EBM Email Content Delivery
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Medarova, Z.
Right arrow Articles by Taylor, R. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Medarova, Z.
Right arrow Articles by Taylor, R. L., Jr.
Experimental Biology and Medicine 227:158-163 (2002)
© 2002 Society for Experimental Biology and Medicine

ORIGINAL ARTICLE

Alloantigen System L Affects the Outcome of Rous Sarcomas1

Zdravka Medarova*, W. Elwood Briles{dagger} and Robert L. Taylor, Jr.*,2

* Department of Animal and Nutritional Sciences, University of New Hampshire, Durham, New Hampshire 03824; and
{dagger} Department of Biological Sciences, Northern Illinois University, DeKalb, Illinois 60115


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
This study was designed to examine the alloantigen system L effects on Rous sarcomas in three B complex genotypes. The parental stock was 50% Modified Wisconsin Line 3 x White Leghorn Line NIU 4 and 50% inbred Line 6.15-5. Pedigree matings of two B2B5 L1L2 sires to five B2B5 L1L2 dams per sire produced experimental chicks segregating for B and L genotypes. Chicks were inoculated with 20 pock-forming units (pfu) of Rous sarcoma virus (RSV) at 6 weeks of age. Tumors were scored six times over 10 weeks postinoculation after which the tumor scores were used to assign a tumor profile index (TPI) to each chicken. Tumor growth over time and TPI were evaluated by repeated-measures analysis of variance and analysis of variance, respectively. Six trials were conducted with a total of 151 chickens. The major histocompatibility (B) complex affected the responses as the B2B2 and B2B5 genotypes had significantly lower tumor growth over time and TPI than the B5B5 genotype. Separate analyses revealed no significant L system effect in B2B2 or B2B5 backgrounds. However, L genotype significantly affected (P < 0.05) both tumor growth over time and TPI in B5B5 chickens. B5B5 L1L2 birds had TPI significantly lower than B5B5 L1L1 chickens but not B5B5 L2L2. Mortality was lower in the B5B5 L1L2 birds than in B5B5 L2L2 chickens. The L system, or one closely linked, affects the growth and ultimate outcome of Rous sarcomas. The response may depend upon the genetic background as well as MHC type.

Key Words: erythrocyte alloantigen • major histocompatibility (B) complex • oncogene • Rous sarcoma virus • tumor


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Genetic variation in antigenic determinants among members of a species produces alloantigens. Numerous alloantigens have been described based on immunogenetic analysis of antisera resulting from exchange of blood between individual animals. Chicken erythrocyte alloantigen systems A, B, C, D, E, H, I, J, K, L, N, P, and R (1) have been identified by serological reactions or by other methods. The B blood group was one of the earliest alloantigen systems described (2). Schierman and Nordskog (3) subsequently found that the B blood group was associated with skin homograft tolerance and thus established that the B system was the major histocompatibility complex (MHC) in the chicken. The B complex has a pivotal role in immune responsiveness and the outcome of pathogenic challenges (4, 5).

Gilmour (6) and Briles (7) independently discovered the L alloantigen system and established that two haplotypes, L1 and L2, segregate. The L locus segregates independently from nine other erythrocyte alloantigen systems (1), but has not been assigned to a linkage group. Alloantigen typing showed that the L system did not segregate (8) in a reference population established for molecular mapping. In addition to the described L haplotype associations with responses to Rous sarcomas virus (RSV)-induced tumors, other investigations have revealed L allele frequency alterations following divergent selection for bursa size (9) and fertility changes among different L genotypes (10). Taylor and Briles (11) examined the effect of eight non-MHC alloantigen systems on resistance and susceptibility to Eimeria tenella in both B2B2 and B2B5 backgrounds. The authors found an association only between the L system and cecal lesions. B2B2L1L1 chickens had higher lesion scores than B2B2L1L2 and B2B2L2L2 chickens. No significant L genotype effect was observed in a B2B5 background.

