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POLYGLUTAMINE TRACT EXPANSION INCREASES PROTEIN S-NITROSYLATION and the BUDDING YEAST ZYGOTE TRANSCRIPTOME by CHUN-LUN NI

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POLYGLUTAMINE TRACT EXPANSION INCREASES PROTEIN S-NITROSYLATION and the BUDDING YEAST ZYGOTE TRANSCRIPTOME by CHUN-LUN NI i POLYGLUTAMINE TRACT EXPANSION INCREASES PROTEIN S-NITROSYLATION AND THE BUDDING YEAST ZYGOTE TRANSCRIPTOME by CHUN-LUN NI Submitted in partial fulfillment of the requirements For the degree of Doctor of Philosophy Dissertation Advisor: Dr. Alan M. Tartakoff Cell Biology Program, Department of Molecular Biology and Microbiology CASE WESTERN RESERVE UNIVERSITY January, 2017 CASE WESTERN RESERVE UNIVERSITY SCHOOL OF GRADUATE STUDIES We hereby approve the dissertation of CHUN-LUN NI Candidate for the Doctor of Philosophy degree. (signer) Piet A. J. de Boer, Ph.D. (chair of the committee) Alan M. Tartakoff, Ph.D. Cathleen R. Carlin, Ph.D. Thomas T. Egelhoff, Ph.D. Xin Qi, Ph.D Man-Sun Sy, Ph.D. (Date) November, 2016 i Table of Contents List of Tables vii List of Figures and Supplementary Figures viii Acknowledgements xii List of Abbreviations xiv Abstract xvi Chapter 1 “Introduction of Huntington’s disease and Huntingtin regulation.” 1 1-1. Genetics of Huntington’s disease (HD) 1 1-1-1. CAG trinucleotide expansion links to HD 2 1-1-2. Polyglutamine expansion and Huntingtin aggregation 2 1-1-3. Evolutionary conservation and the HEAT repeat motif 3 1-2. Huntingtin and cellular physiology 4 1-2-1. Embryogenesis 5 1-2-2. BDNF transport and expression 6 1-2-3. Mitochondrial fragmentation 7 1-2-4. Protein-protein interaction 8 1-3. Huntingtin is regulated by posttranslational modifications 10 ii 1-3-1. Proteolysis 11 1-3-2. Ubiquitination and SUMOylation 13 1-3-3. Phosphorylation 15 1-3-4. Acetylation 19 1-3-5. Myristoylation 19 1-3-6. S-palmitoylation 20 Chapter 2 “Introduction of cysteine modifications” 28 2-1. Overview of cysteine modifications 28 2-2. S-nitrosylation 29 2-3. S-acylation 34 2-4. S-nitrosylation and other posttranslational modifications 36 2-5. Cysteine modifications of the HEAT repeat motif 37 Chapter 3 “Polyglutamine expansion increases protein S-nitrosylation” 40 3-1. Discovery of Huntingtin S-nitrosylation 40 3-2. PolyQ expansion increases protein S-nitrosylation 41 3-2-1. PolyQ expansion increases Htt S-nitrosylation 41 3-2-2. PolyQ expansion increases Ataxin-1 S-nitrosylation 42 iii 3-2-3. PolyQ-dependent high molecular weight species are highly 43 cysteine-modified 3-3. S-nitrosylation and S-acylation occur at multiple sites of Htt 44 3-3-1. Htt N548 fragment S-nitrosylation and S-acylation 44 3-3-2. Full-length Htt S-nitrosylation and S-acylation 45 3-3-3. Identification of a major site of S-nitrosylation and S-acylation 46 3-3-4. Htt Phosphorylation in response to nitric oxide donor treatment 46 3-4. Polyglutamine-induced S-nitrosylation is not a global effect 47 3-4-1. PolyQ-expanded Htt does not change global S-nitrosylation and 47 S-acylation 3-4-2. PolyQ-expanded Htt does not affect gross S-nitrosylation and 47 S-acylation of normal Htt Chapter 4 “Interaction of Huntingtin and nitric oxide synthases (NOS)” 66 4-1. NOS expression increases Htt inclusions 66 4-2. PolyQ-expansion does not markedly increase NOS-Htt interaction 67 Chapter 5 ” Discussion: Polyglutamine expansion and protein S-nitrosylation” 73 5-1. PolyQ modulates specificity of S-nitrosylation and S-acylation 73 iv 5-2. S-Acylation and S-palmitoylation 73 5-3. Inspecting a S-nitrosylated HEAT repeat motif of Htt 74 5-4. Significance of S-nitrosylation of Htt 75 5-5. Future directions 79 Chapter 6 “Zygote formation in S. cerevisiae” 85 6-1. Cell-cell fusion and budding yeast zygote formation 85 6-1-1. Two mating types of budding yeast and the pheromone response 86 6-1-2. Cell membrane fusion and nuclear envelope fusion 87 6-1-3. The yeast spindle pole body 88 6-1-4. Karyogamy deficiency 89 6-1-5. Ploidy and chromosome tethering 90 6-2. Transcriptome profiles of yeast zygotes 92 6-2-1. Budding yeast zygote purification and transcriptome analysis 92 6-2-2. Genetic determinants of budding yeast cell types 92 6-2-3. The pheromone response transcriptome 94 6-2-4. Zygote-specific transcriptome 97 6-3. Discussion 101 v 6-4. Future directions 102 Appendix “Materials & Methods” 130 A1. Reagents 130 A2. Mammalian cell culture and recombinant protein expression 131 A3. Mouse tissues 132 A4. Plasmids used in this study 132 A5. Site-directed mutagenesis 133 A6. Detection of S-nitrosylation and S-acylation by resin-assisted capture 133 A7. Detection of S-nitrosylation and S-acylation sites by LC-MS/MS 134 A8. MS data analysis 136 A9. Fluorescent microscopy study of EGFP-tagged Htt N548 inclusions 137 A10. Htt HEAT repeat motif simulation 137 A11. Yeast strain