Fluorescent Protein Approaches in Alpha Herpesvirus Research
Abstract
:1. Introduction
1.1. A Brief History of Fluorescent Proteins
1.2. Alpha Herpesviruses Strains Expressing Fluorescent Proteins and Biosensors
1.3. Fluorescent Protein Fusions to Viral Proteins in HSV-1 and PRV
Gene/Protein Name | Description/Function | Structural Role | Fusion Location | References | |
---|---|---|---|---|---|
HSV-1 | PRV | ||||
Capsid Proteins | |||||
UL17 | capsid vertex specific component | capsid | C-terminal | [42] | |
UL25 | capsid vertex specific component | capsid | internal | [43] | [44] |
UL35 VP26 | small capsid protein | capsid | N-terminal | [41,45] | [46] |
C-terminal | [47] | ||||
Tegument Proteins | |||||
UL13 | protein kinase | tegument | N-terminal | [48] | |
C-terminal | [48] | ||||
UL16 | interacts with UL21 | tegument | C-terminal | [49] | [50] |
UL21 | interacts with UL16 | N-terminal | [51] | ||
C-terminal | [52]b | ||||
UL31 | nuclear egress | tegument a | N-terminal | [53,54] | [55] |
UL36 VP1/2 | large tegument protein | tegument | N-terminal | [56] | |
C-terminal | [57] | [44] | |||
UL37 | interacts with UL36 | tegument | N-terminal | [57] | |
C-terminal | [58] | [56] | |||
UL41 VHS | RNAase | tegument | N-terminal | [59] | |
UL46 VP11/12 | most abundant tegument protein | tegument | N-terminal | [57] | |
C-terminal | [60] | [50] | |||
UL47 VP13/14 | tegument | N-terminal | [61] | [56] | |
UL48 VP16 | transactivation of viral gene expression | tegument | N-terminal | [62] | |
C-terminal | [57,62] | [56] | |||
UL49 VP22 | secondary envelopment | tegument | N-terminal | [57,63] | [56,64] |
C-terminal | [40,63] | [64] | |||
US1 ICP22 | regulation of viral gene expression | tegument | C-terminal | [65] | |
US3 | protein kinase | tegument | N-terminal | [66] | |
C-terminal | [67]b | [48,68] | |||
US10 | unknown | tegument | C-terminal | [69]c | |
ICP34.5 | tegument | N-terminal | [70] | * | |
ICP0 (EP0) | transactivation of viral gene expression, E3 ubiquitin ligase | tegument | N-terminal | [71] | |
C-terminal | [72] | [73] | |||
internal | [74] | ||||
ICP4 (IE180) | transactivation of viral gene expression | tegument | N-terminal | [75] | |
C-terminal | [76] | [77] | |||
Envelope Proteins | |||||
UL10 gM | glycoprotein M | envelope | N-terminal, intravirion | [78] | [78] |
C-terminal, intravirion | [36,79] | ||||
internal, extravirion | [36] | ||||
UL11 | lipid-anchored membrane protein | envelope | C-terminal | [49] | [49] |
UL20 | multipass transmembrane protein | envelope | [80] | ||
UL22 gH | glycoprotein H, membrane fusion | envelope | N-terminal, extravirion | [81] | |
UL27 gB | glycoprotein B, receptor binding, membrane fusion | envelope | N-terminal, extravirion | [82,83] | |
C-terminal, intravirion | [84] | ||||
UL34 | transmembrane protein, nuclear egress | envelope a | C-terminal | [85]d | |
UL43 | multipass transmembrane protein | envelope | C-terminal, intravirion | [86]d | |
UL44 gC | glycoprotein C, receptor binding | envelope | C-terminal, intravirion | [87] | |
UL49A gN | glycoprotein N | envelope | C-terminal, intravirion | [88] | |
UL51 | lipid-anchored membrane protein | envelope | C-terminal | [89] | |
UL53 gK | glycoprotein K | envelope | C-terminal, extravirion | [90]d | |
US2 | lipid-anchored membrane protein | envelope | N-terminal | [91] | |
US6 gD | glycoprotein D, receptor binding, membrane fusion | envelope | C-terminal, intravirion | [92] | [93] |
US7 gI | glycoprotein I, anterograde axonal transport | envelope | N-terminal, extravirion | [94] | |
US8 gE | glycoprotein E, anterograde axonal transport | envelope | N-terminal, extravirion | [94] | |
C-terminal, intravirion | [95] | ||||
US9 | transmembrane protein, anterograde axonal transport | envelope | N-terminal, intravirion | [37] | [79] |
2. Unique Challenges of Fluorescent Protein-based Approaches in Viruses
2.1. Structure of Virion
2.2. Genome Constraints
2.3. Evolvable and Highly Recombinogenic Genomes
3. How-To: General Strategies and Best Practices
