Two Loci Controlling Genetic Cellular Resistance to Avian Leukosis-Sarcoma Viruses
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1 JOURNAL OF VROLOGY, Oct. 967, p Copyright 967 Americn Society for Microbiology Vol., No. 5 Printed in U.S.A. Two Loci Controlling Genetic Cellulr Resistnce to Avin Leukosis-Srcom Viruses LYMAN B. CRTTENDEN, HOWARD A. STONE, RCHARD H. REAMER, AND WLLAM OKAZAK Regionl Poultry Reserch Lbortory, U. S. Deprtment of Agriculture, Est Lnsing, Michign 8823 Received for publiction 2 April 967 Femle chickens known to be heterozygous for resistnce to subgroups A nd B of the vin leukosis-srcom viruses were mted to mles known to be homozygously resistnt to both. The progeny were ssyed both on the choriollntoic membrne (CAM) nd in tissue culture for resistnce to representtive viruses of the A, B, nd tenttively defined C subgroups. Segregtion rtios of resistnce to A nd B subgroup viruses greed with the previously suggested hypothesis of single-utosoml-recessive genes controlling resistnce to ech subgroup. Mixed infection on the CAM nd replicte plte infection in tissue culture with subgroup A nd B viruses showed tht resistnce to the A nd B subgroups ws inherited independently. Assys with viruses tenttively clssified s subgroup C indicted tht they were lrgely composed of mixture of subgroup A nd B viruses or of prticles possessing the host rnge specificity of both. However, virus stocks of the subgroup C ctegory, s well s some stocks clssified s subgroup B, produced smll numbers of pocks or foci on individuls known to be resistnt to subgroup A nd B viruses. t is suggested tht these Rous srcom virus stocks crry between nd % of true subgroup C virus. The vin leukosis-srcom viruses my be clssified into t lest three subgroups (A, B, nd C), bsed on properties of the virus cot. These properties re host rnge, interference ptterns, nd ntigenic type (6,, 5; Vogt et l., Symposium on Subvirl Crcinogenesis, Ngoy, Jpn, in press). A single-utosoml-recessive gene controls specific cellulr resistnce to the in vitro nd in vivo growth of subgroup A viruses (-3, 8). Similrly, second single-utosoml-recessive gene controls resistnce to subgroup B viruses (, ). t is cler tht resistnce to these virl subgroups is independent t the phenotypic level, becuse ll four combintions of resistnce or susceptibility re found (). However, no studies hve utilized criticl mtings which would revel whether these genes re linked or independent. Preliminry dt from this lbortory suggest tht these genes re, in fct, independently inherited (R. H. Remer, unpublished dt). The present study ws designed specificlly to test this hypothesis, by inocultion of bck-cross progeny from mtings designed to segregte in one-toone rtio of resistnce to susceptibility to both subgroups A nd B with Rous srcom viruses (RSV) representtive of these subgroups. The sme progeny were lso inoculted with viruses tenttively clssified s subgroup C in n ttempt to identify resistnce to this subgroup. MATERALS AND METHODS Phenotypic nd genotypic nomenclture. Vogt nd' shizki () suggested phenotypic nomenclture bsed on the terminology for host bcterium resistnce used by bcteriophge workers. We suggested (3) genotypic terminology, using Rs nd rs for gene symbols representing n bbrevition for RSV. Since it is now known tht these genes control resistnce to leukosis viruses s well s to RSV, nd since it is suspected tht t lest two loci re involved, we hve dopted the terminology presented in Tble. We cll these loci the "tumor virus " (tv) nd the "tumor virus