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Modeling the Evolutionary Loss of Erythroid Genes by Antarctic Icefishes: Analysis of the Hemogen Gene Using Transgenic and Mutant Zebrafish

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Modeling the Evolutionary Loss of Erythroid Genes by Antarctic Icefishes: Analysis of the Hemogen Gene Using Transgenic and Mutant Zebrafish Modeling the evolutionary loss of erythroid genes by Antarctic icefishes: analysis of the hemogen gene using transgenic and mutant zebrafish by Michael J. Peters B.S. in Biology, University of New Hampshire A dissertation submitted to The Faculty of the College of Science of Northeastern University in partial fulfillment of the requirements for the degree of Doctor of Philosophy June 4, 2018 Dissertation directed by H. William Detrich, III Professor of Marine Molecular Biology and Biochemistry 1 Dedication For my Oma Oswald, who started this journey with me. 2 Acknowledgments I would like to thank my advisor, Dr. H William Detrich III, for encouraging me to be innovative and to pursue cutting-edge research. I thank the members of my committee, Drs. Erin Cram, Rebeca Rosengaus, Steven Vollmer, and Leonard Zon for their many helpful suggestions. I enjoyed working alongside Sandra Parker and Carmen Elenberger and appreciate their support. I also enjoyed working with many students including Caroline Benavides, Carolyn Dubnik, Carmen Elenberger, Laura Goetz, Urjeet Khanwalkar, Ben Moran, Alessia Santilli, Eileen Sheehan, Margaret Streeter, Kathleen Shusdock, and Sierra Smith. I especially thank Jonah Levin, who joined the lab as a high school student and has since continued working with me. I thank Corey Allard and Drs. Donald Yergeau and Jeffrey Grim for collecting samples that I used in my studies. I owe thanks to the staff of the Marine Science Center for their support, including Roberto Valdez, Sonya Simpson, Heather Sears, David Dawson, and Ryan Hill. I thank Drs. Joseph Ayers and Justin Ries for use of their facilities and Drs. Isaac Westfield and Ryan Myers for help with scanning electron microscopy. I thank Drs. Camille Berthelot, Melody Clark, James Monaghan, and Leonard Zon for valuable discussions and providing important datasets and materials. I thank Dr. Jill de Jong and her lab for inspiring my interest in zebrafish research. I was pushed to my best by my fellow graduate students at Northeastern University. I am especially grateful to my Mom and Dad for their unending support and for reading every word I write. I am grateful to my siblings Sarah, Katie, Ryan, and Zachary for inspiring me with their passions and positive energy. 3 Abstract of Dissertation The Antarctic icefishes (Channichthyidae) are the only vertebrate taxon whose species do not produce red blood cells, thereby providing a natural mutant model to study the regulators of blood development and disease. To identify novel regulators of erythropoiesis, I compared RNA-Seq transcriptomes from red- and white-blooded notothenioids. I find that both icefishes and their sister taxon, the dragonfishes (Bathydraconidae), model beta-spectrin mutated spherocytic anemia. Icefishes appear to have evolved morph-biased changes in expression of hematopoietic regulatory genes, including down-regulation of the histone acetyltransferase p300 and overexpression of histone deacetylase 1b. In icefishes, I characterize a frameshift mutation that truncates the P300-binding domain of Hemogen, an important erythroid transcription factor. Tol2 and CRISPR/Cas9-generated transgenic zebrafish lines reveal that hemogen is expressed in hematopoietic, renal, neural, and reproductive tissues. I find that two conserved non-coding elements differentially contribute to hemogen expression in primitive and definitive waves of hematopoiesis. CRISPR-generated mutant zebrafish lines, which replicate the C-terminal mutation in icefish hemogen, show severe anemia and growth defects. Furthermore, I show that the function of zebrafish Hemogen is dependent on acidic residues within the TAD. Thus, Antarctic icefishes evolved an intricate system for repression of erythropoiesis that is caused in part by the loss of Hemogen function. 4 Table of Contents Dedication 2 Acknowledgments 3 Abstract of Dissertation 4 Table of Contents 5 List of Figures 6 List of Tables 9 List of Symbols 10 List of Genes 14 Chapter 1: Morph-biased gene expression and sequence divergence typifies disease-like traits of Antarctic icefishes 25 Chapter 2: Divergent Hemogen genes of teleosts and mammals share conserved roles in erythropoiesis: Analysis using transgenic and mutant zebrafish 87 Chapter 3: Erythroid gene discovery using the erythrocyte-null Antarctic icefishes 157 Conclusion 196 References 200 5 List of Figures Introduction Figure 1 Erythropoiesis in the zebrafish 19 Figure 2 Comparison of red- and white-blooded notothenioids 24 Chapter 1 Figure 1 Peripheral blood smears from Antarctic notothenioid fishes 32 Figure 2 Expression profile heatmap