Rous sarcoma is a connective tissue tumor caused by the RSV, an oncogenic RNA virus. Tumors develop after injection of the virus into susceptible chickens. The tumors may regress or progress depending on the level of antitumor immune response produced by the MHC (12, 13). Variation in RSV tumor outcome among identical MHC genotypes from crosses of inbred lines differing at the MHC (12, 14–17), among different inbred lines identical at the B complex (18–20), or among crosses of noninbred lines (21, 22) implicated a role for non-MHC genes. For example, non-MHC T lymphocyte alloantigens, Ly-4 and Th-1, and the B lymphocyte alloantigen Bu-1 interacted to alter the response against RSV tumors in crosses of B2B2 inbred lines (19, 20).

Two previous studies found L alloantigen effects on the response to Rous sarcomas. Collins (23) studied the effect of alloantigen systems C, D, E, I, and L on tumor outcome in the F2 generation of inbred lines 63 x 100 that all had the B2B2 genotype. The C, D, E, and I systems did not influence tumor outcome. On the other hand, the L genotype significantly affected tumor growth in females, but not in males. LePage et al. (24) examined the effect of alloantigen systems A, C, D, E, H, I, L, and P on Rous sarcoma outcome in two B complex genotypes: B5B5, a tumor progressor, and B2B5, a moderate progressor. Alloantigen systems A, C, D, E, H, I, and P had no significant effect on tumor fate. The L genotype correlated with a differential tumor outcome. In the B2B5 genotypic background, the L1L1 chickens had lower tumor size, TPI, and mortality than the L1L2 chickens. Mortality was lower in L1L1 birds compared with L1L2 birds in the B5B5 background.

These earlier experiments indicate significant L alloantigen modulation of immune responses without complete B and L system segregation. The objective of this study is to further investigate L system effects on RSV-induced tumors. We used crosses producing progeny fully segregating for both the B complex and the L alloantigen. This structure allows examination of the L system effects in B genotypes that vary widely in their RSV-induced tumor outcome.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Stock.
Chickens for this study were derived from several lines. Line 6.15-5 is a congenic line (25) that was produced by crossing USDA-ADOL inbred Line 151 (B5B5) to USDA-ADOL inbred Line 61 (B2B2). After 10 backcross generations, heterozygous B2B5 chickens were mated inter se to produce Line 6.15-5 B5B5 birds that have 99.9% of the Line 61 genetic background. Modified Wisconsin Line 3 is an experimental population derived from Wisconsin inbred Line 3 Ancona (95% inbred) (26), originally homozygous for genes of all alloantigen loci except the B system. The modification consisted of introducing alloantigens for selected systems from White Leghorns and backcrossing two or more generations to Line 3. White Leghorn Line NIU 4 was derived over 20 generations from inter se matings of crosses between four commercial parent stocks and selecting for equal frequencies of alloantigens segregating at nine alloantigen loci.

Line 6.15-5 (B5B5 L1L1) dams were mated to B2B2 L1L2 sires from a line cross between modified Wisconsin Line 3 Ancona x White Leghorn line NIU 4 sires (B2B2 L1L2), as described by LePage et al. (24). Chickens from this mating that had the B2B5 L1L2 genotype contained 50% of the Line 6.15-5 genome and were used as parents to produce the experimental progeny. Pedigree matings of two B2B5 L1L2 sires to five B2B5 L1L2 dams per sire produced six hatches having one hundred fifty-one chicks segregating for all possible combinations of B and L genotypes. The birds were hatched at the University of New Hampshire Poultry Research Farm and were wing-banded for identification. Vaccinations against Marek's disease and Newcastle bronchitis were administered at hatch and 10 days, respectively. The chicks were housed in heated brooder batteries with water and food freely available. Six-week-old chicks were transferred to isolation cages for the remainder of the experiment.

Alloantigen Typing.
The chickens were typed for B and L systems in agglutination assays utilizing antisera specific for the haplotypes of the parental stocks (27). When chicks reached 3 weeks of age, 0.5 ml of blood was drawn from the wing vein to cold sodium citrate anticoagulant solution (68 µM sodium citrate/72 µM sodium chloride). Samples were shipped overnight with ice packs to Northern Illinois University. Fifty microliters of a 2% suspension of washed red blood cells was dispensed into tubes containing 100µl of antiserum specific for the B and L system haplotypes of interest. Following a 2-hr room-temperature incubation, the reaction mixtures were transferred to 3°C for an overnight incubation. The following day, cells were resuspended and scored visually for agglutination after a 1-hr incubation at room temperature.