b" (tvb) loci, specifying susceptibility ptterns to the vin tumor virus subgroups A nd B, respectively. The superscripts r nd s stnd for resistnce nd susceptibility, respectively, nd multiple lleles my be designted by numbered superscripts. Virus stocks. Tble 2 gives the virus stocks used, their subgroup clssifiction, nd their bbrevitions. The Bryn high-titer pseudotypes BH-RSV(RAV-) nd BH-RSV(RAV-2) were obtined from P. K. Vogt. These stocks were originlly produced by ctivtion of nonvirus-producing trnsformed (NP) cells with RAV- or RAV-2 which hd been "cloned" by limit dilution (). The BH-RSV (RAV-) seed virus ws propgted once by pssge in the pectorl muscle of line 5 isolted chickens (7); BH-RSV(RAV-2) ws 898 Downloded from on December 23, 28 by guest
2 VOL., 967 LOC FOR AVAN LEUKOSS-SARCOMA VRUSES 899 TABLE. Genotypic nd phenotypic nomenclture for genetic cellulr resistnce to the vin leukosis-srcom viruses controlled by the tv nd tvb loci Susceptibility (S) or resistnce (R) to vin Genotype Phenotype tumor virus subgroup s s bs bs C/O S S s r b bs C/O S S r r bs bs C/A R S s 8 bs br C/O S S s r bs br C/O S S r r bs br C/A R S 8 s br br C/B S R, r br br C/B S R r r b r br CA,B R R propgted in line 7, known to be resistnt to subgroup A viruses. The tumor minces were suspended in.5 M potssium citrte with mg of hylurc;nidse per ml, homogenized in Wring B'endor, nd clrified by centrifugtion t 2, X g in n nterntionl refrigerted centrifuge. The Schmidt-Ruppin stocks, SR-RSV- nd SR- RSV-2, were prepred from heterogeneous mteril obtined from Pdmn Srm (2). These stocks were selected for A nd B subgroup specificity by growing them for five consecutive pssges of superntnt fluid in C/B nd C/A cells, respectively. A second preprtion of SR-RSV-2 ws obtined from P. K. Vogt. This ws pssged on C/A cells nd clssified s predominntly subgroup B. These stocks were propgted in line 5 or line 7 chickens for one pssge s indicted bove. Since it ws pprent, t lest in tissue culture, tht the resistnce to B viruses could be overcome rther esily, the reltive titers of severl of the viruses were determined in C/O nd C/A, B embryos nd in tissue culture. Tenfold dilutions of the virus preprtions were inoculted into the cells or embryos of line 6 nd 7. The logrithm (bse ) of the titers in line 6 (C/O), line 7 (C/A,B), nd the difference between them re given for ech virus in Tble 3. Substntil differences of t lest three logs were observed in both ssy systems on inocultion with both subgroup A viruses. A B The subgroup B viruses showed different picture. Lrge differences in titer were observed on inocultion with BH-RSV(RAV-2). However, the differences in titer in both systems were substntilly lower when two different sources of SR-RSV-2 were used. Therefore, the unexpected susceptibility to these viruses of embryos crrying the b' llele in the homozygous stte must be ttributed to the virus stocks used nd not to the ssy method. For this reson, difficulty ws experienced in identifying the C/B nd C/A,B phenotypes unequivoclly when SR-RSV-2 ws used. The BS-RSV ws prepred s described by Purchse nd Okzki (). The preprtion hs been described by Crittenden nd Okzki (). Both of these stocks hve demonstrted their bility to differentite mong phenotypes on choriollntoic membrne (CAM) ssy (). Mtings. nbred lines 6 nd 7, nd their F, nd bck-cross mtings, were used in this study. Extensive dt hve shown tht line 7 is homozygously resistnt (r r), line 6 is homozygously susceptible (' '), nd the bck-cross progeny of n F, X line 7 mting segregtes in rtio of one resistnt