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• W2045496772 abstract "In 1966, Henry Claman and his colleagues published one of the all-time seminal articles in immunology.1Claman H.N. Chaperon E.A. Triplett R.F. Thymus-marrow cell combinations. Synergism in antibody production.Proc Soc Exp Biol Med. 1966; 122: 1167-1171Crossref PubMed Scopus (440) Google Scholar The article showed that 2 different types of cells, thymocytes and bone marrow–derived cells, had to get together for antibody production to occur. This finding was a very significant result in cellular immunology, and it is also a beautiful example of discovery by accident, an experiment that was actually designed to investigate something else but in the end uncovered something much more important and completely unsuspected. Grand examples of such experiments include Galileo's discovery of the moons of Jupiter. As far as we can tell, he was simply pointing a new instrument, the telescope, at an object at which no one had ever looked so closely before. Another example is Columbus' bumping into America on his way to India. Henry Claman writes that he was trying to find out whether thymocytes could make antibody, a follow-up to Jacques Miller and Robert Good's discoveries about the importance of the thymus, and that he only added the bone marrow cell to keep the irradiated mice alive. As it turned out, this, of course, was the crucial element of the experiment. The thymocyte–bone marrow collaboration experiment has led to our current understanding of antibody production. The result of the experiment also implied several other key features of the immune system, features that were not well appreciated at the time but that have led to multitudes of experiments and discoveries since then. For many years, of course, scientists thought the small lymphocyte, which looked so boring and inactive down the microscope, had no function at all. The Claman experiment helped change everyone's mind about this. In fact, it showed that not only did lymphocytes have functions, but also not all of these cells had the same function. We know that there are many different kinds of lymphocytes. B cells themselves can be in any of a number of states. Likewise, not only do we have different maturational stages of T cells, but also T cells can be any of several classes: cytotoxic, helper, or regulatory. At first thought, this is not at all an obvious property of the immune system. We know that lymph nodes and the spleen have structural organization, but on the whole, they seem to be pretty loose bags of cells, easily dispersed and not in tight contact with each. Matters are even worse in the blood stream and in nonlymphoid tissues, where the cells of the immune system are quite dispersed and might not be in contact with another immune cell at all. Nevertheless, the Claman, Chaperon, and Triplett experiment showed, for the first time, that lymphocytes have to communicate with each other for antibody to be produced. This led to questions about the form of the communication. In the 1960s, after the observations of Miller2Miller J.F. Immunological function of the thymus.Lancet. 1961; 2: 748-749Abstract PubMed Scopus (733) Google Scholar and Good and Gabrielsen3Good R.A. Gabrielsen A.E. The function of the thymus.Med Sci. 1964; 15: 54-61PubMed Google Scholar and the publication of the Claman experiment, the betting was on the idea that antibody was made by the thymocytes and that the bone marrow cells were providing some sort of support. Jacques Miller's work on the thymus was highlighted in a previous Allergy Archives feature.4Cohen S. Jacques Miller on the thymus.J Allergy Clin Immunol. 2005; 116: 1170-1174Abstract Full Text Full Text PDF Google Scholar It was not until the Claman experiment was repeated, with markers on each kind of cell, by Mitchell and Miller5Mitchell G.F. Miller J.F. Cell to cell interaction in the immune response. II. The source of hemolysin-forming cells in irradiated mice given bone marrow and thymus or thoracic duct lymphocytes.J Exp Med. 1968; 128: 821-837Crossref PubMed Scopus (440) Google Scholar that it was realized that the antibody was coming from the bone marrow cells, the B cells. What were the thymocytes up to? Answers to this question came from experiments done in parallel to the B cell/T cell–mixing studies, experiments that showed that B-cell production of antibody to, for example, a hapten, could be helped by simultaneous recognition of some other portion of the antigen, for example, the carrier protein to which the hapten was attached.6Rajewsky K. Schirrmacher V. Nase S. Jerne N.K. The requirement of more than one antigenic determinant for immunogenicity.J Exp Med. 1969; 129: 1131-1143Crossref PubMed Scopus (266) Google Scholar, 7Mitchison N.A. The carrier effect in the secondary response to hapten-protein conjugates. I. Measurement of the effect with transferred cells and objections to the local environment hypothesis.Europ J Immunol. 1971; 1: 10-17Crossref PubMed Scopus (237) Google Scholar Pioneering experiments on such systems led to the idea that recognition of the carrier resulted in help for the B cells making antibody to the hapten. At this point, the discoveries of T and B cells and of help for antibody production came together beautifully, with the realization that T cells provide help, and B cells perform the function. This paradigm is now applied to many aspects of immunity, helper T-cell cooperation with cytotoxic T cells, regulatory T-cell modification of the function of T cells and dendritic cells, the effects of dendritic cell maturation on T-cell responses, and so on. Obviously cells that are not tightly connected could signal to one another with soluble factors. The cells of the immune system are, of course, masters at this kind of communication, using at least 35 different ILs and many other soluble factors, including the IFNs and TNF, which, for one reason or another, never achieved IL nomenclature status. Early in the game, several laboratories followed up the Claman experiment by showing that soluble factors from T cells could drive antibody responses by B cells.8Dutton R.W. Hunter P. The effects of mitogen-stimulated T cells on the response of B cell to antigen and the mechanism of T cell stimulation and of the B cell response.Soc Gen Physiol Ser. 1974; 29: 199-215PubMed Google Scholar, 9Hunter P. Kettman J.R. Mode of action of a supernatant activity from T-cell cultures that nonspecifically stimulates the humoral immune response.Proc Natl Acad Sci U S A. 1974; 71: 512-516Crossref PubMed Scopus (32) Google Scholar, 10Schimpl A. Wecker E. Replacement of T-cell function by a T-cell product.Nat New Biol. 1972; 237: 15-17Crossref PubMed Scopus (394) Google Scholar, 11Watson J. The role of humoral factors in the initiation of in vitro primary immune responses. 3. Characterization of factors that replace thymus-derived cells.J Immunol. 1973; 111: 1301-1313PubMed Google Scholar These soluble factors were given quaint names (“Te deum” was one), but by the end of the 1970s, these names were turning out to be increasingly confusing; for example, at least 4 different terms were used to describe what we now know to be IL-1. Thus the establishment of the IL nomenclature in the late 1970s allowed great clarification of the field. At last, a single term, a term that did not predict any of the functions of the cytokine, could be used to describe each entity. In the end, it turns out that T and B cells must actually touch each other for good B-cell responses to occur. Experiments showing that helper T cells must recognize MHC proteins on B cells led the way, but in the end, the crucial element was the discovery of CD40 and its ligand. B cells do not make good thymus-dependent responses unless CD40 on their surfaces is signaled by encounter with CD40 ligand on T cells.12Banchereau J. de Paoli P. Valle A. Garcia E. Rousset F. Long-term human B cell lines dependent on interleukin-4 and antibody to CD40.Science. 1991; 251: 70-72Crossref PubMed Scopus (531) Google Scholar, 13Covey L.R. Cleary A.M. Yellin M.J. Ware R. Sullivan G. Belko J. et al.Isolation of cDNAs encoding T-BAM, a surface glycoprotein on CD4+ T cells mediating contact-dependent helper function for B cells: identity with the CD40-ligand.Mol Immunol. 1994; 31: 471-484Crossref PubMed Scopus (27) Google Scholar, 14Graf D. Korthauer U. Mages H.W. Senger G. Kroczek R.A. Cloning of TRAP, a ligand for CD40 on human T cells.Eur J Immunol. 1992; 22: 3191-3194Crossref PubMed Scopus (271) Google Scholar Here again, this was not the obvious result. T and B cells live in different areas of lymphoid organs, and it is not obvious how the cells come close enough together to manage CD40–CD40 ligand contact. The solution to this problem is coming from use of a new instrument, the 2-photon microscope, which allows observation in real time of lymphocytes in intact lymph nodes. The instrument shows that when antigen arrives in the lymph node, B cells bind the antigen and move to the edge of the B-cell areas, where they patrol backward and forward, waiting for an antigen-specific T cell to approach the same point and contact them. Then the B and T cells move together for some time, with the B cell leading the way.15Cahalan M.D. Parker I. Close encounters of the first and second kind: T-DC and T-B interactions in the lymph node.Semin Immunol. 2005; 17: 442-451Crossref PubMed Scopus (43) Google Scholar, 16Okada T. Miller M.J. Parker I. Krummel M.F. Neighbors M. Hartley S.B. et al.Antigen-engaged B cells undergo chemotaxis toward the T zone and form motile conjugates with helper T cells.PLoS Biol. 2005; 3: e150Crossref PubMed Scopus (440) Google Scholar The Claman experiment laid the foundations for all these and many other ideas in contemporary immunology, and for this, we owe Henry and his colleagues a great debt." @default.
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• W2045496772 title "Thymocytes and bone marrow cells in 1966: Where did we go from there?" @default.
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