RSV Challenge and Tumor Evaluation.
At six weeks of age, the birds were inoculated in the right wingweb with 20 pfu of the Bryan high-titer strain of RSV (RAV-1), subgroup A. Two weeks following RSV challenge, tumors were scored for size using the following scale: 0, no palpable tumor; 1, small tumor up to 0.5 cm in diameter; 2, tumor >0.5 up to 1.2 cm in diameter; 3, tumor >1.2 cm up to one-half of wingweb area; 4, tumor > one-half of wingweb area, but < entire wingweb area; 5, tumor filling the entire wingweb; 6, massive tumor extended beyond wingweb; and 7, death during the experiment (12). Tumor size was also scored at weeks 3, 4, 6, 8, and 10 postinoculation for a total of six tumor size scores over the 10-week experimental period. The six tumor size scores were then used to assign a TPI to each bird as an indicator of the tumor growth pattern. The TPI values were those of Collins et al. (28) where 1 = complete regression by 70 days postinoculation, or a decreasing slope, or complete regression by 56 days followed by recurrence; 2 = general upward trend, or plateau; slight regression after 56 days; 3 = terminal tumor after 42 days postinoculation; 4 = terminal tumor between 29 and 42 days postinoculation; and 5 = terminal tumor by 28 days postinoculation.

Statistical Analysis.
Tumor scores were analyzed by repeated measures analysis of variance (ANOVA) with hatch, sex, sire, dams within sire, time, B genotype, L genotype, and a B x L interaction as main effects. A large effect of B type led to separate analyses for each B genotype having hatch, sire, dams within sire, time, and L type as main effects. The TPI values were rank transformed and analyzed by ANOVA as described by Conover and Iman (29) with the same independent variables except time as in the repeated measures ANOVA. Significant differences between alloantigen system genotypes were determined using Fisher's protected LSD. Mortality rates were evaluated using chi-square analysis.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Alloantigen system genotypes for B and L segregated independently of each other in the 151 progeny. Repeated measures analysis of tumor score revealed a significant (P = 0.0001) B genotype effect on tumor growth. The significant (P = 0.0001) interaction between time and B genotype indicated that tumor growth differed over time for the B2B2, B2B5, and B5B5 genotypes (Fig. 1AGo). Analysis of the TPI values demonstrated a highly significant B genotype effect (P = 0.0001). The highest mean TPI, found in the B5B5 genotype (n = 31; TPI = 3.35 ± 0.18), was significantly greater than the TPI of B2B2 birds (n = 46; TPI = 1.43 ± 0.16) and B2B5 birds (n = 74; TPI = 1.36 ± 0.10; Fig. 1BGo). The B genotype significantly affected (P = 0.0001) mortality rates of 13.1%, 10.8%, and 77.4% for the B2B2, B2B5, and B5B5 genotypes, respectively (Table IGo, Analysis 1). No differences between males and females were detected.



View larger version (39K):
[in this window]
[in a new window]
  		Figure 1. Effect of B genotype on tumor size scores over a 10-week experimental period (A) and TPI in B2B2 (n = 46), B2B5 (n = 74), and B5B5 (n = 31) chicks inoculated with 20 pfu of Rous sarcoma virus (B). Tumor growth for the three B genotypes differs significantly (P = 0.0001) over time. Bars having no common letter differ significantly (P < 0.05).

 

View this table:
[in this window]
[in a new window]
  		Table I. Contingency Table Chi-Square Analyses of Mortality Due to Rous Sarcomas among Different Genotypes in Modified Wisconsin Line 3 x 6.15-5 White Leghorn Chickens
 
The overwhelming B genotype effect on tumor outcome led to separate analyses of L genotype effects on tumor score, TPI, and mortality within each specific B genotype. Therefore, L1L1, L1L2, and L2L2 birds were analyzed within the B2B2, B2B5, and B5B5 MHC types. No significant effect of L genotype on tumor score over time, TPI, or mortality was evident in either the B2B2 or B2B5 (data not shown) MHC genotype backgrounds. Both the B2B2 and B2B5 genotypes from this mating exhibited strong regression of RSV-induced tumors.

