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Thymic Function and Impaired Maintenance of Peripheral T Cell Populations in Children with Congenital Heart Disease and Surgical Thymectomy

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Thymic Function and Impaired Maintenance of Peripheral T Cell Populations in Children with Congenital Heart Disease and Surgical Thymectomy 0031-3998/05/5701-0042 PEDIATRIC RESEARCH Vol. 57, No. 1, 2005 Copyright © 2004 International Pediatric Research Foundation, Inc. Printed in U.S.A. Thymic Function and Impaired Maintenance of Peripheral T Cell Populations in Children with Congenital Heart Disease and Surgical Thymectomy NANCY J. HALNON, BETH JAMIESON, MARK PLUNKETT, CHRISTINE M.R. KITCHEN, THAO PHAM, AND PAUL KROGSTAD Department of Pediatrics [NJ.H., T.P., P.K.], Department of Medicine [B.J.], Department of Surgery [M.P.], and Department of Molecular and Medical Pharmacology [P.K.], David Geffen School of Medicine at the University of California, Los Angeles, Los Angeles, California, 90095, and UCLA School of Public Health [C.M.R.K.], Los Angeles, California, 90095 ABSTRACT The thymus begins involution in childhood and historically it during a period of immunologic development. We found that was thought to be nonfunctional by adulthood, thus presenting no cardiothoracic surgical procedures, especially if they include contraindication to the routine practice of thymectomy during thymectomy, impair T-cell production and produce long-term cardiothoracic surgery. More recent data suggest, however, that decreases in total lymphocyte count and CD4ϩ and CD8ϩ T-cell the thymus remains active into adulthood and is responsible for subsets, suggesting that long-term maintenance of lymphocyte the low-level production of normal T cells. We hypothesize, populations is disturbed. (Pediatr Res 57: 42–48, 2005) therefore, that incidental thymectomy during cardiothoracic sur- gery in infancy causes long-term changes in the cellular immune Abbreviations system. To investigate this hypothesis, we quantified peripheral MG, myasthenia gravis T-cell subsets and T-cell recombination excision circles in chil- PBMC, peripheral blood mononuclear cells dren with congenital heart disease to measure the impact of RTE, recent thymic emigrants cardiothoracic surgical procedures and thymectomy performed TREC, T cell receptor recombination excision circles Children undergoing corrective or palliative cardiothoracic gery (4–7). However, until recently, it has been difficult to surgeries frequently undergo incidental thymectomy to in- quantify activity of the thymus, even in normal individuals, crease exposure of the surgical field. Although profound im- making it difficult to assess the impact of thymectomy on the mune deficiency is known to result from the absence of a naïve T-cell compartment and on de novo T-cell production thymus during fetal development (1–3), little is known of the and the subsequent effects on adaptive immunity. effects of thymectomy in humans during a period of postnatal Initial attempts to quantify the contribution of thymopoiesis immunologic development. Short-term studies to date have not to the cellular immune system during postnatal development documented overt immune deficiency in infants who have been and into adulthood have focused on the phenotypic measure- subjected to incidental thymectomy during cardiothoracic sur- ment of the naïve T-cell population in peripheral blood. These cells, by definition, are mature, circulating T cells that have not yet encountered their cognate antigens. Naïve T cells were Received June 14, 2004; accepted September 2, 2004. initially identified as CD4ϩ or CD8ϩ cells that also express Correspondence: Paul Krogstad, M.D., Division of Pediatric Infectious Diseases, Mattel Children’s Hospital at UCLA, MDCC 22–442, 10833 LeConte Ave., Los Angeles, CA CD45RA on their surface. Use of multiple-color flow cytom- 90095; e-mail: [email protected] etry has brought into question the reliance on CD45RA ex- Supported by a Research Fellowship Award from the American Academy of Pediatrics pression alone, as up to 10–30% of CD4ϩ or CD8ϩ CD45RAϩ to N.H. and the Laubisch Foundation. The authors would like to acknowledge Mr. Gerald Oppenheim for a seed grant that supported this research. P.K. is an Elizabeth Glaser T cells lack cell-surface markers and cytokine expression Scientist of the Pediatric AIDS Foundation. Flow cytometry was performed in the UCLA profiles characteristic of naïve cells (8). Flow cytometric mark- Jonsson Comprehensive Cancer Center and Center for AIDS Research Flow Cytometry ers also fail to differentiate RTE from naïve T cells produced Core Facility that is supported by National Institutes of Health awards CA-16042 and AI-28697, by the Jonsson Cancer Center, the UCLA AIDS Institute, and the UCLA by clonal expansion in the periphery. However, Douek et al. School of Medicine. (9,10) developed a PCR-based assay that permits quantification DOI: 10.1203/01.PDR.0000147735.19342.DE of cells bearing TREC, which are nonreplicating circular DNA 42 T CELL POPULATIONS AND THYMECTOMY 43 molecules generated during excisional rearrangement of the Quantitation of TREC and cellular DNA. DNA was extracted from PBMC coding sequences for T-cell receptor proteins. TREC remain in using 100 ␮g/mL proteinase