Cell Lines for the Development of African Swine Fever Virus Vaccine Candidates: An Update
Abstract
:1. Introduction
2. Porcine Macrophages: The Main Target of African Swine Fever Virus
2.1. African Swine Fever Virus Entry and Receptor
2.2. Porcine Monocyte and Derived Macrophages
2.3. Bone-Marrow-Derived Macrophages
2.4. Porcine Alveolar Macrophages
2.5. Porcine Renal-Derived Macrophages
3. Other Porcine Primary Cell Lines
3.1. Dendritic Cells
3.2. Endothelial Cells
4. Monkey-Derived Continuous Cell Lines
4.1. Vero Cells
4.2. COS Cells
4.3. MS Cells
4.4. CV1 Cells
4.5. Marc-145
4.6. MA-104 Cells
5. Human Continuous Cell Lines
HEK293T Cells
Cell Line | Species of Cell Origin | Tissue of Cell Origin | Mechanism of Immortalization | Susceptibility to Field Isolates | Susceptibility to Adapted Isolates | Advantages | Disadvantages |
---|---|---|---|---|---|---|---|
VERO | African green monkey: Chlorocebus sabaeus [103] | Kidney epithelial cells [103] | Spontaneous, unknown process [104] | Low susceptibility to virulent isolates (BA71, Tangani, Hinde, Huganda, Lisbon60) [61,65,66,80] | - Adapted strain from Tengani [65] - BA71V [66,67] - ASFV-G/V [61] - Lisbon60V [80] | - Widely used to characterize function of several ASFV genes [68], proteomic analysis [68,69], mechanisms of viral entry [72,73,74], transcription and replication [69,70] - Titration by plaque formation [65,66] | - Genomic mutation during adaptation → reduction of virulence and immunogenicity in pigs [61,67,79,80,81] |
COS | African green monkey: Chlorocebus sabaeus [105] | From CV1 (see below) [105] | From CV1 (transformation with a mutant strain of Simian Virus 40 (SV40), which codes for the wild-type T-antigen) [105] | - E70 [82] - Malawi 82 [82] - Uganda [82] - Lisbon57 [82] - Lisbon60 [20,82] - Mozam68 [82] - CC83 [82] | - BA71V [20,30,82] - BA71ΔCD2 [81] - NH/P68 [82] - ΔEP153R [20,30,82] | - Used for production of large amount of virus [20], and studies on virus entry mechanisms [87,88] - Plaque titration [66,82] - Construction of deleted ASFV mutants [81,89] - BA71ΔCD2 –> stability and integrity in its genome [81] - BA71 → no changes in virulence and immunogenity [81] | - NH/P68 derived mutants → genomic mutations during passages relevant to protection [89] |
MS | African green monkey [62,106] | Kidney [62,106] | Unknown process | - Low susceptibility to virulent to field isolate E70 [62] | - E70MS14, E70MS44, E70MS81 [62,63,90] | - Not plaque for titration [62] - Genomic mutation during adaptation → reduction of virulence and immunogenicity in pigs [62,90] | |
CV1 | African green monkey: Cercopithecus Aethiops [107] | Fibroblast-like cells derived from kidney tissue [107] | Transformation with a mutant strain of Simian Virus 40 (SV40), which codes for the wild-type T-antigen [107] | - E75 [91] - Stavropol 01/80 [93] | - E75CV1 [91] | - Plaque titration - E75CV1 → 100% protection against challenge with homologous E75 in pigs [91] but not against heterologous BA71 [92]. | - Stavropol 01/80 → Genomic mutation, during adaptation, with reduction of virulence and immunogenicity in pigs [93] |
Marc-145 | African green monkey Chlorocebus aethiops [94,108] | Fetal kidney epithelial cells, subpopulation of MA-104 [94,108] | MA-104 derived [94] | -D/ASF/POT/Vietnam/2019, D/ASF/POB/Vietnam/2019, although only three passages were monitored [95]. | Unable to support the growth of ASFV Pol18/28298/Out111 [96] and ASFV-HLJ/18 [45]. | ||
MA-104 | African green monkey: Cercopithecus aethiops [97,108] | Fetal kidney epithelial cells [97,108] | Spontaneously immortalized cell line [97] | - ASFV-G [97] - BA71 [97] - D/ASF/POT/Vietnam/2019, D/ASF/POB/Vietnam/2019 [95] - MW039157 [50] | - MW287337 [50] | - Suitable for ASFV isolation → able to detect ASFV with a TCID50 sensitivity comparable to that of primary swine macrophages [97] - Hemadsorption [97] - Genome stability during 15 passages of a genotype II ASFV isolates [98]. | More studies required its suitability to grow ASFV strains for large-scale vaccine production. |
