; 7:3.
42. Guindon S, Lethiec F, Duroux P, Gascuel O. PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 2005; 33:W557-W559.
43. Abascal F, Zardoya R, Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005; 21:2104-2105.
44. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003; 19:1572-1574.
45. Morais S, Knoll-Gellida A, André M, Barthe C, Babin PJ. Conserved expression of alternative splicing variants of peroxisomal acyl-CoA oxidase 1 in vertebrates and developmental and nutritional regulation in fish. Physiol Genomics 2007; 28:239-252.
46. Bogerd J, Babin PJ, Kooiman FP, André M, Ballagny C, Van Marrewijk WJA, Van der Horst D. Molecular characterization and gene expression in the eye of the apolipophorin II/I precursor from Locusta migratoria. J Comp Neurol 2000; 427:546-558.
47. Knoll-Gellida A, André M, Gattegno T, Forgue J, Admon A, Babin PJ. Molecular phenotype of zebrafish ovarian follicle by serial analysis of gene expression and proteomic profiling, and comparison with the transcriptomes of other animals. BMC Genomics 2006; 7:46.
48. Femandez-Trujillo MA, Porta J, Borrego JJ, Alonso MC, Alvarez MC, Bejar J. Cloning and expression analysis of Mx cDNA from Senegales sole (Solea senegalensis). Fish Shellfish Immunol 2006; 21:577-582.
49. Yuan JS, Reed A, Chen F, Steward CN Jr. Statistical analysis of real-time PCR data. BMC Bioinformatics 2006; 7:85.
50. Lee PD, Sladek R, Greenwood CMT, Hudson TJ. Control genes and variability: absence of ubiquitous reference transcripts in diverse mammalian expression studies. Genome Res 2002; 12:292-297.
51. Hill AA, Brown EL, Whitley MZ, Tucker-Kellogg G, Hunter CP, Slonim DK. Evaluation of normalization procedures for oligonucleotides array data based on spiked cRNA controls. Genome Biol 2001; 2:0055.1-0055.13.
52. Van de Peppel J, Kemmeren P, van Bakel H, Radonjic M, van Leenen D, Holstege FC. Monitoring global messenger RNA changes in externally controlled microarrays experiments. EMBO Rep 2003; 4:387-393.
53. Kanno J, Aisaki K, Igarashi K, Nakatsu N, Ono A, Kodama Y, Nagao T. "Per cell" normalization method for mRNA measurement by quantitative PCR and microarrays. BMC Genomics 2006; 7:64.
54. Bujo H, Hermann M, Kaderli MO, Jacobsen L, Sugawara S, Nimpf J, Yamamoto T, Schneider WJ. Chicken oocyte growth is mediated by an eight ligand binding repeat member of the LDL receptor family. EMBO J 1994; 13:5165-5175.
55. Bujo H, Yamamoto T, Hayashi K, Hermann M, Nimpf J, Schneider WJ. Mutant oocytic low density lipoprotein receptor gene family member causes atherosclerosis and female sterility. Proc Natl Acad Sci USA 1995; 92:9905-9999.
56. Perry MM, Gilbert AB. Yolk transport in the ovarian follicle of the hen (Gallus domesticus): lipoprotein-like particles at the periphery of the oocyte in the rapid growth phase. J Cell Sci 1979; 39:257-272.
57. Takahashi S, Kawarabayasi Y, Nakai T, Sakai J, Yamamoto T. Rabbit very low density lipoprotein receptor: a low density lipoprotein receptor-like protein with distinct ligand specificity. Proc Natl Acad Sci U S A 1992; 89:9252-9256.
58. Bujo H, Lindstedt KA, Hermann M, Dalmau LM, Nimpf J, Schneider WJ. Chicken oocytes and somatic cells express different splice variants of a multifunctional receptor. J Biol Chem 1995; 270:23546-23551.
59. Nimpf J, Schneider WJ. The VLDL receptor: an LDL receptor relative with eight ligand binding repeats, LR8. Atherosclerosis 1998; 141:191-202.
60. Iijima H, Miyazawa M, Sakai J, Magoori K, Ito MR, Suzuki H, Nose M, Kawarabayasi Y, Yamamoto TT. Expression and characterization of a very low-density lipoprotein receptor variant lacking the O-linked sugar region generated by alternative splicing. J Biochem 1998; 124:747-755.
61. Magrané J, Casaroli-Marano RP, Reina M, Gåfvels M, Vilaró S. The role of O-linked sugars in determining the very low-density lipoprotein receptor stability or release from the cell. FEBS Lett 1999; 451:56-62.
62. Okabayashi K, Shoji H, Nakamura T, Hashimoto O, Asashima M, Sugino H. cDNA cloning and expression of the Xenopus laevis vitellogenin receptor. Biochem Biophys Res Commun 1996; 224:406-413.
63. Stifani S, Le Menn F, Rodriguez JN, Schneider WJ. Regulation of oogenesis: the piscine receptor for vitellogenin. Biochim Biophys Acta 1990; 1045:271-279.
64. Tao Y, Berlinsky DL, Sullivan CV. Characterization of a vitellogenin receptor in white perch (Morone americana). Biol Reprod 1996; 55:646-656.
