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Incomplete Restoration of the Bursa-Dependent Immune System

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Incomplete Restoration of the Bursa-Dependent Immune System Proc. Nat. Acad. Sci. USA Vol. 71, No. 3, pp. 957-961, March 1974 Incomplete Restoration of the Bursa-Dependent Immune System After Transplantation of Allogeneic Stem Cells into Immunodeficient Chicks (bursa of Fabricius/cell cooperation/cyclophosphamide/germinal centers/ histocompatibility antigens) PAAVO TOIVANEN, AULI TOIVANEN, AND TAPANI SORVARI Departments of Medical Microbiology, Medicine and Pathological Anatomy, Turku University, 20520 Turku, Finland Communicated by Robert A. Good, November 5, 1973 ABSTRACT Transplantation of allogeneic cells from The experiments to be described ill this paper indicate that bursa of Fabricius into cyclophosphamide-treated, im- munodeficient chicks resulted in immunological tolerance tranlsplantation of allogenieic stem cells into immun-odeficient to donor line skin grafts; graft-versus-host disease did not chicks results only in an incomplete restoration of the B im- occur. Allogeneic bursal stem cells taken from 3-day-old mune system even though GVH disease can be avoided. donors induced restoration of bursal morphology, of antibody formation to Brucella abortus and of occurrence of pyroninophilic cells and immunoglobulin-bearing cells MATERIALS AND METHODS in the peripheral lymphoid tissues. Secondary response to Experimental Design. Chicks treated with CY develop a sheep red blood cells and production of germinal centers were not restored. Transplantation of histocompatible permanllet severe hypogammaglobulinemia and atrophhy of bursal stem cells resulted in a complete reconstitution of the bursa (6, 7, 9). In this study, CY-treated 3-day-old chicks the bursa-dependent lymphoid system, both in function were transplanted with allogeneic bursa cells from 3-day-old and in morphology. Allogeneic postbursal stem cells taken donors (bursal stem cells) or from 10-wk-old donors (post- from the bursa of 10-week-old donors had a reconstitutive bursal stem cells). The controls include similar transplanta- effect only on the production of antibodies to Brucella. Transplanted stem cells maintained their functional po- tions using histocompatible donors as well as untransplanlted tential in the allogeneic environment, since, when trans- CY-treated and normal birds. Four to 5 weeks after cell ferred back to histocompatible hosts, they displayed nor- transplantation, the chickens were stimulated with Brucella mal function. These findings indicate that a complete abortus and sheep red blood cells (SRBC); antibody responses functional and morphological restoration of the bursa- in dependent immune system cannot be achieved without and histological changes the bursa, spleen, and cecal tonsils identity of the donor and recipient at loci near to or identi- were studied. cal with those determining the major histocompatibility antigens, even though graft-versus-host disease is avoided. Chickens. White Leghorn line P and line V chickens from This identity permits a full cooperation of the donor and our own colonies were used. B3oth lines are homozygous at the host cells. major histocompatibility locus: line P is of genotype B2B2 and the line V of genotype B15B'5. Individuals within the line Successful transplantation of allogeneic lymphoid cells in man are identical by the mixed leukocyte reaction; between the has been largely limited to the use of related donors com- individuals of different lines a strong reaction is obtained in patible with the recipients in major transplantation antigens-, both directions. As donors for skin grafting, White Leghorn and/or by mixed leukocyte reaction. Whenever other donors chickens of a random-bred line 53 were also employed. have been used, the major problem has been the graft-versus- host (GVH) disease (1, 2). For instance, in the treatment of CY Treatment. CY (LUike Oy, Turku, Finland) was in- severe combined immunodeficiency, transplantation of HL-A jected intraleritoneally on four consecutive days starting on unidentical stem cells has led to permanent immunological the day of hatching. A dose of 3.0 mg per chick per day was reconstitution of the patient in only three cases (3-5). used for line P chickens, and 4.0 mg per chick per day for the Chicks treated with cyclophosphamide (CY) in the newly- line V chickens. hatched period provide a unique experimental model for studying the fate of transplanted bursa-dependent (B) stem Cell Transplantations were made intravenously into 3-day- old chicks, more than 6 hr after the final CY inijection. cells in immunodeficient hosts (6, 7). The superiority of this model is particularly due to the reticular microenvironment Alntigenic Stimulation with SRBC and Brucella abortus was in the bursa of Fabricius left intact by the CY