to one susceptible in response to inocultion with BS-RSV, which is predominntly subgroup A (, 3, ). Tble presents the susceptibility of these lines upon inocultion with nd. t is cler from these dt nd other unpublished dt (Crittenden) tht line 6 is homozygously susceptible to (b8 be), wheres line 7 is segregting for resistnce to this subgroup B virus. However, subline 2 of line 7 ppers to be homozygously resistnt (br br) to this subgroup. This sme segregtion pttern is seen with, suggesting possible reltionship with subgroup B. Thirty-nine F, femles from reciprocl cross mtings of lines 6 nd 7 were vilble for study. Since the subline origin of the line 7 prent ws unknown, these dms could hve been double heterozygotes (' r, bs bt) or homozygously susceptible to subgroup B while heterozygous for susceptibility to subgroup A (t' r, b br). These femles were mted to mles of subline 2 of line 7, known to be r,, br bt. A preliminry test of these mtings by inocultion on the CAM with BH-RSV(RAV-2) reveled 2 which produced t lest two resistnt progeny. These 2 mtings were ssumed to be the double bck-cross or test-cross mtings pproprite for one test of independent segregtion. Tht is, if these genes re independent, the two prentl (C/O, C/A,B) nd the two recombi- TABLE 2. Stocks of virus used nd their subgroup identity ccording to Vogt nzd shizki () Stock Subgroup A B C or unknown Bryn high-titer RSV pseudotypes BH-RSV (RAV-) BH-RSV (RAV-2) Schmidt-Ruppin RSV SR-RSV- SR-RSV-2 Bryn Stndrd RSV BS-RSV Hrris RSV Crr-Zilber RSV Prgue RSV CZ-RSV Downloded from on December 23, 28 by guest
3 9 CRTTENDEN ET AL. J. VROL. TABLE 3. Differences in titer-s (logo) of pirs of subgroup A nd B virus preprtionts in line 6 (CO) nd lin7e 7 (C/A, B) embryos whenl ssyed in tissue culture nid on the CAM Assy BH-RSV(RAV-) Subgroup A SR-RSV- BH-RSV(RAV/-2) Subgroup B SR-RSV-2 Tissue culture ssy Line 6 (C/O) titer. Line 7 (C/A, B) titer... Difference... CAM ssy Line 6 (C/O) titer... Line 7 (C/A, B) titer... Difference <. > < 2. > l < > lb More thn one entry mens tht the titrtion ws repeted. The second entry represents virus obtined from P. K. Vogt nd propgted by us. TABLE. Tbultioni of cpproximte pock counits on the embryonic cloriolllntoic membrnes of linles 6 n2d 7 nd their cross fter iniocultiont of HA -RS V nid Line 6 6 X Subline All All 2 3 All 2 3 noculum Estimtes over 2. Pock count O l + Totl nnt (C/A, C/B) phenotypes should occur in equl frequency. Assy procedures. The CAM nd tissue culture ssy procedures were essentilly those previously described (3) nd follow the procedures given by Groupe et l. () nd Temin nd Rubin (3). RESULTS CAM ssys. Twenty-two test-cross mtings were used for the CAM ssy experiments. The 3 DLUTON DLUTON. ra L] - 5 t 5 ~~~~~~V 2 9; Number of Pocks FG.. Distribution of pock counts ont the CAM of test-cross embryos inzoculted with two dilutions of BH-RSV(RAV-). CAM numbers were grouiped for tbultion in successive five-pock ctegories. Dt represent one of three settings of eggs. Pocks becme confluent when more thn 3 were present; therefore, ll membrnes showing 3 or more pocks were tbulted s 3+. eggs from these mtings were incubted in consecutive biweekly settings. n ech setting, group of line 6 (C/O) nd line 7 (C/A,B) eggs were set s known susceptible nd resistnt controls, nd these behved s expected. Four different inocul were used in concentrtions which would give n verge of t lest pocks per 7 Downloded from on December 23, 28 by guest