The L genotype, however, exerted a significant influence on tumor score, TPI, and mortality in the B5B5 genotypic background. Repeated measures analysis of tumor score indicated a significant change in tumor size over time (P = 0.0001), as well as a significant L genotype x time interaction (P = 0.00017). The overall pattern of tumor growth was an increase in tumor size 2, 3, and 4 weeks postinoculation, followed by a lower rate of tumor size increase in B5B5 L1L2 (n = 14) compared with either the B5B5 L1L1 (n = 5) or B5B5 L2L2 (n = 12) genotypes (Fig. 2AGo). Tumor size at 10 weeks postinoculation was diminished in the L1L2 genotype (5.43 ± 0.6) compared with either the L1L1 (7.00 ± 0.0) or L2L2 (6.83 ± 0.2) genotypes.



View larger version (38K):
[in this window]
[in a new window]
  		Figure 2. Effect of L alloantigen genotype on tumor size scores over a 10-week experimental period (A) and TPI in B5B5 L1L1 (n = 5), B5B5 L1L2 (n = 14), and B5B5 L2L2 (n = 12) chicks inoculated with 20 pfu of Rous sarcoma virus (B). Tumor growth for the three L genotypes differs significantly (P = 0.00017) over time. Bars having no common letter differ significantly (P < 0.05).

 
ANOVA of the TPI values also found a significant L genotype effect on tumor outcome (P = 0.023) in B5B5 chickens. The L1L2 genotype had TPI of 2.93 ± 0.3, which was significantly lower than the TPI values of L1L1 (4.00 ± 0.3), but not L2L2 (3.58 ± 0.3) chickens (Fig. 2BGo). Furthermore, chi-square analysis of mortality differences revealed a significant L effect (P = 0.046). The L1L2 genotype had the lowest mortality rate (57.1%), whereas the L2L2 and L1L1 genotypes had mortality rates of 91.7% and 100%, respectively (Table IGo, Analysis 2).


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Segregating combinations of two B and two L haplotypes produced nine different genotype combinations in the experimental progeny. The results are consistent with the differential B2B2 and B5B5 genotype effects on retroviral oncogene tumors reported previously. B2B2 chickens regress RSV tumors or v-src DNA tumors, whereas B5B5 hosts progress these tumors (12, 30). The same divergent B complex responses are evident in tumor metastasis (31, 32) as well as in immunity to a second inoculation of RSV or v-src DNA (32, 33). Other B complex haplotypes also differ in their responses to RSV tumors or v-src DNA tumors (34–36). Heterozygous B2B5 chickens usually have less tumor regression than B2B2 chickens (12, 31). The current study assessed different mating types compared with former experiments, therefore the profound similarity in B2B2 and B2B5 genotypes tumor growth may be due to non-MHC genes.

The L alloantigen genotypes were analyzed within each B genotype to eliminate the possibility that the powerful B complex effect would overcome any L system effects. No significant L effect was evident in either the B2B2 or B2B5 genotypic background, as both genotypes regressed tumors. A significant L influence, however, was evident in the B5B5 background. This result suggests that the robust tumor regression found in B2B2 and B2B5 birds masks the weak L effect, which becomes obvious only in the B5B5 progressor background. Based upon tumor growth over time, TPI, and mortality, the L1L2 genotype mitigated the progressive effect of the B5B5 genotype and did so significantly compared with the L1L1 genotype.