treatment, to accomlplished oni day 29 and day 36 after the cell transplanta- the ease of prel)aration of bursal stem cells, and to the in- tion (9). In the experiment with a serial cell transfer, a third ability of bursa cells to produce GVH reactions (8). We have stimulation was given on day 42. Both antigens were ad- recently demonstrated that transplantation of histocompat- ministered on each occasion. ible bursal or postbursal stem cells (9) into CY-treated chicks leads to a restoration of humoral immune functions (6, 7). Demonstraticn of Surface Imnunoglobldins. Suspensions of sl)leen lymiphocytes isolated by the Boy3um method (10) and Abbreviations: B, bursa-dependent or bursa-equivalent-de- of bursa lymphocytes were used. Rabbit antiserum to chicken pendent; CY, cyclophosphamide; GVH, graft-versus-host; immunooglobulinis and fluoresceini-isotlhiocy aiiate-conijugated SRBC, sheep red blood cell; T, thymus-dependent; wk, week. sheep antiserum to rabbit gammaglobulin were l)rel)ared in 957 Downloaded by guest on September 24, 2021 958 Immunology: Toivanen et al. Proc. Nat. Acad. Sci. USA 71 (1974) TABLE 1. Mortality after transplantation of allogeneic lin-fixed samples (12), with hematoxylin and eosin, and with lymphoid cells into 3-day-old CY-treated chicks van Gieson hematoxylin. Cells transplanted Recipients Statistics. X2 test and Student's t-test were used. No. Donor Deaths RESULTS (millions) line* Line* No. (%)t Source Ml1ortality from GVH Disease. When marrow, spleen, or None P 15 0 thymus cells from 10-wk-old line V donors were transplanted 3-day bursa 20 V P 15 0 into 3-day-old CY-treated recipients of line P, mortality due 10-wk bursa 100 V P 15 7 to the GVH disease was 80-100% in 60 days (Table 1). In a 10-wk thymus 100 V P 15 100 reverse combination, with the cell donors from line P and the 10-wk marrow 100 V P 15 80 recipients from line V, the mortality was 36-93%. With bursa 16 94 10-wk spleen 100 V P cells, either from 10-wk or 3-day-old donors, the mortality None V 15 7 was or nil in both combinations of donors and recip- 3-day bursa 20 P V 15 0 negligible 10-wk bursa 100 P V 15 0 ients used. Marrow, spleen, or thymus cells from 3-day-old 10-wk thymus 100 P V 14 93 donors were not used, since they are known not to contain 10-wk marrow 100 P V 14 36 stem cells for the B cell line (6). 10-wk spleen 100 P V 14 57 Line P lymphocytes were significantly (P < 0.01) less effective in producing GVH reactions than line V lymphocytes. Transplantation of cells from the same organs into histocom- This is in accordance with the data of Longenecker et al. (13) patible CY-treated recipients resulted in a mortality <7%. indicating that B2 allele is associated with a low GVH com- * Line Vr is of genotype B'5B15, line P of genotype B2B2. petence. All of our data presented below suggest that this low t In 60 days after transplantation. rate of proliferation in an allogeneic environment is not re- stricted to the cells responsible for the GVH activity but also includes bursa cells. The indirect immunofluorescence staining our laboratory. Antibody Formation. Transplantation of allogeneic bursal of living cells in suspension was at 4° (11). The performed stem cells (2 X 107 bursa cells from 3-day-old donors) into stained cells were examined with a Zeiss fluorescence micro- CY-treated chicks resulted in a significant restoration of anti- a fluorescein-isothiocyanate interference primary scope using body formation to Brucella when compared to the control filter, a 530 nm secondary filter, and a 100W halogen light birds treated with CY without a cell (Table 2). source. Cells with > three fluorescent spots on the membrane transplantation Responses to Brucella found in the birds transplanted with were recorded positive. allogeneic cells were only slightly less than those found after Skin Grafting. Full thickness skin grafts of 15 X 15 mm the transplantation of histocompatible cells. In a striking were taken from under the wing, of donors age-matched with contrast to these observations, only in one instance was a the recipients. They were placed onto a graft bed under the significant effect of the allogeneic transplantation found in wing and held in place with sutures. The grafts were observed the response to SRBC: when line V cells were transferred daily and a full stuffing was considered a rejection. into line P chickens, most of the recipients resl)onded to the first stimulation with SRBC. In the other allogeneic donor- Antibody Titrations, Autopsies, and Microscopic Examina- recipient combination, no response was observed to the first tion were carried out as previously (9). Tissue sections were stimulation with SRBC. Secondary responses to SRBC were stained with methyl-green-pyronin stain modified for forma- negligible in both of the allogeneic combinations. When histo- TABLE 2. Antibody responses
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