Yeast Models of Amyotrophic Lateral Sclerosis Type 8 Mimic Phenotypes Seen in Mammalian Cells Expressing Mutant VAPBP56S
Abstract
:1. Introduction
2. Materials and Methods
2.1. Yeast Strains, Growth Conditions, and Reagents
2.2. Plasmids
2.3. Plate-Based Growth Assays
2.4. Kinetic Growth Assays
2.5. Fluorescence Microscopy and Image Processing
2.6. Quantification of ER Inclusion Size
2.7. Comparison of Human ALS-Linked Proteins with Putative Yeast Homologs
2.8. Statistical Analysis and Generation of SuperPlots
3. Results
3.1. Loss of SCS2 and SCS22 Causes ER Collapse and Sensitivity to ER Stress
3.2. Expression of SCS2, but Not scs2P51S, P58S, Corrects ER Morphology and Stress Sensitivity Defects in scs2∆ scs22∆ Cells
3.3. Heterologous Expression of VAPBWT, but Not VAPBP56S, Complements ER Morphology and Stress Senstitivity in scs2∆ scs22∆ Cells
3.4. Multiple ER-Resident Proteins Localize to Inclusion-like Structures in SCS-Deficient Cells
3.5. Kinetic Growth Assays Reveal Differences in Tunicamycin Sensitivity in Yeast ALS8 Model Cells
3.6. Potential Use of Yeast as a Model for Study of Other Types of ALS
4. Discussion
4.1. Yeast as a Model System for Study of Neurodegenerative Diseases
4.2. Yeast ALS8 Models May Facilitate Studies of VAPBP56S-Related Cellular Pathology
4.3. Similarities and Differences between ALS8 Models
4.4. Yeast May Provide Opportunities and Approaches for Study of Other ALS Subtypes
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Strain | Genotype | Source |
---|---|---|
W303 1 | MATa leu2-3,112 trp1-1 can1-100 ura3-1 his3-11,15 | Laboratory strain |
DPY2271 | MATa leu2-3,112::LEU2 | This study |
DPY2275 | MATa leu2-3,112::LEU2 Sec61-GFP::HIS3 | This study |
DPY2287 | MATa scs2::KANMX6 leu2-3,112::LEU2 Sec61-GFP::HIS3 | This study |
DPY2290 | MATa scs22::HPHMX4 leu2-3,112::LEU2 | This study |
DPY2295 | MATa scs22::HPHMX4 leu2-3,112::LEU2 Sec61-GFP::HIS3 | This study |
DPY2298 | MATa scs2::KANMX6 scs22::HPHMX4 leu2-3,112::LEU2 | This study |
DPY2301 | MATa scs2::KANMX6 scs22::HPHMX4 leu2-3,112::LEU2 Sec61-GFP::HIS3 | This study |
DPY2309 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:SCS2::LEU2 | This study |
DPY2311 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:SCS2::LEU2 Sec61-GFP::HIS3 | This study |
DPY2317 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:scs2P51S, P58S::LEU2 | This study |
DPY2319 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:scs2P51S, P58S::LEU2 Sec61-GFP::HIS3 | This study |
DPY2339 | MATa scs2::KANMX6 leu2-3,112::LEU2 | This study |
DPY2822 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:hsVAPB::LEU2 Sec61-GFP::HIS3 | This study |
DPY2823 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:hsVAPBP56S::LEU2 Sec61-GFP::HIS3 | This study |
DPY2854 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:hsVAPB::LEU2 | This study |