4 Vol-., 967 LOC FOR AVAN LEUKOSS-SARCOMA VRUSES 9 TABLE 5. Segregtiont rtios of test-cross embryos susceptible nd resistnt to four inocul of Rous srcom virus Sex No. No. Virus Test-cross mting of suse X (ol X 9) em- cepresis- tnt bryo tibie BH-RSV (RAV-) 7 X (7 X 6) e X (7 X 6) X (6X7) e 3 6 7X (6X7) Totl BH-RSV (RAV-2) 7 X (7 X 6) e X (7 X 6) X (6 X 7) e X (6X7) Totl 23 2 BH-RSV (RAV-) 7 X (7 X 6) e 37 mixed with BH- 7 X (7 X 6) RSV (RAV-2) 7X (6X7) e 37 7 X (6 X 7) Totl 5 5 7X (7X6) dp 5 9 7X (7X6) X (6 X 7) d' 5 6 7X (6X7) Totl 79 9 membrne. The sex of ech embryo ws determined when the pocks were counted. Representtive distributions of pock counts for embryos inoculted with BH-RSV(RAV-) re given in Fig.. The -3 dilution ws used to provide most of the segregtion dt collected in three settings. Any embryo inoculted with this dilution showing four or fewer pocks ws considered resistnt. t is cler tht the distributions re bimodl nd tht it ws not difficult to differentite between resistnt nd susceptible embryos. The segregtion dt re given in Tble 5. These dt re grouped by sex of the embryo nd the reciprocl mting sttus of the dm in order to evlute ny possible influence of sex linkge. The fct tht chi-squre tests showed no significnt heterogeneity of segregtion rtios mong the four mting type-sex groups indicted tht this locus is not on the sex chromosome. The rtio of 73 susceptible to 66 resistnt embryos grees very well with the : rtio expected for subgroup A viruses, ssuming tht susceptibility is controlled by single-utosoml-dominnt gene. Similr results with BH-RSV(RAV-2) were obtined (Fig. 2 nd Tble 5). Although the segregtion rtios re not s close to : s in the cse of BH-RSV(RAV-), they still gree.r z 2[ 2 VARci.2 x -' DLUTON.2 x ' DLUTON Blrl o VA 7" V Number of Pocks FG. 2. Distribution ofpock counlts on the CAM of test-cross embryos inoculted with two dilutions of BH-RSV(RA V-2). with the single-utosoml-gene hypothesis for the control of resistnce to subgroup B viruses. The next inoculum used ws mixture of BH-RSV(RAV-) nd BH-RSV (RAV-2) in such concentrtions tht ech virus lone should hve produced n verge count of t lest pocks. f the tv nd tvb genes were t the sme locus or closely linked, one would expect only the prentl C/O nd C/A,B phenotypes in equl frequency. However, if tv nd tvb were locted t unlinked loci, the recombinnt C/A nd C/B phenotypes would be expected in frequency equl to the prentl C/O nd C/A, B phenotypes. This would give 3: rtio of susceptible nd prtilly susceptible (C/O, C/A, nd C/B) to resistnt (C/A,B) phenotypes. This method of testing for linkge in the RSV system ws first used by Pyne nd Biggs (9). Agin, the segregtion rtios were found to be homogeneous (Tble 5). The very close fit to 3: rtio of susceptible to resistnt embryos shows tht these two single-gene systems re not t closely linked loci. Figure 3 gives the distribution of pock counts for one of 2 E L j Number of Pcks FG. 3. Distribution of pock counzts on the CAM of test-cross embryos inoculted with mixture of BH-RSV(RA V-) nd BH-RSV(RA V-2). Dt represeiit one of two settings of eggs. Downloded from on December 23, 28 by guest
