The Kinetics of DEAE-Dextran-induced Cell Sensitization to Transfection

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1 J. gen. Virol. (1973), x8, Printed in Great Britain The Kinetics of DEAE-Dextran-induced Cell Sensitization to Transfection (Accepted 19 October 972 ) DEAE-dextran has commonly been found to more effectively enhance transfection when mixed with the virus nucleic acid before cell inoculation (mixed-inoculum method) than when it is used to pretreat the cells before inoculation (Pagano & Vaheri, 965; Bachrach, 1966; Koch, Quintrell & Bishop, 1966; Pagano, McCutchan & Vaheri, 967; Tovell & CoRer, 1967). We have found, however, that the cells are only transiently sensitized to transfection by pretreatment, and that this method, optimally employed, can give much greater enhancement than the mixed-inoculum method. Part of these results have appeared in abstract form (A1-Moslih & Dubes, 1972). Two picornaviruses were used: the BRU~HLDE strain of poliovirus type i on the eta and kappa (Chapin & Dubes, 1964) and LLC-MK2 lines of rhesus monkey kidney cells, a line of chimpanzee liver cells (Dr W. V. Hartwell), and the HeLa and KB lines of human carcinoma cells; and a rapid (r) mutant of the WALLACE strain of echovirus type 7 on cultures of eta and LLC-MK2 cells. This r mutant, isolated after selective passages on eta cells, produces plaques about 3 times larger in diameter than wild-type WALLACE virus. The cells were grown as sheets under medium S (Chapin & Dubes, 964). From high-titre serum-free virus stocks which had been grown in eta cells under medium S minus serum, virus RNA preparations were made using three serial extractions with phenol at o C (Gierer & Schramm, 956). For enhancement, three procedures were tested: the mixed-inoculum method essentially as employed by Pagano & Vaheri (1965), the cell pretreatment and posttreatment methods. n each case, the cell sheet in a 6o mm Petri dish was incubated at 23 C in 5 ml phosphate-buffered saline (PBS) of Dulbecco & Vogt 0954) minus CaC12 and MgC12 (medium A) for 5 min. Then the sheet was either pretreated with DEAEdextran, or directly inoculated with the virus RNA either mixed or unmixed with DEAEdextran. Each DEAE-dextran-pretreated cell sheet was washed 3 times, each time with 5 ml medium A, after pretreatment and before inoculation with RNA. n each case, unless otherwise noted, the RNA inoculum was incubated with the cell sheet at 23 C for 15 rain. For the post-treatment procedure, after incubation with the virus RNA, the cell sheet was washed once with 5 ml medium A. n all cases, each cell sheet was finally washed with 5 ml balanced salt solution of Hanks & Wallace (949). Representative data showing the considerably greater enhancement of transfection of eta cells afforded by the pretreatment method, as versus the mixed-inoculum method, are shown in Table t. Essentially similar results were obtained in tests of the transfection of kappa, chimpanzee liver, HeLa, and KB cells by poliovirus RNA. Using LLC-MK~ cells, the pretreatment method also afforded greater enhancement of transfection by either poliovirus RNA or echovirus RNA than the mixed-inoculum method, but the differences were slight. The post-treatment method gave no enhancement. Attempts were made, using eta cells and echovirus RNA, to increase the relative effectiveness of the mixed-inoculum method by testing various combinations of different concentrations of DEAE-dextran, temperatures, and durations of incubation of the mixed inoculum with the cells, as well as using PBS instead of medium A as RNA diluent. n none of these P:

2 90 Short communications Table. Comparisons of DEAE-dextran pretreatment and mixed-inoeulum methods RNA* Expt. Echovirus type 7 1 Number of plaques/platet t Pretreatment method~: Poliovirus type oo Mixed-inoculum method 2z o * For a given experiment, the inoculum RNA concentration was constant. t Eta cell sheets were used. Counts above 350 plaques/plate were rough estimations. :~ Washed cells were incubated with DEAE-dextran at mg/ml at 23 C for 9 min (except t5 rain for Expts. 1 and 2), washed three times with medium A, using 5 ml/wash, and then incubated with virus RNA at 23 C for ~5 min. Washed cells were incubated with a mixture of DEAE-dextran at ~ mg/ml and virus RNA at 23 C for 15 min. O combinations did the mixed-inoculum method approach the optimal pretreatment method in effectiveness. The kinetics of cell sensitization by pretreatment was found to be markedly dependent on the concentration of DEAE-dextran and on the temperature (Fig. ). The sensitization was followed by a marked desensitization process (Fig. ). From the data of Fig. ~, and other experiments, several conclusions can be reached: the optimum temperature for pretreatment is dependent on the duration of the pretreatment. For example, with DEAEdextran at mg/ml, when the duration is t5 min, the optimum temperature is ~8 C; but when the duration is < 5 or > 15 min, the optimum temperature is > ~8 C or < 8 C, respectively. That is, these two variables show an inverse relationship. n sum then, the three variables DEAE-dextran concentration, temperature, and time are closely interrelated in determining the cell sensitization obtained in the pretreatment method; and it is meaningful to speak of the optimal value for one of these three variables only when the values of the other two variables are specified. As our standard system, we use 2 3 C for 9 min, where the optimum concentration of DEAE-dextran is ~ mg/ml. These values were obtained using eta cells and echovirus RNA, but similar values were obtained using other cell/rna systems (Fig. ). The enhancement given by the pretreatment method was independent, or nearly independent, of ph of the pretreatment buffer over the range 6"4 to 8.o, but strikingly dependent on the buffer tonicity, with the optimal tonicity being approximately isotonic. After very short pretreatment, the cells underwent further sensitization even after washing off the free DEAE-dextran; such further sensitization was shown both for poliovirus RNA P:

