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Josette Bangcaya Thesis IGF-I, IGF-II and IGF-IR expression as molecular markers for egg quality in mullet and grouper Josette Pesayco Bangcaya Bachelor of Science in Fisheries School of Life Science Queensland University of Technology Brisbane, Queensland Australia A dissertation submitted for the degree of Masters in Applied Science (Research) 2004 2 Keywords: Insulin-like growth factor (IGF)-I, IGF-II, IGF-I Receptor, egg quality, vitellogenin, enzyme-linked immunosorbent assay, quantitative polymerase chain reaction, mullet, grouper 3 ABSTRACT Common measures of egg quality have been survival to specific developmental stages, higher hatching rate of fertilized eggs and final production of fry. Determinants of egg quality are variable among and between teleost species and no common unified criteria have been established. Maternally inherited genes influence egg quality and early embryo development is partially programmed by the messenger ribonucleic acid (mRNA). Among the genes, the insulin family is important for growth functions and the presence of their transcripts in the ovary, oocytes and embryos implies their involvement during the reproductive process and their relevance to egg quality. The insulin-like growth factor (IGF) system has three components, the ligands IGF-I and II, the IGFBPs (insulin-like growth factor binding proteins) and the IGF receptors that mediate biological activity of the ligands. Vitellogenin (Vtg) is the major source of nutrients for the developing embryo and elevated levels in female fish plasma signals gonadal development preceding spawning. In oviparous fish where the developing embryo is dependent on the stored food in the yolk, vitellogenin levels in the egg could indicate its capability to support embryonic growth. This study aimed to develop molecular tools, specifically probes for IGF-I, IGF-II and IGF-IR, for the evaluation of fish egg quality. These probes would be used to determine expression levels of IGF-I, IGF-II and IGF-IR during egg development to assess their potential as molecular indicators for egg quality. In addition, this study also aimed to establish an enzyme-linked immunoassay (ELISA) for quantifying Vtg in fish eggs and determine if differences in Vtg levels could be linked to fertilization and hatching success. Through reverse-transcription polymerase chain reaction (RT-PCR) putative complementary deoxyribonucleic acid (cDNA) fragments of IGF-I, IGF-II and IGF-IR were cloned and sequenced from mullet (Mugil cephalus) and grouper (Epinephelus coioides). The relative expression ratio of the three genes in the eggs of mullet and grouper were assayed by quantitative PCR (QPCR) and calculated using the Pfaffl 4 method (Pfaffl, 2001). Levels of vitellogenin in different batches of mullet eggs were quantified by ELISA. Spawned eggs of grouper were grouped into low (<60%) or high (>60%) fertilization rate (FR) and the fertilized eggs that were incubated until hatching were grouped into medium (>90%) or high (>90%) hatching rate (HR). Samples were categorized into sinking eggs, late embryo and hatched larvae. Relative expression ratio of IGF-II was significantly high (P<0.01) compared to IGF-I and IGF-IR in all samples examined. All three genes were strongly expressed in sinking eggs compared to either late embryo or hatched larvae. However, there was no significant interaction effect between the genes and the samples analyzed. Mullet samples all came from a high FR and high HR group and were categorized into sinking, multicell stage, blastula, gastrula, late embryo and hatched larvae. There was a significant interaction effect (P<0.01) between gene and stage, showing that genes are differentially expressed during embryonic development. IGF-II was strongly expressed relative to the other genes in all stages examined and was highest during the gastrula stage. Vtg levels were examined in mullet oocytes and egg samples that were grouped into 4; oocytes from females that subsequently spawned, had fertilized eggs which hatched (Group A); oocytes from females that did not spawn, therefore no fertilization and no hatching (Group B); eggs that were stripped, artificially fertilized but no hatching (Group C); and eggs that were spawned, assumed to be fertilized but did not hatch (Group D). Group A showed a trend of higher Vtg levels than the other three but this result was not statistically significant. 