Two prior studies examined the L alloantigen system influence on Rous sarcomas. Among the F2 generation of B2B2 inbred lines 63 x 100, tumor fate was affected significantly by L genotype (23). Females of the L1L1 genotype had significantly lower TPI than the L2L2 genotype. No L genotype effect was found in males. LePage et al. (24) tested B2B5 and B5B5 progeny that segregated for at least two alleles of eight non-B alloantigen systems. Significant L alloantigen effects on Rous sarcomas were found in both B complex backgrounds. The L1L1 genotype was associated with lower tumor scores, TPI, and mortality than the L1L2 genotype in a B2B5 background. Lower mortality was found in B5B5 L1L1 chickens than in B5B5 L1L2 chickens.

The apparent disagreement of the present data with previous studies may be attributed to several factors. First, each study used a mating type with a different genetic background. Collins (23) used progeny from the cross of two inbred lines, LePage et al. (24) used progeny that were 50% Modified Wisconsin Line 3 and 50% White Leghorns, and the current study used progeny that consisted of 50% inbred line 6-15.5 and 50% Modified Wisconsin Line 3 x NIU 4 White Leghorns. Second, LePage et al. (24) used a higher virus dose (30 pfu) than this experiment (20 pfu). Virus dose may influence tumor growth in progressive genotypes (37), such as B5B5. Third, the current study is the only one that utilizes full segregation of B and L haplotypes. Effects of background genes, other than B and L, cannot be completely excluded by the results.

Growth and subsequent division of tumor cells as well as cellular recruitment via viral-replication genes (30) affect RSV tumor growth. T cells are principally responsible for RSV tumor regression (17, 19, 38, 39). Cross-reactions between tumor antigens and certain MHC haplotypes may impinge on antigen recognition. The B5 antigen cross-reacted to one or more RSV tumor antigens because Rous sarcoma progression increased in B2B2 chickens previously made tolerant to the B5 antigen from progressor chickens compared with untreated B2B2 controls (40, 41). Tumor regressor Line CB B12B12 chickens progressed a transplantable v-src-induced tumor after they were made tolerant to Line CC B4B4 or CB.R1, (B-F12 B-G4). This result supported a cross-reaction between the B4 antigen and a v-src tumor antigen (36).

The L1L2 genotype advantage in B5B5 tumor outcome indicates complementation. The host response to a tumor is a complex reaction to a multitude of antigens (42). Particular heterozygous combinations of MHC molecules may facilitate tumor or viral antigen recognition (43). Compared with the homozygotes, a heterozygote may complement through either improved recognition efficiency of the same number of antigens or increased recognition of additional antigens. The L1L2 genotype or closely linked genes, in B5B5 chickens of the current study, may have enhanced the immune response against RSV tumors by interacting with an effector molecule, facilitating viral or tumor antigen interaction with effector molecules or partially overcoming the B5 antigen-associated tolerance to tumor antigens. These effects might be accomplished through increased T cell activation, B complex antigen expression, or both.

Plachy (44) described MHC and non-MHC gene complementation in crosses of the Prague congenic inbred lines, CB (B12B12), CB.I (B7B7), and inbred line IA (B7B7). Chickens of the B12B7 genotype from either CB x CB.I or CB x IA matings had more regressing tumors than either B12B12 or B7B7 chickens, indicating complementation between the B12 and B7 haplotypes. In addition, greater tumor regression was evident in the B12B7 genotype CB x IA chickens than in the same genotype from the CB x CB.I mating, denoting a non-MHC gene effect that was complementary. Matings of Line CC (B4B4) with CB.I and IA revealed similar MHC and non-MHC complementation that was independent of age. B4B7 chickens from the CC x IA mating had more tumor regression than CC x CB.I cross (44).

Other non-MHC genes have demonstrated complementary effects on the outcome of Rous sarcomas. Gilmour et al. (19) studied progeny derived from inbred line crosses identical for the MHC (B2B2) but segregating for Ly-4 and Th-1 non-MHC T cell-surface antigen genes. A homozygous/heterozygous interaction was found in that Ly-4aLy-4a/Th-1aTh-1b and Ly-4aLy-4b/Th-1aTh-1a genotypes had increased RSV tumor regression. The interaction between the a and b haplotypes occurred when the other locus was the aa genotype. Another example of complementation occurred between non-MHC B and T cell alloantigens, Bu-1 and Ly-4. Progeny from a different cross of B2B2 inbred lines had greater RSV tumor regression due to complementation between the Ly-4a and Bu-1b alleles or the Ly-4b and Bu-1a alleles (20).

