Tissue Antigens (1976), 8, 373-378 Published by Munksgaard, Copenhagen, Denmark N o part may be reproduced by any process without written permission from the author(s)
Joint Report of the Fourth Japan HLA Workshop: B Cell Workshop 1 M. Matsuyama7, T. Mori7, M. Aizawa', T. Akaza', T . Hasegawa", T. Inou", K. Itakura", T. Juji', M. Kiuchi3, M.R. Mickey", S. Naitog, K. Nomoto', K. Ohkochi', S. Saito", S. Sekiguchi4, P. I. Terasaki'', K. Tsuji', and T. Yoshida'. 'Hokkaido University, *Tokyo University, %hiba University, 4Kawasaki Ida Hospital, 5Tokai University, 'Aichi Cancer Center and Hamamatsu Medical College, 'Osaka University, 'Kyushu University, 'Fukuoka University, "Sapporo Medical College, "Tokyo University, Institute of Medical Science, "University of California at Los Angeles
Received for publication 27 September 1976, accepted 6 October 1976
Report of B-cell typing workshop of Japan I n o r d e r to study the B-cell specificities in the Japanese population, a large series of 405 Japanese were tested with a series of 51 pregnancy sera from Japanese that were specific for B lymphocytes a n d non-reactive with T lymphocytes. As a point of reference, 63 Caucasians were also tested with the same antisera a n d 5 Caucasian B-cell typing sera were utilized in testing the Japanese cells. T h e testing was done by 12 different laboratories, all using the same basic lymphocyte cytotoxicity test, consisting of isolating B lymphocytes by rosetting with sheep red blood cells, incubation with rabbit complement in t h e second stage, a n d followed by staining the dead cells with eosin. The evidence obtained, that many distinct B-cell
specificities probably exist in the Japanese population, is of great interest. T w o of these specificities have a n association with Terasaki B groups 1 a n d 4 (found first in Caucasians), while the remaining sera detect specificities of new groups. I n this workshop, 110 antisera were initially exchanged a n d tested on a panel of 480 B-cells and 480 T-cells from the same donors. This extensive testing of the sera on T lymphocytes has enabled us to identify sera containing contaminating antibodies of the HLA-A, -B, a n d -C loci. Sera containing activity against more than 5% of the test panel of T lymphocytes were eliminated from further consideration. In addition, sera that reacted with less than 5% of the B cells were not considered for this analysis,
This study was supported with funds from the Japanese Ministry of Education, Basis of Immunology and Cooperative Research 112101 and a grant from the National Institutes of Health, RR-3.
374
M . MATSUYAMA E T A L
since such reactivity was thought to be within the expected range of technical errors. The 56 remaining sera are the subject of this report. Chi-square, correlation coefficients and Mickey’s Boolean regression analysis were employed for statistical evaluation of the data. Eleven of the laboratories involved
in this workshop in Japan each tested 40-50 cells from healthy Japanese control subjects and the one laboratory in Los Angeles tested 65 healthy Caucasians. The laboratory numbers are those used to identify the authors of this report. Sera are referred to by their workshop numbers given in Table 1 .
