利用核磁共振光譜分析石斑魚神經壞死病毒鞘蛋白外突出結構之動態與分子機制

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研究生：	裴翠娜 Sterbova, Petra
論文名稱：	利用核磁共振光譜分析石斑魚神經壞死病毒鞘蛋白外突出結構之動態與分子機制 An NMR investigation of the molecular mechanism of grouper nervous necrosis virus protrusion dynamics
指導教授：	章為皓 Chang, Wei-Hau 蘇士哲 Sue, Shih-Che
口試委員:	張七鳳 Chang, Chi-Fon 張雯 Chang, Wen 陳佩燁 Chen, Rita Pei-Yeh 吳育騏 Wu, Yu-Chi Eugene
學位類別：	博士 Doctor
系所名稱：	生命科學暨醫學院 - 生物資訊與結構生物研究所 Institute of Bioinformatics and Structural Biology
論文出版年：	2024
畢業學年度：	112
語文別：	英文
論文頁數：	126
中文關鍵詞：	核磁共振光譜、蛋白結構、病毒突起結構域、pH敏感蛋白、神經壞死病毒
外文關鍵詞：	nuclear magnetic resonance spectroscopy, protein structure, viral protrusion domain, pH sensitivity, nervous necrosis virus
相關次數：	點閱：1 下載：0
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由神經壞死病毒（nervous necrosis virus; NNV）引起的病毒性腦病及視網膜病（viral encephalopathy and retinopathy; VER）爆發對魚類養殖業造成了毀滅性的影響。NNV是一種來自Nodaviridae科的簡單無套膜病毒，其殼蛋白的表面包含了六十個獨特的突起。這些突起對病毒與宿主細胞的相互作用以及病毒的感染性至關重要。NNV外殼上的突起利用唾液酸來附著於細胞表面，並透過胞吞作用進入細胞。然而，對於明確的感染機制以及病毒與宿主相互作用的資訊仍然缺乏，使得抗病毒策略的開發困難重重。
NNV表面的突起結構是由外殼蛋白的三個突起結構域（protrusion domain；P-domain）所組成。現有的NNV結構顯示，這些突起結構在病毒表面上具有高動態性，且P-domain在NNV表面採取多重的構型。為了解釋NNV 感染過程中P-domain的構型資訊，我們利用核磁共振光譜分析從石斑魚NNV殼蛋白序列中分離的P-domain蛋白（胺基酸214-338）在溶液中的構型，並藉由調整酸鹼值（pH值）來模擬不同的感染階段。研究結果顯示了P-domain對pH值的敏感，在低pH環境下會引發構型變化並伴隨自我組裝。而對於以單體（monomer）形式存在於中性pH值溶液中的P-domain，依據光譜所推定的結構顯示出一個先前未識別的口袋結構，該結構以一個高活動性的長肽環（胺基酸311-330）所勾勒而出。分子對接分析顯示，該口袋結構中的胺基酸殘基可與唾液酸的末段相互作用。進一步的分子動力學模擬顯示，該口袋結構中的部分胜肽在酸性條件下轉變為β鏈，並促成形變後的P-domain形成三聚體。此外，我們發現連接P-domain和NNV外殼的鏈結蛋白在低pH值下進行不同構型間的轉換。鏈結蛋白的可塑性歸因於位於鏈結蛋白和P-domain連接處的脯胺酸（P221）發生順反異構化。
我們的研究結果揭示了NNV病毒表面突起結構因pH值變化所引發的構型轉換機制，並提供了有關病毒與宿主之間相互作用的結構新見解，此研究成果對於開發針對NNV的抗病毒水產養殖策略至關重要。

The outbreaks of viral encephalopathy and retinopathy (VER) caused by nervous necrosis virus (NNV) have had a devastating impact on the fish farming industry. NNVs are small non enveloped viruses from Nodaviridae family. The NNV capsid contains sixty distinct protrusions on the virus particle surface. These protrusions are essential for virus interactions with host cells and virus infectivity. The NNV protrusions bind to sialic acid to attach to the cell surface and to initiate virus entry to cells via endocytosis, however our understanding of the infection mechanism and virus-host interactions critical for anti-viral strategies development is limited.
The protrusions on the NNV surface are formed by three protrusion domains (P domain) of the capsid protein. The available structures of NNV revealed that protrusions are highly dynamic on the virus surface and indicated that P-domain adopts different configurations on the NNV surface. To gain an understanding of the P-domain conformations underlying NNV infection, we studied the isolated P-domain (aa 214-338) of dragon grouper NNV in solution using nuclear magnetic resonance (NMR) in pH conditions mimicking different stages of virus entry. Our results revealed that the P-domain is pH sensitive and undergoes low-pH-induced conformational change coupled with self-assembly. The P-domain is monomer at neutral pH and the determined solution structure of the P-domain monomer revealed a long flexible loop in the P-domain (amino acids 311-330) outlining a previously unidentified pocket. Molecular docking analysis showed that the terminal sialic acid inserted into this pocket and formed interactions with conserved residues delineating the binding pocket. Molecular dynamics (MD) simulations showed that part of this loop converted to a β strand under acidic conditions. This new P-domain conformation allowed formation of P domain trimer. Additionally, we discovered that a flexible linker connecting the P-domain to NNV shell interconverts between different conformations at low pH. The malleability of the linker is attributed to a cis-trans isomerisation of peptidyl bond of P221 located at the junction between linker and the P-domain. Our findings have uncovered novel pH-dependent conformational switching mechanisms underlying NNV protrusion dynamics, and have provided new structural insights into complex NNV-host interactions critical for development of strategies against NNV in aquaculture.