Genes other than the MHC can affect the RSV tumor progressive B5B5 genotype. Collins et al. (22) examined Rous sarcoma metastasis in B5B5 hosts from two populations: (Line 61 x Line 151) F5 White Leghorn cross and (Line 61 x Line 151) F5 Leghorn x Line UNH 105 New Hampshire F2. The incidence of tumor metastasis was significantly lower in the B5B5 White Leghorn x UNH 105 cross than in the B5B5 White Leghorn population, suggesting a possible non-MHC background effect on metastasis. Another study found that B5B5 birds having alloantigen haplotypes D1+ or I8+ had significantly lower TPI than those with D1- or I8- (24). Mortality in B5B5 chickens was lowered by the L1L1 genotype compared with the L1L2 genotype (24). However, that study used chickens with a different genetic background and used two B genotypes with three L genotypes compared with the current research that has full segregation of B and L genotypes.

The present experiments revealed that the B complex and the L alloantigen system significantly affected tumor growth over time, TPI, and mortality due to RSV-induced tumors. This work also adds unique information regarding L alloantigen effects on the immune response to Rous sarcomas in the context of B2 and B5 haplotype segregation. Complementation by the L1L2 genotype in the B5B5 birds supports the conclusion that the L alloantigen system, or some closely linked gene(s), has significant effects on the fate of Rous sarcomas. Further research should examine possible interactions between the L system, different B haplotypes, and other non-MHC genes.


   Acknowledgments
 
The authors are grateful to Lynda Caron (Department of Animal and Nutritional Sciences, University of New Hampshire) for technical support. We also thank Ruth Briles and Linda Yates from the Department of Biological Sciences (Northern Illinois University) for technical assistance in genotyping. Preparation of typing antisera was supported by grants DCB-8718672, DCB-9020138, and MCB-9631979 from the National Science Foundation.


   Footnotes
 
1 This is Scientific Contribution Number 2080 from the New Hampshire Agricultural Experiment Station. Back

2 To whom requests for reprints should be addressed at Department of Animal and Nutritional Sciences, University of New Hampshire, Kendall Hall, Durham, NH 03824. E-mail: bob.taylor{at}unh.edu Back