5 TABLE OF CONTENTS Page number Paragraph of key words 2 Abstract 3 List of tables 7 List of figures 8 List of abbreviations 9 Statement of original authorship 11 Acknowledgement list 12 Chapter 1. Introduction 14 Egg quality 16 Insulin-like growth factors 20 Quantitative polymerase chain reaction 25 Enzyme-linked immunosorbent assay (ELISA) 26 Chapter 2. Materials and Methods: Molecular Tools Development 28 Animals and egg samples 28 Spawning and egg collection 29 Gene cloning and sequencing 30 Quantitative polymerase chain reaction assay 37 Vitellogenin purification and ELISA development 40 Chapter 3. Materials and Methods: Molecular Tools Application 44 Quantitative polymerase chain reaction assay on eggs 44 Vitellogenin ELISA 45 Chapter 4. Results 47 Gene cloning 47 Quantitative polymerase chain reaction assay 50 Vitellogenin purification and ELISA in mullet 60 Chapter 5. Discussion and Conclusion 64 Appendix 1. Poster presented to the 6th International Marine Biotechnology Conference in Chiba, Japan (21-27 September 2003) 69 6 TABLE OF CONTENTS Page number Appendix 2. Spawning protocol for mullet 70 Appendix 3. Pfaffl formula 72 Appendix 4. Mullet and grouper egg samples 73 Bibliography 74 7 LIST OF TABLES Page number Table 1. Primer pairs used to amplify IGF-I, IGF-II and IGF-IR sequences in the respective mullet and grouper tissues 47 Table 2. Primer pairs designed for QPCR assay 53 Table 3. Master mix of reaction components for QPCR 54 Table 4. Reaction efficiencies and r2 values for QPCR 54 Table 5a. Mean relative expression ratio of target genes in grouper 57 Table 5b. Mean relative expression ratio of target genes in mullet 58 Table 6a. ANOVA of grouper data based on fertilization rate 59 Table 6b. ANOVA of grouper data based on hatching rate 59 Table 7. ANOVA of mullet egg data 60 Table 8. Log means of relative expression ratio in mullet 60 Table 9. Group means of Vtg concentration in mullet sample homogenates 63 Table 10. ANOVA of data of Vtg concentration in mullet egg homogenates 63 8 LIST OF FIGURES Page number Fig 1. Male and female mullet 15 Fig 2. Grouper 16 Fig 3a. Gel photo of amplified mullet IGF-IR cDNA fragments 49 Fig 3b. Gel photo of amplified grouper IGF-IR cDNA fragments 49 Fig 3c. Gel photo of amplified grouper IGF-I cDNA fragment 49 Fig 3d. Gel photo of amplified grouper IGF-II cDNA fragment 49 Fig 4. Alignment of IGF-IR sequence in mullet, grouper and turbot 51 Fig 5. Alignment of grouper IGF-I sequence with other fish species 52 Fig 6. Alignment of grouper IGF-II sequence with other fish species 52 Fig 7. Photomicrograph of grouper egg samples 55 Fig 8. Photomicrograph of mullet egg samples 56 Fig 9. Elution profile of purified Vtg from mullet plasma 62 Fig 10. ELISA standard curve for mullet Vtg 62 9 LIST OF ABBREVIATIONS AA arachidonic acid AGRF Australian Genome Research Facility ANOVA Analysis of Variance BIARC Bribie Island Aquaculture Research Centre bp base pairs cDNA complementary deoxyribonucleic acid Ct crossing threshold dATP 2’-deoxyadenosine 5-triphosphate dCTP 2’-deoxycytosine 5’-triphosphate dGTP 2’-deoxyguanasine 5’-triphosphate DNA deoxyribonucleic acid dNTP deoxynucleotide triphosphate dTTP 2’-deoxythymidine 5’triphosphate EBI European Bioinformatics Institute EDTA ethylenedinitro tetraacetic acid ELISA enzyme-linked immunosorbent assay EPA eicosapentanoic acid FR fertilization rate GnRHa gonadotropin releasing hormone analog HR hatching rate IGF-I insulin-like growth factor I IGF-II insulin-like growth factor II IGF-IR insulin-like growth factor I receptor IPTG isopropyl-beta-D-thiogalactopyranoside kb kilobases kD kilodalton LB Amp Luria-Bertani ampicillin LHRHa luteinizing hormone releasing hormone analog LSD Least Significant Differences mRNA messenger ribonucleic acid 10 NCBI National Center for Biotechnology Information NFC National Fisheries Centre PBS phosphate buffered saline PCR polymerase chain reaction PES polyethersulfone PMSF phenylmethylsulfonyl flouride QPCR quantitative polymerase chain reaction RNA ribonucleic acid RT-PCR reverse-transcriptase polymerase chain reaction SDS-PAGE sodium dodecyl sulfate-polyacrylamide gel electrophoresis Tm melting temperature TMB tetramethylbenzidine UDG uracil-DNA glycosylase Vtg vitellogenin X-gal 5-bromo-4-chloro-3-indolyl-ß-D-galactoside 11 STATEMENT OF ORIGINAL AUTHORSHIP The work contained in this dissertation has not been previously submitted for a degree or diploma at any other higher educational institution. To the best of my knowledge and belief, the dissertation contains no material previously published or written by another person except where due reference is made. Signed :_____________________________ Date: _______________________________ 12 ACKNOWLEDGEMENT Praise and thanks to God Almighty for the guidance and love He has showered me in accomplishing this work, His presence has always been a guiding light throughout this journey. To Drs. Joebert Toledo, Felix Ayson and Evelyn de Jesus, whose belief in my ability to make it through the unchartered waters gave me confidence to go through with this degree. To John Allwright Fellowship of Australian Centre for International Agricultural Research
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