HEK293T | Human [45] | Kidney epithelial [45] | Transformation with sheared Adenovirus 5 DNA [109] | - Low susceptibility to OURT88/3 [102] and ASFV-HLJ/18 [45] | - Adapted strain from ASFV-HLJ/18 (ASFV-P121) [45] - OURT 88/3-ΔTK-GFP [102] | - Efficiently and high replication of the attenuated virus [45] - Hemadsorption [45] - Clear cytopathic effect [45] | ASFV-HLJ/18 → Genomic mutation during adaptation (mainly at the MGF genes) [45] → potential reduction of virulence and immunogenicity in pigs [45] |
6. Porcine Continuous Cell Lines
6.1. PK Cell Lines
6.2. WSL Cells
6.3. Immortalized Porcine Alveolar Macrophages
6.4. Immortalized Porcine Kidney Macrophages
6.5. Plum Island Porcine Epithelial Cells
6.6. Zuckerman Macrophage-4
6.7. A4C2 and A4C2/9k Cells
6.8. PSGK-60 and PPK-66b
Cell Line | Species of Cell Origin | Tissue of Cell Origin | Mechanism of Immortalization | Susceptibility to Field Isolates | Susceptibility to Adapted Isolates | Advantages | Disadvantages |
---|---|---|---|---|---|---|---|
PK | Pig [110,112,129] | Kidney [110,112,129] | Spontaneously immortalized cell line [129] | - PK2a: extremely low susceptibility to several ASFV strains: Spencer, Portuguese, Gasson, Madrid n. 1, Madrid n. 2 [110] - PK/A/C/13: extremely low susceptibility to Uganda and Hinde: [112] - PK15: extremely low susceptibility to Tengani [111,114] | -PK2a: susceptibility to ASFV strains after several passages on PK2a (Spencer, Portuguese, Gasson, Madrid n. 1, Madrid n. 2) [110] - PK/A/C/13: susceptibility to Uganda and Hinde after several passages on PK cells [112] - PK15, PK9, and PK0809: Attenuated Uganda, BA71V [46]. - PK15: strain derived from Tengani through passages on PK15 [111,114] | - Plaque titration (with plaque size heterogeneity) [110,112]. - Clear cytopathic effects [110] - Hemadsorption [110] | - Plaque formation limited to culture-adapted ASFV strains [30,110]. - PK15 no able to support the growth of ASFV-HLJ/18 strain [45], Benin 97/1, Virulent Uganda [46]. - PK9, and PK0809 no susceptible to Benin 97/1, Virulent Uganda [46]. - PK15 no able to support the growth of D/ASF/POT/Vietnam/2019, D/ASF/POB/Vietnam/2019 [95] - Spencer, Portuguese, Gasson adapted to PK cells → genomic mutation during adaptation with reduction of virulence in pigs but only partial protection against challenge with homologous strain [110] - Hinde isolates passaged 75 times in PK2a → reduction of virulence in pigs but only partial protection to challenge to parental strain; survived pigs only partial protection to other ASFV isolates [65] |
WSL | Wild boar (fetus) [20,30,116] | Lung [20,30,116] | Spontaneously immortalized cell line [130] | - CC83, Malawi 82, Uganda, Lisbon 57, E70 [30] -ASFV-Kenya1033-IXL [118] | - NH/P68 [18,115] - ΔEP153R, Hinde attenuated, Uganda attenuated NH/P68, BA71V [30] - NHV-dTK-EGFP [116] - ASFV-KeΔA238L strain (generated by deletion of the gene A238 by ASFV-Kenya1033- IXL) [119] - OUTR88/3 [102] | - ASFV-Kenya1033-IXL and ASFV-KeΔA238L → genomic stability during passages in WSL [118,119] - NH/P68 ASFV strain produced in WSL cells (10 passages) → in vivo in pigs induced a similar infection pattern to that of NH/P68 passaged in PAM [18,115] - ASFV-Kenya-1033-IX produced in WSL cells (more than 20 passages) → retained the virulence in vivo [118] | - Slight or unnoticeable cytopathic effects [20,30] - No ability to efficiently support the growth of E70 or Armenia/07 [18,115]. - Promising results, but in vivo studies are required to evaluate its suitability to grow ASFV strains for large-scale vaccine production (protection to challenge). |
IPAM | Sus scrofa [30] | Porcine alveolar macrophages [30,122] | Porcine myeloid cell lines established by transfecting primary porcine alveolar macrophage cultures with plasmid pSV3neo, carrying genes for SV40 large T antigen [30,122] | - Low susceptibility to few virulent isolates, including E70, CC83 [30] - Low susceptibility to field isolateLillie SI/85 [122] | - Uganda attenuated, Hinde attenuated [30] - 3D4/2, 3D4/21, and 3D4/31: growth of the attenuated ASFV-Lisbon 61 supported in different degrees. [122] | - Unable to maintain replication of the ASFV-HLJ/18 strain [45] - Weak susceptibility to BA71V, NH/P68, Malawi82, Lisbon57 [30]. - No susceptible to infection with Armenia/07 or NH/P68 [18,115]. | |
