Identification of serum factors to enhance viral transduction of human cardiomyocytes

https://doi.org/10.1007/s00392-024-02526-y

Tim Afting (Göttingen)1, B. Berecic (Göttingen)1, M. Rinn (Göttingen)1, E. Schoger (Göttingen)1, M. Tiburcy (Göttingen)1, T. Brügmann (Göttingen)2

1Universitätsmedizin Göttingen Institut für Pharmakologie und Toxikologie Göttingen, Deutschland; 2Universitätsmedizin Göttingen Institut für Herz- und Kreislaufphysiologie Göttingen, Deutschland

 

Background:
The use of adeno-associated viruses (AAV) is to date one of the most efficient methods for gene transfer in vivo as well as in vitro. However, the clinical application of AAV for heart failure was hampered by insufficient transduction of the heart (CUPID-trial) and preclinical data suggests high inter-individual variability in transduction efficiency.  Therefore, it is of high clinical relevance to increase transduction efficiency without causing unacceptable side effects by high doses.

Hypothesis:
Transduction efficiency of AAV in human iPSC-derived cardiomyocytes can be significantly enhanced by incubating the vector with human sera prior to infection.

Methods and Results:
Human cardiomyocytes were obtained by directed differentiation of iPSC and plated in 96 well plates (5x10E5/well). AAV serotype 2.9 with a Green Fluorescent Protein (GFP) reporter were incubated with human sera from individual donors (n=2) as well as pooled human sera (n=2) from various donors before being added to the cardiomyocytes. We tested the effect of various vector genome concentrations per well (VG/well), ranging from 1E+08 to 1E+11. GFP fluorescence was monitored in live cells for 7-10 days (Sartorius Incucyte®). Cells were fixed and subsequently stained with an antibody against sarcomeric α-actinin before being imaged with a confocal cytometer and analysed with a custom algorithm to determine the transduction efficiency. To achieve a transduction of 50% of cells per well, 1E+10 VG/well in the serum-abstinent condition was needed whereas human serum reduced this to 2.3E+09 VG/well, p<0.05, n=3-7 per concentration. Serum dilution reduced this transduction enhancing effect. Apart from the use of untreated serum, modifications were undertaken to narrow down the responsible factor(s) for the enhancing effect, like size separation of the sera via Amicon® Ultra Centrifugal Filters. Interestingly, the serum fraction > 10 kDa showed a high transduction efficiency (83% ± 6%; p < 0,05 vs. AAV only, n=8) whereas the serum fraction < 10 kDa (47% ± 12%, n=8) was comparable to AAV only (37% ± 9%; n=11). Interestingly, some sera which did not have the positive effect performed better after complete depletion of immunoglobulins via Protein-A & -G-resin, especially in lower vector concentrations like 1E+09 VG/well.

Conclusion:
Human serum significantly increases AAV2.9 transduction efficiency in iPSC-derived cardiomyocytes by a yet unidentified serum factor. Neutralizing antibodies play a key role in impeding successful transduction, even when an enhancing factor is present.

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