Abstract.......................................................................................................................................5
摘要................................................................................................................................................7
Acknowledgements................................................................................................................9
List of Abbreviations.............................................................................................................12
List of Figures...........................................................................................................................14
List of Tables.............................................................................................................................16
  Introduction.......................................................................................................................20
1    Aquaculture and VER disease..................................................................................20
2    Viruses and their classification................................................................................21
3    The Nodaviridae family..............................................................................................22
4    The capsid protein of betanodavirus....................................................................23
5    Overview of virus life cycle........................................................................................26
6    Betanodavirus cellular receptors............................................................................28
7    Non-enveloped virus entry via endocytosis......................................................28
8    Determined structures of NNV virus-like particles..........................................30
9    Thesis objectives...........................................................................................................33
  Materials and Methods..................................................................................................35
1    GNNV-P construct design, mutagenesis.............................................................35
2    GNNV-P expression and purification....................................................................36
2.1    Expression of 15N-labeled and 13C, 15N-labeled GNNV-P.....................36
2.2    Expression of U-D, 13C, 15N-labeled GNNV-P..............................................37
3    Nuclear magnetic resonance (NMR) spectroscopy.........................................37
3.1    Chemical shift resonance assignment...............................................................37
3.2    GNNV-P structure determination.......................................................................39
3.3    Hydrogen-deuterium exchange (HDX).............................................................39
3.4    Chemical shift perturbation (CSP) analysis and secondary chemical
shifts calculation........................................................................................................40
3.5    15N transverse (T2) relaxation measurement.................................................40
4    Far-UV circular dichroism (CD).................................................................................42
5    Sedimentation velocity analytical ultracentrifugation....................................42
6    Molecular dynamics simulation...............................................................................43
7    Molecular docking........................................................................................................44
  Results...................................................................................................................................45
1    GNNV-P is pH sensitive in solution........................................................................45
2    GNNV-P contains highly pH sensitive regions...................................................47
3    GNNV-P molecules form low-pH-induced oligomers in solution.............49
4    GNNV-P structure determined in solution revealed a flexible region aa
311-330.............................................................................................................................50
5    Molecular dynamics simulations predict that GNNV-P forms trimer at pH
0........................................................................................................................................52
6    Site-directed mutagenesis identified key residues at the GNNV-P trimer
interface............................................................................................................................53
7    Subregion of the GNNV-P F’-G’ loop undergoes pH dependent
conformational change...............................................................................................57
8    GNNV-P linker adopts different conformations at acidic pH.......................59
9    The open conformation of the F’-G’ loop outlines a sialic acid binding
pocket................................................................................................................................61
  Discussion.............................................................................................................................63
1    NNV P-domain undergoes pH-dependent structural transitions and self-
assembly............................................................................................................................63
2    The role of P-domain conformational change in pH sensing during NNV
endocytosis......................................................................................................................64
3    Deep pocket formed by F’-G’ loop and binding to sialic acid................67
4    The malleability of the linker connecting P-domain and S-domain...........69
  Conclusion............................................................................................................................71
  Supplementary Figures....................................................................................................72
  Supplementary Tables......................................................................................................83
  References.............................................................................................................................85
  Appendix...............................................................................................................................92
1    Cryo-EM structures of GNNV virus-like particles at different pH................92
2    Analysis of GNNV-P molecular mass at pH 5.0 by mass spectrometry.....94
3    Measurement of GNNV-P T2 relaxation time at pH 7.0 and pH 5.0
indicates GNNV P oligomer formation at low pH.............................................95
4    GNNV-P monomer-oligomer equilibrium in solution at pH 5.5..................99
5    Secondary structure analysis of GNNV-P at pH 7.0 and pH 5.0................103
5.1    GNNV-P analysis of secondary structure using backbone chemical
shifts.............................................................................................................................103
5.2    Analysis of GNNV-P secondary structure using circular dichroism
spectroscopy.............................................................................................................105
6    Comparison of 1H-15N HSQC spectra of 15N- and U-2H, 13C, 15N-
labeled GNNV-P at pH 5.0......................................................................................109
7    Analysis of GNNV-P pH sensitive residues in GNNV-P Q322A mutant.
...........................................................................................................................................111
8    The effect of salt concentration on GNNV-P oligomerization..................115
9    Buffer effect on the GNNV-P chemical shift and self-assembly at pH 6.0
...........................................................................................................................................118
10    Differential scanning calorimetry analysis of GNNV-P thermal stability at
pH 7.0 and pH 5.0....................................................................................................123
11    1H-15N HSQC spectra of GNNV-P mutants – R276A, W280A, H281Y
........................................................................................................................................124
12    1H-15N HSQC spectra of GNNV-P mutants –Q322A, I323A, L324A..125
13    1H-15N HSQC spectra of GNNV-P mutants – P326A...............................126

                                

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