Table 1 Summaries of B-Cell Frequencies, Correlated Clusters (X‘), and JW Groups (Mickey’s Analysis) Workshop Lab Serum SourceNo. Serum I 0
% B Cell Pos
Mickey’s Anal.ysis
Japn
Cauc
N=405 N=63
Serum SourceNo. Serum I 0
Cluster 1
% B Cell Pos Mickey’s Japn Cauc Analysis N=405 N=63
Miscellaneous Associations
12-A7165.22
1
11
30
46
7-6147
0
5
14
96
10-K-047
1,2,3,5
32
50
7-6-543
16
11
12 0
106 95
10-K-040
2,3,5,8,9
42
41 52
56
8-KY2757
0
7
105
11-L-147
1,2,6
25
86
57
8-KY2628
0
11
0
39
6-F-2004
6,s
22
58
36
6-F-2001
0
6
12
1,5,6,8
41
87
52
8-KY2465
0
5
10
39
75
9
2-8-327
0
7
5
13
0 0
4
37
6-F-2002
27
5-E5-264
38
6-F-2003
8
23
50
89
9-1-1428
8
20
33
28
2-6-665 5-E5-394
10
16 4
22
4-0-55
6
16
51
41
7-6-031
0
12
14
40
6-F-2005
6
14
81
51
7-6-546
0
5
7
44
7-6 -133
6
12
55
65
8-Ky2755
0
8
12
47
7-6-154
6
16
89
107
2
6
9
54
8-KY2464
6
17
60
17
4-0-50
11
17
2
71
9-1-861
6
16
42
78
7-6-139
6,12
20
100
55
15 19
13
83
9-1-1015
6,18
22
60
33
5-EG-10
7,8
11 10 38
2
45
9-1-1000 8-KY2525
30
5-EG-33
6,20
21
94
34
5-E5-359
32
23
*69
8-KY2754
0
6
0
72
9-1-864
7 9
21
24
*87
9-1-1419
0
6
3
*85
9-1-1020
14
13
12
*
5,6,8,14,17
12-F7007.00
56
Individual Sera (No rpO.35)
Possible cluster 1 sera in Japanese only. Cluster 2 91
9-1-1477
0
10
0
7 8
2-8-516
0
13
3
101
10-K-179
0
8
8
2-8-555
0
21
19
108
12-3357.12
3
5
19
12
2-8-496
0
9
7
110
12-00000.00 5
6
25
64
8-KY2451
0
10
2
109 10
12-04037.34 2-6-790
5
23
2
13
17
4
11 10
4
11
2-8-601
18
60
8-KY997
18
7
24
21
22
26
22
85
87
25
28
22
33
32
26
22
25
26
23
27
32
x
29
30
25
20
27
30
29
36
43
24
34
32
39
41
42
32
30 54
26
23
34
37
21
38
x
25
x
37
44 44
24
20
-37
44
x
21
51
40
31
40
24
39
32
22
41
35
46
35
38
60
50
31
x
73
35
35
54
55
42
29
22
21
47
-
28
23
25
35
33
43
22
45
38
38
34 42
x
21 44
26
31
31
x
32
26
70 69
33
x
32
44
26
25
23
29
32
30
50
26
52
43
62
50
31
40
30
21
83
x
34
45a
46
26
43
27
29
20
25
36
42
71
47
43
29
68
45
24
69
54
"Sera 45,69 are 100%positive and 0% respectively in Caucasians, therefore - indicates no r value calculated.
26
28
30
6ga
27
22
27
30
28
30
22
23
30
38
28
30
47
45
x
34
32
30
39
x
58
26
35
29
27
21
30
89
x
55
26
38
41
34
27
34
83
27
40
38
49
30
31
43
54
x
26
37
21
22
26
27
20
X
21
39
24
30
21
22
21
38 22
43
32
X
45a
71
21
47
54
-
29
44
28
22
20
40
20
21
38
22
89
45
38
22
44 24
27
37
39
95
33
27
x
70 32
31
105
26
24
91
x
105
X 22
96
95
106
96
106
Serum
Values are r
42 36
x
-
33
x
-
29
-33
23
49
-
85
6ga
Table 2 Cluster 1 Correlations 100. Associations with r < 0.20 are omitted. Upper-right half is Caucasians ( N = 61), lower-left half is Japanese ( N = 405).
X
-
30
21
87
u1
01 rl
n M r r
W
376
M. MATSUYAMA ET A L
Values are r X
Table 3 Cluster 2 Correlations 100. Associations with r < 0.20 are omitted. Upper-right half is Caucasians ( N = 61),lower-left half is Japanese ( N = 405).