65. Hiramatsu N, Chapman RW, Lindzey JK, Haynes MR, Sullivan CV. Molecular characterization and expression of vitellogenin receptor from white perch (Morone americana). Biol Reprod 2004; 70:1720-1730.
66. Li A, Sadasivam M, Ding JL. Receptor-ligand interaction between vitellogenin receptor (VtGR) and vitellogenin (Vtg), implications on low-density lipoprotein receptor and apolipoprotein B/E. J Biol Chem 2003; 278:2799-2806.
67. Prat F, Coward K, Sumpter JP, Tyler CR. Molecular characterization and expression of two ovarian lipoprotein receptors in the Rainbow Trout, Oncorhynchus mykiss. Biol Reprod 1998; 58:1146-1153.
68. Babin PJ. Plasma lipoproteins and apolipoproteins distribution as a function of density in the rainbow trout (Salmo gairdneri). Biochem J 1987; 246:425-429.
69. Babin PJ, Vernier JM. Plasma lipoproteins in fish: a review. J Lipid Res 1989; 30:467-489.
70. Wallaert C, Babin PJ. Age-related, sex-related and seasonal changes of plasma lipoprotein concentrations in trout. J Lipid Res 1994; 35:1619-1633.
71. Babin PJ, Deryckere F, Gannon F. Presence of an extended duplication in the low density lipoprotein receptor-binding domain of apolipoprotein B. Cloning and characterization of the domain in salmon. Eur J Biochem 1995; 230:45-51.
72. Durliat M, André M, Babin PJ. Conserved protein motifs and structural organization of a fish gene homologous to mammalian apolipoprotein E. Eur J Biochem 2000; 267:549-559.
73. Poupard G, André M, Durliat M, Ballagny C, Bœuf G, Babin PJ. Apolipoprotein E gene expression correlates with endogenous lipid nutrition and yolk syncytial layer lipoprotein synthesis during fish development. Cell Tissue Res 2000; 300:251-261
74. Shen X, Steyrer E, Retzek H, Sanders EJ, Schneider WJ. Chicken oocyte growth: receptor-mediated yolk deposition. Cell Tissue Res 1993; 272:459-471.
75. Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001; 122:829-838.
76. Wang Y, Ge W. Spatial expression patterns of activin and its signaling system in the zebrafish ovarian follicle: evidence for paracrine action of activin on the oocytes. Biol Reprod 2003; 69:1998-2006.
77. Donato DM, Hiramatsu N, Arey KM, Hiramatsu K, Donato DM, Kennedy AM, Morton CL, Hara A, Sullivan CV. Atresia in temperate basses: cloning of hatching enzyme (choriolysin) homologues from atretic ovaries. Fish Physiol Biochem 2003; 28:329-330.
78. Walzem RL, Davis PA, Hansen RJ. Overfeeding increases very low density lipoprotein diameter and causes the appearance of a unique lipoprotein particle in association with failed yolk deposition. J Lipid Res 1994; 35:1354-1366.
79. Flower DR. The lipocalin protein family: structure and evolution. Biochem J 1996; 318:1-14.
80. Storch J, Thumser AEA. The fatty acid transport function of fatty acid-binding proteins. Biochim Biophys Acta 2000; 1486:28-44.
81. Chmurzynska A. The multigene family of fatty acid-binding proteins (FABPs): function, structure and polymorphism. J Appl Genet 2006; 47:39-48.
82. Richieri GV, Ogata RT, Zimmerman AW, Veerkamp JH, Kleinfeld AM. Fatty acid binding proteins from different tissues show distinct patterns of fatty acid interactions. Biochem 2000; 39:7197-7204.
83. Hanhoff T, Lücke C, Spener F. Insights into binding of fatty acids by fatty acid binding proteins. Mol Cell Biochem 2002; 239:45-54.
84. Hertzel AV, Bernlohr DA. The mammalian fatty acid-binding protein multigene family: molecular and genetic insights into function. Trends Endocrinol Metab 2000; 11:175-180.
85. Sharma MK, Liu RZ, Thisse C, Thisse B, Denovan-Wright EM, Wright JM. Hierarchical subfunctionalization of fabpla, fabp1b and fabp10 tissue-specific expression may account for retention of these duplicated genes in the zebrafish (Danio rerio) genome. FEBS J 2006; 273:3216-3229.
86. Vayda ME, Londraville RL, Cashon RE, Costello L, Sidell BD. Two distinct types of fatty acid-binding protein are expressed in heart ventricle of Antartic teleost fishes. Biochem J 1998; 330:375-382.
87. Esteves A, Ehrlich R. Invertebrate intracellular fatty acid binding proteins. Comp Biochem Physiol C Toxicol Pharmacol 2006; 142:262-274.
88. Liu JX, Gui JF. Expression pattern and developmental behaviour of cellular nucleic acid-binding protein (CNBP) during folliculogenesis and oogenesis in fish. Gene 2005; 356:181-192.
89. Kamo A, Araki Y, Maeda K, Watanabe H. Characteristics of invasive cells found in between zona pellucida and oocyte during follicular atresia in mice. Zygote 2004; 12:269-276.