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Dietert MF, Taylor RL Jr, Dietert RR. Avian blood groups. Poult Sci Rev 4:87–105, 1992.
  2. Briles WE, McGibbon WH, Irwin MR. On multiple alleles effecting cellular antigens in the chicken. Genetics 35:633–652, 1950.[Free Full Text]
  3. Schierman LW, Nordskog AW. Relationship of blood type to histocompatibility in chickens. Science 134:1008–1009, 1961.[Abstract/Free Full Text]
  4. Dietert RR, Taylor RL Jr, Dietert MF. Biological functions of the chicken major histocompatibility complex. Crit Rev Poult Biol 3:111–129, 1991.
  5. Kaufman J, Salomonsen J. The ``minimal essential Mhc'' revisited: both peptide-binding and cell surface expression of MHC molecules are polymorphisms selected by pathogens in chickens. Hereditas 127:67–73, 1997.[Medline]
  6. Gilmour DG. Segregation of genes determining red cell antigens at high levels of inbreeding in chickens. Genetics 44:14–33, 1959.[Free Full Text]
  7. Briles WE. Additional blood group systems in the chicken. Ann NY Acad Sci 97:173–183, 1962.
  8. Crittenden LB, Provencher L, Santangelo L, Levin I, Abplanalp H, Briles RW, Briles WE, Dodgson JB. Characterization of a red jungle fowl by white Leghorn backcross reference population for molecular mapping of the chicken genome. Poult Sci 72:334–348, 1993.
  9. Scott TR, Oduho GW, Glick B, Hagan F, Briles WE, Yamamoto Y. Erythrocyte alloantigen diversity and some immunological effects of the B system in related New Hampshire strains. Poult Sci 67:1210–1217, 1988.[Medline]
  10. DeSilva PLG. Heterozygocity at red cell antigen locus L and fertility in chickens. Genetics 51:41–48, 1965.[Free Full Text]
  11. Taylor RL Jr, Briles WE. Non-MHC alloantigen effects on resistance and susceptibility to Eimeria tenella. Poultry Sci 79(Suppl. 1):39, 2000.
  12. Collins WM, Briles WE, Zsigray RM, Dunlop WR, Corbett AC, Clark KK, Marks JL, McGrail TP. The B locus (MHC) in the chicken: association with the fate of RSV-induced tumors. Immunogenetics 5:333–343, 1977.
  13. Schierman LW, Watanabe DH, McBride RA. Genetic control of Rous sarcoma regression in chickens: linkage with the major histocompatibility complex. Immunogenetics 5:325–332, 1977.
  14. Brown DW, Collins WM, Zsigray RM, Briles WE. A non-MHC genetic influence on response to Rous sarcoma virus-induced tumors in chickens. Avian Dis 28:884–899, 1984.[Medline]
  15. Plachy J, Hala K, Benda V. Regression of tumors induced by virus in Rous sarcoma different inbred lines of chickens. Folia Biol (Praha) 25:335–336, 1979.
  16. Plachy J. Hierarchy of the B (MHC) haplotypes controlling resistance to Rous sarcomas in a model of inbred lines of chickens. Folia Biol (Praha) 30:412–425, 1984.
  17. Plachy J, Benda V, Karakoz I, Spatenkova Z. Different importance of primary lymphoid organs for Rous sarcoma regression in inbred lines of chickens. Folia Biol (Praha) 30:177–188, 1984.
  18. Collins WM, Heinzelmann EW, Corbett AC, Zsigray RM, Dunlop WR. Rous sarcoma regression in seven highly inbred lines of white leghorns. Poult Sci 59:1172–1177, 1980.[Medline]
  19. Gilmour DG, Collins WM, Fredricksen TL, Auclair B, Clark KK, Urban WE Jr. Influence of non-MHC T lymphocyte alloantigens on regression of Rous sarcomas in the chicken. Immunogenetics 17:43–54, 1983.[Medline]
  20. Gilmour DG, Collins WM, Fredricksen TL, Urban WE. Genetic interaction between non-MHC T- and B-cell alloantigens in response to Rous sarcomas in chickens. Immunogenetics 23:1–6, 1986.[Medline]
  21. Collins WM, Briles WE, Corbett AC, Clark KK, Zsigray RM, Dunlop WR. B locus (MHC) effect upon regression of RSV-induced tumors in noninbred chickens. Immunogenetics 9:97–100, 1979.
  22. Collins WM, Brown DW, Ward PH, Dunlop WR, Briles WE. MHC and non-MHC genetic influences on Rous sarcoma metastasis in chickens. Immunogenetics 22:315–321, 1985.[Medline]
  23. Collins WM. Genetic influences on the fate of RSV-induced tumors in chickens. In: Poultry Breeders of America, Eds. Proceedings of the 28th National Breeder's Roundtable. Kansas City, MO: Poultry Breeders of America, pp1–14, 1979.
  24. LePage KT, Briles WE, Kopti F, Taylor RL Jr. Nonmajor histocompatibility complex alloantigen effects on the fate of Rous sarcomas. Poult Sci 79:343–348, 2000.[Abstract/Free Full Text]