Serum 7
7
8
12
64
x
47
70
8
48
x
57 58
12 64
29
X
20
109
109
10
11
60 21
70 35
50
42
57
81
24
100
48 57
Cauc
32
X
26
36
x
10
27
34
41
39
x
11
39
40
35
35
32
41
X
60
45
31
36
33
23
34
50
x
Japanese Note:
Low Frequencies i n Caucasians f o r t h i s Cluster
From a simple chi-square analysis and the selection of groups of sera that showed the highest correlations, the 1,485 pair combinations can be reduced to two clusters of sera which indicate associations (Tables 2 and 3) and a listing of paired sera showing associations (Table 4). Because of some distinct differences for reactivity of certain sera in the two races, the Caucasians and Japanese were examined separately. As shown in Table 2, 18 sera fell within one large cluster which showed association with several sera of that cluster. It can be noted that within this group some sera showed extremely high associations with each other in the Japanese, such as an r value of 0.60 between serum 47 an 45 and r of 0.58 for serum 37 with serum 27. T h e T e B group 1 serum 106 appears to fall within this cluster, although the association is not strong. Two combinations have high associations in both Japanese and Caucasians, with r values of 0.70 and 0.91 between sera 95 and 96 and r values of 0.54 and 0.73 between sera 40 and 47. Several combinations had highher associations in Caucasians, such as an r value of 0.69 for sera 39 and 54, r = 0.68 for sera 38 and 54, r = 0.70for sera 54 and 83 and r = 0.69 for sera 71 and 83. This group of sera may represent a subdivi-
sion within cluster 1 for Caucasians. It should be noted that sera 69, 85, and 87 fit into cluster 1 in Japanese but not in Caucasians. T h e second largest cluster of sera (Table 3) appears to be related to T e B group 4 (serum 109). T h e associations within this cluster are not as high as within the first cluster. T h e high r values in Caucasians may be invalid because of the low frequency of these particular sera in Caucasians. Sera pairs that resulted in r values greater than 0.35 in either race but did not fit into clusters 1 or 2 are listed in Table 4. These paired sera, which showed associations, may be considered to be nuclei for further clusters. Mickey’s Boolean regression analysis has permitted the further breakdown of these clusters into groups. As can be seen in Table 1, the sera, classified for 20 groups, fell into groups within the clusters and represent a further refinement of the clusters. Within cluster 1, certain sera can be provisionally subdivided into groups. T h e predominant group is JW6 (Japanese workshop group 6). These sera can also be seen to show high associations among themselves (Table 2). Thus, we can assume that such sera may be the best ones defining the best-defined
377
B CELL WORKSHOP 1
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N
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m 4 N
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378
M. M A T S U Y A M A E T A L
L 0
I
0
I63
50
80
I20
I
I
I
I
1 1
i
40
80
I20
I03
Figure I . Allelic pattern in Japanese of five Te B-cell groups defined by Caucasian sera. B groups 1 and 2 are part of the first B-cell locus and B groups 3, 4,and 5 are part of the second B-cell locus. The figure was d r a w n using all data from four of the Japanese laboratories. group of the workshop. Perhaps the most evidence was found in this workshop that striking feature about the specificities is the the allelism of the antigens may be the same assignment of so many different specificities in the two races. T h e 5 sera representing the by the regression analysis. Such a degree of 5 B-cell specificities of Terasaki were found diversity may be attributed to genuine diffe- to produce an allelic pattern of reactivity in rences in specificities, although the possibilJapanese (Fig. 1). Groups 1 and 2 o n one ity of generation by technical difficulties locus were negatively associated, and groups must he considered. 