IPKM | Pig [123] | Primary porcine kidney-derived macrophages [123] | Immortalization by transfection with recombinant lentivirus vectors carrying the gene for SV40 large T antigen (SV40LT) in combination with the gene for porcine telomerase reverse transcriptase (pTERT) [123] | - Armenia07 [23] - Kenya05/Tk-1 [23] - E75 [23] | - Lisbon60V (VERO cell-adapted isolate) [23] | - Clear cytopathic effect [23] - Hemadsorption [23] - Plaques formation → rapid isolation and purification of different strains [23] -Armenia07 → good genomic stability with only one non-synonymous nucleotide replacement detected in the CP530R region at passages 10 and 15 [23] | Promising results, but in vivo studies are required to evaluate its suitability to grow ASFV strains for large-scale vaccine production. |
PIPEC | Pig (fetus) [124] | Kidney [124] | 60 passages from the LFPKaVb6 (a porcine fetal kidney cell line [124]). | - ASFV-G-ΔI177L → generation of ASFV-G- ΔI177LΔLVR after several passages [125] | - ASFV-G- ΔI177LΔLVR efficiently replicated in PIPEC and after 30 passages no additional genomic mutation [125]. - ASFV-G-ΔI177LΔLVR → safe and protective (100% protection against challenge with parental virulent ASFV-G) [125]. | Promising results, but more studies are required to evaluate its suitability to grow ASFV strains for large-scale vaccine production. | |
ZMAC-4 | Pig (fetus) [126] | Lung macrophages [126]. | Spontaneously immortalized cell line [126]. | - Benin 1997/1, - Georgia 2007/1, - Malawi LIL20/1, - Tengani, - MOZ 94/1, - ZOM 2/84, - Dominican Republic [126] | - OUTR88/3 - NH/P68 [126] | - Efficiently supported the growth of Georgia 2007/1 to levels similar to bone-marrow-derived macrophages [126]. - 12 passages of the attenuated OURT88/3 ASFV in ZMAC-4 cells → safe and protective (able to induce a 100% protective response in pigs against challenge with virulent ASFV) [126] | Promising results, but more studies are required to evaluate its suitability to grow ASFV strains for large-scale vaccine production. |
A4C2 and A4C2/9k | Pig [93] | Hybrid cell lines of SPEV TK with swine lymphocytes [93] | Not described [93] | -Stavropol 01/08 [93] - Sveromorsk 2010, Volgograd/Kalach 2012, Tver/Zavidovo [93] | - Hemadsorption was visible after adding 0.5% suspension of pig erythrocytes [93]. | - Stavropol at passage 14 in the A4C2/9k maintained the proper virulent titers strain [93] - Stavropol at passages 24 and 33 → loss of pathogenicity in pigs but no protection to challenge with parental virulent strain [93]. | |
PSGK-60/PPK-66b | Pig [93] | Kidney [93] | Not described [93] | - Stavropol 01/08 in PSGK-60 and PPK-66b [93] - TSP-080 and TS-7 (two ASFV strains derived from ASFV Kiravira-67) in PPK-66b [128] - Uganda in PPK-66b [128] | - TSP-080/300 (derived from TSP-080) in PPK-66b [128] - TS-7/230 (derived from TS-7) in PPK-66b [128] - Uk-50 (derived from Uganda): PPK-66b [128] | - Stavropol 01/08: maintained virulent properties → infected pigs died [93] - TSP-080/300 and TS-7/230 →Low-reactogenic and able to protect pigs against challenge with the corresponding parental strain [128]. | - No hemadsorption [93] -Promising results, but more studies are required to evaluate its suitability to grow ASFV strains for large-scale vaccine production. |
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Meloni, D.; Franzoni, G.; Oggiano, A. Cell Lines for the Development of African Swine Fever Virus Vaccine Candidates: An Update. Vaccines 2022, 10, 707. https://doi.org/10.3390/vaccines10050707
Meloni D, Franzoni G, Oggiano A. Cell Lines for the Development of African Swine Fever Virus Vaccine Candidates: An Update. Vaccines. 2022; 10(5):707. https://doi.org/10.3390/vaccines10050707
Chicago/Turabian StyleMeloni, Dionigia, Giulia Franzoni, and Annalisa Oggiano. 2022. "Cell Lines for the Development of African Swine Fever Virus Vaccine Candidates: An Update" Vaccines 10, no. 5: 707. https://doi.org/10.3390/vaccines10050707