  25. Dix MC, Taylor RL Jr. Differential antibody responses in 6.B major histocompatibility (B) complex congenic chickens. Poult Sci 75:203–207, 1996.[Medline]
  26. McGibbon WH. The genetics of green spotting on shanks of Ancona chickens. J Hered 69:97–100, 1978.[Abstract/Free Full Text]
  27. Briles WE, Briles RW. Identification of haplotypes of the chicken major histocompatibility complex (B). Immunogenetics 15:449–459, 1982.[Medline]
  28. Collins WM, Zervas NP, Urban WE Jr, Briles WE, Aeed PA. Response of B complex haplotypes B22, B24, and B26 to Rous sarcomas. Poult Sci 64:2017–2019, 1985.[Medline]
  29. Conover WJ, Iman RL. Rank transformations as a bridge between parametric and nonparametric statistics. Am Statistician 35:124–129, 1981.
  30. Taylor RL Jr, Ewert DL, England JM, Halpern MS. Major histocompatibility (B) complex control of the growth pattern of v-src DNA-induced primary tumors. Virology 191:477–479, 1992.[Medline]
  31. Collins WM, Dunlop WR, Zsigray RM, Briles RW, Fite RW. Metastasis of Rous sarcoma tumors in chickens is influenced by the major histocompatibility (B) complex and sex. Poult Sci 65:1642–1648, 1986.[Medline]
  32. Taylor RL Jr, England JM, Kopen GC, Christou AA, Halpern MS. Major histocompatibility (B) complex control of the formation of v-src-induced metastases. Virology 205:569–573, 1994.[Medline]
  33. Guyre PM, Zsigray RM, Collins WM, Dunlop WR. Major histocompatibility complex (B): effect on the response of chickens to a second challenge with Rous sarcoma virus. Poult Sci 61:829–834, 1982.[Medline]
  34. Plachy J, Karakoz I, Benda V. Concomitant immunity leads to retardation or acceleration of the growth of Rous sarcomas in genetically resistant or susceptible inbred lines of chickens. Folia Biol (Praha) 32:334–348, 1986.[Medline]
  35. Svoboda J, Plachy J, Hejnar J, Karakoz, I, Guntaka RV, Geryk, J. Tumor induction by the LTR, v-src, LTR DNA in four B (MHC) congenic lines of chickens. Immunogenetics 35:309–315, 1992.[Medline]
  36. Plachy J, Hala K, Hejnar J, Geryk J, Svoboda J. src-specific immunity in inbred chickens bearing v-src DNA- and RSV-induced tumors. Immunogenetics 40:257–265, 1994.[Medline]
  37. Vincent SC, Taylor RL Jr. Virus dilution affects the anti-Rous sarcoma response of progressor but not regressor major histocompatibility (B) complex genotypes. Poult Sci 67:1491–1496, 1988.[Medline]
  38. Cotter PF, Collins WM, Dunlop WR, Corbett AC. The influence of thymectomy on Rous sarcoma regression. Avian Dis 20:75–78, 1976.[Medline]
  39. Powell PC, Hala K, Bock G, Dietrich H, Wick G. Immune mechanisms in Rous sarcoma regression. In: Weber WT, Ewert DL, Eds. Avian Immunology. New York: Alan Liss, pp207–218, 1987.
  40. Heinzelmann EW, Zsigray RM, Collins WM. Cross-reactivity between RSV-induced tumour antigen and B5 MHC alloantigen in the chicken. Immunogenetics 13:29–37, 1981.[Medline]
  41. Heinzelmann EW, Zsigray RM, Collins WM. Increased growth of RSV-induced tumours in chickens partially tolerant to MHC alloantigens. Immunogenetics 12:275–284, 1981.[Medline]
  42. Brown DW, Collins WM, Ward PH, Briles WE. Complementation of major histocompatibility haplotypes in regression of Rous sarcoma virus-induced tumors in noninbred chickens. Poult Sci 61:409–413, 1982.[Medline]
  43. Lukacs NW, Briles WE, Briles RW, Taylor RL Jr. Response of major histocompatibility (B) complex haplotypes B22, B26 and B30 to Rous sarcomas. Poult Sci 68:233–237, 1989.[Medline]
  44. Plachy J. Age-dependent complementation of the B (MHC) alleles and a non-B allele controlling resistance to progression of Rous sarcomas, and genetic independence of resistance to induction of tumours in the model of inbred lines of chickens. Folia Biol (Praha) 31:284–296, 1985.[Medline]
Received for publication June 25, 2001. Accepted for publication October 26, 2001.





This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Medarova, Z.
Right arrow Articles by Taylor, R. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Medarova, Z.
Right arrow Articles by Taylor, R. L., Jr.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS