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Studies of Thymic Function with Emphasis on the Role of the Thymus in Oncogenesist

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Studies of Thymic Function with Emphasis on the Role of the Thymus in Oncogenesist [CANCER RESEARCH 26 Part I, 551-574, April 1966] Studies of Thymic Function with Emphasis on the Role of the Thymus in Oncogenesist LLOYDW. LAW National Cancer Institute, Bethesda, Maryland This presentation will be concerned with 2 general topics: organ to other sites occurs with a selective seeding in spleen (a) our present knowledge of thymic structure and function, lymph nodes, and other lymphoid organs. but particularly the latter, as revealed by the results of recent For a more detailed discussion of the ontogeny of the thymus experiments in several species of animals following early thymic and its microscopic anatomy, the reader is referred to the studies ablation, and (b) consideration of the precise role of the thymus in of Smith (97) and of Ruth et al. (92). the initiation and suppression of neoplastic growths. Pertaining to Thymic Structure and Function Origin and Early Structure of the Thymus In most species the thymus is located in the upper anterior The thymus is a compound organ consisting of 3 quite different part of the chest. Exceptions are the chicken and guinea pig. cell systems: (a) lymphoid cells, (b) reticulum cells, and (c) The absolute size varies from species to species but the absolute e[)ithehal cells. The latter 2 may be referred to as the epithelial size of thymic lobules appears to be remarkably uniform in the reticulum cell complex. The thymus in mammals arises as various species, suggesting that there may be a critical limit for paired structures from the endoderm of the 3rd and 4th branchial the size of a thymic lobule. The incompletely divided lobules are [)OUcheS. Thymic tissue on each side, along with parathyroid composed of a medulla of mixed cells of the ej)ithelial reticulum elements, migrates caudally and eventually reaches the upper complex and lymphoid cells surrounded by a cortex in which mediastinum. In some strains of mice deposits of thymic tissue tightly packed lymphoid cells are embedded in a meshwork of remain in the thyroid-parathyroid area as ectopic thymus and epithehal reticulum cells. The lymphoid cortex has certain probably become functional (49). The thymus remains irnrely features which set it apart from other lymphoid organs. The epithelial with a connective tissue capsule of mesenchyme until mitotic activity in lymphoid cells is higher by 5- to 10-fold than the end of the 2nd month in man and until sometime near 18—19 in lymphoid cells of spleen, lymph nodes, Peyer's l)atches, etc., days after fertilization in the mouse (3). and with advancing age this activity remains high. This high There has Leen a running controversy over the years con mitotic activity is probably determined by the unique epithelial cerning the origin of lymphoid elements in this embryonic reticulum cell elements of the thymus. The evidence for the role epithelial structure. Some authors maintained that thymic round of the medulla in cortical function has been reviewed by Metcalf cells were of mesodermal origin arising from mesenchyme outside (66). In the thymus cortex of normal animals, in contrast to the thymus with subsequent migration into the organ or from other lymphoid organs, lymphoid follicles and germinal centers mesenchymal cells which had migrated into the epithelial thymus. usually are not present and plasma cells are infrequent. Others contended that lymphoid elements arose directly from The rate of production of lymphocytes in the thymus appears reticulum epithelium. Recently Auerbach (3) analyzed the not to be influenced by antigenic stimulation, partial thymec morphogenetic events in thymic development in mouse thymus tomy, resection of other lymphoid organs or the presence of organ cultures at a time when epithelium and mesenchyme are multiple thymic grafts. Lymphoid cells within the thymus, how quite distinct and observed an in situ lymphopoiesis, apparently ever, are known to be subjected to the same hormonal regulation from epithelial components. Host migrating cells, thymus as lymphoid cells in other organs. Also the fact that there is no mesoderm, and generalized mesenchyme appeared not to con increase in mitotic frequency or regeneration of thymic frag tribute to this initial lymphoid population of cells. Timewise, this ments following partial thymectomy strongly suggests that differentiation precedes to appearance of lymphoid cells in other thymic lymphopoiesis is associated with an intrinsic stimulus lymphoid organs. It may therefore be considered that the thymus related to certain unique structures scattered throughout the is “themajor primordium of the mammalian lymphoid system― thymus (see Metcalf, Ref. 66). and that migration of lymphoid cells from this primary lymphoid Certain other characteristic features of thymic lymphoid elements have recently been demonstrated by serologic methods. Thymic lymphocytes have been shown to possess distinctive 1 G. H. A. Clowes Memorial Lecture, presented at the 56th antigens (79, 87) and they have also been shown to have a dis Annual Meeting of the American Association for Cancer Research tinctive sensitivity to the cytotoxic effect of guinea pig serum on April 8, 1965, Philadelphia, Pennsylvania. (28) and of natural isoantibodies present in the sera of certain Received for publication December 1, 1965. normal mice (94). APRIL 1966 551 Downloaded from cancerres.aacrjournals.org on October 5, 2021. © 1966 American Association for Cancer Research. Lloyd W. Law Table 1 lists some of the structural and functional differences birth in this laboratory are shown in Table 2. Strain and age of between thymus and other lymphoid organs. mouse at thymectomy significantly affect the severity and onset Functionally, there is no doubt that lymphoid cells recovered of the “wasting―syndrome. C3H mice commonly show diarrhea from the thymus are quite distinct from those of other sources and “ruffled―fur whereas these conditions have not been such as lymph nodes, spleen, and Peyer's patches (7) ; it is also observed among the other inbred strains used in this laboratory. clear that at least a major portion of thymic lymphoid cells are Some strains of mice do not show “wasting.―Signsof wasting or not special types of lymphoid cells, at least in the adult animal of disturbed growth patterns have not been observed in our and that thymic stem cells are being replaced continually by NIH (Swiss-Webster) strain following thymic removal, nor was immigrant cells (66). Lymphocyte migration studies show that there observed a peripheral lymphopenia (see Table 3) ; yet these there exists a slow but continuous afferent stream of cells to the neonatally thymectomized mice show a strikingly altered thymus from the circulation (24). The nature of these immigrant response to infection with LCM virus (57) and have a deficient cells and the site or origin is unsolved. Residence, however, with homograft rejection mechanism to neopla.stic growths (un in the microenvironment of the thymus appears to influence the published observation). An absence of wasting but a selective function of these cells (73). effect of neonatal thymectomy on certain immunologic responses has been observed also in C57BL/6J mice (9). Effects of Neonatal Thymectomy The striking “wasting―describedin the hamster (Mesocricetus auralus) following neonatal thymectomy by Sherman et at. (95) The unique structural and functional characteristics of the thymus, its pattern of growth attaining maximum size very TABLE 1 early in life, the evidence that it represents the primordium of MORPHOLOGIC AND FUNCTIONAL DIFFERENCES lymphoid cell populations at least in the mouse, all suggest that BETWEEN THYMUS AND OTHER LYMPHOID the thymus indeed directs the immunologic development and ORGANS responsiveness of the mammal. That it is an organ of vital Th importance was shown by @Iiller(69) and by Martinez et at. (62) tissueLymphocytesSmallerEpithelial ymusNonthymic lymphoid who performed surgical removal of the thymus in laboratory mice within 24 hr after birth. The consequences of early thymectomy may be grouped under cellsPresentAbsentMitoticreticular 3 syndromes the relationship of one to the other of which is not activity5—lOXXHassall as yet completely understood : (a) failure of normal bodily corpusclesPresentAbsentLymphoid‘S growth and early mortality (wasting) ; (b) lymphocyte depletion; andAbsentPresentgerminalfollicles (c) immunologic deficits. centersPlasma cellsInfrequentPresentSite The lethal “wasting―syndrome has been observed in rats (40) of localantigenic—+response and hamsters (95) as well as in certain strains of mice. The results obtained following thymectomy within 24 hr after TABLE 2 MORTALITY IN NEONATALLY THYMECTOMIZED MICE OF DIFFERENT STRAINSC of dead! age at death (days)RemarC3Hf/Lw2863/76StrainNo. littersNo. No. thymectomizedMean and range incompleteC3Hf/Bi1015/22 (85%)58.4 (30—148)13 (68%)64.4 (40—97)2 incomplete 5 with ectopic thymic tissueBALB/c73/13 (23%)85 (80—95)3 incomplete 7/13 with ectopic thymic tissueC57BL/Ka611/21 (52%)66 (39—125)4 incomplete 3/3 with ectopic thymic tissueDBA/2929/35 incomplete(BL (83%)72.4 (44—84)6 incompleteNIH150/63Alivex C3H)F12047/54 (87%)94.0 (30—180)7 14 months a Age at thymectomy: <24 hr. 552 CANCER RESEARCH VOL. 26 Downloaded from cancerres.aacrjournals.org on October 5, 2021. © 1966 American Association for Cancer Research. Thymic Function TABLE 3 EFFECT OF NEONATAL THYMECTOMY ON PERIPHERAL LEtJKOCYTES of leukocytes/cu mmL/G StrainNo.Age (wk)No. ratio°TotalLyznpho GranulocytesC3Hf/LwIntact or sham214-67,320 (4,000—14,600)45402,7801.64Thymectomy at birth354—65,170 (2,000—10,500)13453,8250.35DBA/2Intactorsham8911,200 (7,750-12,900)60455,1551.17Thymectomy at birth20 (7,100—29,700) 0.43NIH 109 1119,620 15,990 479510,400 9,1950.89 (8,750-27,500)9220 (Swiss-Webster)Sham106—86,880 (5,300—10,600)29003,9800.75Thymectomy at birth106—86,430 (3,200—9,500)34702,9601.17 a L, lymphocytes; G, granulocytes. has not been observed in this laboratory nor by Roosa et at. (88). agent or its product. Neonatally thymectomized mice because of Immunologic deficiencies do occur nevertheless in these animals.
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