DPY2855 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:hsVAPBP56S::LEU2 | This study |
DPY2952 | MATa leu2-3,112::LEU2 Sec61-GFP::HIS3 Rtn1-mScarlet1::NATMX4 | This study |
DPY2953 | MATa scs2::KANMX6 leu2-3,112::LEU2 Sec61-GFP::HIS3 Rtn1-mScarlet1::NATMX4 | This study |
DPY2954 | MATa scs22::HPHMX4 leu2-3,112::LEU2 Sec61-GFP::HIS3 Rtn1-mScarlet1::NATMX4 | This study |
DPY2955 | MATa scs2::KANMX6 scs22::HPHMX4 leu2-3,112::LEU2 Sec61-GFP::HIS3 Rtn1-mScarlet1::NATMX4 | This study |
DPY2956 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:SCS2::LEU2 Sec61-GFP::HIS3 Rtn1-mScarlet1::NATMX4 | This study |
DPY2957 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:scs2P51S, P58S::LEU2 Sec61-GFP::HIS3 Rtn1-mScarlet1::NATMX4 | This study |
DPY2958 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:hsVAPB::LEU2 Sec61-GFP::HIS3 Rtn1-mScarlet1::NATMX4 | This study |
DPY2959 | MATa scs2::KANMX6 scs22::HPHMX4 leu2:hsVAPBP56S::LEU2 Sec61-GFP::HIS3 Rtn1-mScarlet1::NATMX4 | This study |
Plasmid | Description | Source |
---|---|---|
pRS405 | LEU2 integrating plasmid | [42] |
pRS413 | CEN HIS3 empty vector | [42] |
pRS416 | CEN URA3 empty vector | [42] |
pDP0558 | SCS2.413 [CEN HIS3] | This study |
pDP0559 | scs2P51S, P58S.413 [CEN HIS3] | This study |
pDP0562 | SCS2.405 [LEU2] | This study |
pDP0563 | scs2P51S, P58S.405 [LEU2] | This study |
pDP0900 | PSCS2-hsVAPBWT-TSCS2.416 [CEN URA3] | This study |
pDP0901 | PSCS2-hsVAPBP56S-TSCS2.416 [CEN URA3] | This study |
pDP0911 | PSCS2-hsVAPBWT-TSCS2.405 [LEU2] | This study |
pDP0912 | PSCS2-hsVAPBP56SS-TSCS2.405 [LEU2] | This study |
pHDEL | pRS416.DsRed-HDEL [CEN URA3] | [43] |
ALS Type | Human Gene (Accession) | Yeast Homolog | Identity (%) a | Human Mutation (Yeast Analog) a | Suppl. File | Refs. |
---|---|---|---|---|---|---|
ALS1 | SOD1 (NP_000445.1) | SOD1 | 54.9 | A4T/V(A4); C6F(A6); G12R(A12); G16S(G16); E21K(E21); G37R(G37); G41D/S(A42); H43R(R44); F45C(F46); H46R(H47); G72S(G73); H80R(H81); L84V(M85); G85R(G86); D90A(D91); G93A/C/R(G94); D95N(K97); E100G(K101); I104F(I105); L106V(L107); I113T(V114); V119∆ or V120∆(V118 or V119) b; L126T(L127); S134N(S135); A145T(A146); I151T(L152) | 2-1 | [45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66] |
ALS4 | SETX (AAI37351.1) | SEN1 | 23.1 | No conserved ALS-linked mutations SCA-linked c: M271I(I137); E343*(K230) d; Q653K(Q404); Q868*(N587); R1363*(N895); L1976R(I1370); L1977F(I1371); P2213L(P1622) | 2-2 | [67,68,69,70,71,72] |
ALS8 | VAPB (NP_004729.1) | SCS2 SCS22 | 26.34 28.57 | T46I(T41); P56S(P51) T46I(T38); P56S(P48) | 2-3 | [28,73] |
ALS11 | FIG4 (NP055660.1) | FIG4 | 38.03 | D53Y(E72); R183*(K195) BTOP-linked e: D783V(H776) CMT4J-linked f: L17P(L35); I41T(I59); F98fsTer102(F109); G253fsTer261(G244); E302K(E293) YVS-linked g: L175P(L187); K278WfsTer6(H269); T422NfsTer6(S422) | 2-4 | [74,75,76,77,78,79] |
ALS13 | ATXN2 (AAB19200.1) | PBP1 | 24.06 | No conserved ALS-linked mutations; (CAG)n repeat expansion (n = 27–33 in ALS13) | 2-5 | [80] |
ALS14/ FTD-ALS6 | VCP (AAI10914.1) | CDC48 | 69.48 | R155H/C(R165); R159G/S(R169); D395G(D405); D592N(D602) IBMPFD1-linked h: N91Y(N101); R95G(R105); R155P(R165); R159H(R169); R191Q(R201); A232E(A242) CMT2Y-linked i: G97E(G107); E185K(E195) | 2-6 | [81,82,83,84,85,86,87,88] |
ALS15 | UBQLN2 (NP_038472.2) | DSK2 | 30.31 | No conserved ALS-linked mutations | 2-7 | |
ALS16 | SIGMAR1 (NP_005857.1) | ERG2 | 31.6 | E102Q(E104) | 2-8 | [89] |
ALS17/ FTD-ALS7 | CHMP2B (NP_054762.2) | DID4 | 28.17 | D148Y(N152); Q165*(K170); Q206H(R224) | 2-9 | [90,91,92] |
ALS18 | PFN1 (AAA36486.1) | PFY1 | 29.03 | No conserved ALS-linked mutations | 2-10 | |
ALS20 | HNRNPA1 (NP_112420.1) | HRP1 | 33.33 | D314N(D490); N319S(N497) IBMPFD3-linked j: D314V(D490) | 2-11 | [93] |
ALS22 | TUBA4A (AAH09238.1) | TUB1 TUB3 | 74.44 72.3 | T145P(T146); R215C(R216); R320C/H(R321); A383T(S384); W407*(W408) Macrothrombocytopenia: V181M(V182), E183Q(E184) T145P(T146); R215C(R216); R320C/H(R321); A383T(S384); W407*(W408) Macrothrombocytopenia: V181M(V182), E183Q(E184) | 2-12 | [94,95] |
ALS25 | KIF5A (AAA20231.1) | SMY1 | 26.49 | No conserved ALS-linked mutations Spastic paraplegia 10: R204Q(R234); D232N(D262); G235E(G265); N256S(N286); R280C/H(R319) | 2-13 | [96,97,98,99,100] |
ALS26 | TIA1 (NP_071505.2) | PUB1 | 34.82 | No conserved ALS-linked mutations | 2-14 | |
ALS27 | SPTLC1 (NP_006406.1) | LCB1 | 35.32 | Y23F(Y55); F40∆, S41∆ (L72, S73); S331Y(G378) HSAN1A k: C133Y/W(C180); V144D(V191); S331F(G379); A352V(V399) | 2-15 | [101,102,103,104,105] |
FTD-ALS2 | CHCHD10 (AAH65232.1) | MIX17 | 35.25 | S59L(S70) SMAJ-linked l: G66V(G77) IMMD-linked m: G58R(G69) | 2-16 | [106,107,108] |
FTD-ALS5 | CCNF (AAH12349.1) | CLN1 CLN2 CLN3 | 18.14 19.66 22.75 | R392T(Q337) R392T(H136) S195R(A2); S621G(S423) | 2-17 | [108] |
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Stump, A.L.; Rioux, D.J.; Albright, R.; Melki, G.L.; Prosser, D.C. Yeast Models of Amyotrophic Lateral Sclerosis Type 8 Mimic Phenotypes Seen in Mammalian Cells Expressing Mutant VAPBP56S. Biomolecules 2023, 13, 1147. https://doi.org/10.3390/biom13071147
Stump AL, Rioux DJ, Albright R, Melki GL, Prosser DC. Yeast Models of Amyotrophic Lateral Sclerosis Type 8 Mimic Phenotypes Seen in Mammalian Cells Expressing Mutant VAPBP56S. Biomolecules. 2023; 13(7):1147. https://doi.org/10.3390/biom13071147
Chicago/Turabian StyleStump, AnnaMari L., Daniel J. Rioux, Richard Albright, Guiliano L. Melki, and Derek C. Prosser. 2023. "Yeast Models of Amyotrophic Lateral Sclerosis Type 8 Mimic Phenotypes Seen in Mammalian Cells Expressing Mutant VAPBP56S" Biomolecules 13, no. 7: 1147. https://doi.org/10.3390/biom13071147