3 Short communications 9 o O 60 ~ 30 Y -'3 E 90 ~ 6o 3O % DEAE-dextran at 2000 ltg'ml l) EAE-dextran at 300/~g 133l //~ LLC-MK ceils A C Eta cells t a~ i t 60 -MK2 cells D 30 ~ KB cells! Time (rain) 100 Fig. i. Cell sensitization as a function of duration of pretreatment of cells with DEAE-dextran. Eta cells were used in A and B. Echovirus RNA was used in A, B and C; and poliovims RNA in D. DEAE-dextran was at mg/ml except in A. Pretreatment was at 23 C in A, C and D, and at 37 C in B. For B, C and D, the arithmetic mean plaque counts were normalized. (Fig. 2) and echovirus RNA. This result indicates that some further step beyond mere attachment of the DEAE-dextran to the cells is required for full cell sensitization. Cells which had been markedly desensitized by prolonged pretreatment with DEAEdextran could be fully resensitized with fresh solution of DEAE-dextran. Some of the early reports (see above) of low or no cell sensitization by DEAE-dextran were probably due to overlong incubation of the DEAE-dextran with the cells before inoculation with RNA; for example, Pagano & Vaheri 0965) pretreated their cells at 37 C for 2 h. More recently, Koch & Bishop (i968) and Wentzky & Koch 097) reported that cell pretreatment with DEAE-dextran gave moderately large enhancement of transfection, but still less than that given by the mixed-inoculum method. To sum up, we conclude from our experiments that DEAE-dextran enhances transfection by sensitizing the cell, that this sensitization process consists of at least two steps, that sensitization is quickly followed by a markedly temperature-dependent desensitization process, and that, after desensitization, the cells are fully resensitizable by fresh solution of DEAE-dextran. P:

4 9 2 Short communications e- E 10< o [ i Time (rain) Fig. 2. Kinetics of further cell sensitization. Eta cell sheets were pretreated with DEAE-dextran at 1 mg/ml at 37 C for rain, then washed 3 times and incubated at 23 C for various periods of time before inoculating them with poliovirus RNA. The arithmetic mean plaque count data have been normalized. This work was done in partial fulfilment of the requirements of the University of Nebraska for the PhD degree for M.. A1-Moslih. Department of Medical Microbiology University of Nebraska College of Medicine Omaha, Nebraska 68to5, U.S.A. M.. AL-MOSLH G. R. DUBES REFERENCES AL-MOSLm, M. L & DUBES, G. R. (972)- Studies of the enhancement by diethylaminoethyl (DEAE)-dextran of transfection by picornavirus ribonucleic acid (RNA). Genetics 7x, s 2. BACHRACH, H. L. (966). Ribonucleic acid of foot-and-mouth-disease virus: an ultrasensitive plaque assay. Proceedings of the Society of Experimental Biology and Medicine r23, CHAVN, M. & DUBES, G. R. (964). Characteristics of five rhesus monkey kidney cell lines. Proceedings of the Society of Experimental Biology and Medicine ns, DULBECCO, R. & root, M. 0954). Plaque fomaation and isolation of pure lines with poliomyelitis viruses. Journal of Experimental Medicine 99, OERER, a. & SCHRAMM, O. (956). nfectivity of ribonucleic acid from tobacco mosaic virus. Nature, London x77, 702-7o3. HANKS, J. H. & WALLACE, R. E. (949). Relation of oxygen and temperature in the preservation of tissues by refrigeration. Proceedings of the Society of Experimental Biology and Medicine 7 r, 196-2oo. Koch, ~. & ~snov, J. M. (968). The effect of polycations on the interaction of viral RNA with mammalian cells: studies on the infectivity of single- and double-stranded poliovirus RNA. Virology 35, KOCH, G., QUNTRELL, ~. & msnov, s. i. (1966). An agar cell-suspension plaque assay for isolated viral RNA. Biochemical and Biophysical Research Communications 24, 3o4-3o9. PAGANO, J. S., MCCUTCHAN, J. H. & VAHER, A. (1967). Factors influencing the enhancement of the infectivity of poliovirus ribonucleic acid by diethylaminoethyl-dextran. Journal of Virology x, P:

5 Short communications 93 'A~ANO, J. S. & VAaER, a. (~965). Enhancement of infectivity of poliovirus RNA with diethylaminoethyldextran (DEAE-D). Archiv fiir die gesamte VirusJbrschung x7, TOVELL, D. a. & OLTER, J. S. (~967). Observations on the assay of infectious viral ribonucleic acid: effect of DMSO and DEAE-dextran. Virology 32, WENTZKY, P. & KOCH, O. (971). nfluence of polycations on the interaction between poliovirus multistranded ribonucleic acid and HeLa cells. Journal of Virology 8, 35-4o. (Received ~ August 972 ) P:

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