3, 4, and 5 on the second locus were also Of considerable interest is the difference negatively associated, a result previously in reactivity against a panel of Japanese reported in Caucasians (1). Caucasians versus a panel of Caucasian cells. As given in tested in the workshop were excluded in Table 1, certain marked differences in fre- constructing this figure. Thus, the Caucasian sera which had previously been shown quency were found. For example, within cluster 1 , all 18 sera (omitting 69,85,87) to producce such a picture of allelism when reacted with a higher frequency in Cauca- tested on Caucasians, also reacted with sians than in Japanese. T h e most extreme Japanese cells tested in Japanese laboratories in exactly the same allelic relaexample, serum 45, reacted with 20% of Japanese and 100% of Caucasians. T h e tionship. consistency of higher reactivity in Caucasians within this cluster of sera reconfirms Reference 1. the validity of the cluster in reflecting a Saito, S., Terasaki P.I., Rachelefsky, G . , Park, M.S. & Mickey, M.R. Transplant Proc. (in press). limited set of underlying specificities. T h e cluster 2 sera are also remarkable in that 8 of Address: the sera reacted in the reverse fashion; that Paul I. Terasaki, Ph.D. is, the B sera reacted with a higher fre- Department of Surgery University of California quency in Japanese than in Caucasians. 1000 Veteran Avenue Although it can thus be safely assumed Los Angeles that many differences in frequency of B-cell California antigens will be found in the two races, USA
Joint Report of the Fourth Japan HLA Workshop: B Cell Workshop 1 M. Matsuyama7, T. Mori7, M. Aizawa', T. Akaza', T . Hasegawa", T. Inou", K. Itakura", T. Juji', M. Kiuchi3, M.R. Mickey", S. Naitog, K. Nomoto', K. Ohkochi', S. Saito", S. Sekiguchi4, P. I. Terasaki'', K. Tsuji', and T. Yoshida'. 'Hokkaido University, *Tokyo University, %hiba University, 4Kawasaki Ida Hospital, 5Tokai University, 'Aichi Cancer Center and Hamamatsu Medical College, 'Osaka University, 'Kyushu University, 'Fukuoka University, "Sapporo Medical College, "Tokyo University, Institute of Medical Science, "University of California at Los Angeles
Received for publication 27 September 1976, accepted 6 October 1976
Report of B-cell typing workshop of Japan I n o r d e r to study the B-cell specificities in the Japanese population, a large series of 405 Japanese were tested with a series of 51 pregnancy sera from Japanese that were specific for B lymphocytes a n d non-reactive with T lymphocytes. As a point of reference, 63 Caucasians were also tested with the same antisera a n d 5 Caucasian B-cell typing sera were utilized in testing the Japanese cells. T h e testing was done by 12 different laboratories, all using the same basic lymphocyte cytotoxicity test, consisting of isolating B lymphocytes by rosetting with sheep red blood cells, incubation with rabbit complement in t h e second stage, a n d followed by staining the dead cells with eosin. The evidence obtained, that many distinct B-cell
specificities probably exist in the Japanese population, is of great interest. T w o of these specificities have a n association with Terasaki B groups 1 a n d 4 (found first in Caucasians), while the remaining sera detect specificities of new groups. I n this workshop, 110 antisera were initially exchanged a n d tested on a panel of 480 B-cells and 480 T-cells from the same donors. This extensive testing of the sera on T lymphocytes has enabled us to identify sera containing contaminating antibodies of the HLA-A, -B, a n d -C loci. Sera containing activity against more than 5% of the test panel of T lymphocytes were eliminated from further consideration. In addition, sera that reacted with less than 5% of the B cells were not considered for this analysis,
This study was supported with funds from the Japanese Ministry of Education, Basis of Immunology and Cooperative Research 112101 and a grant from the National Institutes of Health, RR-3.
374
M . MATSUYAMA E T A L
since such reactivity was thought to be within the expected range of technical errors. The 56 remaining sera are the subject of this report. Chi-square, correlation coefficients and Mickey’s Boolean regression analysis were employed for statistical evaluation of the data. Eleven of the laboratories involved
in this workshop in Japan each tested 40-50 cells from healthy Japanese control subjects and the one laboratory in Los Angeles tested 65 healthy Caucasians. The laboratory numbers are those used to identify the authors of this report. Sera are referred to by their workshop numbers given in Table 1 .
Table 1 Summaries of B-Cell Frequencies, Correlated Clusters (X‘), and JW Groups (Mickey’s Analysis) Workshop Lab Serum SourceNo. Serum I 0
% B Cell Pos
Mickey’s Anal.ysis
Japn
Cauc
N=405 N=63
Serum SourceNo. Serum I 0
Cluster 1
% B Cell Pos Mickey’s Japn Cauc Analysis N=405 N=63
Miscellaneous Associations
12-A7165.22
1
11
30
46
7-6147
0
5
14
96
10-K-047
1,2,3,5
32
50
7-6-543
16
11
12 0
106 95
10-K-040
2,3,5,8,9
42
41 52
56
8-KY2757
0
7
105
11-L-147
1,2,6
25
86
57
8-KY2628
0
11
0
39
6-F-2004
6,s
22
58
36
6-F-2001
0
6
12
1,5,6,8
41
87
52
8-KY2465
0
5
10
39
75
9
2-8-327
0
7
5
13
0 0
4
37
6-F-2002
27
5-E5-264
38
6-F-2003
8
23
50
89
9-1-1428
8
20
33
28
2-6-665 5-E5-394
10
16 4
22
4-0-55
6
16
51
41
7-6-031
0
12
14
40
6-F-2005
6
14
81
51
7-6-546
0
5
7
44
7-6 -133
6
12
55
65
8-Ky2755
0
8
12
47
7-6-154
6
16
89
107
2
6
9
54
8-KY2464
6
17
60
17
4-0-50
11
17
2
71
9-1-861
6
16
42
78
7-6-139
6,12
20
100
55
15 19
13
83
9-1-1015
6,18
22
60
33
5-EG-10
7,8
11 10 38
2
45
9-1-1000 8-KY2525
30
5-EG-33
6,20
21
94
34
5-E5-359
32
23
*69
8-KY2754
0
6
0
72
9-1-864
7 9
21
24
*87
9-1-1419
0
6
3
*85
9-1-1020
14
13
12
*
5,6,8,14,17
12-F7007.00
56
Individual Sera (No rpO.35)
Possible cluster 1 sera in Japanese only. Cluster 2 91
9-1-1477
0
10
0
7 8
2-8-516
0
13
3
101
10-K-179
0
8
8
2-8-555
0
21
19
108
12-3357.12
3
5
19
12
2-8-496
0
9
7
110
12-00000.00 5
6
25
64
8-KY2451
0
10
2
109 10
12-04037.34 2-6-790
5
23
2
13
17
4
11 10
4
11
2-8-601
18
60
8-KY997
18
7
24
21
22
26
22
85
87
25
28
22
33
32
26
22
25
26
23
27
32
x
29
30
25
20
27
30
29
36
43
24
34
32
39
41
42
32
30 54
26
23
34
37
21
38
x
25
x
37
44 44
24
20
-37
44
x
21
51
40
31
40
24
39
32
22
41
35
46
35
38
60
50
31
x
73
35
35
54
55
42
29
22
21
47
-
28
23
25
35
33
43
22
45
38
38
34 42
x
21 44
26
31
31
x
32
26
70 69
33
x
32
44
26
25
23
29
32
30
50
26
52
43
62
50
31
40
30
21
83
x
34
45a
46
26
43
27
29
20
25
36
42
71
47
43
29
68
45
24
69
54
"Sera 45,69 are 100%positive and 0% respectively in Caucasians, therefore - indicates no r value calculated.
26
28
30
6ga
27
22
27
30
28
30
22
23
30
38
28
30
47
45
x
34
32
30
39
x
58
26
35
29
27
21
30
89
x
55
26
38
41
34
27
34
83
27
40
38
49
30
31
43
54
x
26
37
21
22
26
27
20
X
21
39
24
30
21
22
21
38 22
43
32
X
45a
71
21
47
54
-
29
44
28
22
20
40
20
21
38
22
89
45
38
22
44 24
27
37
39
95
33
27
x
70 32
31
105
26
24
91
x
105
X 22
96
95
106
96
106
Serum
Values are r
42 36
x
-
33
x
-
29
-33
23
49
-
85
6ga
Table 2 Cluster 1 Correlations 100. Associations with r < 0.20 are omitted. Upper-right half is Caucasians ( N = 61), lower-left half is Japanese ( N = 405).
X
-
30
21
87
u1
01 rl
n M r r
W
376
M. MATSUYAMA ET A L
Values are r X
Table 3 Cluster 2 Correlations 100. Associations with r < 0.20 are omitted. Upper-right half is Caucasians ( N = 61),lower-left half is Japanese ( N = 405).
Serum 7
7
8
12
64
x
47
70
8
48
x
57 58
12 64
29
X
20
109
109
10
11
60 21
70 35
50
42
57
81
24
100
48 57
Cauc
32
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Japanese Note:
Low Frequencies i n Caucasians f o r t h i s Cluster
From a simple chi-square analysis and the selection of groups of sera that showed the highest correlations, the 1,485 pair combinations can be reduced to two clusters of sera which indicate associations (Tables 2 and 3) and a listing of paired sera showing associations (Table 4). Because of some distinct differences for reactivity of certain sera in the two races, the Caucasians and Japanese were examined separately. As shown in Table 2, 18 sera fell within one large cluster which showed association with several sera of that cluster. It can be noted that within this group some sera showed extremely high associations with each other in the Japanese, such as an r value of 0.60 between serum 47 an 45 and r of 0.58 for serum 37 with serum 27. T h e T e B group 1 serum 106 appears to fall within this cluster, although the association is not strong. Two combinations have high associations in both Japanese and Caucasians, with r values of 0.70 and 0.91 between sera 95 and 96 and r values of 0.54 and 0.73 between sera 40 and 47. Several combinations had highher associations in Caucasians, such as an r value of 0.69 for sera 39 and 54, r = 0.68 for sera 38 and 54, r = 0.70for sera 54 and 83 and r = 0.69 for sera 71 and 83. This group of sera may represent a subdivi-
sion within cluster 1 for Caucasians. It should be noted that sera 69, 85, and 87 fit into cluster 1 in Japanese but not in Caucasians. T h e second largest cluster of sera (Table 3) appears to be related to T e B group 4 (serum 109). T h e associations within this cluster are not as high as within the first cluster. T h e high r values in Caucasians may be invalid because of the low frequency of these particular sera in Caucasians. Sera pairs that resulted in r values greater than 0.35 in either race but did not fit into clusters 1 or 2 are listed in Table 4. These paired sera, which showed associations, may be considered to be nuclei for further clusters. Mickey’s Boolean regression analysis has permitted the further breakdown of these clusters into groups. As can be seen in Table 1, the sera, classified for 20 groups, fell into groups within the clusters and represent a further refinement of the clusters. Within cluster 1, certain sera can be provisionally subdivided into groups. T h e predominant group is JW6 (Japanese workshop group 6). These sera can also be seen to show high associations among themselves (Table 2). Thus, we can assume that such sera may be the best ones defining the best-defined
377
B CELL WORKSHOP 1
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Figure I . Allelic pattern in Japanese of five Te B-cell groups defined by Caucasian sera. B groups 1 and 2 are part of the first B-cell locus and B groups 3, 4,and 5 are part of the second B-cell locus. The figure was d r a w n using all data from four of the Japanese laboratories. group of the workshop. Perhaps the most evidence was found in this workshop that striking feature about the specificities is the the allelism of the antigens may be the same assignment of so many different specificities in the two races. T h e 5 sera representing the by the regression analysis. Such a degree of 5 B-cell specificities of Terasaki were found diversity may be attributed to genuine diffe- to produce an allelic pattern of reactivity in rences in specificities, although the possibilJapanese (Fig. 1). Groups 1 and 2 o n one ity of generation by technical difficulties locus were negatively associated, and groups must he considered. 3, 4, and 5 on the second locus were also Of considerable interest is the difference negatively associated, a result previously in reactivity against a panel of Japanese reported in Caucasians (1). Caucasians versus a panel of Caucasian cells. As given in tested in the workshop were excluded in Table 1, certain marked differences in fre- constructing this figure. Thus, the Caucasian sera which had previously been shown quency were found. For example, within cluster 1 , all 18 sera (omitting 69,85,87) to producce such a picture of allelism when reacted with a higher frequency in Cauca- tested on Caucasians, also reacted with sians than in Japanese. T h e most extreme Japanese cells tested in Japanese laboratories in exactly the same allelic relaexample, serum 45, reacted with 20% of Japanese and 100% of Caucasians. T h e tionship. consistency of higher reactivity in Caucasians within this cluster of sera reconfirms Reference 1. the validity of the cluster in reflecting a Saito, S., Terasaki P.I., Rachelefsky, G . , Park, M.S. & Mickey, M.R. Transplant Proc. (in press). limited set of underlying specificities. T h e cluster 2 sera are also remarkable in that 8 of Address: the sera reacted in the reverse fashion; that Paul I. Terasaki, Ph.D. is, the B sera reacted with a higher fre- Department of Surgery University of California quency in Japanese than in Caucasians. 1000 Veteran Avenue Although it can thus be safely assumed Los Angeles that many differences in frequency of B-cell California antigens will be found in the two races, USA