5 92 CRTTENDEN ET AL. J. VROL. TABLE 6. Meditn nd rntge offocus coulnts onl conitrol liine 6 nzd linle 7 cells inioculted with six strins of RSV ini trils - Subgroup A Subgroup B Subgroup C Line Phenotype mintion SR-RS'-l BS-RSV- SR-RSV-2 CZ-RSV 6 C/O Medin 2,8 3,+ 2,38 3,+ 3,+ 3,+ Rnge 52-3,+ 6-3,+ 7-(3,+,-3,+,-3,+,52-3,+ 7 C/A, B Medin Rnge Pocks becme confluent when counts were more thn 3, per 6-ml plstic dish. the two settings inoculted with the mixture. t is cler tht the distribution is bimodl, but no cler distinction cn be mde between the C/O nd selectively resistnt (C/A nd C/B) phenotypes. Vogt nd shizki (5) suggested tht belongs to third or C subgroup. Since the C/A,B subline of line 7 nd line 6 (C/O) were found to be resistnt nd susceptible to these viruses, these sme mtings were pproprite for studying segregtion rtios with this virus stock. Agin, segregtion rtios were found to be homogeneous, nd 3: rtio of susceptible to resistnt embryos ws observed (Tble 5). This suggests tht susceptibility to this virus stock is controlled by two independent loci, perhps iv nd tvb. Tissue culture ssy. Secondry cell cultures of single embryo my be inoculted with different virus stocks in seprte pltes to estimte the embryo phenotype. This is n obvious dvntge when more thn one virus subgroup is involved. The test-cross embryos from four F dms were used for tissue culture ssy. Primry cell cultures were mde ech week from test-cross embryos, one line 6 (C/O) embryo, nd one line 7 (C/A,B) embryo. Replicte secondry cultures were inoculted in 6-mm plstic pltes with ech of six virus preprtions in concentrtions which would give n verge of t lest, foci per plte. Two pltes from ech embryo were held s uninoculted controls. The medin nd rnge of focus counts on line 6 nd 7 control pltes for the trils re given in Tble 6. n ech cse, the subgroup A viruses produced high focus counts on the line 6 (C/O) nd no foci on the line 7 (C/A, B) cell sheets. However, foci were noticed on some of the C/A,B cell sheets when inoculted with subgroup B nd C viruses. The significnce of these foci will be considered in the Discussion. t ws rbitrrily decided to cll embryos with %- or less of the line 6 control count resistnt for the purpose of clssifying culture. Tble 7 gives the phenotypic clssifiction of TABLE 7. Phenotypes of test-cross embryos, bsed on susceptibility to SR-RSV- nd SR-RSV-2 o;ily, with % of the linte 6 focus coutnts s the cr'iterionl of' resistnice Dm C/o C/A C/B C/A,B Totl Totl test-cross embryos bsed on the susceptibility of embryo tissue cultures to SR-RSV- nd SR-RSV-2 (stocks produced t this lbortory). nocultion with SR-RSV- gve rtio of 62 susceptible (C/O nd C/B) to 65 resistnt (C/A nd C/A,B), n excellent fit to the expected : segregtion t the tv locus. For SR-RSV-2, the rtio ws 73 susceptible (C/O nd C/A) to 5 resistnt (C/B nd C/A,B). This rtio is not significntly different from :. The rtio of 72 prentl (C/O, C/AB) to 55 recombinnt (C/A, C/B) phenotypes, while showing n excess of prentl phenotypes, is not significntly different from the : rtio expected for independent segregtion. To investigte the possibility tht genes independent of the tv nd tvb loci control cell surfce property specific for the proposed subgroup C viruses, composite tbultion of the cellulr phenotypes from ll six inocul ws mde. Sufficient informtion ws vilble for clssifiction of 22 embryos. Agin, the criterion used to define resistnce ws plting efficiency of % or less compred with the line 6 controls. The involvement of three independent loci in the genetic cellulr resistnce seen in our mteril would led to the ppernce of eight cellulr phenotypes in equl frequencies. However, only four phenotypes occurred in pprecible frequency (Tble 8). The phenotypes for susceptibility nd resistnce to the subgroup A nd B viruses segregted pproximtely : nd were independent s Downloded from on December 23, 28 by guest