K (Boehringer Ingelheim, Ridgefield, CT) diluted T cells after their maturation and release from the thymus to the in 10 mM Tris and 0.5 mM EDTA. Samples were incubated for1hat56°C and then for10 min at 95°C. TREC were quantified using real-time PCR analysis, periphery. Although they are diluted as cells proliferate, the using the 5' nuclease (TaqMan) assay and the ABI Prism 7700 sequence number of TREC serves as a parameter of thymopoiesis (11– detector system (Applied Biosystems, Foster City, CA) as previously described 13). The use of these techniques has demonstrated that the (19). A 25-␮L PCR mixture consisted of 5 ␮L of genomic DNA extract, 1ϫ ␮ thymus normally remains active well into adulthood, and that PCR buffer containing 20 mM Tris and 50 mM KCl, 3.5 mM MgCl2,1 L5 ␮ its function is required for reconstitution of immune function mM dNTP, 1 L 12.5 pM forward primer (CACATCCCTTTCAACCAT- GCT), 1 ␮L 12.5 pM reverse primer (GCCAGCTGCAGGGTTTAGG), 1 ␮L during treatment for HIV infection, and after cytolytic cancer 5 ␮M probe (FAM-5'ACACCTCTGGTTTTTGTAAAGGTGCCACT-3'- chemotherapy or bone marrow transplantation (10,14–18). TAMRA) (MegaBases, Chicago, IL), 0.25 ␮L10␮M BD 636 reference dye To investigate the long-term effects of thymectomy during (MegaBases), and 0.125 ␮L platinum Taq polymerase. The PCR conditions were immune development in young children, we have examined set at 95°C for 5 min, 95°C for 30 s, and 60°C for 1 min for 40 cycles. A standard 6 thymic function and peripheral T-cell populations in children curve for TREC copy number was established with a range of 25 to10 copies of plasmid containing signal joint TREC (kindly provided by D. Doueck) (10). All between 2 mo and 17 y after surgery for repair or palliation of samples were analyzed in triplicate using a single lot of serially diluted plasmid as congenital cardiac lesions. We evaluated the long-term conse- standards for all assays. The mean of the triplicate TREC values was used for data quences of incidental thymectomy in infancy in a cohort of analysis. As previously described, the coefficient of variation among replicates was subjects with congenital heart disease who have undergone less than 20% for nearly all samples (19). corrective or palliative surgical procedures early in life, com- The number of cells in each test sample was confirmed using real-time PCR to amplify CCR5 DNA sequences using a primer-probe combination supplied paring subjects with complete thymectomy with those without by D. Douek. A 25-␮L PCR mixture consisted of 5 ␮L of genomic DNA prior surgery, and those whose thymus was spared during extract, 1ϫ PCR buffer containing 20 mM Tris and 50 mM KCl, 3.5 mM ␮ ␮ surgery. MgCl2,1 L 5 mM dNTP, 1 L 12.5 pM forward primer (TACCTGCT- CAACCTGGCCAT), 1 ␮L 12.5 pM reverse primer (TTCCAAAGTCCCACT- GGGC), 1 ␮L5␮M probe (5'FAM-TTTCCTTCTTACTGTCCCCTTCT- METHODS GGGCTC-TAMRA3'), 0.25 ␮L10␮M Blue 636 reference dye, and 0.125 ␮L platinum Taq polymerase using PCR conditions as described for TREC analysis. We used an estimate of 8 ␮g of DNA per million PBMC. Results Selection of study subjects. Subjects with a history of congenital heart were expressed as TREC/106 cells. Using a standard curve with a range of 25 disease presenting for evaluation before an initial or repeat cardiothoracic to 106 TREC/sample, the assay has a limit of detection of approximately surgical procedure were recruited for study. Sixty-nine individuals ranging 400–3000 TREC/million PBMC depending on the number of cells analyzed. from 1 mo to 18 y in age were enrolled after informed consent was obtained For samples with undetectable TREC levels, values were recorded at the limit according to a protocol reviewed and approved by the UCLA Medical Insti- of detection for the individual sample. tutional Review Board. Medical history was obtained, including age, specific Cell staining and flow cytometry. Whole-blood cell staining was done to congenital cardiac diagnosis, recent and past infectious illnesses, and history of determine the percentages of CD3ϩ CD4ϩ, CD3ϩ CD8ϩ, and CD4ϩ prior surgical procedures. To eliminate the confounding effects severe physical CD45RAϩ CD62Lϩ T cells. Staining used CD8-conjugated FITC, CD3- debilitation might have on immune function, subjects were recruited only from conjugated phycoerythrin (PE), CD4-conjugated allophycocyanin (APC), those well enough to await elective surgical procedures. The subjects with or peridinin chlorophyll protein (PerCP), CD45RA-conjugated FITC, and asthma (two individuals) and one subject with a history of cardiac transplan- CD62L-conjugated PE antibodies (BD Biosciences, San Diego, CA) according tation had no history of recent steroid use. to the manufacturer’s instructions. Cells were acquired on a FACSCalibur flow Subjects were excluded if they had a history of 22q11 chromosomal cytometer and the data were analyzed using CellQuest Software (BD Bio- deletion (by fluorescence in situ hybridization) or recent infections. Subjects, sciences). For selected subjects cryopreserved PBMC were reanalyzed to who after evaluation did not undergo a surgical procedure or for whom quantify cells with simultaneous expression of CD4ϩ, CD27ϩ, and CD45RAϩ intraoperative visualization of midline structures did not occur (e.g.
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