growth and zygote purification 138 A12. RNA purification and microarray analysis 139 A13. Microarray data analysis 140 A14. Gene Ontology (GO) analysis 141 Bibliography 151 vi List of Tables Table 1-1 Htt-interacting proteins 25 Table 1-2 Age- and cerebellum-specific interactomes in HD mouse model 26 Table 1-3 Htt posttranslational modifications (PTMs) 27 Table 3-1 Summary of SNO and S-acylation sites in Htt N548Q15 and 63 N548Q128 Table 3-2 Summary of increased SNO and phosphorylation of Htt 65 N548Q15 by the nitric oxide donor eCysNO Table 6-1 Spindle pole body genes 115 Table 6-2 Pheromone-responsive genes (top 100) 116 Table 6-3 A subset of pheromone-responsive genes 119 Table 6-4 Zygote-specific genes 120 Table 6-5 Zygote-specific genes (ordered by type) 125 Table 6-6 Additional Type I zygote-specific genes 126 Table 6-7 Type II-IV zygote-specific genes with manually-clustered 127 functions Table 6-8 Peak expression of zygote-specific genes in haploid cells 128 vii List of Figures and Supplementary Figures Figure 1-1 Htt is a conserved protein 22 Figure 1-2 Full-length Htt, Htt N-terminal fragment and posttranslational 24 modifications Figure 2-1 Reduced form of glutathione (GSH), thioredoxin (Trx), or 39 coenzyme A (CoA) denitrosylates SNO modifications via transnitrosylation Figure 3-1 Htt constructs 49 Figure 3-2 PolyQ expansion increases S-nitrosylation of Htt 50 Figure 3-3 PolyQ expansion increases S-nitrosylation of Ataxin-1 52 Figure 3-4 PolyQ expansion in Ataxin-1 and Htt N548 proteins increases 54 S-nitrosylated and S-acylated high molecular weight (HMW) species Figure 3-5 The high molecular weight (HMW) species of Ataxin-1Q85 do 56 not disappear at 37ºC incubation with sample buffer Figure 3-6 Summary of the SNO and S-acylation sites identified by 57 LC-MS/MS viii Figure 3-7 The fragment beyond the N-terminal region is S-nitrosylated and 58 S-acylated Figure 3-8 The C214S mutation reduces Htt S-nitrosylation and S-acylation 59 in the context of the normal polyQ tract Figure 3-9 Expression of polyQ-expanded Htt does not significantly increase 60 S-nitrosylation and S-acylation of global proteins Figure 3-10 Expression of polyQ-expanded Htt does not significantly increase 61 S-nitrosylation and S-acylation of wild-type Htt Figure 4-1 Co-expression of nitric oxide synthase (NOS) promotes Htt N548 68 inclusion formation Figure 4-2 Inclusions of N548-EGFP in cells expressing nitric oxide 70 synthase Figure 4-3 NOS co-expansion increases S-nitrosylation of Htt N548Q15 and 71 NOS-N548 interaction is not significantly affected by polyQ expansion Figure 5-1 Local environment of S-nitrosylated cysteine residues of Htt 80 Figure 5-2 Flanking sequences of S-nitrosylated cysteine residues of Htt 81 ix Figure 5-3 Full-length Htt is S-nitrosylated in mouse tissues and polyQ 82 expansion increases S-nitrosylation of full-length Htt expressed in neuron-like PC12 cells Figure 5-4 Cellular dysfunctions result from Htt oligomers 84 Figure 6-1 Life cycle of budding yeast (S. cerevisiae) 103 Figure 6-2 Structure and protein components of budding yeast spindle pole 105 body Figure 6-3 Yeast cell-type specificity regulation 106 Figure 6-4 Upregulated haploid MATa- and MATα-specific genes that are 107 identified in both previous studies and in this study Figure 6-5 Downregulated genes in diploid cells that are identified in both 108 previous studies and in this study Figure 6-6 Pheromone-responsive genes identified in both studies and their 109 expression profiles Figure 6-7 Zygote-specific genes and clustered gene functions 111 Figure 6-8 Identified genes whose products are involved in the chromosome 113 organization and segregation x Figure 6-9 Identified genes whose products are involved in the respiratory 114 chain of mitochondria Figure S1 Detection of protein S-nitrosylation by SNO-RAC and protein 142 S-acylation by acyl-RAC Figure S2 Determination of S-nitrosylated and S-acylated cysteine residues 144 by Mass spectrometry (MS) Figure S3 MS/MS analysis 146 Figure S4 Separation of yeast zygote cells and pheromone-stimulated 150 haploid cells by flow cytometry xi Acknowledgements First of all, I would like to thank Dr. Tartakoff for supporting me through these years to develop this thesis. I appreciate the committee members (Dr. de Boer, Dr. Carlin, Dr. Egelhoff, Dr. Qi, and Dr. Sy), who have made great efforts to help me improve the organization of this thesis. For the S-nitrosylation study, I would like to thank Dr. Stamler and his team, especially Dr. Seth, Dr. Fonseca, and Dr. Hayashi. As to the mass spectrometry, I would like to thank Dr. Wang in the Center for Proteomics and Bioinformatics, CWRU. I also thank Dr. Xiao in the Department of Pathology for the structure simulation and suggestions. I feel grateful to Dr.
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