3.1. Choice of Fluorescent Protein
3.1.1. Fluorescent Protein Dimerization
3.1.2. Fluorescent Protein Maturation Time
Fluorescent Protein | t1/2 (min) | References |
---|---|---|
Blue | ||
mTagBFP2 | 12 | [116] |
Cyan | ||
SCFP3A | 82 | [117] |
mCerulean3, mTurquoise2 | a | [118] |
Green | ||
wild-type Aequorea GFP | 37–83 b | [119,120] |
EGFP, mEGFP | 10–65 b | [120,121] |
Emerald | 8 | [120] |
mNeonGreen | <10 | [122] |
TagGFP2 | 18 | [123] |
Yellow | ||
Venus, mVenus | 28–72 b | [117,120] |
SYFP2 | 55 | [117] |
Orange | ||
mKO2 | 108 | [124] |
mOrange2 | 270 | [125] |
Red | ||
DsRed | ~600 | [9] |
mRFP1 | <60 | [9,125] |
mCherry | 15–40 b | [9,125,126] |
mStrawberry | 50 | |
TagRFP-T | 100 | [125] |
FusionRed | 130 | [127] |
Far-Red | ||
mKate2 | <20 | [126] |
mNeptune | 35 | [128] |
3.1.3. Fluorescent Protein pH Sensitivity
Compartment | pH | References |
---|---|---|
Cytoplasm | 7.2–7.4 | [129,130] |
Nucleus | 7.4–7.8 | [131,132] |
Secretory Pathway | ||
Endoplasmic Reticulum | 7.2 | [129] |
cis-Golgi | 6.7 | [129] |
trans-Golgi | 6.0 | [129] |
Secretory Vesicles | 5.2–5.7 | [129] |
Endocytic Pathway | ||
Early and Recycling Endosomes | 6.3–6.5 | [129] |
Late Endosomes | 6.0 | [129] |
Lysosomes | 5.5 | [129] |
Fluorescent Protein | pKa | Notes | Reference |
---|---|---|---|
Blue | |||
mTagBFP2 | 2.7 | [116] | |
Cyan | as a class, cyan FPs are relatively pH insensitive | ||
ECFP, mCerulean | 4.7 | [133] | |
mTFP1 | 4.3 | [134] | |
mCerulean3 | 3.2 | [135] | |
mTurquoise2 | 3.1 | [118] | |
Green | as a class, green FPs are moderately pH sensitive | ||
mEGFP, mEmerald | 6.0 | [136] | |
mNeonGreen | 5.7 | [122] | |
mTagGFP2 | 5.0 | [123] | |
T-Sapphire | 4.9 | a UV-excited green FP | |
superecliptic pHluorin | 7.2 | purposely optimized to be very pH sensitive | [137] |
Yellow | as a class, modern yellow FPs are moderately pH sensitive | ||
EYFP | 6.9 | very pH sensitive, newer variants are somewhat improved | |
mVenus, SYFP2 | 6.0 | [117,138] | |
mCitrine | 5.7 | [136] | |
Orange | |||
mKO2 | 5.0–5.5 | [125] | |
mOrange, mOrange2 | 6.5–7.5 | very pH sensitive | [125] |
Red | as a class, red FPs are relatively pH insensitive | ||
mRFP1, mCherry, mStrawberry | ≤4.5 | [9] | |
TagRFP-T | 4.0 | [125] | |
FusionRed | 4.6 | [127] | |
Far-Red | |||
mKate2 | 5.4 | [126] | |
mNeptune | 5.8 | [128] |
3.2. Choice of Fluorescent Protein Insertion Site and Linker
3.3. Choice of Excitation Light Sources
4. Case Studies: Discussion of Particular Fluorescent Protein Fusions
4.1. PRV Membrane Protein US9
4.2. HSV-1 and PRV Capsid Protein VP26
4.2.1. Compensatory Mutations that May Affect FP-VP26 Expression
4.2.2. Fluorescent Protein Dimerization
4.2.3. Assemblons
4.2.4. Description and Characterization of New VP26 Fusions in PRV
5. Comparison to Immunofluorescence
6. Beyond Traditional Fluorescence Microscopy
6.1. Fluorescent Protein Fusions as Proteomics Probes
6.2. Flow Virometry
6.3. Herpes Past the Diffraction Barrier
Acknowledgments
Conflicts of Interest
References
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Hogue, I.B.; Bosse, J.B.; Engel, E.A.; Scherer, J.; Hu, J.-R.; Del Rio, T.; Enquist, L.W. Fluorescent Protein Approaches in Alpha Herpesvirus Research. Viruses 2015, 7, 5933-5961. https://doi.org/10.3390/v7112915
Hogue IB, Bosse JB, Engel EA, Scherer J, Hu J-R, Del Rio T, Enquist LW. Fluorescent Protein Approaches in Alpha Herpesvirus Research. Viruses. 2015; 7(11):5933-5961. https://doi.org/10.3390/v7112915
Chicago/Turabian StyleHogue, Ian B., Jens B. Bosse, Esteban A. Engel, Julian Scherer, Jiun-Ruey Hu, Tony Del Rio, and Lynn W. Enquist. 2015. "Fluorescent Protein Approaches in Alpha Herpesvirus Research" Viruses 7, no. 11: 5933-5961. https://doi.org/10.3390/v7112915
APA StyleHogue, I. B., Bosse, J. B., Engel, E. A., Scherer, J., Hu, J. -R., Del Rio, T., & Enquist, L. W. (2015). Fluorescent Protein Approaches in Alpha Herpesvirus Research. Viruses, 7(11), 5933-5961. https://doi.org/10.3390/v7112915