6 VOL., 967 TABLE 8. LOC FOR AVAN LEUKOSS-SARCOMA VRUSES Cell phenotypes of test-cross embryos determined by use of % of the line 6 focus counts s the criterion of resistnice for ll six virus stocks Dm C/O C/A C/B C/C C/A, B C/A, C C/B, C C/A, B, C Totl Totl before. However, the response to the proposed subgroup C viruses gve segregtion rtio of 9 susceptible to 3 resistnt, 3: rtio, s ws found on the CAM ssy with. Furthermore, subgroup C susceptibility is clerly dependent on both the tv nd tvb loci. Tht is, the cells susceptible to either A or B subgroups (or both) re usully susceptible to subgroup C. The 3 : rtio observed is consequence of this dependence. As pointed out in the previous section, it ws sometimes difficult to identify the cellulr phenotypes with certinty. We believe tht the cses in which presumptive subgroup C susceptibility or resistnce ppers to be independent of the phenotypes controlled by the tv nd tvb loci represent errors of clssifiction. DsCUSSON Both the CAM nd tissue culture ssy systems confirm tht two single-utosoml-dominnt genes control susceptibility to subgroup A nd B viruses, respectively. There is no evidence of sex linkge becuse the segregtion of progeny of F dms produced by reciprocl mtings of lines 6 nd 7 ws :. Also, mle nd femle progeny ech gve : rtios of susceptibility to resistnce on CAM ssy. Results of both methods of ssy susceptibility indicte tht the genes controlling to subgroup A nd B viruses re inherited independently, showing tht the tv nd tvb loci re not closely linked. CZ-RSV nd hve been tenttively plced in subgroup C (5). The present dt indicte tht the bility of these viruses to infect cells is influenced by both the tv nd tvb loci. This suggests tht these virus preprtions re pproximtely equl mixtures of subgroup A nd B viruses or tht single prticles possess protein cot properties complementry to cell surfce sites for ttchment or entry of both subgroup A nd B viruses. The ltter could occur either by genetic recombintion of the subgroup A nd B controlling elements so tht they occur in one prticle, or by production of protein envelopes with both specificities by dul infection with subgroup A nd B viruses, tht is, phenotypic mixing. nvestigtions of cloned virus stocks re necessry to differentite mong these severl lterntives. Recent studies by Vogt (Virology, in press) show tht phenotypic mixing mong two subgroups, A nd B, does occur in the vin tumor viruses. A smll proportion of embryos ppered to hve phenotypes for susceptibility to subgroup C viruses independent of the tv nd tvb loci. t is unlikely tht these re due to close linkge of tvc locus to the other two loci, for two resons. First, segregtion of three susceptible embryos to one resistnt embryo is observed fter inocultion with these viruses, wheres : rtio would be expected if single tvc locus controlled resistnce. Second, if third locus were closely linked to the tv nd tvb loci, these lso should show evidence of linkge with ech other. They do not. t is most likely tht the exceptionl phenotypes occurred through misclssifiction, but the possibility of their existence should not be ignored. t is cler, then, tht t lest the mjor portions of the CZ-RSV nd stocks re probbly not of third subgroup, C, t lest by host rnge criteri. The successful infection of C/A,B cells nd embryos, prticulrly with subgroup B viruses, rises the question of the degree of resistnce controlled by these loci. At lest two lterntives to true infection of C/A,B cells with subgroup A or B viruses exist. One is tht some vible cells re present in the inoculum nd produce foci or pocks through trnsplnttion nd virus production. This is possible becuse the inocul