of differentially expressed genes 36 Figure 3 Gene ontology enrichment for differentially expressed genes 40 Figure 4 Association networks for DE genes in the icefish head kidney 44 Figure 5 Three tissue-specific clusters of hematopoietic genes are differentially expressed in the head kidneys of Ps. georgianus and P. charcoti 48 Figure 6 Differential expression of hematopoietic regulators 52 Figure 7 Deleterious substitutions in erythroid genes from icefishes 55 Figure 8 The dragonfish P. charcoti is a natural mutant model for beta-spectrin mutated spherocytic anemia 57 Figure 9 Functional mutations occur in the interaction domains of Hemogen, Gata1, and P300 64 Figure 10 Whole protein acetylation in the head kidneys of red- and white-blooded notothenioids 68 6 Chapter 2 Figure 1 Zebrafish si:dkey-25o16.2 and human hemogen are orthologous and encode related proteins that differ in size 93 Figure 2 hemogen expression in zebrafish embryos 99 Figure 3 Alternative promoters drive hemogen expression in hematopoietic and nonhematopoietic tissues in zebrafish 103 Figure 4 Conserved elements in the zebrafish hemogen promoter are predicted targets for transcription factors 108 Figure 5 Gata1 binds distal and proximal promoter elements to regulate hemogen expression in zebrafish 111 Figure 6 Promoter elements have distinct roles in driving hematopoietic, renal, and testicular expression of hemogen in transgenic Tg(hemgn:mCherry) zebrafish 115 Figure 7 Morpholino targeting of hemogen inhibits erythropoiesis in embryonic zebrafish 118 Figure 8 CRISPR/Cas9 mutagenesis of the third exon of zebrafish hemogen impairs primitive and definitive erythropoiesis 124 Chapter 3 Figure 1 The erythroid gene hemogen is mutated in Antarctic icefishes 161 Figure 2 hemogen is expressed in hematopoietic, renal, and neural tissues in red- blooded notothenioids 164 7 Figures 3 A truncated isoform of hemogen is highly expressed in icefishes and is translated 169 Figure 4 Overexpression of icefish hemogen in zebrafish blocks primitive erythropoiesis 172 Figure 5 A novel MABP-containing protein (mabpcp) is an RBC-specific gene that was lost in icefishes 174 Figure 6 Modeling a truncated cd33-related Siglec (cd33rSig) from icefishes in mutant zebrafish 180 8 List of Tables Chapter 1 Table 1 Hematopoietic genes are differentially expressed in the icefish head kidney 84 Table 2 GO enrichment of genes under different selective pressures in two red- and two white-blooded notothenioids 84 Table 3 GO enrichment for genes with deleterious substitutions found in two white- blooded icefishes but not in two red-blooded notothenioids 85 Table 4 Table of primers 85 Table 5 Icefishes have predicted deleterious substitutions in targets of human diseases 86 Chapter 2 Table S1 Sequences of primer and oligonucleotides used in experiments 156 Chapter 3 Table S1 Primer Sequences 194 Table S2 Oligos for CRISPR gRNA template 195 9 List of Symbols AGM Aorta gonad mesonephros ALL Acute lymphocytic leukemia AML Acute myeloid leukemia ATP Adenosine triphosphate B-ALL B-cell acute lymphoblastic leukemia BWS Beckwith-Wiedemann syndrome bZIP Basic leucine zipper domain CBF-AML Core binding factor acute myeloid leukemia CC Coiled coil domain CHT Caudal hematopoietic tissue Ce Corpus cerebelli CL-XPosure Clear-blue X-ray film CLL Chronic lymphocytic leukemia CML Chronic myeloid leukemia CMP Common myeloid progenitor COFS Cerebro oculo facio skeletal syndrome CRISPR Clustered Regularly Interspaced Short Palindromic Repeats CT domain C-terminal cystine knot-like domain CT-ZF C-terminal zinc finger CV Caudal vein Cyto Cytoplasmic domain C2H2 Cys2-His2 zinc finger 10 DA Dorsal aorta DBA Diamond-Blackfan anemia DED1 Death effector domain DLBCL Diffuse large B-cell lymphoma DS-AMKL Acute megakaryoblastic leukemia in Down syndrome ECL Enhanced chemiluminescence EGFP Enhanced green fluorescent protein G Glomerulus HCP Hereditary Coproporphyria HDR Homology directed repair HK Head kidney HNSCC Head and neck squamous cell carcinoma HRP Horseradish peroxidase HS Hereditary spherocytic anemia ICM Intermediate cell mass Ig Immunoglobulin IgG Immunoglobulin G ITIM Immunoreceptor tyrosine-based inhibition motif LDS Lithium dodecyl sulfate MAE Myoclonic astatic epilepsy MABP MVB12-associated beta prism domain MHB Midbrain-hindbrain-boundary MO Medulla oblongata 11 MPN Myeloproliferative neoplasms NH-terminus Amino-terminus NHEJ Non-homologous end joining NLS Nuclear localization signal PBI Peripheral blood island PD Pronephric ducts PHD Plant homeodomain ProE Proerythroblast PTK Protein tyrosine kinase PVDF Polyvinylidene fluoride RING-finger Really interesting new gene finger domain SCN Severe congenital neutropenia SDS-PAGE Sodium dodecyl sulfate-polyacrylamide gel electrophoresis Se Sertoli cells Siglec Sialic acid-binding immunoglobulin-type lectin SNF Sucrose non-fermentable ST Seminiferous tubules TAD Transactivation domain TALEN Transcription activator-like
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