were centrifuged but not filtered or subjected to ultrsonic vibrtion. However, ech inoculum did go through t lest two cycles of freezing nd thwing. t seems unlikely tht the presence of vible cells is the full explntion, becusethemethods of preprtion of the two SR-RSV-2 stocks were very similr to the methods used for the stock showing lrger differences in titer between the C/O nd C/A,B phenotypes (Tble 3). The fct tht difference in titer found with the reltively pure stock of BH-RSV(RAV-2) ws much greter thn in the cse of SR-RSV-2 suggests tht prticulrly the SR-RSV,, nd CZ-RSV stocks my contin to % of true subgroup C Downloded from on December 23, 28 by guest
7 9 CRTTENDEN ET AL. J. VROL. virus which does grow in C/A, B cells. Observtions by Vogt, shizki, nd Duff (Proceedings of the Symposium on Subvirl Crcinogenesis, Ngoy, Jpn, in press) confirm the presence of lrge proportion of subgroup A nd B viruses in the nd CZ-RSV stocks. Furthermore, they found evidence for smll proportion of virus plting on C/A,B cells in these stocks. The fct tht RAV-5 ws isolted from SR-RSV (5) nd hs been shown to be lrgely subgroup C suggests tht our stocks of SR-RSV-2 could hve been mixed with virus of this subgroup. Therefore, it seems most likely tht virl mixtures explin the unexpected susceptibility of C/B embryos nd cells. LTERATURE CTED. CRFTENDEN, L. B., AND W. OKAZAK Genetic influence of the Rs locus on susceptibility to vin tumor viruses.. Neoplsms induced by RPL2 nd three strins of Rous srcom virus. J. Ntl. Cncer nst. 35: CRTTENDEN, L. B., AND W. OKAZAK Genetic influence of the Rs locus on susceptibility to vin tumor viruses.. Rous srcom virus ntibody production fter strin RPL2 virus inocultion. J. Ntl. Cncer nst. 36: CRTTENDEN, L. B., W. OKAZAK, AND R. H. REAMER. 96. Genetic control of responses to Rous srcom nd strin RPL2 viruses in the cells, embryos, nd chickens of two inbred lines. Nt]. Cncer nst. Monogrph 7: GROUPE, V., V. C. DUNKEL, AND R. A. MANAKER mproved pock counting method for the titrtion of Rous srcom virus in embryonted eggs. J. Bcteriol. 7: HANAFUSA, H., AND T. HANAFUSA Determining fctor in the cpcity of Rous srcom virus to produce tumors in mmmls. Proc. Ntl. Acd. Sci. U. S. 55: SHZAK, R., AND P. K. VOGT mmunologicl reltionships mong envelope ntigens of vin tumor viruses. Virology 3: OKAZAK, W. 96. Discussion. Ntl. Cncer nst. Monogrph 7: PAYNE, L. N., AND P. M. BGGS. 96. Differences between highly inbred lines of chickens in the response to Rous srcom virus of the choriollntoic membrne nd of embryonic cells in tissue culture. Virology 2: PAYNE, L. N., AND P. M BGGS Genetic bsis of cellulr susceptibility to the Schmidt- Ruppin nd Hrris strins of Rous srcom virus. Virology 29: PURCHASE, H. G., AND W. OKAZAK. 96. Morphology of foci produced by stndrd preprtions of Rous srcom virus. J. Ntl. Cncer nst. 32: RUBN, H Genetic control of cellulr susceptibility to pseudotypes of Rous srcom virus. Virology 26: SARMA, P. S., R. J. HUEBNER, AND D. ARMSTRONG. 96. A simplified tissue culture tube neutrliztion test for Rous srcom virus ntibodies. Proc. Soc. Exptl. Biol. Med. 5: TEMN, H. M., AND H. RUBN Chrcteristics of n ssy of Rous srcom virus nd Rous srcom cells in tissue culture. Virology 6: VOGT, P. K., AND R. SHZAK Reciprocl ptterns of genetic resistnce to vin tumor viruses in two lines of chickens. Virology 26: VOGT, P. K., AND R. SHZAK Ptterns of virus interference in the vin leukosis nd srcom complex. Virology 3: Downloded from on December 23, 28 by guest
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